Risks to Health and Well-Being From Radio-Frequency Radiation Emitted by Cell Phones and Other Wireless Devices

EVIEW ARTICLE

Front. Public Health, 13 August 2019 | https://doi.org/10.3389/fpubh.2019.00223

Risks to Health and Well-Being From Radio-Frequency Radiation Emitted by Cell Phones and Other Wireless Devices

Anthony B. Miller1*Margaret E. Sears2L. Lloyd Morgan3Devra L. Davis3Lennart Hardell4Mark Oremus5 and Colin L. Soskolne6,7

  • 1Dalla Lana School of Public Health, University of Toronto, Toronto, ON, Canada
  • 2Ottawa Hospital Research Institute, Prevent Cancer Now, Ottawa, ON, Canada
  • 3Environmental Health Trust, Teton Village, WY, United States
  • 4The Environment and Cancer Research Foundation, Örebro, Sweden
  • 5School of Public Health and Health Systems, University of Waterloo, Waterloo, ON, Canada
  • 6School of Public Health, University of Alberta, Edmonton, AB, Canada
  • 7Health Research Institute, University of Canberra, Canberra, ACT, Australia

Radiation exposure has long been a concern for the public, policy makers, and health researchers. Beginning with radar during World War II, human exposure to radio-frequency radiation1 (RFR) technologies has grown substantially over time. In 2011, the International Agency for Research on Cancer (IARC) reviewed the published literature and categorized RFR as a “possible” (Group 2B) human carcinogen. A broad range of adverse human health effects associated with RFR have been reported since the IARC review. In addition, three large-scale carcinogenicity studies in rodents exposed to levels of RFR that mimic lifetime human exposures have shown significantly increased rates of Schwannomas and malignant gliomas, as well as chromosomal DNA damage. Of particular concern are the effects of RFR exposure on the developing brain in children. Compared with an adult male, a cell phone held against the head of a child exposes deeper brain structures to greater radiation doses per unit volume, and the young, thin skull’s bone marrow absorbs a roughly 10-fold higher local dose. Experimental and observational studies also suggest that men who keep cell phones in their trouser pockets have significantly lower sperm counts and significantly impaired sperm motility and morphology, including mitochondrial DNA damage. Based on the accumulated evidence, we recommend that IARC re-evaluate its 2011 classification of the human carcinogenicity of RFR, and that WHO complete a systematic review of multiple other health effects such as sperm damage. In the interim, current knowledge provides justification for governments, public health authorities, and physicians/allied health professionals to warn the population that having a cell phone next to the body is harmful, and to support measures to reduce all exposures to RFR.

Introduction

We live in a generation that relies heavily on technology. Whether for personal use or work, wireless devices, such as cell phones, are commonly used around the world, and exposure to radio-frequency radiation (RFR) is widespread, including in public spaces (12).

In this review, we address the current scientific evidence on health risks from exposure to RFR, which is in the non-ionizing frequency range. We focus here on human health effects, but also note evidence that RFR can cause physiological and/or morphological effects on bees, plants and trees (35).

We recognize a diversity of opinions on the potential adverse effects of RFR exposure from cell or mobile phones and other wireless transmitting devices (WTDs) including cordless phones and Wi-Fi. The paradigmatic approach in cancer epidemiology, which considers the body of epidemiological, toxicological, and mechanistic/cellular evidence when assessing causality, is applied.

Carcinogenicity

Since 1998, the International Commission on Non-Ionizing Radiation Protection (ICNIRP) has maintained that no evidence of adverse biological effects of RFR exist, other than tissue heating at exposures above prescribed thresholds (6).

In contrast, in 2011, an expert working group of the International Agency for Research on Cancer (IARC) categorized RFR emitted by cell phones and other WTDs as a Group 2B (“possible”) human carcinogen (7).

Since the IARC categorization, analyses of the large international Interphone study, a series of studies by the Hardell group in Sweden, and the French CERENAT case-control studies, signal increased risks of brain tumors, particularly with ipsilateral use (8). The largest case-control studies on cell phone exposure and glioma and acoustic neuroma demonstrated significantly elevated risks that tended to increase with increasing latency, increasing cumulative duration of use, ipsilateral phone use, and earlier age at first exposure (8).

Pooled analyses by the Hardell group that examined risk of glioma and acoustic neuroma stratified by age at first exposure to cell phones found the highest odds ratios among those first exposed before age 20 years (911). For glioma, first use of cell phones before age 20 years resulted in an odds ratio (OR) of 1.8 (95% confidence interval [CI] 1.2–2.8). For ipsilateral use, the OR was 2.3 (CI 1.3-4.2); contralateral use was 1.9 (CI 0.9-3.7). Use of cordless phone before age 20 yielded OR 2.3 (CI 1.4–3.9), ipsilateral OR 3.1 (CI 1.6–6.3) and contralateral use OR 1.5 (CI 0.6–3.8) (9).

Although Karipidis et al. (12) and Nilsson et al. (13) found no evidence of an increased incidence of gliomas in recent years in Australia and Sweden, respectively, Karipidis et al. (12) only reported on brain tumor data for ages 20–59 and Nilsson et al. (13) failed to include data for high grade glioma. In contrast, others have reported evidence that increases in specific types of brain tumors seen in laboratory studies are occurring in Britain and the US:

• The incidence of neuro-epithelial brain cancers has significantly increased in all children, adolescent, and young adult age groupings from birth to 24 years in the United States (1415).

• A sustained and statistically significant rise in glioblastoma multiforme across all ages has been described in the UK (16).

The incidence of several brain tumors are increasing at statistically significant rates, according to the 2010–2017 Central Brain Tumor Registry of the U.S. (CBTRUS) dataset (17).

• There was a significant increase in incidence of radiographically diagnosed tumors of the pituitary from 2006 to 2012 (APC = 7.3% [95% CI: 4.1%, 10.5%]), with no significant change in incidence from 2012 to 2015 (18).

• Meningioma rates have increased in all age groups from 15 through 85+ years.

• Nerve sheath tumor (Schwannoma) rates have increased in all age groups from age 20 through 84 years.

• Vestibular Schwannoma rates, as a percentage of nerve sheath tumors, have also increased from 58% in 2004 to 95% in 2010-2014.

Epidemiological evidence was subsequently reviewed and incorporated in a meta-analysis by Röösli et al. (19). They concluded that overall, epidemiological evidence does not suggest increased brain or salivary gland tumor risk with mobile phone (MP) use, although the authors admitted that some uncertainty remains regarding long latency periods (>15 years), rare brain tumor subtypes, and MP usage during childhood. Of concern is that these analyses included cohort studies with poor exposure classification (20).

In epidemiological studies, recall bias can play a substantial role in the attenuation of odds ratios toward the null hypothesis. An analysis of data from one large multicenter case-control study of RFR exposure, did not find that recall bias was an issue (21). In another multi-country study it was found that young people can recall phone use moderately well, with recall depending on the amount of phone use and participants’ characteristics (22). With less rigorous querying of exposure, prospective cohort studies are unfortunately vulnerable to exposure misclassification and imprecision in identifying risk from rare events, to the point that negative results from such studies are misleading (823).

Another example of disparate results from studies of different design focuses on prognosis for patients with gliomas, depending upon cell phone use. A Swedish study on glioma found lower survival in patients with glioblastoma associated with long term use of wireless phones (24). Ollson et al. (25), however, reported no indication of reduced survival among glioblastoma patients in Denmark, Finland and Sweden with a history of mobile phone use (ever regular use, time since start of regular use, cumulative call time overall or in the last 12 months) relative to no or non-regular use. Notably, Olsson et al. (25) differed from Carlberg and Hardell (24) in that the study did not include use of cordless phones, used shorter latency time and excluded patients older than 69 years. Furthermore, a major shortcoming was that patients with the worst prognosis were excluded, as in Finland inoperable cases were excluded, all of which would bias the risk estimate toward unity.

In the interim, three large-scale toxicological (animal carcinogenicity) studies support the human evidence, as do modeling, cellular and DNA studies identifying vulnerable sub-groups of the population.

The U.S. National Toxicology Program (NTP) (National Toxicology Program (2627) has reported significantly increased incidence of glioma and malignant Schwannoma (mostly on the nerves on the heart, but also additional organs) in large animal carcinogenicity studies with exposure to levels of RFR that did not significantly heat tissue. Multiple organs (e.g., brain, heart) also had evidence of DNA damage. Although these findings have been dismissed by the ICNIRP (28), one of the key originators of the NTP study has refuted the criticisms (29).

A study by Italy’s Ramazzini Institute has evaluated lifespan environmental exposure of rodents to RFR, as generated by 1.8 GHz GSM antennae of cell phone radio base stations. Although the exposures were 60 to 6,000 times lower than those in the NTP study, statistically significant increases in Schwannomas of the heart in male rodents exposed to the highest dose, and Schwann-cell hyperplasia in the heart in male and female rodents were observed (30). A non-statistically significant increase in malignant glial tumors in female rodents also was detected. These findings with far field exposure to RFR are consistent with and reinforce the results of the NTP study on near field exposure. Both reported an increase in the incidence of tumors of the brain and heart in RFR-exposed Sprague-Dawley rats, which are tumors of the same histological type as those observed in some epidemiological studies on cell phone users.

Further, in a 2015 animal carcinogenicity study, tumor promotion by exposure of mice to RFR at levels below exposure limits for humans was demonstrated (31). Co-carcinogenicity of RFR was also demonstrated by Soffritti and Giuliani (32) who examined both power-line frequency magnetic fields as well as 1.8 GHz modulated RFR. They found that exposure to Sinusoidal-50 Hz Magnetic Field (S-50 Hz MF) combined with acute exposure to gamma radiation or to chronic administration of formaldehyde in drinking water induced a significantly increased incidence of malignant tumors in male and female Sprague Dawley rats. In the same report, preliminary results indicate higher incidence of malignant Schwannoma of the heart after exposure to RFR in male rats. Given the ubiquity of many of these co-carcinogens, this provides further evidence to support the recommendation to reduce the public’s exposure to RFR to as low as is reasonably achievable.

Finally, a case series highlights potential cancer risk from cell phones carried close to the body. West et al. (33) reported four “extraordinary” multifocal breast cancers that arose directly under the antennae of the cell phones habitually carried within the bra, on the sternal side of the breast (the opposite of the norm). We note that case reports can point to major unrecognized hazards and avenues for further investigation, although they do not usually provide direct causal evidence.

In a study of four groups of men, of which one group did not use mobile phones, it was found that DNA damage indicators in hair follicle cells in the ear canal were higher in the RFR exposure groups than in the control subjects. In addition, DNA damage increased with the daily duration of exposure (34).

Many profess that RFR cannot be carcinogenic as it has insufficient energy to cause direct DNA damage. In a review, Vijayalaxmi and Prihoda (35) found some studies suggested significantly increased damage in cells exposed to RF energy compared to unexposed and/or sham-exposed control cells, others did not. Unfortunately, however, in grading the evidence, these authors failed to consider baseline DNA status or the fact that genotoxicity has been poorly predicted using tissue culture studies (36). As well funding, a strong source of bias in this field of enquiry, was not considered (37).

Children and Reproduction

As a result of rapid growth rates and the greater vulnerability of developing nervous systems, the long-term risks to children from RFR exposure from cell phones and other WTDs are expected to be greater than those to adults (38). By analogy with other carcinogens, longer opportunities for exposure due to earlier use of cell phones and other WTDs could be associated with greater cancer risks in later life.

Modeling of energy absorption can be an indicator of potential exposure to RFR. A study modeling the exposure of children 3–14 years of age to RFR has indicated that a cell phone held against the head of a child exposes deeper brain structures to roughly double the radiation doses (including fluctuating electrical and magnetic fields) per unit volume than in adults, and also that the marrow in the young, thin skull absorbs a roughly 10-fold higher local dose than in the skull of an adult male (39). Thus, pediatric populations are among the most vulnerable to RFR exposure.

The increasing use of cell phones in children, which can be regarded as a form of addictive behavior (40), has been shown to be associated with emotional and behavioral disorders. Divan et al. (41) studied 13,000 mothers and children and found that prenatal exposure to cell phones was associated with behavioral problems and hyperactivity in children. A subsequent Danish study of 24,499 children found a 23% increased odds of emotional and behavioral difficulties at age 11 years among children whose mothers reported any cell phone use at age 7 years, compared to children whose mothers reported no use at age 7 years (42). A cross-sectional study of 4,524 US children aged 8–11 years from 20 study sites indicated that shorter screen time and longer sleep periods independently improved child cognition, with maximum benefits achieved with low screen time and age-appropriate sleep times (43). Similarly, a cohort study of Swiss adolescents suggested a potential adverse effect of RFR on cognitive functions that involve brain regions mostly exposed during mobile phone use (44). Sage and Burgio et al. (45) posit that epigenetic drivers and DNA damage underlie adverse effects of wireless devices on childhood development.

RFR exposure occurs in the context of other exposures, both beneficial (e.g., nutrition) and adverse (e.g., toxicants or stress). Two studies identified that RFR potentiated adverse effects of lead on neurodevelopment, with higher maternal use of mobile phones during pregnancy [1,198 mother-child pairs, (46)] and Attention Deficit Hyper-activity Disorder (ADHD) with higher cell phone use and higher blood lead levels, in 2,422 elementary school children (47).

A study of Mobile Phone Base Station Tower settings adjacent to school buildings has found that high exposure of male students to RFR from these towers was associated with delayed fine and gross motor skills, spatial working memory, and attention in adolescent students, compared with students who were exposed to low RFR (48). A recent prospective cohort study showed a potential adverse effect of RFR brain dose on adolescents’ cognitive functions including spatial memory that involve brain regions exposed during cell phone use (44).

In a review, Pall (49) concluded that various non-thermal microwave EMF exposures produce diverse neuropsychiatric effects. Both animal research (5052) and human studies of brain imaging research (5356) indicate potential roles of RFR in these outcomes.

Male fertility has been addressed in cross-sectional studies in men. Associations between keeping cell phones in trouser pockets and lower sperm quantity and quality have been reported (57). Both in vivo and in vitro studies with human sperm confirm adverse effects of RFR on the testicular proteome and other indicators of male reproductive health (5758), including infertility (59). Rago et al. (60) found significantly altered sperm DNA fragmentation in subjects who use mobile phones for more than 4 h/day and in particular those who place the device in the trousers pocket. In a cohort study, Zhang et al. (61) found that cell phone use may negatively affect sperm quality in men by decreasing the semen volume, sperm concentration, or sperm count, thus impairing male fertility. Gautam et al. (62) studied the effect of 3G (1.8–2.5 GHz) mobile phone radiation on the reproductive system of male Wistar rats. They found that exposure to mobile phone radiation induces oxidative stress in the rats which may lead to alteration in sperm parameters affecting their fertility.

Related Observations, Implications and Strengths of Current Evidence

An extensive review of numerous published studies confirms non-thermally induced biological effects or damage (e.g., oxidative stress, damaged DNA, gene and protein expression, breakdown of the blood-brain barrier) from exposure to RFR (63), as well as adverse (chronic) health effects from long-term exposure (64). Biological effects of typical population exposures to RFR are largely attributed to fluctuating electrical and magnetic fields (6567).

Indeed, an increasing number of people have developed constellations of symptoms attributed to exposure to RFR (e.g., headaches, fatigue, appetite loss, insomnia), a syndrome termed Microwave Sickness or Electro-Hyper-Sensitivity (EHS) (6870).

Causal inference is supported by consistency between epidemiological studies of the effects of RFR on induction of human cancer, especially glioma and vestibular Schwannomas, and evidence from animal studies (8). The combined weight of the evidence linking RFR to public health risks includes a broad array of findings: experimental biological evidence of non-thermal effects of RFR; concordance of evidence regarding carcinogenicity of RFR; human evidence of male reproductive damage; human and animal evidence of developmental harms; and limited human and animal evidence of potentiation of effects from chemical toxicants. Thus, diverse, independent evidence of a potentially troubling and escalating problem warrants policy intervention.

Challenges to Research, From Rapid Technological Advances

Advances in RFR-related technologies have been and continue to be rapid. Changes in carrier frequencies and the growing complexity of modulation technologies can quickly render “yesterdays” technologies obsolete. This rapid obsolescence restricts the amount of data on human RFR exposure to particular frequencies, modulations and related health outcomes that can be collected during the lifespan of the technology in question.

Epidemiological studies with adequate statistical power must be based upon large numbers of participants with sufficient latency and intensity of exposure to specific technologies. Therefore, a lack of epidemiological evidence does not necessarily indicate an absence of effect, but rather an inability to study an exposure for the length of time necessary, with an adequate sample size and unexposed comparators, to draw clear conclusions. For example, no case-control study has been published on fourth generation (4G; 2–8 GHz) Long-term Evolution (LTE) modulation, even though the modulation was introduced in 2010 and achieved a 39% market share worldwide by 2018 (71).

With this absence of human evidence, governments must require large-scale animal studies (or other appropriate studies of indicators of carcinogenicity and other adverse health effects) to determine whether the newest modulation technologies incur risks, prior to release into the marketplace. Governments should also investigate short-term impacts such as insomnia, memory, reaction time, hearing and vision, especially those that can occur in children and adolescents, whose use of wireless devices has grown exponentially within the past few years.

The Telecom industry’s fifth generation (5G) wireless service will require the placement of many times more small antennae/cell towers close to all recipients of the service, because solid structures, rain and foliage block the associated millimeter wave RFR (72). Frequency bands for 5G are separated into two different frequency ranges. Frequency Range 1 (FR1) includes sub-6 GHz frequency bands, some of which are bands traditionally used by previous standards, but has been extended to cover potential new spectrum offerings from 410 to 7,125 MHz. Frequency Range 2 (FR2) includes higher frequency bands from 24.25 to 52.6 GHz. Bands in FR2 are largely of millimeter wave length, these have a shorter range but a higher available bandwidth than bands in the FR1. 5G technology is being developed as it is also being deployed, with large arrays of directional, steerable, beam-forming antennae, operating at higher power than previous technologies. 5G is not stand-alone—it will operate and interface with other (including 3G and 4G) frequencies and modulations to enable diverse devices under continual development for the “internet of things,” driverless vehicles and more (72).

Novel 5G technology is being rolled out in several densely populated cities, although potential chronic health or environmental impacts have not been evaluated and are not being followed. Higher frequency (shorter wavelength) radiation associated with 5G does not penetrate the body as deeply as frequencies from older technologies although its effects may be systemic (7374). The range and magnitude of potential impacts of 5G technologies are under-researched, although important biological outcomes have been reported with millimeter wavelength exposure. These include oxidative stress and altered gene expression, effects on skin and systemic effects such as on immune function (74). In vivo studies reporting resonance with human sweat ducts (73), acceleration of bacterial and viral replication, and other endpoints indicate the potential for novel as well as more commonly recognized biological impacts from this range of frequencies, and highlight the need for research before population-wide continuous exposures.

Gaps in Applying Current Evidence

Current exposure limits are based on an assumption that the only adverse health effect from RFR is heating from short-term (acute), time-averaged exposures (75). Unfortunately, in some countries, notably the US, scientific evidence of the potential hazards of RFR has been largely dismissed (76). Findings of carcinogenicity, infertility and cell damage occurring at daily exposure levels—within current limits—indicate that existing exposure standards are not sufficiently protective of public health. Evidence of carcinogenicity alone, such as that from the NTP study, should be sufficient to recognize that current exposure limits are inadequate.

Public health authorities in many jurisdictions have not yet incorporated the latest science from the U.S. NTP or other groups. Many cite 28-year old guidelines by the Institute of Electrical and Electronic Engineers which claimed that “Research on the effects of chronic exposure and speculations on the biological significance of non-thermal interactions have not yet resulted in any meaningful basis for alteration of the standard” (77)2.

Conversely, some authorities have taken specific actions to reduce exposure to their citizens (78), including testing and recalling phones that exceed current exposure limits.

While we do not know how risks to individuals from using cell phones may be offset by the benefits to public health of being able to summon timely health, fire and police emergency services, the findings reported above underscore the importance of evaluating potential adverse health effects from RFR exposure, and taking pragmatic, practical actions to minimize exposure.

We propose the following considerations to address gaps in the current body of evidence:

• As many claim that we should by now be seeing an increase in the incidence of brain tumors if RFR causes them, ignoring the increases in brain tumors summarized above, a detailed evaluation of age-specific, location-specific trends in the incidence of gliomas in many countries is warranted.

• Studies should be designed to yield the strongest evidence, most efficiently:

➢ Population-based case-control designs can be more statistically powerful to determine relationships with rare outcomes such as glioma, than cohort studies. Such studies should explore the relationship between energy absorption (SAR3), duration of exposure, and adverse outcomes, especially brain cancer, cardiomyopathies and abnormal cardiac rythms, hematologic malignancies, thyroid cancer.

➢ Cohort studies are inefficient in the study of rare outcomes with long latencies, such as glioma, because of cost-considerations relating to the follow-up required of very large cohorts needed for the study of rare outcomes. In addition, without continual resource-consuming follow-up at frequent intervals, it is not possible to ascertain ongoing information about changing technologies, uses (e.g., phoning vs. texting or accessing the Internet) and/or exposures.

➢ Cross-sectional studies comparing high-, medium-, and low-exposure persons may yield hypothesis-generating information about a range of outcomes relating to memory, vision, hearing, reaction-time, pain, fertility, and sleep patterns.

• Exposure assessment is poor in this field, with very little fine-grained detail as to frequencies and modulations, doses and dose rates, and peak exposures, particularly over the long-term. Solutions such as wearable meters and phone apps have not yet been incorporated in large-scale research.

• Systematic reviews on the topic could use existing databases of research reports, such as the one created by Oceania Radiofrequency Science Advisory Association (79) or EMF Portal (80), to facilitate literature searches.

• Studies should be conducted to determine appropriate locations for installation of antennae and other broadcasting systems; these studies should include examination of biomarkers of inflammation, genotoxicity, and other health indicators in persons who live at different radiuses around these installations. This is difficult to study in the general population because many people’s greatest exposure arises from their personal devices.

• Further work should be undertaken to determine the distance that wireless technology antennae should be kept away from humans to ensure acceptable levels of safety, distinguishing among a broad range of sources (e.g., from commercial transmitters to Bluetooth devices), recognizing that exposures fall with the inverse of the square of the distance (The inverse-square law specifies that intensity is inversely proportional to the square of the distance from the source of radiation). The effective radiated power from cell towers needs to be regularly measured and monitored.

Policy Recommendations Based on the Evidence to Date

At the time of writing, a total of 32 countries or governmental bodies within these countries4 have issued policies and health recommendations concerning exposure to RFR (78). Three U.S. states have issued advisories to limit exposure to RFR (8183) and the Worcester Massachusetts Public Schools (84) voted to post precautionary guidelines on Wi-Fi radiation on its website. In France, Wi-Fi has been removed from pre-schools and ordered to be shut off in elementary schools when not in use, and children aged 16 years or under are banned from bringing cell phones to school (85). Because the national test agency found 9 out of 10 phones exceeded permissible radiation limits, France is also recalling several million phones.

We therefore recommend the following:

1. Governmental and institutional support of data collection and analysis to monitor potential links between RFR associated with wireless technology and cancers, sperm, the heart, the nervous system, sleep, vision and hearing, and effects on children.

2. Further dissemination of information regarding potential health risk information that is in wireless devices and manuals is necessary to respect users’ Right To Know. Cautionary statements and protective measures should be posted on packaging and at points of sale. Governments should follow the practice of France, Israel and Belgium and mandate labeling, as for tobacco and alcohol.

3. Regulations should require that any WTD that could be used or carried directly against the skin (e.g., a cell phone) or in close proximity (e.g., a device being used on the lap of a small child) be tested appropriately as used, and that this information be prominently displayed at point of sale, on packaging, and both on the exterior and within the device.

4. IARC should convene a new working group to update the categorization of RFR, including current scientific findings that highlight, in particular, risks to youngsters of subsequent cancers. We note that an IARC Advisory Group has recently recommended that RFR should be re-evaluated by the IARC Monographs program with high priority.

5. The World Health Organization (WHO) should complete its long-standing RFR systematic review project, using strong modern scientific methods. National and regional public health authorities similarly need to update their understanding and to provide adequate precautionary guidance for the public to minimize potential health risks.

6. Emerging human evidence is confirming animal evidence of developmental problems with RFR exposure during pregnancy. RFR sources should be avoided and distanced from expectant mothers, as recommended by physicians and scientists (babysafeproject.org).

7. Other countries should follow France, limiting RFR exposure in children under 16 years of age.

8. Cell towers should be distanced from homes, daycare centers, schools, and places frequented by pregnant women, men who wish to father healthy children, and the young.

Specific examples of how the health policy recommendations above, invoking the Precautionary Principle, might be practically applied to protect public health, are provided in the Annex.

Author Contributions

All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.

Conflict of Interest Statement

The authors declare that this manuscript was drafted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest, although subsequent to its preparation, DD became a consultant to legal counsel representing persons with glioma attributed to radiation from cell phones.

Acknowledgments

The authors acknowledge the contributions of Mr. Ali Siddiqui in drafting the Policy Recommendations, and those from members of the Board of the International Network for Epidemiology in Policy (INEP) into previous iterations of this manuscript. We are grateful to external reviewers for their thoughtful critiques that have served to improve both accuracy and presentation.This manuscript was initially developed by the authors as a draft of a Position Statement of INEP. The opportunity was then provided to INEP’s 23 member organizations to endorse what the INEP Board had recommended, but 12 of those member organizations elected not to vote. Of the 11 that did vote, three endorsed the statement, two voted against it, and six abstained. Ultimately, the Board voted to abandon its involvement with what it determined to be a divisive topic. The authors then decided that, in the public interest, the document should be published independent of INEP.

Footnotes

1. ^Per IEEE C95.1-1991, the radio-frequency radiation frequency range is from 3 kHz to 300 GHz and is non-ionizing.

2. ^The FCC adopted the IEEE C95.1 1991 standard in 1996.

3. ^When necessary, SAR values should be adjusted for age of child in W/kg.

4. ^Argentina, Australia, Austria, Belgium, Canada, Chile, Cyprus, Denmark, European Environmental Agency, European Parliament, Finland, France, French Polynesia, Germany, Greece, Italy, India, Ireland, Israel, Namibia, New Zealand, Poland, Romania, Russia, Singapore, Spain, Switzerland, Taiwan, Tanzania, Turkey, United Kingdom, United States.

References

1. Carlberg M, Hedendahl L, Koppel T, Hardell L. High ambient radiofrequency radiation in Stockholm city, Sweden. Oncol Lett. (2019) 17:1777–83. doi: 10.3892/ol.2018.9789

PubMed Abstract | CrossRef Full Text | Google Scholar

2. Hardell L, Carlberg M, Hedendahl LK. Radiofrequency radiation from nearby base stations gives high levels in an apartment in Stockholm, Sweden: a case report. Oncol Lett. (2018) 15:7871–83. doi: 10.3892/ol.2018.8285

PubMed Abstract | CrossRef Full Text | Google Scholar

3. Halgamuge MN. Review: weak radiofrequency radiation exposure from mobile phone radiation on plants. Electromagn Biol Med. (2017) 36:213–35. doi: 10.1080/15368378.2016.1220389

PubMed Abstract | CrossRef Full Text | Google Scholar

4. Odemer R, Odemer F. Effects of radiofrequency electromagnetic radiation (RF-EMF) on honey bee queen development and mating success. Sci Total Environ. (2019) 661:553–62. doi: 10.1016/j.scitotenv.2019.01.154

PubMed Abstract | CrossRef Full Text | Google Scholar

5. Waldmann-Selsam C, Balmori-de la Plante A, Breunig H, Balmori A. Radiofrequency radiation injures trees around mobile phone base stations. Sci Total Environ. (2016) 572:554–69. doi: 10.1016/j.scitotenv.2016.08.045

PubMed Abstract | CrossRef Full Text | Google Scholar

6. ICNIRP. 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. (1998) 74:494–522.

Google Scholar

7. IARC. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Non-ionizing Radiation, Part 2: Radiofrequency Electromagnetic Fields. Lyon: International Agency for Research on Cancer (2013). p. 102.

Google Scholar

8. Miller AB, Morgan LL, Udasin I, Davis DL. Cancer epidemiology update, following the 2011 IARC evaluation of radiofrequency electromagnetic fields (Monograph 102). Environ Res. (2018) 167:673–83. doi: 10.1016/j.envres.2018.06.043

PubMed Abstract | CrossRef Full Text | Google Scholar

9. Hardell L, Carlberg M. Mobile phone and cordless phone use and the risk for glioma – analysis of pooled case-control studies in Sweden, 1997-2003 and 2007-2009. Pathophysiology. (2015) 22:1–13. doi: 10.1016/j.pathophys.2014.10.001

PubMed Abstract | CrossRef Full Text | Google Scholar

10. Hardell L, Carlberg M, Söderqvist F, Kjell HM. Pooled analysis of case-control studies on acoustic neuroma diagnosed 1997-2003 and 2007-2009 and use of mobile and cordless phones. Int J Oncol. (2013) 43:1036–44. doi: 10.3892/ijo.2013.2025

PubMed Abstract | CrossRef Full Text | Google Scholar

11. Hardell L, Carlberg M, Gee D. Chapter 21: Mobile phone use and brain tumour risk: early warnings, early actions? In: Late Lessons From Early Warnings, Part 2. European Environment Agency, Copenhagen. Denmark (2013). Available online at: https://www.eea.europa.eu/publications/late-lessons-2/late-lessons-chapters/late-lessons-ii-chapter-21/view (accessed August 25, 2018)

Google Scholar

12. Karipidis K, Elwood M, Benke G, Sanagou M, Tjong L, Croft RJ. Mobile phone use and incidence of brain tumour histological types, grading or anatomical location: a population-based ecological study. BMJ Open. (2018) 8:e024489. doi: 10.1136/bmjopen-2018-024489

CrossRef Full Text | Google Scholar

13. Nilsson J, Järås J, Henriksson R, Holgersson G, Bergström S, Estenberg J. No evidence for increased brain tumour incidence in the Swedish national cancer register between years 1980-2012. Anticancer Res. (2019) 39:791–6. doi: 10.21873/anticanres.13176

PubMed Abstract | CrossRef Full Text | Google Scholar

14. Gittleman HR, Ostrom QT, Rouse CD, Dowling JA, de Blank PM, Kruchko CA, et al. Trends in central nervous system tumor incidence relative to other common cancers in adults, adolescents, and children in the United States, 2000 to 2010. Cancer. (2015) 121:102–12. doi: 10.1002/cncr.29015

PubMed Abstract | CrossRef Full Text | Google Scholar

15. Ostrom QT, Gittleman H, de Blank PM, Finlay JL, Gurney JG, McKean-Cowdin R, et al. Adolescent and young adult primary brain and central nervous system tumors diagnosed in the United States in 2008-2012. Neuro-Oncology. (2016) 18 (suppl. 1):1–50. doi: 10.1093/neuonc/nov297

PubMed Abstract | CrossRef Full Text | Google Scholar

16. Philips A, Henshaw DL, Lamburn G, O’Carroll MJ. Brain tumours: rise in glioblastoma multiforme incidence in England 1995–2015 suggests an adverse environmental or lifestyle factor. J Public Health Environ. (2018) 2018:7910754. doi: 10.1155/2018/2170208

CrossRef Full Text | Google Scholar

17. Central Brain Tumor Registry of the United States. Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States. Annual Reports. 2007–2017. (2017)

Google Scholar

18. Ostrom QT, Gittleman H, Truitt G, Boscia A, Kruchko C, Barnholtz-Sloan JS. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2011–2015. Neuro-Oncology. (2018) 20:1–86. doi: 10.1093/neuonc/noy131

PubMed Abstract | CrossRef Full Text | Google Scholar

19. Röösli M, Lagorio S, Schoemaker MJ, Schüz J, Feychting M. Brain and salivary gland tumors and mobile phone use: evaluating the evidence from various epidemiological study designs. Annu Rev Public Health. (2019) 40:221–38. doi: 10.1146/annurev-publhealth-040218-044037

PubMed Abstract | CrossRef Full Text | Google Scholar

20. Söderqvist F, Carlberg M, Hardell L. Review of four publications on the Danish cohort study on mobile phone subscribers and risk of brain tumours. Rev Environ Health. (2012) 27:51–8. doi: 10.1515/reveh-2012-0004

CrossRef Full Text | Google Scholar

21. Vrijheid M, Deltour I, Krewski D, Sanchez M, Cardis E. The effects of recall errors and of selection bias in epidemiologic studies of mobile phone use and cancer risk. J Expo Sci Environ Epidemiol. (2006) 16:371–84. doi: 10.1038/sj.jes.7500509

PubMed Abstract | CrossRef Full Text | Google Scholar

22. Goedhart G, van Wel L, Langer CE, de Llobet Viladoms P, Wiart J, Hours M, et al. Recall of mobile phone usage and laterality in young people: the multinational Mobi-Expo study. Environ Res. (2018) 165:150–7. doi: 10.1016/j.envres.2018.04.018

PubMed Abstract | CrossRef Full Text | Google Scholar

23. Brzozek C, Benke KK, Zeleke BM, Abramson MJ, Benke G. Radiofrequency electromagnetic radiation and memory performance: sources of uncertainty in epidemiological cohort studies. Int J Environ Res Public Health. (2018) 15:E592. doi: 10.3390/ijerph15040592

PubMed Abstract | CrossRef Full Text | Google Scholar

24. Carlberg M, Hardell L. Decreased survival of glioma patients with astrocytoma grade IV (glioblastoma multiforme) associated with long-term use of mobile and cordless phones. Int J Environ Res Public Health. (2014) 11:10790–805. doi: 10.3390/ijerph111010790

PubMed Abstract | CrossRef Full Text | Google Scholar

25. Olsson A, Bouaoun L, Auvinen A, Feychting M, Johansen C, Mathiesen T, et al. Survival of glioma patients in relation to mobile phone use in Denmark, Finland and Sweden. J Neurooncol. (2019) 141:139–49. doi: 10.1007/s11060-018-03019-5

PubMed Abstract | CrossRef Full Text | Google Scholar

26. National Toxicology Program. NTP Technical Report on the Toxicology and Carcinogenesis Studies in Hsd:Sprague-Dawley SD Rats Exposed to Whole-Body Radio Frequency Radiation at a Frequency (900 MHz) and Modulations (GSM and CDMA) Used by Cell Phones. NTP TR 595. (2018). Available online at: https://ntp.niehs.nih.gov/ntp/about_ntp/trpanel/2018/march/tr595peerdraft.pdf (accessed August 25, 2018).

Google Scholar

27. National Toxicology Program. NTP Technical Report on the Toxicology and Carcinogenesis Studies in B6C3F1/N Mice Exposed to Whole-Body Radio Frequency Radiation at a Frequency (1800 MHz) and Modulations (GSM and CDMA) Used by Cell Phones. NTP TR 596. (2018). Available online at: https://ntp.niehs.nih.gov/ntp/about_ntp/trpanel/2018/march/tr596peerdraft.pdf (accessed August 25, 2018).

Google Scholar

28. ICNIRP. ICNIRP Note on Recent Animal Carcinogenesis Studies. Munich (2018). Available online at: https://www.icnirp.org/cms/upload/publications/ICNIRPnote2018.pdf (accessed September 29, 2018).

Google Scholar

29. Melnick RL. Commentary on the utility of the National Toxicology Program study on cellphone radiofrequency radiation data for assessing human health risks despite unfounded criticisms aimed at minimizing the findings of adverse health effects. Environ Res. (2019) 168:1–6. doi: 10.1016/j.envres.2018.09.010

CrossRef Full Text | Google Scholar

30. Falcioni L, Bua L, Tibaldi E, Lauriola M, De Angelis L, Gnudi F, et al. Report of final results regarding brain and heart tumors in Sprague-Dawley rats exposed from prenatal life until natural death to mobile phone radiofrequency field representative of a 1.8 GHz GSM base station environmental emission. Environ Res. (2018) 165:496–503. doi: 10.1016/j.envres.2018.01.037

CrossRef Full Text | Google Scholar

31. Lerchl A, Klose M, Grote K, Wilhelm AF, Spathmann O, Fiedler T, et al. Tumor promotion by exposure to radiofrequency electromagnetic fields below exposure limits for humans. Biochem Biophys Res Commun. (2015) 459:585–90. doi: 10.1016/j.bbrc.2015.02.151

PubMed Abstract | CrossRef Full Text | Google Scholar

32. Soffritti M, Giuliani L. The carcinogenic potential of non-ionizing radiations: the cases of S-50 Hz MF, and 1.8 GHz GSM radiofrequency radiation. Basic Clin Pharmacol Toxicol. (2019). doi: 10.1111/bcpt.13215

PubMed Abstract | CrossRef Full Text | Google Scholar

33. West JG, Kapoor NS, Liao SY, Chen JW, Bailey L, Nagourney RA. Multifocal breast cancer in young women with prolonged contact between their breasts and their cellular phones. Case Rep Med. (2013) 2013:354682. doi: 10.1155/2013/354682

PubMed Abstract | CrossRef Full Text | Google Scholar

34. Akdag M, Dasdag S, Canturk F, Akdag MZ. Exposure to non-ionizing electromagnetic fields emitted from mobile phones induced DNA damage in human ear canal hair follicle cells. Electromagn Biol Med. (2018) 37:66–75. doi: 10.1080/15368378.2018.1463246

PubMed Abstract | CrossRef Full Text | Google Scholar

35. Vijayalaxmi, Prihoda TJ. Comprehensive review of quality of publications and meta-analysis of genetic damage in mammalian cells exposed to non-ionizing radiofrequency fields. Radiat Res. (2019) 191:20–30. doi: 10.1667/RR15117.1

PubMed Abstract | CrossRef Full Text | Google Scholar

36. Corvi R, Madia F. In vitro genotoxicity testing–can the performance be enhanced? Food Chem Toxicol. (2017) 106:600–8. doi: 10.1016/j.fct.2016.08.024

PubMed Abstract | CrossRef Full Text | Google Scholar

37. Huss A, Egger M, Hug K, Huwiler-Müntener K, Röösli M. Source of funding and results of studies of health effects of mobile phone use: systematic review of experimental studies. Environ Health Perspect. (2007) 115:1–4. doi: 10.1289/ehp.9149

PubMed Abstract | CrossRef Full Text | Google Scholar

38. Redmayne M, Smith E, Abramson MJ. The relationship between adolescents’ well-being and their wireless phone use: a cross-sectional study. Environ Health. (2013) 12:90. doi: 10.1186/1476-069X-12-90

PubMed Abstract | CrossRef Full Text | Google Scholar

39. Fernández C, de Salles AA, Sears ME, Morris RD, Davis DL. Absorption of wireless radiation in the child versus adult brain and eye from cell phone conversation or virtual reality. Environ Res. (2018) 167:694–9. doi: 10.1016/j.envres.2018.05.013

CrossRef Full Text | Google Scholar

40. De-Sola Gutiérrez J, Rodríguez de Fonseca F, Rubio G. Cell-phone addiction: a review. Front Psychiatry. (2016) 7:175. doi: 10.3389/fpsyt.2016.00175

CrossRef Full Text | Google Scholar

41. Divan HA, Kheifets L, Obel C, Olsen J. Prenatal and postnatal exposure to cell phone use and behavioral problems in children. Epidemiology. (2008) 19:523–9. doi: 10.1097/EDE.0b013e318175dd47

PubMed Abstract | CrossRef Full Text | Google Scholar

42. Sudan M, Olsen J, Arah OA, Obel C, Kheifets L. Prospective cohort analysis of cellphone use and emotional and behavioural difficulties in children. J Epidemiol Community Health. (2016) 70:1207–13. doi: 10.1136/jech-2016-207419

PubMed Abstract | CrossRef Full Text | Google Scholar

43. Walsh JJ, Barnes JD, Cameron JD, Goldfield GS, Chaput JP, Gunnell KE, et al. Associations between 24 hour movement behaviours and global cognition in US children: a cross-sectional observational study. Lancet Child Adolesc Health. (2018) 2:783–91. doi: 10.1016/S2352-4642(18)30278-5

PubMed Abstract | CrossRef Full Text | Google Scholar

44. Foerster M, Thielens A, Joseph W, Eeftens M, Röösli M. A prospective cohort study of adolescents’ memory performance and individual brain dose of microwave radiation from wireless communication. Environ Health Perspect. (2018) 126:077007. doi: 10.1289/EHP2427

PubMed Abstract | CrossRef Full Text | Google Scholar

45. Sage C, Burgio E. Electromagnetic fields, pulsed radiofrequency radiation, and epigenetics: how wireless technologies may affect childhood development. Child Dev. (2018) 89:129–36. doi: 10.1111/cdev.12824

PubMed Abstract | CrossRef Full Text | Google Scholar

46. Choi KH, Ha M, Ha EH, Park H, Kim Y, Hong YC, et al. Neurodevelopment for the first three years following prenatal mobile phone use, radio frequency radiation and lead exposure. Environ Res. (2017) 156:810–17. doi: 10.1016/j.envres.2017.04.029

PubMed Abstract | CrossRef Full Text | Google Scholar

47. Byun YH, Ha M, Kwon HJ, Hong YC, Leem JH, Sakong J, et al. Mobile phone use, blood lead levels, and attention deficit hyperactivity symptoms in children: a longitudinal study. PLoS ONE. (2013) 8:e59742. doi: 10.1371/journal.pone.0059742

PubMed Abstract | CrossRef Full Text | Google Scholar

48. Meo SA, Almahmoud M, Alsultan Q, Alotaibi N, Alnajashi I, Hajjar WM. Mobile phone base station tower settings adjacent to school buildings: impact on students’ cognitive health. Am J Mens Health. (2018) 13:1557988318816914. doi: 10.1177/1557988318816914

PubMed Abstract | CrossRef Full Text | Google Scholar

49. Pall ML. Microwave frequency electromagnetic fields (EMFs) produce widespread neuropsychiatric effects including depression. J Chem Neuroanat. (2016) 75:43–51. doi: 10.1016/j.jchemneu.2015.08.001

PubMed Abstract | CrossRef Full Text | Google Scholar

50. Deniz OG, Suleyman K, Mustafa BS, Terzi M, Altun G, Yurt KK, et al. Effects of short and long term electromagnetic fields exposure on the human hippocampus. J Microsc Ultrastruct. (2017) 5:191–7. doi: 10.1016/j.jmau.2017.07.001

PubMed Abstract | CrossRef Full Text | Google Scholar

51. Eghlidospour M, Amir G, Seyyed MJM, Hassan A. Effects of radiofrequency exposure emitted from a GSM mobile phone on proliferation, differentiation, and apoptosis of neural stem cells. Anatomy Cell Biol. (2017) 50:115–23. doi: 10.5115/acb.2017.50.2.115

PubMed Abstract | CrossRef Full Text | Google Scholar

52. Aldad TS, Gan G, Gao XB, Taylor HS. Fetal radiofrequency radiation exposure from 800-1900 Mhz-Rated cellular telephones affects neurodevelopment and behavior in mice. Sci Rep. (2012) 2:312. doi: 10.1038/srep00312

PubMed Abstract | CrossRef Full Text | Google Scholar

53. Huber R, Treyer V, Borbély AA, Schuderer J, Gottselig JM, Landolt HP, et al. Electromagnetic fields, such as those from mobile phones, alter regional cerebral blood flow and sleep and waking EEG. J Sleep Res. (2002) 11:289–95. doi: 10.1046/j.1365-2869.2002.00314.x

PubMed Abstract | CrossRef Full Text | Google Scholar

54. Huber R, Treyer V, Schuderer J, Berthold T, Buck A, Kuster N, et al. Exposure to pulse-modulated radio frequency electromagnetic fields affects regional cerebral blood flow. Eur J Neurosci. (2005) 21:1000–6. doi: 10.1111/j.1460-9568.2005.03929.x

PubMed Abstract | CrossRef Full Text | Google Scholar

55. Volkow ND, Tomasi D, Wang GJ, Vaska P, Fowler JS, Telang F, et al. Effects of cell phone radiofrequency signal exposure on brain glucose metabolism. JAMA. (2011) 305:808–13. doi: 10.1001/jama.2011.186

PubMed Abstract | CrossRef Full Text | Google Scholar

56. Kostoff RN, Lau CGY. Combined biological and health effects of electromagnetic fields and other agents in the published literature. Technol Forecast Soc Change. (2013) 80:1331–49. doi: 10.1016/j.techfore.2012.12.006

CrossRef Full Text | Google Scholar

57. Adams JA, Galloway TS, Mondal D, Esteves SC, Mathews F. Effect of mobile telephones on sperm 421 quality: a systematic review and meta-analysis. Environ Int. (2014) 70:106–12. doi: 10.1016/j.envint.2014.04.015

CrossRef Full Text | Google Scholar

58. Houston BJ, Nixon B, King BV, De Iuliis GN, Aitken RJ. The effects of radiofrequency electromagnetic radiation on sperm function. Reproduction. (2016) 152:R263–76. doi: 10.1530/REP-16-0126

PubMed Abstract | CrossRef Full Text | Google Scholar

59. Kesari KK, Agarwal A, Henkel R. Radiations and male fertility. Reprod Biol Endocrinol. (2018) 16:118. doi: 10.1186/s12958-018-0431-1

PubMed Abstract | CrossRef Full Text | Google Scholar

60. Rago R, Salacone P, Caponecchia L, Sebastianelli A, Marcucci I, Calogero AE, et al. The semen quality of the mobile phone users. J Endocrinol Invest. (2013) 36:970–4. doi: 10.3275/8996

PubMed Abstract | CrossRef Full Text | Google Scholar

61. Zhang G, Yan H, Chen Q, Liu K, Ling X, Sun L, et al. Effects of cell phone use on semen parameters: results from the MARHCS cohort study in Chongqing, China. Environ Int. (2016) 91:116–21. doi: 10.1016/j.envint.2016.02.028

PubMed Abstract | CrossRef Full Text | Google Scholar

62. Gautam R, Singh KV, Nirala J, Murmu NN, Meena R, Rajamani P. Oxidative stress-mediated alterations on sperm parameters in male Wistar rats exposed to 3G mobile phone radiation. Andrologia. (2019) 51:e13201. doi: 10.1111/and.13201

PubMed Abstract | CrossRef Full Text | Google Scholar

63. BioInitiative Working Group. A Rationale for Biologically-Based Exposure Standards for Low-Intensity Electromagnetic Radiation. BioInitiative. (2012) Available online at: https://www.bioinitiative.org/ (accessed August 25, 2018).

Google Scholar

64. Belyaev I. Dependence of non–thermal biological effects of microwaves on physical and biological variables: implications for reproducibility and safety standards. In: Giuliani L, Soffritti M, Editors. Non–Thermal Effects and Mechanisms of Interaction Between Electromagnetic Fields and Living Matter, Vol. 5. Bologna: Ramazzini Institute (2010). p. 187–218.

Google Scholar

65. Barnes F, Greenebaum B. Some effects of weak magnetic fields on biological systems: RF fields can change radical concentrations and cancer cell growth rates. In: IEEE Power Electronics Magazine 3, (March) (2016). p. 60–8.

Google Scholar

66. Panagopoulos DJ, Johansson O, Carlo GL. Evaluation of specific absorption rate as a dosimetric quantity for electromagnetic fields bioeffects. PLoS ONE. (2013) 8:e62663. doi: 10.1371/journal.pone.0062663

PubMed Abstract | CrossRef Full Text | Google Scholar

67. Ying L, Héroux P. Extra-low-frequency magnetic fields alter cancer cells through metabolic restriction. Electromagn Biol Med. (2013) 33:264–75. doi: 10.3109/15368378.2013.817334

CrossRef Full Text | Google Scholar

68. Belyaev I, Dean A, Eger H, Hubmann G, Jandrisovits R, Kern M, et al. EUROPAEM EMF guideline 2016 for the prevention, diagnosis and treatment of EMF-related health problems and illnesses. Rev Environ Health. (2016) 31:363–97. doi: 10.1515/reveh-2016-0011

PubMed Abstract | CrossRef Full Text | Google Scholar

69. Heuser G, Heuser SA. Functional brain MRI in patients complaining of electrohypersensitivity after long term exposure to electromagnetic fields. Rev Environ Health. (2017) 32:291–9. doi: 10.1515/reveh-2017-0014

CrossRef Full Text | Google Scholar

70. Belpomme D, Hardell L, Belyaev I, Burgio E, Carpenter DO. Thermal and non-thermal health effects of low intensity non-ionizing radiation: an international perspective. Environ Pollut. (2018) 242:643–58. doi: 10.1016/j.envpol.2018.07.019

PubMed Abstract | CrossRef Full Text | Google Scholar

71. Anonymous. LTE Achieves 39% Market Share Worldwide. (2018). Available online at: http://www.microwavejournal.com/articles/30603-lte-achieves (accessed September 29, 2018).

Google Scholar

72. Rappaport TS, Sun S, Mayzus R, Zhao H, Azar Y, Wang K, et al. Millimeter wave mobile communications for 5G cellular: it will work! IEEE Access. (2013) 1:335–49. doi: 10.1109/ACCESS.2013.2260813

CrossRef Full Text | Google Scholar

73. Beltzalel N, Ben Ishai P, Feldman Y. The human skin as a sub-THz receiver – Does 5G pose a danger to it or not? Environ Res. (2018) 163:208–16. doi: 10.1016/j.envres.2018.01.032

CrossRef Full Text | Google Scholar

74. Russell CL. 5G wireless telecommunications expansion: public health and environmental implications. Environ Res. (2018) 165:484–95. doi: 10.1016/j.envres.2018.01.016

CrossRef Full Text | Google Scholar

75. Federal Communication Commission. Radio Frequency Safety 13-39 Section 112. 37. First Report and Order March 29, 2013 (2013). Available online at: https://apps.fcc.gov/edocs_public/attachmatch/FCC-13-39A1.pdf (accessed August 25, 2018).

Google Scholar

76. Alster N. Captured Agency: How the Federal Communications Commission Is Dominated by the Industries It Presumably Regulates. Cambridge, MA: Edmond J. Safra Center for Ethics Harvard University (2015).

Google Scholar

77. Institute of Electrical and Electronic Engineers. (IEEE)IEEE c95.1 IEEE Standard for Safety Levels with respect to Human Exposure to Radio Frequency Electromagnetic Fields, 3 kHZ to 300 GHz. (1991) Available online at: https://ieeexplore.ieee.org/document/1626482/(accessed August 25, 2018).

Google Scholar

78. Environmental Health Trust. Database of Worldwide Policies on Cell Phones, Wireless and Health (2018) Available online at: https://ehtrust.org/policy/international-policy-actions-on-wireless/ (accessed August 25, 2018).

Google Scholar

79. Leach V, Weller S, Redmayne M. Database of bio-effects from non-ionizing radiation. A novel database of bio-effects from non-ionizing radiation. Rev Environ Health. (2018) 33:273–80. doi: 10.1515/reveh-2018-0017

PubMed Abstract | CrossRef Full Text | Google Scholar

80. EMF Portal of the RWTH Aachen University. (2018). Available online at: https://www.emf-portal.org/en (accessed October 10, 2018).

Google Scholar

81. CDPH. CDPH Issues Guidelines on How to Reduce Exposure to Radio Frequency Energy from Cell Phones. (2017) Available online at: https://www.cdph.ca.gov/Programs/OPA/Pages/NR17-086.aspx (accessed August 25, 2018).

Google Scholar

82. Connecticut Department of Public Health. Cell Phones: Questions and Answers about Safety. (2017) Available online at: https://portal.ct.gov/-/media/Departments-and-Agencies/DPH/dph/environmental_health/eoha/Toxicology_Risk_Assessment/050815CellPhonesFINALpdf.pdf?la=en (accessed August 25, 2018).

Google Scholar

83. Massachusetts, United States of America. Legislative Update on Bills on Wireless and Health. (2017) Available onlilne at: https://ehtrust.org/massachusetts-2017-bills-wireless-health/ (accessed August 25, 2018).

Google Scholar

84. Worcester School Committee Precautionary Option on Radiofrequency Exposure. (2017). Available online at: http://wpsweb.com/sites/default/files/www/school_safety/radio_frequency.pdf (accessed August 25, 2018).

Google Scholar

85. Samuel H. The Telegraph. France to Impose Total Ban on Mobile Phones in Schools. (2018). Available online at: https://www.telegraph.co.uk/news/2017/12/11/france-impose-total-ban-mobile-phones-schools/ (accessed August 25, 2018).

Google Scholar

86. Moskowitz JM. Berkeley Cell Phone “Right to Know” Ordinance. (2014). Available online at: https://ehtrust.org/policy/the-berkeley-cell-phone-right-to-know-ordinance and Available online at: https://www.saferemr.com/2014/11/berkeley-cell-phone-right-to-know.html (accessed September 29, 2018).

Google Scholar

Annex: Examples of Actions for Reducing RFR Exposure

1. Focus actions for reducing exposure to RFR on pregnant women, infants, children and adolescents, as well as males who might wish to become fathers.

2. Reduce, as much as possible, the extent to which infants and young children are exposed to RFR from Wi-Fi-enabled devices such as baby monitors, wearable devices, cell phones, tablets, etc.

3. Avoid placing cell towers and small cell antennae close to schools and homes pending further research and revision of the existing exposure limits. In schools, homes and the workplace, cable or optical fiber connections to the Internet are preferred. Wi-Fi routers in schools and daycares/kindergartens should be strongly discouraged and programs instituted to provide Internet access via cable or fiber.

4. Ensure that WTDs minimize radiation by transmitting only when necessary, and as infrequently as is feasible. Examples include transmitting only in response to a signal (e.g., accessing a router or querying a device, a cordless phone handset being turned on, or voice or motion activation). Prominent, visible power switches are needed to ensure that WTDs can be easily turned on only when needed, and off when not required (e.g., Wi-Fi when sleeping).

5. Lower permitted power densities in close proximity to fixed-site antennae, from “occupational” limits to exposure limits for the general public.

6. Update current exposure limits to be protective against the non-thermal effects of RFR. Such action should be taken by all heath ministries and public health agencies, as well as industry regulatory bodies. Exposure limits should be based on measurements of RFR levels related to biological effects (2).

7. Ensure that advisories relating to cell phone use are placed in such a way that purchasers can find them easily, similar to the Berkeley Cell Phone “Right to Know” Ordinance (86).

8. Advise the public that texting and speaker mode are preferable to holding cell phones to the ear. Alternatively, use hands-free accessories for cell phones, including air tube headsets that interrupt the transmission of RFR.

9. When possible, keep cell phones away from the body (e.g., on a nearby desk, in a purse or bag, or on a mounted hands-free accessory in motor vehicles).

10. Delay the widespread implementation of 5G (and any other new technology) until studies can be conducted to assess safety. This includes a wide range of household and community-wide infrastructure WTDs and self-driving vehicles, as well as the building of 5G minicells.

11. Fiber-optic connections for the Internet should be made available to every home, office, school, warehouse and factory, when and where possible.

Glossary

www.frontiersin.org

Keywords: brain cancer, electromagnetic hypersensitivity, glioma, non-cancer outcomes, policy recommendations, radiofrequency fields, child development, acoustic neuroma

Citation: Miller AB, Sears ME, Morgan LL, Davis DL, Hardell L, Oremus M and Soskolne CL (2019) Risks to Health and Well-Being From Radio-Frequency Radiation Emitted by Cell Phones and Other Wireless Devices. Front. Public Health 7:223. doi: 10.3389/fpubh.2019.00223

Received: 10 April 2019; Accepted: 25 July 2019;
Published: 13 August 2019.

Edited by:Dariusz Leszczynski, University of Helsinki, Finland

Reviewed by:Lorenzo Manti, University of Naples Federico II, Italy
Sareesh Naduvil Narayanan, Ras al-Khaimah Medical and Health Sciences University, United Arab Emirates

Copyright © 2019 Miller, Sears, Morgan, Davis, Hardell, Oremus and Soskolne. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Anthony B. Miller, ab.miller@utoronto.ca

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https://www.frontiersin.org/articles/10.3389/fpubh.2019.00223/full

MA: Pittsfield health official says city lacks ‘expertise’ to probe cell tower Health complaints

Pittsfield health official says city lacks ‘expertise’ to probe cell tower complaints

Ruling goes against Pittsfield cell tower neighbors, but fight might continue (copy)
An aerial view of the 115-foot monopole that Verizon Wireless erected in a south Pittsfield neighborhood in 2020. The city’s health director says her department does not have the expertise to evaluate neighborhood complaints of health impacts from the tower.EAGLE FILE PHOTO

PITTSFIELD — The city’s director of public health said her department is ill-equipped to fulfill the City Council’s request to investigate reports from neighbors who believe that cellular radiation emitted from the tower off South Street is causing health problems.

Director Gina Armstrong responded to the council’s investigation request in a brief letter for its Tuesday meeting, writing that the city’s Board of Health might consider making a referral to the state Department of Public Health, since the Pittsfield Health Department isn’t qualified to weigh in.

“The Health Department is not qualified and does not have the expertise to accurately assess the residents’ health concerns, nor is the Health Department qualified to assess the causes of the residents’ health concerns,” Armstrong said.

Experts told CNET that more research on the wavelengths used by 5G, or fifth-generation, cellular technology would be helpful, but that nothing to date suggests that people should be concerned. The World Health Organization says “no adverse health effect has been causally linked” to 5G or any other cellular frequency, but it supports additional research “into the possible long-term health impacts of all aspects of mobile-telecommunications.”

Ruling goes against Pittsfield cell tower neighbors, but fight might continue

Ruling goes against Pittsfield cell tower neighbors, but fight might continue

PITTSFIELD — The tower stands. For now. An effort by Pittsfield neighbors to subject a new cell tower to a fresh municipal review came up short in Berkshire Superior Court. But, plaintiffs …

Some neighbors of the tower, located at the back of 877 South St., have voiced concerns about the 115-foot Verizon Wireless cell tower at multiple council meetings and in the courts. One of them is Courtney Gilardi of Alma Street, who says her daughter started experiencing headaches, dizziness and nausea in August, and later learned that her symptoms started the day that the tower went into service. According to Gilardi, her daughter wasn’t the only neighbor who reported “having a sudden onset of symptoms since the activation of the cell tower.”

Armstrong’s letter was “disappointing,” given neighbors’ hopes “that we could work together with the city to be able to get some answers, and get some relief,” Gilardi said. She said she is considering running to succeed Ward 4 Councilor Chris Connell, who is not seeking reelection. She said the city largely has been unresponsive to neighbors’ concerns about the tower, an experience that, she said, “has everything to do with” her interest in running for the council.

In January, the City Council voted unanimously to request that the Health Department investigate “health concerns that have been reported by some of the residents that live near the cell tower … since its activation and report back” findings and remedies. Armstrong, whose letter comes in response to the petition, didn’t respond to requests for comment Monday.

Connell filed the petition with Ward 5 Councilor Patrick Kavey, and said the Health Department should document the residents’ reports, at bottom, and hire an expert to guide a review if needed. Connell said the “city’s just trying to wash their hands of the whole situation, and I think it’s deplorable.”

Kavey noted that Pittsfield and other communities generally have limited authority over decisions about telecommunications, as regulated by the Federal Communications Commission. He said it’s unclear to him whether cellular radiation from the tower could be related to the neighbors’ reported health issues, and a Health Department review would have helped clarify the issue.

“If our Health Department is unable to look into the health concerns of our residents, then who is?” he said. “The bottom line is, we have been hearing about these health concerns for the last seven, eight months, and no one has looked into them.”

Amanda Burke can be reached at

aburke@berkshireeagle.com, on Twitter

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Recent advances in the effects of microwave radiation on brains

Military Medical Research logoMilitary Medical Research

Recent advances in the effects of microwave radiation on brains

https://mmrjournal.biomedcentral.com/articles/10.1186/s40779-017-0139-0

Military Medical Research volume 4, Article number: 29 (2017) Cite this article

Abstract

This study concerns the effects of microwave on health because they pervade diverse fields of our lives. The brain has been recognized as one of the organs that is most vulnerable to microwave radiation. Therefore, in this article, we reviewed recent studies that have explored the effects of microwave radiation on the brain, especially the hippocampus, including analyses of epidemiology, morphology, electroencephalograms, learning and memory abilities and the mechanisms underlying brain dysfunction. However, the problem with these studies is that different parameters, such as the frequency, modulation, and power density of the radiation and the irradiation time, were used to evaluate microwave radiation between studies. As a result, the existing data exhibit poor reproducibility and comparability. To determine the specific dose-effect relationship between microwave radiation and its biological effects, more intensive studies must be performed.

Background

Microwaves are electromagnetic waves with frequencies ranging from 300 MHz to 300 GHz. Microwaves are widely used in households, industry, communications, and medical and military buildings, and they provide substantial contributions to the development of human society. However, with its popularization, increasing attention has been paid to its influence on humans. Electromagnetic radiation can be absorbed by organisms, in which it causes a series of physiological and functional changes. Many intricate electrical activities occur in the central nervous system, including learning and memory, which are therefore vulnerable to electromagnetic radiation. Moreover, the popularization of mobile phones has made them the main source of brain exposure to radiation. Therefore, the central nervous system is considered one of the most sensitive organs that is targeted by microwave radiation [12]. A large number of studies have shown that microwave radiation can cause a series of adverse reactions in the central nervous system, including sleep disorders in addition to learning and memory impairments.

Microwaves are widely used in broadcasting, communications and many industrial fields. In broadcasting, the sources of microwaves are mainly FM radio and TV broadcasting antennas, which produce frequencies ranging from 80 to 800 MHz. In communications, the microwaves come from mobile phones and their base stations and microwave links, in addition to cordless phones, terrestrial trunked radios, blue tooth devices, wireless local area networks and many other applications. The frequencies of these devices are listed in Table 1. In industrial fields, exposure is usually occupational, and its sources include the surgical and physiotherapeutic use of diathermy, dielectric heating (i.e., heating and vulcanization applications), microwave ovens, magnetic resonance imaging (MRI) medical diagnostic equipment, radar, military and research microwave systems, electricity-supplying networks, and electricity-distributing and transmitting equipment [3].Table 1 Source and frequency range of microwaveFull size table

Based on this background, in this review, we first summarized the effects of microwave radiation on the central nervous system, including the epidemiology, morphology, electroencephalograms, learning and memory abilities and mechanisms of underlying brain dysfunction from the perspective of synaptic structures and functions, oxidative stress and apoptosis, protein synthesis, genes and individual susceptibility and energy metabolism.

Epidemiology

In 2011, the International Agency for Research on Cancer (IARC) announced that microwave radiation has potentially carcinogenic effects (2B). However, it concurrently also declared that the carcinogenic potential of mobile communications equipment was limited to glioma [4].

Exposure to mobile phones

Of the numerous studies performed to explore the effects of mobile communication devices on humans, only a few have shown that cell phones and brain tumors are statistically correlated. For example, people who have used mobile phones for more than 10 years have a clearly higher risk of brain tumors. Those who are accustomed to using their mobile phone ipsilaterally presented a probability that was twice that of people who don’t [5,6,7]. However, most studies have not supported the conclusion that cell phones cause brain tumors [8,9,10,11,12]. One study reported by the Interphone study group [13] showed that there was no increase in the risk of glioma or meningioma in users of mobile phones. It has been suggested that there is an increased risk of glioma at the highest exposure levels, but biases and errors prevent causal interpretations of these data. Additionally, Larjabaara et al. [14] found that gliomas are not preferentially located in the parts of the brain with the highest exposure. Finally, Hardell et al. [15] assessed the use of mobile and cordless phones in 347 cases of melanoma in the head and neck region and 1184 controls and found no increased risk.

Occupational exposure

Industrial exposure

In long-term epidemiological investigations of large population with occupational exposure, the results have not been consistent. Dasdag et al. [16] investigated workers who worked at a television transmitter station with a frequency ranging between 202 and 209 MHz, 694–701 MHz, 750–757 MHz, or 774–781 MHz and at a medium-wave broadcasting station. Their answers to questionnaires showed that the workers suffered from symptoms including headaches, fatigue, stress and sleeplessness. Most of the workers recovered when they left the source of microwave radiation. In addition, another study showed that significant psychiatric symptoms were observed in people who worked in these areas. In particular, somatization, obsessive compulsivity, paranoid ideation and psychoticism were reported [17].

Military exposure

Standard devices used by military personnel that may pose electromagnetic hazards include radars and missile systems. In a report by the Poland Department of Microwave Safety, occupational exposure to electromagnetic fields was analyzed in the work environment of personnel of 204 devices divided into 5 groups (surface-to-air missile system radars, aircraft and helicopters, communication devices, surveillance and height finder radars, airport radars and radio navigation systems). In 57% of military devices, Polish soldiers work in occupational protection zones. In 35% of cases, soldiers work in intermediate and hazardous zones and in 22%—only in the intermediate zone. In 43% of devices, military personnel are not exposed to an electromagnetic field.

The visual reaction time and short-term memory of healthy male and female workers at a radar site with a frequency range of 2–18 GHz was recorded with a simple blind computer-assisted-visual reaction time test or modified Wechsler Memory Scale test. The results indicated that radar microwave radiation leads to a decreased reaction time and lower short-term memory performance [18]. Among radar workers exposed to 14–18 GHz microwaves, the somatic symposium anxiety and insomnia, social dysfunction and severe depression were caused [19]. Singh et al. [20] divided the radar workers into three sets: control group (n = 68), exposure group I (n = 40, exposed to 8–12 GHz) and exposure group II (n = 58, working with radar at 12.5–18.0 GHz). The three groups were further divided into two groups according to their years of service (up to 10 years and >10 years) to investigate the effect of years of exposure to radar. Melatonin and serotonin levels were estimated, which play important roles in the nervous system. The results demonstrated the ability of electric magnetic field (EMF) to influence plasma melatonin and serotonin concentrations in radar workers. The results were significant for the range from 12.5–18.0 GHz with a service period greater than 10 years. Additionally, people exposed to military microwave sources were more vulnerable to brain tumors. Richter et al. [2122] found a higher incidence of brain cancer in radar technicians and a shortened incubation period (i.e., less than 10 years). Szmigielski [23] collected retrospective data for Polish soldiers over 15 years and showed that the prevalence of brain cancer was higher in each age group.

Effects of microwave radiation on children

Because a child’s nervous system is growing and their head is more vulnerable to radiation energy, studies that have specifically addressed whether the nervous systems of children are more susceptible to electromagnetic radiation have been performed. However, there is little scientific evidence to demonstrate that children are more sensitive to electromagnetic radiation than adults [2425].

Positive effects

With the increasing number of applications that use microwave technology, its negative effects on the human body have attracted attention. However, its beneficial effects should not be ignored [26]. For example, it can shorten reaction times so that people can better cope with danger. Mortazavi et al. [27] found that college students’ visual reaction times were significantly shorter after 10 min of phone-induced microwave radiation. This conclusion is consistent with the results of a previously reported study that showed that short-term exposure to microwave radiation can reduce reaction times and improve cognitive functions, attention and short-term memory capacity [28,29,30,31,32,33,34]. Moreover, the risk of developing Alzheimer’s disease is 30–40% lower in people who use a mobile phone for more than 10 years than in other individuals [35]. The above results indicate a positive biological effect of microwave radiation and present a challenge with regard to how people can benefit from microwave radiation.

Above all, because of biases and variations in investigation methods, no conclusive evidence has been presented that microwaves cause cancer. We should ensure that we avoid excessive exposure to microwave radiation in daily life activities and use mobile phones appropriately despite information about its positive effects. In the population with occupational exposure, proper protective measures should be taken to avoid unnecessary harm. These conclusions are presented in Table 2.Table 2 Epidemiological studies of microwavesFull size table

The influence of microwave radiation on the central nervous system

Negative effects

A popular focus among researchers is the damage that microwave radiation causes in the central nervous system, in which it can impair learning and memory.

The Morris water maze has been widely used in neurobehavioral tests [36]. This classical method is often used to test learning and memory abilities after exposure to microwave radiation. Sareesh et al. [37] exposed male Wistar rats (10–12 weeks old) to a Global System for Mobile Communication (GSM) (900/1800 MHz) mobile phone that was in vibrating mode (i.e., no ring tone). In the treated rats, 50 calls were missed each day for 4 weeks, and the spatial memory abilities of the rats were tested after the experimental period. They found that escape times were substantially decreased when the animals were trained while exposed to the phone. In the probe test, the exposed group could not locate the platform and exhibited a significantly higher mean latency (i.e., 3-fold higher) to reach the target quadrant, and they spent only half the time that the controls spent in the target quadrant. These results indicated that mobile phone exposure affected the acquisition of learned responses in Wistar rats. Wang et al. [38] exposed Wistar rats to a 2.856 GHz pulsed microwave field for 6 min. The fields had an average power density of 0, 5, 10 or 50 mW/cm2. The results showed that at 6 h, 1 d and 3 d after exposure, the groups in which the average power density was 10 mW/cm2 or 50 mW/cm2 displayed significant deficits in spatial learning and memory. Additionally, the number of crossings was significantly lower at 3 d after microwave radiation.

Neutral effects

Researchers have also used the 12-arm maze test on rats to test spatial working ability after exposure to 2.45 GHz pulse microwave radiation. Lai et al. [39] exposed rats to microwaves (500 pps, pulse width = 2 μs, and average whole body-specific absorption rate (SAR) = 0.6 W/kg) for an exposure duration of 45 min, and a significant decline was observed in the rats’ performance, indicating that microwave radiation influenced their working memory. However, these experimental results remain to be supported in repeated experiments [40,41,42]. Cassel et al. [41] exposed rats to 2.45 GHz microwaves (2 μ pulse width, 500 pps, and SAR 0.6 W/kg) for 45 min and found that microwave-induced behavioral alterations measured by Lai had more to do with factors related to performance bias than to spatial working memory. Cosquer et al. [40] also repeated the experiment only and found that radial-arm maze performance in rats remained unchanged. Cobb et al. [42] found similar results. Thus, Cosquer et al. [40] concluded that despite the differences in the conditions used in the experiments, space limitations and whether the wall of the maze was clear did not substantially influence outcomes.

Positive results were obtained in Morris water maze tests that demonstrated that microwaves influenced learning and memory in rats. However, these effects were not observed in radial arm maze tests. One reason for this difference may be that the water maze experiment is driven by aversion, whereas the arm maze experiment is driven by appetite. The former is now recognized worldwide as a method for evaluating learning and memory, while the latter is viewed as more susceptible to other factors. The conclusions are shown in Table 3.Table 3 The influence of microwave radiation on learning and memoryFull size table

The influence of microwave radiation on the morphology of the brain

The central nervous system, especially the hippocampus, is highly sensitive to microwave radiation [4344]. Previous studies have shown that in unexposed control rats, hippocampal neurons are aligned in neat rows in which the edges are clear, nuclei are clear, nucleoli can be observed, and pyramidal cells do not exhibit obvious necrosis. However, in rats treated with long-term exposure to radiation, neurons exhibit edema and are arranged irregularly. Nuclear pyknosis and capillary congestion are also observed.

Regarding the ultra-structure of the hippocampus, symptoms including neuronal atrophy, mitochondrial swelling, crest reduction and a disordered arrangement were observed, the rough endoplasmic reticulum exhibited cystic expansion, the number of synaptic vesicles decreased, and the synaptic cleft was widened (2.45 GHz pulsed microwave field at an average power density of 1 mW/cm2 for 3 h/d for up to 30 days [45] and an average power density of 2.5, 5, or 10 mW/cm2 for 6 min/d for up to 1 month resulted in an average calculated SAR of 1.05, 2.1, and 4.2 W/kg, respectively [46]). The hippocampus plays roles in learning and memory, and the results of these studies suggest that the deficits in learning and memory functions observed after exposure to microwave irradiation might be due to abnormalities induced in hippocampal structures.

The influence of microwave radiation on electroencephalograph (EEG) data

Brain electrical activity originates from the membrane potential of the neuron itself and the fluctuation in membrane potential. The transduction of a nerve impulse and the postsynaptic potential produced by it result in synaptic transmission. EEG data reflect the functional state of the brain by enlarging the autologous weak bioelectricity recorded by the EEG-recording instrument [47]. An abnormal EEG is closely associated with damaged cognitive ability. EEG is often used as a tool to diagnose Alzheimer’s disease [48]. Most studies have suggested that microwave radiation can cause EEG abnormalities in experimental animals and participants, but some negative results have also been reported in studies using low-power microwaves.

Vorobyov et al. [1] used 10 freely moving rats in which carbon electrodes were implanted in the cortex and dorsomedial hypothalamus. Of these, five rats were repeatedly exposed to extremely low-frequency microwaves (915 MHz; pulse width, 20 ms; average power density, 0.3 mW/cm2; repetition frequency, 4.0 Hz; intermittently for 1 min, ‘On’ for 1 min, and ‘Off’ for 10 min; SAR, 0.7 mW/g) and 5 were in the sham group. The authors detected the EEG within the frequency bands of 0.5–30.0 Hz for 5 consecutive days. The results showed that in normal EEGs, the θ (3.2–6.0 Hz) and β2 (17.8–30.5 Hz) waves were mainly concentrated in the cortex, while the α (6.0–17.8 Hz) waves were mainly concentrated in the hypothalamus. After exposure, the levels of β2 waves in the hypothalamus increased more than those in the cortex, leading to a significant reduction in the deviation of the two EGGs. The results indicated that repeated low-level exposure to extremely low frequency microwaves affects brain functioning and provide an additional approach to analyzing the underlying mechanisms.

In a study investigating the influence of low-frequency microwave (450 MHz) radiation on EEG, Hinrikus et al. [49] found that microwave radiation enhanced brain wave energy, decreased brain wave frequency, and increased the amplitude and power of delta frequency bands, indicating a decrease in learning ability [50,51,52,53]. More data are available regarding opinions on potential health effects of exposure to electromagnetic fields [3].

Many recent studies have reported that microwaves exposure affects EEG results [54,55,56,57]. Suhhova et al. [58] exposed volunteers to microwaves at a frequency of 450 MHz for 10 repeated intervals of 1 min of irradiation and 1 min off. The SAR of the two groups were 0.303 W/kg and 0.003 W/kg. A resting eyes-closed electroencephalogram was used to continuously record the results, which showed that there was an increase in the power of the α, β1 and β2 frequency bands in the 0.303 W/kg group and in the β2 frequency bands in the 0.003 W/kg group. Statistically significant changes were detected in the EEG-α bands of six individuals and in the β1 and β2 bands of four subjects in the higher SAR group. In the lower SAR group, the α, β1 and β2 bands were affected in the three subjects. This study also revealed the dose-dependent relationship of the modulated microwave effect: decreasing the SAR 100-fold reduced the associated changes in the EEG by three- to six-fold and decreased the number of affected subjects but did not completely eliminate the effects.

The influence of microwave radiation on postnatal development

Maternal exposure to Wi-Fi radio frequencies led to various adverse neurological effects in the offspring. Othman et al. [59] exposed Wistar albino pregnant rats to a 2.45 GHz Wi-Fi signal for 2 h/d throughout the gestation period and found that the neurodevelopment, cerebral stress equilibrium and cholinesterase activity of the offspring were affected. To investigate the potential combined influence of maternal restraint stress and 2.45 GHz Wi-Fi signal exposure on postnatal development and behavior in the offspring of exposed rats, control, Wi-Fi-exposed, restrained and both Wi-Fi-exposed and restrained groups were established. Each Wi-Fi exposure and restraint occurred for 2 h/d during gestation until parturition. The results showed that gestational Wi-Fi exposure and restraint adversely affected offspring neurodevelopment and behavior in adulthood. The progeny brain oxidative balance and serum biochemistry, such as phosphorus, magnesium, glucose, triglycerides and calcium levels, were disrupted [60].

Zhang et al. [61] found that after pregnant rats were irradiated with 9.417 GHz microwaves, the behavior of their offspring differed, and the outcome was sex-dependent. An increase in anxiety-related behaviors and a decrease in depression-related behavior were observed in both female and male offspring. However, impaired learning and memory were only observed in males. Zhang proposed that the sex-dependent relationship between microwaves and the behavior of offspring may be related to sex hormones, and female rats may be equivalently protected by reducing oxidative stress levels.

Mechanisms underlying learning and memory are damaged by microwave irradiation

Synaptic structures and functions

Synapses are special structures that are involved in the transmission of electrochemical signals between neurons in the central nervous system. Synaptic plasticity is a special function of synapses, which play an important role in learning and memory processes [46], including structural and functional plasticity. After exposure to microwave radiation, during synaptic structural plasticity, presynaptic vesicles accumulate or empty, mitochondria are damaged, postsynaptic membranes are perforated, postsynaptic lengths and postsynaptic density distributions are abnormal, mossy fiber growth is inhibited during learning and memory functions, dendritic filopodial densities and activities are decreased, and there is a significant reduction of the dendritic spine density and dendritic fragment length [62]. Functional plasticity is affected in other ways, including the abnormal release and uptake of brain amino acids such as choline and monoamine neurotransmitters, a decrease in excitatory postsynaptic potential amplitudes and spikes in long-term potentiating (LTP) in the medial perforated pathway (MPP) in the dentate gyrus (DG) [27].

In vitro studies

Ning et al. [63] exposed rat hippocampal neurons to microwaves (SAR values of 0.8 W/kg and 2.4 W/kg at an average power density of 1800 MHz/d) and observed the formation of dendritic filopodial and dendritic branches and the maturation of dendritic spines in neurons from day 6 to 14. Additionally, in the 2.4 W/kg group, neuronal filopodial density and activity were lower on day 8, and there was a reduction of the dendritic spine maturity on day 14. In the group treated with 0.8 W/kg, there was no significant change. Thus, in the early developmental stage, chronic exposure to 2.4 W/kg GSM microwaves may influence dendritic development and the formation of excitatory synapses in cultures of hippocampal neurons. Xu et al. [64] exposed cultured rat hippocampal neurons to GSM 1800 MHz microwaves (SAR, 2.4 W/kg) and observed a selective decrease in the amplitude of α-amino-3-hydroxy-5-methyl-4-soxazole propionic acid (AMPA) miniature excitatory postsynaptic currents (mEPSCs). However, there was no change in the frequency of AMPA mEPSCs or the amplitudes of N-methyl-d-aspartate (NMDA) mEPSCs. Furthermore, the expression of postsynaptic density 95 (PSD-95) in cultured neurons was decreased. Thus, these results suggest that the 2.4 W/kg GSM 1800 MHz microwaves may reduce excitatory synaptic activity and the number of excitatory synapses in cultured rat hippocampal neurons.

In vivo studies

Wang et al. [65] irradiated Wistar rats with 10, 30 and 50 mW/cm2 microwaves, and the results showed that in the cerebral cortex, only glycine (Gly) and asparagine (Asp) levels were increased. Microwaves of 50 mW/cm2 increased the levels of the major excitatory amino acids Asp and glutamic acid (Glu) and the inhibitory amino acids gamma-aminobutyric acid (GABA) and Gly, while 6 h later in the 30 mW/cm2 group, the level of Gly was reduced in the cerebral cortex. However, Li et al. [50] exposed Wistar rats to 2.856 GHz microwaves at an average power density of 5, 10, 20 or 30 mW/cm2 for 6 min three times per week for up to 6 weeks and found that on day 14 after irradiation, the levels of Asp and Glu were lower in the hippocampus in the group treated with 5 mW/cm2 but higher in the group treated with 30 mW/cm2, The levels of GABA were elevated. After 28 days, the levels of Glu and Tau in the hippocampus and cerebrospinal fluid were lower, indicating that the cognitive damage induced by microwave radiation is associated with a decrease in Glu [6667].

Synaptic vesicles form in different parts of neurons and contain high concentrations of substances that are transferred from the neuron. When nerve endings are excited, the vesicles release their contents into the synaptic cleft, resulting in synaptic transmission. The normal function of synaptic vesicles depends on the normal expression of related proteins. Wang et al. [68] radiated Wistar rats with microwaves (30 mW/cm2; SAR value, 14.1 W/kg), and then detected the expression of synaptic vesicle-associated proteins and found that synaptophys in I and VAMP-2, which are synaptic fusion proteins, and synaptic vesicle proteins were abnormally expressed to different degrees. The authors therefore proposed that synaptic conduction disorders are associated with damage to cognitive functions. Qiao et al. [62] irradiated Wistar rats, hippocampal synaptosomes and differentiated PC12 cells using microwaves (average power density, 30 mW/cm2) for 5 min, and the results showed that the post-exposure spatial memory of the rats was significantly decreased, the post-exposure levels of phosphorylated synapsin I (p-synapsin I) and GABA were decreased in the rat and cell experiments, and the post-exposure levels of vesicular GABA transporter and p-synapsin I were increased in small clear synaptic vesicles (which were abnormally assembled in presynaptic terminals) in the rat experiments. Exposure to microwaves and silencing p-synapsin I reduced the release of GABA, and maximum reduction was achieved when both were combined, indicating a synergistic effect. Xu et al. found that long-term treatment with a low dose of microwave radiation reduced the activity and the number of excitatory synapses.

NMDA receptors

Among the variety of neurotransmitters, glutamate is the most abundant endogenous amino acid in the mammalian central nervous system. It influences both learning and memory in rats [67]. In the CNS, glutamic acid binds and plays physiological roles with the following two receptors: ionotropic glutamate and metabolic glutamate. The ionotropic receptors consist of NMDA receptors and non-NMDA receptors.

N-methyl-D-aspartic acid receptor (NMDAR) is a tetramer composed of two NR1 and two NR2 subunits or two NR3 subunits that perform the functions of NMDAR [6970], and NMDAR plays key roles in synapse development, synaptic plasticity and neurological diseases. LTP induction involves a signal transduction cascade that includes the release of glutamate from synaptic vesicles, activation of NMDAR at postsynaptic membranes, entry of Ca2+, and activation of Ca2+/calmodulin-dependent protein kinases (CaM kinases) II, IV and mitogen-activated protein kinase (MAPK) [71]. Xiong et al. [46] found that by excessively activating the NMDA receptor signaling pathway, microwaves undermine hippocampal synaptic plasticity, explaining the damage observed in learning and memory abilities in radiated rats. Wang et al. [72] found that 2.856 GHz, 50 mW/cm2 pulsed microwave radiation caused persistent spatial memory impairments, disordered neurotransmitters, and varying degrees of damage in the hippocampus and synapses. The levels of NMDA receptor subunits were increased 1 month after irradiation. NR2B plays a key role in LTP and was decreased from the 3rd to the 18th month post-treatment, and long-term exposure to high doses of radiation may therefore damage cognitive functions. This effect is similar to the decrease observed in NR2B in rats. It has also been reported that acute exposure to continuous waves of 900 MHz EMF or 900 MHz waves that were modulated to an amplitude of 50 Hz increased reactive oxygen species (ROS) levels and DNA fragmentation as a result of the hyperstimulation of glutamate receptors [73].

Oxidative stress and apoptosis

Oxidative stress refers to an imbalance between oxidants and antioxidants in vivo and is characterized by a biochemical state that tends toward oxidization, including the formation of oxygen free radicals (i.e., ROS) and nitrogen radicals reactive nitrogen species (RNS), which play major roles in oxidation. Numerous mechanisms can activate oxidative stress, including electromagnetic radiation, and thereby cause molecular damage. This damage plays a key role in the structural and functional changes that are accelerated by neuronal degeneration. It has been reported that microwave radiation can induce lipid peroxidation of cell membranes and produce apoptotic signals [7475]. Microwave radiation can induce oxidative and nitrosative stress, which lead to hippocampal neuronal and non-neuronal apoptosis via the oxidative damage of cellular constituents (i.e., nucleic acids, proteins and lipids) and subsequent over expression of p53, which up-regulates Bax and down-regulates pro-caspase-3 and full-length/uncleaved poly-ADP-ribose polymerase (PARP) 1, eventually inducing neuronal degeneration via apoptosis [76]. Chronic microwave exposures were executed with 2.45 GHz of either modulated (power density, 0.029 mW/cm2; specific absorption rate, 0.019 W/kg with a sinusoidal modulation of 400 Hz) or non-modulated continuous sinusoidal wave (power density, 0.033 mW/cm2; specific absorption rate, 0.023 W/kg) for 2 h daily for 1 month. The results suggested that chronic non-modulated, but not modulated, microwave radiation may cause anxiety-like and depression-like behaviors and calcium- and NO-related biochemical changes in the brain [77].

In vitro studies

Shahin found that regardless of whether exposure was long-term or short-term, 2.45 GHz microwaves increased oxidative/nitrosative stress, which potentially led to apoptosis in hippocampal subfield neurons and non-neuronal cells as a result of p53-dependent/−independent activation. Mack et al. [78] exposed differentiated astroglial cells that were cultured for 14 days in vitro to either continuous 900 MHz waves or 900 MHz waves modulated in amplitude at 50 Hz using a sinusoidal wave form and 100% modulation index for 5, 10, or 20 min. The strength of the electric field (rms value) at the sample position was 10 V/m. A significant increase in ROS levels and DNA fragmentation were observed only after the astrocytes were exposed to modulated EMF for 20 min, perhaps as a result of hyperstimulation of glutamate receptors. To investigate the effects of microwaves radiation on apoptotic activity, cell viability, and cell cycle progression, which can provide information about microwaves radiation effects on neural cells over the period from embryonic stages to infants. Human SH-SY5YNB cells were exposed to 2.1 GHz W-CDMA modulated microwave radiation for 24 h at a specific absorption rate of 0.491 W/kg. The results showed that 2.1 GHz W-CDMA-modulated microwave radiation did not cause apoptotic cell death but altered cell cycle progression [79].

In vivo studies

Joubert et al. [80] found that irradiation with 900 MHz, 2 W/kg continuous microwaves for 24 h induced an increase in rat neuronal apoptosis. Motawi et al. [81] reported a study exploring the influence of mobile phone microwave radiation on oxidative stress and apoptosis in rat brains. The experimental rats were divided into six groups of 3 adult rats and 3 young rats in each group (with control, GSM alone and call-receiving subgroups in each group). After irradiation was applied for 2 h/d for 60 d, the authors observed the following: microwave radiation produced by mobile phones damaged the brains of adult and young rats, the damage caused by mobile phones in the calling state was significantly more severe than that observed in the standby group, and the neurons of young rats were more seriously injured than those of adult rats. The direct cause of the observed neuronal damage may have been apoptosis induced by the microwave radiation, and an indirect cause may have been an increase in permeability of the blood-brain barrier (BBB), which would allow the traversal of toxic substances that could cause damage. Dasdag et al. [82] exposed animals to 900 MHz microwave radiation for 2 h/d for 10 months and removed the brain tissues. The final apoptosis score in the exposed group was significantly reduced, and the total antioxidant capacity and catalysis observed in the experimental group was increased. Therefore, the authors concluded that exposure to a radiofrequency of 900 MHz might trigger the neoplastic process because it produces a relative increase in the number of potentially long-lived cells.

Protein synthesis

It is widely accepted that protein synthesis occurs in neuronal dendrites and may be the cellular basis of learning and memory, during which local protein synthesis and synaptic plasticity are closely linked to the efficiency of communication between neurons. The effects of microwave radiation on protein synthesis in brain remain undetermined.

Fragopoulou et al. [83] found that long-term exposure to microwave radiation (typical mobile phone, at an SAR level range of 0.17–0.37 W/kg for 3 h daily for 8 months, or wireless digital enhanced cordless telecommunications/telephone (DECT) base at an SAR level range of 0.012–0.028 W/kg for 8 h/d for 8 months) induced the synthesis of 143 proteins, including some neuronal function-associated proteins such as glial fibrillary acidic protein (GFAP), glial maturation factor (GMF), apolipo protein E, heat-shock protein, cytoskeletal proteins and some proteins that are associated with metabolism in the brain.

Verma et al. [84] and Sharma et al. [85] found that protein levels were reduced in rat brains following microwave radiation, which may have been caused by the excessive consumption or a reduction of the synthesis of proteins, and reduced protein synthesis can be caused by the following processes: (1) excessive activation of RNA enzymes; (2) mRNA consumption or the formation and maturation of RNA enzymes. Microwave radiation can cause tissue damage by inducing localized microstructural damage to proteins [8687]. It has been reported that microwave radiation can decrease both the number and the density of dendritic spines [63]. Dendritic spines, which are small protrusions that extend from dendritic shafts, are also cellular compartments containing signaling molecules that are important for synaptic transmission and plasticity [88,89,90,91]. These spines have been reported to share a close relationship with learning and memory abilities, and when protein synthesis in dendritic spines is blocked, new spine growth and the development of long spines are both decreased [91].

Dasdag et al. [92] found that 900 MHz microwave radiation emitted by mobile phones increased protein carbonyl levels in the brains of rats, suggesting that 900 MHz microwave radiation can alter some biomolecules such as proteins.

In summary, there is evidence that microwave radiation can lead to alterations in protein synthesis or protein modifications; however, the results are controversial. This phenomenon may be explained by the varied radiation dosage adopted in these studies.

Genes and individual susceptibility

miRNAs are non-coding sequences with a length of approximately 22 nucleotides that have roles in cell development and differentiation and are also linked to signal transduction and tumorigenesis. Some studies have proposed that miRNAs play important roles in nerve regeneration, neurodegenerative diseases, and the pathogenesis of neuroblastoma and schizophrenia [93,94,95]. More than 50% of miRNAs are found in cancer-associated regions of the genome or in fragile sites, suggesting that miRNAs also play important roles in the pathogenesis of neoplasias [96]. Dasdag et al. [97] found that long-term exposure to 900 MHz radiation decreased the level of rno-miR107and that the whole body (rms) SAR value was 0.0369 W/kg, bridging the gap in the interaction between radio frequency radiation (FR) and miRNAs. Studies have also suggested that long-term exposure to 2.4 GHz microwave radiation may lead to adverse effects, as observed in neurodegenerative diseases that originate from the altered expression of some miRNAs. The authors found that 2.4 GHz microwave radiation reduced the expression of some miRNAs such as miR-106b-5p and miR-107 [98]. Zhao et al. [99] used a microarray and quantitative real-time PCR to analyze the miRNA expression profile in the hippocampus on days 7 and 14 after irradiation with a microwave at 30 mW/cm2. The authors predicted the differential expression of genes associated with transcription, translation and receptor functions (in addition to brain-related and signaling pathway-related) using the iRDB, miRbase and miRanda databases. They summarized the characteristics and functions of hippocampus-related miRNAs following irradiation with microwaves, and these data laid a foundation that clarified the molecular mechanisms underlying microwave-induced injury to hippocampal learning and memory and suggested potential therapeutic targets. To investigate the effects of 2.4 GHz Wi-Fi radiation on multisensory integration in rats, a cross-modal visual-tactile object recognition (CMOR) task was performed by four variations of the spontaneous object recognition (SOR) test including the standard SOR, tactile SOR, visual SOR, and CMOR tests. The results of this study showed that chronic exposure to Wi-Fi electromagnetic waves might impair both unimodal and cross-modal encoding of information. The increase in M1 receptor gene expression along with the impairment of novel preferences in Wi-Fi-exposed animals may suggest a possible role of the cholinergic system in the detrimental effects of Wi-Fi radiation on multisensory integration [100].

Megha et al. [101] exposed rats to microwave radiation at frequencies of 0, 900, 1800 and 2450 MHz (SARs: 0, 0.59, 0.58 and 0.66 mW/kg, respectively) using a transverse electromagnetic cell for 2 months for 2 h/d, 5 d/week. Subsequently, significantly more DNA damage was observed in the exposed groups than in the sham group, and their study also indicated that oxidative stress and inflammation caused DNA damage in response to low-intensity microwave exposure. To investigate whether exposure of rat brains to GMS microwaves induced DNA breaks and changes in gene expression, Belyaev et al. [102] exposed rats to 9.15 MHz microwaves (SAR: 0.4 mW/g) for 2 h. They found that in the cerebellum of all the exposed animals, 11 genes were up-regulated from 1.34- to 2.74-fold, and one gene was down-regulated 0.48-fold. The induced genes encoded proteins with a variety of functions, including neurotransmitter regulation, BBB maintenance, and melatonin production. The study also showed that exposure to GSM microwaves at 915 MHz did not induce detectable DNA double-strand breaks but affected the expression of genes in rat brain cells.

Merola et al. [103] found that microwave radiation caused DNA single-strand and double-strand breaks in vivo in populations submitted to occupational exposure, and the incidence of micronuclei in lymphocytes was significantly increased. However, other reports have indicated that unlike ionizing radiation, the microwave radiation produced by mobile phones does not possess sufficient energy to directly damage DNA. Most bioassay and genotoxicity or mutation studies that have been performed in vitro have reported that exposure to microwave radiation at non-thermal levels does not have mutagenic/genotoxic/carcinogenic effects. Qutob et al. [104] found that exposure to a 1.9 GHz pulse-modulated RF field for 4 h at 0.1, 1.0, and 10 W/kg did not affect gene expression in U87MG glioblastoma cells.

Starting with a single nucleotide polymorphism (SNP) site, Wang et al. [105] identified stable C-T mutation sites at 217 points by screening for SNPs in the GRIN2B promoter region in rats. After exposure to microwave irradiation (an average power density of 30 mW/m2 for 5 min/d on five days a week for two consecutive months), the expression of NR2B was decreased in rats, the level of Glu was increased in the hippocampus and cerebrospinal fluid, spatial memory ability was decreased among rats with the TT genotype, and there was no change in the CC type and TC type animals. In the cell experiments, the T allele was significantly more vulnerable to microwaves than the C allele with regard to its transcription factor binding ability and the transcriptional activity and mRNA and protein expression of NR2B. These results explain the genetic mechanisms by which microwave radiation induces damage to learning and memory.

Energy metabolism

Glucose is the main energy source and is closely related to brain neurotransmitters and cholesterol synthesis [106]. In addition, glucose is also related to cognitive functions, and reductions in the metabolism and uptake of glucose have been observed in local regions of the brain in Alzheimer’s patients [107108]. Damage to learning abilities and reduction of glucose utilization in the limbic system of adult rats are closely linked [109]. In the rat hippocampus, glucose uptake plays an important role in spatial learning and memory processes. The rats in the study showed increases in spatial memory and glucose transporters, and this phenomenon indicated a corresponding increase in glucose uptake. In contrast, a central injection of a glucose carrier inhibitor induced injury to memories [110]. Kwon et al. [111] found that the rate of glucose metabolism in the brains of rats was lower after short-term exposure to microwave radiation, and the blood glucose management reduced the damage that was caused by microwave radiation due to the decreased glucose uptake (2.45 MHz, 1 mW/cm2, continuous radiation for 30 d at 3 h/d), as were learning and memory capacity. The mechanism by which microwave radiation decreases glucose, resulting in impaired learning and memory in rats, may be related to an increase in the synthesis and release of acetylcholine in the hippocampus. Numerous studies have shown that increased acetylcholine is related to promotion of the effect of glucose on memory [112,113,114]. Concurrently, in the hippocampus, acetylcholine can promote learning and memory [115116]. An increasing level of acetylcholine can increase the concentration of free calcium ions in synapses, but its concentration was decreased by 60% after exposure to microwave irradiation [117]. It has been proposed that by enhancing the functions of acetylcholine, glucose can increase the concentration of free calcium ions in the synapse to reverse microwave-induced damage to learning and memory.

It has been shown that neurons are sensitive to reductions in the availability of adenosine triphosphate (ATP), the main source of energy in mitochondria, which have been reported to be vulnerable to microwave radiation [118]. Microwaves can influence mitochondria by damaging their structure [45], reducing ATP levels and affecting the activity of relevant enzymes such as succinate dehydrogenase (SDH) and cytochrome coxidase (COX) [119,120,121]. The potential mechanisms underlying these damaging effects range from gene expression alterations in the respiratory chain, membrane damage, Ca2+ overloading, and DNA impairment [122,123,124,125,126,127,128].

Summary

It is noteworthy that most of the above mentioned studies were based on the theory that the effects caused by microwaves are non-thermal. However, a recent report [3] published by the Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR) noted that discussions about the thermal and non-thermal effects are misleading. Because the frequency of microwaves is sufficiently high that the energy is absorbed, the subsequent heating of tissue becomes its major mechanism, and most biochemical and physiological responses are temperature-dependent. Thus, the committee suggested that in the future, studies should explore the border between thermal and non-thermal effects and that specific effects, such as triggering the onset of thermoregulatory reactions, should be defined.

Conclusion

With the popularity of microwave technology, microwave effects on the human body have become a common topic of concern, and the central nervous system is recognized as a target organ system that is sensitive to microwave radiation. However, to date, with the exception of high-power microwave radiation, which has widely established hazardous effects, the biological effects of microwaves remain controversial. In epidemiology, there is no conclusive evidence showing that microwaves have carcinogenic effects. Concurrently, the discovery that microwaves have positive biological effects has presented new challenges for research and applications in this field. The results of EEG and analyses of the structure of the brain after radiation have also confirmed the influence of microwaves. Studies have extensively explored the underlying mechanisms by which microwaves influence learning and memory functions, especially synaptic structures and functions, oxidative stress and apoptosis, protein synthesis, genes and individual susceptibility and energy metabolism. Previous studies have produced a large amount of information, and some progress has been made in theory, but the mechanisms have not yet been fully determined, and many points are still disputed. The largest problem in these studies is that they used different parameters, such as the frequency, modulation, power density and irradiation time, to apply microwave radiation, in addition to using a variety of research methods. Therefore, their reproducibility and comparability are poor. To determine the precise dose-effect relationship between microwave radiation and its biological effects, further detailed studies must be performed.

Abbreviations

AMPA:

α-amino-3-hydroxy-5-methyl-4-soxazole propionic acidAsp:

Asparaginic acidATP:

Adenosine triphosphateBBB:

Blood-brain barrierCaM kinases:

Ca2+/calmodulin-dependent protein kinasesCMOR:

Cross-modal visual-tactile object recognitionCOX:

Cytochrome coxidaseCTFs:

Carboxyl-terminal fragmentsDECT:

Digital enhanced cordless telecommunications/telephoneDG:

Dentate gyrusEEG:

ElectroencephalographEMF:

Electric magnetic fieldFR:

Frequency radiationGABA:

Gamma-aminobutyric acidGFAP:

Fibrillary acidic proteinGlu:

Glutamic acidGly:

GlycineGMF:

Glial maturation factorGSM:

Global system for mobile communicationIARC:

International agency for research on cancerLTP:

Long term potentiationMAPK:

Mitogen-activated protein kinaseMEPSCs:

Miniature excitatory postsynaptic currentsMPP:

Medial perforant pathMRI:

Magnetic resonance imagingNMDA:

N-methyl-D-aspartateNMDAR:

N-methyl-D-aspartic acid receptorsPARP:

Poly-ADP-ribose polymerasePSD-95:

Postsynaptic density 95RNS:

Reactive nitrogen speciesROS:

Reactive oxygen speciesSAR:

Specific absorption rateSCENIHR:

Scientific committee on emerging and newly identified health risksSDH:

Succinate dehydrogenaseSNP:

Single nucleotide polymorphismSOR:

Spontaneous object recognition

References

  1. 1.Vorobyov V, Janac B, Pesic V, Prolic Z. Repeated exposure to low-level extremely low frequency-modulated microwaves affects cortex-hypothalamus interplay in freely moving rats: EEG study. Int J Radiat Biol. 2010;86:376–83.CAS PubMed Article Google Scholar 
  2. 2.Eliyahu I, Luria R, Hareuveny R, Margaliot M, Meiran N, Shani G. Effects of radiofrequency radiation emitted by cellular telephones on the cognitive functions of humans. Bioelectromagnetics. 2006;27:119–26.PubMed Article Google Scholar 
  3. 3.Sage C, Carpenter D, Hardell L. Comments on SCENIHR: opinion on potential health effects of exposure to electromagnetic fields. Bioelectromagnetics. 2015;36:480–4.Article Google Scholar 
  4. 4.Szmigielski S. Cancer risks related to low-level RF/MW exposures, including cell phones. Electromagn Biol Med. 2013;32:273–80.PubMed Article Google Scholar 
  5. 5.Kan P, Simonsen SE, Lyon JL, Kestle JR. Cellular phone use and brain tumor: a meta-analysis. J Neuro-Oncol. 2008;86:71–8.Article Google Scholar 
  6. 6.Khurana VG, Teo C, Kundi M, Hardell L, Carlberg M. Cell phones and brain tumors: a review including the long-term epidemiologic data. Surg Neurol. 2009;72:205–14.PubMed Article Google Scholar 
  7. 7.Myung SK, Ju W, McDonnell DD, Lee YJ, Kazinets G, Cheng CT, et al. Mobile phone use and risk of tumors: a meta-analysis. J Clin Oncol. 2009;27:5565–72.PubMed Article Google Scholar 
  8. 8.Johansen C, Boice JD, McLaughlin JK, Olsen JH. Cellular telephones and cancer—a nationwide cohort study in Denmark. J Natl Cancer Inst. 2001;93:203–7.CAS PubMed Article Google Scholar 
  9. 9.Muscat JE, Malkin MG, Thompson S, Shore RE, Stellman SD, McRee D, et al. Handheld cellular telephone use and risk of brain cancer. JAMA. 2000;284:3001–7.CAS PubMed Article Google Scholar 
  10. 10.Lönn S, Ahlbom A, Hall P, Feychting M. Long-term mobile phone use and brain tumor risk. Am J Epidemiol. 2005;161:526–35.PubMed Article Google Scholar 
  11. 11.Frei P, Poulsen AH, Johansen C, Olsen JH, Steding-Jessen M, Schüz J. Use of mobile phones and risk of brain tumours: update of Danish cohort study. BMJ. 2011;343:522–4.
  12. 12.Schüz J, Jacobsen R, Olsen JH, Boice JD, McLaughlin JK, Johansen C. Cellular telephone use and cancer risk: update of a nationwide Danish cohort. J Natl Cancer Inst. 2006;98:1707–13.PubMed Article Google Scholar 
  13. 13.Interphone study group. Brain tumour risk in relation to mobile telephone use: results of the INTERPHONE international case-control study. Int J Epidemiol. 2010;39:675–94.Article Google Scholar 
  14. 14.Larjavaara S, Schüz J, Swerdlow A, Feychting M, Johansen C, Lagorio S, et al. Location of gliomas in relation to mobile telephone use: a case-case and case-specular analysis. Am J Epidemiol. 2011;174:2–11.PubMed Article Google Scholar 
  15. 15.Hardell L, Carlberg M, Mild KH, 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;18:325–33.PubMed Article Google Scholar 
  16. 16.Dasdag S, Balci K, Celik M, Batun S, Kaplan A, Bolaman Z, et al. Neurologic and biochemical findings and CD4/CD8 ratio in people occupationally exposed to RF and microwave. Biotechnol Biotechnol Equip. 1992;6:37–9.Article Google Scholar 
  17. 17.Oto R, Akdaǧ Z, Daşdaǧ S, Celik Y. Evaluation of Psychologic parameters in people occupationally exposed to radiofrequencies and microwave. Biotechnol Biotechnol Equip. 1994;8:71–4.Article Google Scholar 
  18. 18.Mortazavi SMJ, Taeb S, Dehghan N. Alterations of visual reaction time and short term memory in military radar personnel. Iran J Public Health. 2013;42:428.PubMed PubMed Central Google Scholar 
  19. 19.Naser D, Shahram T. Adverse health effects of occupational exposure to radiofrequency radiation in airport surveillance radar operators. Indian J Occup Environ Med. 2013;17:7–11.Article Google Scholar 
  20. 20.Singh S, Mani KV, Kapoor N. Effect of occupational EMF exposure from radar at two different frequency bands on plasma melatonin and serotonin levels. Int J Radiat Biol. 2015;91:426–34.CAS PubMed Article Google Scholar 
  21. 21.Richter ED, Berman T, Ben-Michael E, Laster R, Westin JB. Cancer in radar technicians exposed to radiofrequency/microwave radiation: sentinel episodes. Int J Occup Environ Health. 2000;6:187–93.CAS PubMed Article Google Scholar 
  22. 22.Richter ED, Berman T, Levy O. Brain cancer with induction periods of less than 10 years in young military radar workers. Arch Environ Health. 2002;57:270–2.PubMed Article Google Scholar 
  23. 23.Szmigielski S. Cancer morbidity in subjects occupationally exposed to high frequency (radiofrequency and microwave) electromagnetic radiation. Sci Total Environ. 1996;180:9–17.CAS PubMed Article Google Scholar 
  24. 24.Otto M, von Mühlendahl KE. Electromagnetic fields (EMF): do they play a role in children’s environmental health (CEH)? Int J Hyg Environ Health. 2007;210:635–44.PubMed Article Google Scholar 
  25. 25.Aydin D, Feychting M, Schüz J, Andersen TV, Poulsen AH, Prochazka M, et al. Predictors and overestimation of recalled mobile phone use among children and adolescents. Prog Biophys Mol Biol. 2011;107:356–61.PubMed Article Google Scholar 
  26. 26.Mortazavi S, Tavakkoli-Golpayegani A, Haghani M, Mortazavi S. 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. 2014;12:75.PubMed PubMed Central Article Google Scholar 
  27. 27.Mortazavi S, Rouintan M, Taeb S, Dehghan N, Ghaffarpanah A, Sadeghi Z, et al. Human short-term exposure to electromagnetic fields emitted by mobile phones decreases computer-assisted visual reaction time. Acta Neurol Belg. 2012;112:171–5.CAS PubMed Article Google Scholar 
  28. 28.Koivisto M, Revonsuo A, Krause C, Haarala C, Sillanmäki L, Laine M, et al. Effects of 902 MHz electromagnetic field emitted by cellular telephones on response times in humans. Neuroreport. 2000;11:413–5.CAS PubMed Article Google Scholar 
  29. 29.Preece A, Iwi G, Davies-Smith A, Wesnes K, Butler S, Lim E, et al. Effect of a 915-MHz simulated mobile phone signal on cognitive function in man. Int J Radiat Biol. 1999;75:447–56.
  30. 30.Koivisto M, Krause CM, Revonsuo A, Laine M, Hämäläinen H. The effects of electromagnetic field emitted by GSM phones on working memory. Neuroreport. 2000;11:1641–3.CAS PubMed Article Google Scholar 
  31. 31.Edelstyn N, Oldershaw A. The acute effects of exposure to the electromagnetic field emitted by mobile phones on human attention. Neuroreport. 2002;13:119–21.PubMed Article Google Scholar 
  32. 32.Lee TM, Ho SM, Tsang LY, Yang SY, Li LS, Chan CC. Effect on human attention of exposure to the electromagnetic field emitted by mobile phones. Neuroreport. 2001;12:729–31.CAS PubMed Article Google Scholar 
  33. 33.Smythe JW, Costall B. Mobile phone use facilitates memory in male, but not female, subjects. Neuroreport. 2003;14:243–6.PubMed Article Google Scholar 
  34. 34.Dasdag S, Balci K, Ayyildiz M, Celik M, Tekes S, Kaplan A. Blood biochemical parameters of the radio-link station. Eastern J Med. 1999;4:10–2.Google Scholar 
  35. 35.Schüz J, Waldemar G, Olsen JH, Johansen C. Risks for central nervous system diseases among mobile phone subscribers: a Danish retrospective cohort study. PLoS One. 2009;4:e4389.PubMed PubMed Central Article CAS Google Scholar 
  36. 36.Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods. 1984;11:47–60.CAS PubMed Article Google Scholar 
  37. 37.Narayanan SN, Kumar RS, Potu BK, Nayak S, Mailankot M. Spatial memory perfomance of wistar rats exposed to mobile phone. Clinics. 2009;64:231–4.
  38. 38.Wang H, Peng R, Zhou H, Wang S, Gao Y, Wang L, et al. Impairment of long-term potentiation induction is essential for the disruption of spatial memory after microwave exposure. Int J Radiat Biol. 2013;89:1100–7.CAS PubMed Article Google Scholar 
  39. 39.Lai H, Horita A, Guy AW. Microwave irradiation affects radial-arm maze performance in the rat. Bioelectromagnetics. 1994;15:95–104.CAS PubMed Article Google Scholar 
  40. 40.Cosquer B, Kuster N, Cassel JC. Whole-body exposure to 2.45 GHz electromagnetic fields does not alter 12-arm radial-maze with reduced access to spatial cues in rats. Behav Brain Res. 2005;161:331–4.PubMed Article Google Scholar 
  41. 41.Cassel JC, Cosquer B, Galani R, Kuster N. Whole-body exposure to 2.45 GHz electromagnetic fields does not alter radial-maze performance in rats. Behav Brain Res. 2004;155:37–43.PubMed Article Google Scholar 
  42. 42.Cobb BL, Jauchem JR, Adair ER. Radial arm maze performance of rats following repeated low level microwave radiation exposure. Bioelectromagnetics. 2004;25:49–57.PubMed Article Google Scholar 
  43. 43.Kesari KK, Behari J. Fifty-gigahertz microwave exposure effect of radiations on rat brain. Appl Biochem Biotechnol. 2009;158:126–39.CAS PubMed Article Google Scholar 
  44. 44.Li M, Wang Y, Zhang Y, Zhou Z, Yu Z. Elevation of plasma corticosterone levels and hippocampal glucocorticoid receptor translocation in rats: a potential mechanism for cognition impairment following chronic low-power-density microwave exposure. J Radiat Res (Tokyo). 2008;49:163–70.CAS Article Google Scholar 
  45. 45.Li Z, Peng RY, Wang SM, Wang LF, Gao YB, Ji D, et al. Relationship between cognition function and hippocampus structure after long-term microwave exposure. Biomed Environ Sci. 2012;25:182–8.PubMed Google Scholar 
  46. 46.Xiong L, Sun CF, Zhang J, Gao YB, Wang LF, Zuo HY, et al. Microwave exposure impairs synaptic plasticity in the rat hippocampus and pc12 cells through over-activation of the nmda receptor signaling pathway. Biomed Environ Sci. 2015;28:13–24.PubMed Google Scholar 
  47. 47.Srinivasan R. Anatomical constraints on source models for high-resolution EEG and MEG derived from MRI. Technol Cancer Res Treat. 2006;5:389.PubMed PubMed Central Google Scholar 
  48. 48.Jeong J. EEG dynamics in patients with Alzheimer’s disease. Clin Neurophysiol. 2004;115:1490–505.PubMed Article Google Scholar 
  49. 49.Hinrikus H, Bachmann M, Lass J, Karai D, Tuulik V. Effect of low frequency modulated microwave exposure on human EEG: individual sensitivity. Bioelectromagnetics. 2008;29:527–38.PubMed Article Google Scholar 
  50. 50.Li HJ, Peng RY, Wang CZ, Qiao SM, Yong Z, Gao YB, et al. Alterations of cognitive function and 5-HT system in rats after long term microwave exposure. Physiol Behav. 2015;140:236–46.CAS PubMed Article Google Scholar 
  51. 51.Vakalopoulos C. The EEG as an index of neuromodulator balance in memory and mental illness. Front Neurosci. 2014;8:63.PubMed PubMed Central Article Google Scholar 
  52. 52.Thuröczy G, Kubinyi G, Bodo M, Bakos J, Szabo L. Simultaneous response of brain electrical activity (EEG) and cerebral circulation (REG) to microwave exposure in rats. Rev Environ Health. 1994;10:135–48.PubMed Article Google Scholar 
  53. 53.Chizhenkova R. Slow potentials and spike unit activity of the cerebral cortex of rabbits exposed to microwaves. Bioelectromagnetics. 1988;9:337–45.CAS PubMed Article Google Scholar 
  54. 54.Nakatani-Enomoto S, Furubayashi T, Ushiyama A, Groiss SJ, Ueshima K, Sokejima S, et al. Effects of electromagnetic fields emitted from W-CDMA-like mobile phones on sleep in humans. Bioelectromagnetics. 2013;34:589–98.PubMed Article Google Scholar 
  55. 55.Schmid MR, Murbach M, Lustenberger C, Maire M, Kuster N, Achermann P, et al. Sleep EEG alterations: effects of pulsed magnetic fields versus pulse-modulated radio frequency electromagnetic fields. J Sleep Res. 2012;21:620–9.PubMed Article Google Scholar 
  56. 56.Vecchio F, Babiloni C, Lizio R, Fallani FV, Blinowska K, Verrienti G, et al. Resting state cortical EEG rhythms in Alzheimer’s disease: toward EEG markers for clinical applications: a review. Suppl Clin Neurophysiol. 2012;62:223–36.Article Google Scholar 
  57. 57.Perentos A, Cuesta-Soto F, Canciamilla A, Vidal B, Pierno L, Losilla NS, et al. Using a ring resonator notch filter for optical carrier reduction and modulation depth enhancement in radio-over-fiber links. Phot J. 2013;5:5500110.Article CAS Google Scholar 
  58. 58.Suhhova A, Bachmann M, Karai D, Lass J, Hinrikus H. Effect of microwave radiation on human EEG at two different levels of exposure. Bioelectromagnetics. 2013;34:264–74.PubMed Article Google Scholar 
  59. 59.Othman H, Ammari M, Rtibi K, Bensaid N, Sakly M, Abdelmelek H. Postnatal development and behavior effects of in-utero exposure of rats to radiofrequency waves emitted from conventional WiFi devices. Environ Toxicol Pharmacol. 2017;52:239–47.CAS PubMed Article Google Scholar 
  60. 60.Othman H, Ammari M, Sakly M, Abdelmelek H. Effects of prenatal exposure to WIFI signal (2.45 GHz) on postnatal development and behavior in rat: influence of maternal restraint. Behav Brain Res. 2017;326:291.CAS PubMed Article Google Scholar 
  61. 61.Zhang Y, Li Z, Gao Y. Effects of fetal microwave radiation exposure on offspring behavior in mice. J Radiat Res (Tokyo). 2015;56:261–8.CAS Article Google Scholar 
  62. 62.Qiao S, Peng R, Yan H, Gao Y, Wang C, Wang S, et al. Reduction of Phosphorylated Synapsin I (Ser-553) leads to spatial memory impairment by attenuating GABA release after microwave exposure in Wistar rats. PLoS One. 2014;9:e95503.PubMed PubMed Central Article Google Scholar 
  63. 63.Ning W, Chiang H, Yang W. Effects of GSM 1800 MHz on dendritic development of cultured hippocampal neurons. Acta Pharmacol Sin. 2007;28:1873–80.CAS PubMed Article Google Scholar 
  64. 64.Xu S, Ning W, Xu Z, Zhou S, Chiang H, Luo J. Chronic exposure to GSM 1800-MHz microwaves reduces excitatory synaptic activity in cultured hippocampal neurons. Neurosci Lett. 2006;398:253–7.CAS PubMed Article Google Scholar 
  65. 65.Wang L, Hu X, Peng R. Influence of long-term microwave radiation on contents of amino acids and monoamines in urine of Wistar rats. Chin J Indus Hyg. 2010;28:445.CAS Google Scholar 
  66. 66.Myhrer T. Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks. Brain Res Rev. 2003;41:268–87.CAS PubMed Article Google Scholar 
  67. 67.Riedel G, Platt B, Micheau J. Glutamate receptor function in learning and memory. Behav Brain Res. 2003;140:1–47.CAS PubMed Article Google Scholar 
  68. 68.Wang L, Peng R, Hu X, Gao Y, Wang S, Zhao L, et al. Abnormality of synaptic vesicular associated proteins in cerebral cortex and hippocampus after microwave exposure. Synapse. 2009;63:1010–6.CAS PubMed Article Google Scholar 
  69. 69Cull-Candy SG, Leszkiewicz DN. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE. 2004;2004:1–9.
  70. 70Furukawa H, Singh SK, Mancusso R, Gouaux E. Subunit arrangement and function in NMDA receptors. Nature. 2005;438:185–92.CAS PubMed Article Google Scholar 
  71. 71Ito K, Hirao A, Arai F, Takubo K, Matsuoka S, Miyamoto K, et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med. 2006;12:446–51.CAS PubMed Article Google Scholar 
  72. 72Wang H, Peng R, Zhao L, Wang S, Gao Y, Wang L, et al. The relationship between NMDA receptors and microwave induced learning and memory impairment: a long term observation on Wistar rats. Int J Radiat Biol. 2014:1–25.
  73. 73Campisi A, Gulino M, Acquaviva R, Bellia P, Raciti G, Grasso R, et al. Reactive oxygen species levels and DNA fragmentation on astrocytes in primary culture after acute exposure to low intensity microwave electromagnetic field. Neurosci Lett. 2010;473:52–5.CAS PubMed Article Google Scholar 
  74. 74Ozben T. Oxidative stress and apoptosis: impact on cancer therapy. J Pharm Sci. 2007;96:2181–96.CAS PubMed Article Google Scholar 
  75. 75Dasdag S, Bilgin H, Akdag M, Celik H, Aksen F. Effect of long term mobile phone exposure on oxidative-antioxidative processes and nitric oxide in rats. Biotechnol Biotechnol Equip. 2008;22:992–7.Article Google Scholar 
  76. 76Shahin S, Banerjee S, Singh SP, Chaturvedi CM. 2.45 GHz Microwave Radiation Impairs Learning and Spatial Memory via Oxidative/Nitrosative Stress Induced p53-Dependent/Independent Hippocampal Apoptosis: Molecular Basis and Underlying Mechanism. Toxicol Sci. 2015;148:1–50.
  77. 77Kumar M, Singh SP, Chaturvedi CM. Chronic nonmodulated microwave radiations in mice produce anxiety-like and depression-like behaviours and calcium- and NO-related biochemical changes in the brain. Exp Neurobiol. 2016;25:318–27.PubMed PubMed Central Article Google Scholar 
  78. 78Mack A, Georg T, Kreis P, Eickholt BJ. Defective actin dynamics in dendritic spines: cause or consequence of age-induced cognitive decline? Biol Chem. 2016;397:223–9.PubMed Article CAS Google Scholar 
  79. 79Kayhan H, Esmekaya MA, Saglam AS, Tuysuz MZ, Canseven AG, Yagci AM, et al. Does MW radiation affect gene expression, apoptotic level, and cell cycle progression of human sh-sy5y neuroblastoma cells? Cell Biochem Biophys. 2016;74:99–107.CAS PubMed Article Google Scholar 
  80. 80Joubert V, Bourthoumieu S, Leveque P, Yardin C. Apoptosis is induced by radiofrequency fields through the caspase-independent mitochondrial pathway in cortical neurons. Radiat Res. 2008;169:38–45.CAS PubMed Article Google Scholar 
  81. 81Motawi TK, Darwish HA, Moustafa YM, Labib MM. Biochemical modifications and neuronal damage in brain of young and adult rats after long-term exposure to mobile phone radiations. Cell Biochem Biophys. 2014;70:845–55.CAS PubMed Article Google Scholar 
  82. 82Dasdag S, Akdag MZ, Aksen F, Bashan M, Buyukbayram H. Does 900 MHZ GSM mobile phone exposure affect rat brain? Electromagn Biol Med. 2004;23:201–14.CAS Article Google Scholar 
  83. 83Fragopoulou AF, Samara A, Antonelou MH, Xanthopoulou A, Papadopoulou A, Vougas K, et al. Brain proteome response following whole body exposure of mice to mobile phone or wireless DECT base radiation. Electromagn Biol Med. 2012;31:250–74.CAS PubMed Article Google Scholar 
  84. 84Verma RK, Sisodia R, Bhatia A. Radioprotective role of Amaranthus Gangeticus Linn.: a biochemical study on mouse brain. J Med Food. 2002;5:189–95.CAS PubMed Article Google Scholar 
  85. 85Sharma A, Sisodia R, Bhatnagar D, Saxena VK. Spatial memory and learning performance and its relationship to protein synthesis of Swiss albino mice exposed to 10 GHz microwaves. Int J Radiat Biol. 2014;90:29–35.CAS PubMed Article Google Scholar 
  86. 86Calabrò E, Condello S, Currò M, Ferlazzo N, Caccamo D, Magazù S, et al. Modulation of HSP response in SH-SY5Y cells following exposure to microwaves of a mobile phone. World J Biol Chem. 2012;3:34–40.PubMed PubMed Central Article Google Scholar 
  87. 87Calabrò E, Magazù S. Inspections of mobile phone microwaves effects on proteins secondary structure by means of Fourier transform infrared spectroscopy. J Electromagnet Anal. 2010;2010
  88. 88Koch C, Zador A. The function of dendritic spines: devices subserving biochemical rather than electrical computation. J Neurosci. 1993;13:413–22.CAS PubMed Google Scholar 
  89. 89Harris KM. Structure, development, and plasticity of dendritic spines. Curr Opin Neurobiol. 1999;9:343–8.CAS PubMed Article Google Scholar 
  90. 90Nimchinsky EA, Sabatini BL, Svoboda K. Structure and function of dendritic spines. Annu Rev Physiol. 2002;64:313–53.CAS PubMed Article Google Scholar 
  91. 91Johnson OL, Ouimet CC. Protein synthesis is necessary for dendritic spine proliferation in adult brain slices. Brain Res. 2004;996:89–96.CAS PubMed Article Google Scholar 
  92. 92Dasdag S, Akdag MZ, Kizil G, Kizil M, Cakir DU, Yokus B. Effect of 900 MHz radio frequency radiation on beta amyloid protein, protein carbonyl, and malondialdehyde in the brain. Electromagn Biol Med. 2012;31:67–74.CAS PubMed Article Google Scholar 
  93. 93Im HI, Kenny PJ. MicroRNAs in neuronal function and dysfunction. Trends Neurosci. 2012;35:325–34.CAS PubMed PubMed Central Article Google Scholar 
  94. 94Abe M, Bonini NM. MicroRNAs and neurodegeneration: role and impact. Trends Cell Biol. 2013;23:30–6.CAS PubMed Article Google Scholar 
  95. 95Baer C, Claus R, Plass C. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res. 2013;73:473–7.CAS PubMed Article Google Scholar 
  96. 96Stahlhut Espinosa CE, Slack FJ. The role of microRNAs in cancer. Yale J Biol Med. 2006;79:131–40.PubMed Google Scholar 
  97. 97Dasdag S, Akdag MZ, Erdal ME, Erdal N, Ay OI, Ay ME, et al. Long term and excessive use of 900 MHz radiofrequency radiation alter microRNA expression in brain. Int J Radiat Biol. 2015;91:306–11.CAS PubMed Article Google Scholar 
  98. 98Dasdag S, Akdag MZ, Erdal ME, Erdal N, Ay OI, Ay ME, et al. Effects of 2.4 GHz radiofrequency radiation emitted from Wi-Fi equipment on microRNA expression in brain tissue. Int J Radiat Biol. 2015;91:555–61.CAS PubMed Article Google Scholar 
  99. 99Zhao L, Sun C, Xiong L, Yang Y, Gao Y, Wang L, et al. MicroRNAs: novel mechanism involved in the pathogenesis of microwave exposure on rats’ hippocampus. J Mol Neurosci. 2014;53:222–30.CAS PubMed Article Google Scholar 
  100. 100Hassanshahi A, Shafeie SA, Fatemi I, Hassanshahi E, Allahtavakoli M, Shabani M, et al. The effect of Wi-Fi electromagnetic waves in unimodal and multimodal object recognition tasks in male rats. Neurol Sci. 2017;38:1069–76.
  101. 101Megha K, Deshmukh PS, Banerjee BD, Tripathi AK, Ahmed R, Abegaonkar MP. Low intensity microwave radiation induced oxidative stress, inflammatory response and DNA damage in rat brain. Neurotoxicology. 2015;51:158–65.CAS PubMed Article Google Scholar 
  102. 102Belyaev IY, Koch CB, Terenius O, Roxström-Lindquist K, Malmgren LO, Sommer HW, et al. 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;27:295–306.CAS PubMed Article Google Scholar 
  103. 103Merola P, Marino C, Lovisolo G, Pinto R, Laconi C, Negroni A. Proliferation and apoptosis in a neuroblastoma cell line exposed to 900 MHz modulated radiofrequency field. Bioelectromagnetics. 2006;27:164–71.CAS PubMed Article Google Scholar 
  104. 104Qutob S, Chauhan V, Bellier P, Yauk C, Douglas G, Berndt L, et al. Microarray gene expression profiling of a human glioblastoma cell line exposed in vitro to a 1.9 GHz pulse-modulated radiofrequency field. Radiat Res. 2006;165:636–44.CAS PubMed Article Google Scholar 
  105. 105Wang LF, Tian DW, Li HJ, Gao YB, Wang CZ, Zhao L, et al. Identification of a novel rat nr2b subunit gene promoter region variant and its association with microwave-induced neuron impairment. Mol Neurobiol. 2016;53:2100–11.CAS PubMed Article Google Scholar 
  106. 106Gibson GE, Jope R, Blass J. Decreased synthesis of acetylcholine accompanying impaired oxidation of pyruvic acid in rat brain minces. Biochem J. 1975;148:17–23.CAS PubMed PubMed Central Article Google Scholar 
  107. 107Mosconi L, Tsui WH, Rusinek H, De Santi S, Li Y, Wang GJ, et al. Quantitation, regional vulnerability, and kinetic modeling of brain glucose metabolism in mild Alzheimer’s disease. Eur J Nucl Med Mol Imaging. 2007;34:1467–79.CAS PubMed Article Google Scholar 
  108. 108Nicholson RM, Kusne Y, Nowak LA, LaFerla FM, Reiman EM, Valla J. Regional cerebral glucose uptake in the 3xTG model of Alzheimer’s disease highlights common regional vulnerability across AD mouse models. Brain Res. 2010;1347:179–85.CAS PubMed Article Google Scholar 
  109. 109Gage FH, Kelly P, Bjorklund A. Regional changes in brain glucose metabolism reflect cognitive impairments in aged rats. J Neuro. 1984;4:2856–65.CAS Google Scholar 
  110. 110Choeiri C, Staines W, Miki T, Seino S, Messier C. Glucose transporter plasticity during memory processing. Neuroscience. 2005;130:591–600.CAS PubMed Article Google Scholar 
  111. 111Kwon MS, Vorobyev V, Kännälä S, Laine M, Rinne JO, Toivonen T, et al. GSM mobile phone radiation suppresses brain glucose metabolism. J Cereb Blood Flow Metab. 2011;31:2293–301.CAS PubMed PubMed Central Article Google Scholar 
  112. 112Durkin TP, Messier C, de Boer P, Westerink B. Raised glucose levels enhance scopolamine-induced acetylcholine overflow from the hippocampus: an in vivo microdialysis study in the rat. Behav Brain Res. 1992;49:181–8.CAS PubMed Article Google Scholar 
  113. 113Ragozzino ME, Unick KE, Gold PE. Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. P Nat Acad. 1996;93:4693–8.CAS Article Google Scholar 
  114. 114Messier C, Durkin T, Mrabet O, Destrade C. Memory-improving action of glucose: indirect evidence for a facilitation of hippocampal acetylcholine synthesis. Behav Brain Res. 1990;39:135–43.CAS PubMed Article Google Scholar 
  115. 115Gold PE. Acetylcholine modulation of neural systems involved in learning and memory. Neurobiol Learn Mem. 2003;80:194–210.CAS PubMed Article Google Scholar 
  116. 116Gold PE. Acetylcholine: cognitive and brain functions. Neurobiol Learn Mem. 2003;80:177.PubMed Article Google Scholar 
  117. 117Krylova I, Dukhanin A, Il’in A, Kuznetsova EY, Balaeva N, Shimanovskii N, et al. Effect of microwave radiation on learning and memory. Bull Exp Biol Med. 1992;114:1620–2.Article Google Scholar 
  118. 118Wang L, Li X, Peng R, Gao Y, Zhao L, Wang S, et al. A metabolomic approach to screening urinary metabolites upon microwave exposure in monkeys. Mil Med Sci. 2011;35:369–78.CAS Google Scholar 
  119. 119Sanders AP, Joines WT. The effects of hyperthermia and hyperthermia plus microwaves on rat brain energy metabolism. Bioelectromagnetics. 1984;5:63–70.CAS PubMed Article Google Scholar 
  120. 120Zhao L, Peng RY, Gao YB, Wang SM, Wang LF, Dong J, et al. Mitochondria morphologic changes and metabolic effects of rat hippocampus after microwave irradiation. Chin J Radiol Med Prot. 2007;27:602–4.CAS Google Scholar 
  121. 121Wang Q, Cao Z. Effect of microwave electromagnetic fields on activity of energy metabolism cytochrome oxidase in cerebral cortical neurons of postnatal rats. J Environ Health. 2005;22:329–31.CAS Google Scholar 
  122. 122Ongwijitwat S, Wong-Riley MT. Is nuclear respiratory factor 2 a master transcriptional coordinator for all ten nuclear-encoded cytochrome c oxidase subunits in neurons? Gene. 2005;360:65–77.CAS PubMed Article Google Scholar 
  123. 123Chandrasekaran K, Hatanpää K, Rapoport SI, Brady DR. Decreased expression of nuclear and mitochondrial DNA-encoded genes of oxidative phosphorylation in association neocortex in Alzheimer disease. Mol Brain Res. 1997;44:99–104.CAS PubMed Article Google Scholar 
  124. 124Ellis CE, Murphy EJ, Mitchell DC, Golovko MY, Scaglia F, Barceló-Coblijn GC, et al. Mitochondrial lipid abnormality and electron transport chain impairment in mice lacking α-synuclein. Mol Cell Biol. 2005;25:10190–201.CAS PubMed PubMed Central Article Google Scholar 
  125. 125Caubet R, Pedarros-Caubet F, Chu M, Freye E, de Belem RM, Moreau J, et al. A radio frequency electric current enhances antibiotic efficacy against bacterial biofilms. Antimicrob Agents Chemother. 2004;48:4662–4.CAS PubMed PubMed Central Article Google Scholar 
  126. 126Kang D, Hamasaki N. Mitochondrial transcription factor a in the maintenance of mitochondrial DNA. Ann N Y Acad Sci. 2005;1042:101–8.CAS PubMed Article Google Scholar 
  127. 127Li H, Li C. Apoptosis gene expression and their relationship to mtDNA mutation in tumor tissues of gynecologic oncology patients. Chin J Birth Health Hered. 2003;11:34–6.Google Scholar 
  128. 128Lu M, Zhu J, Qian C, Wang G, Nie J, Tong J. Biological effects of 2450 MHz microwave combined with γ-rays on rat cultured gliacytes. J Radiat Proc. 2010;3:46–50.Google Scholar 

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This work was supported by the National Natural Science Foundation of China (61571455).

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  1. Laboratory of Experimental Pathology, Beijing Institute of Radiation Medicine, Beijing, 100850, ChinaWei-Jia Zhi, Li-Feng Wang & Xiang-Jun Hu

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WJZ wrote the paper and outlined this manuscript, LFW and XJH provided a detailed guidance throughout the article. All of the authors read and approved the final manuscript.

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Zhi, WJ., Wang, LF. & Hu, XJ. Recent advances in the effects of microwave radiation on brains. Military Med Res 4, 29 (2017). https://doi.org/10.1186/s40779-017-0139-0

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Keywords

  • Microwave
  • Central nervous system