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Review on health effects related to mobile phones. Part II: results and conclusions

Moussa, Mayada M.R.

The Journal Of The Egyptian Public Health Association: December 2011 - Volume 86 - Issue 5 and 6 - p 79–89
doi: 10.1097/01.EPX.0000406204.36949.49
Review article
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Background Part 1 of this review was published in the Journal of Egyptian Association of Public Health 2010; 85(5, 6):337–345. It included the introduction and methodology. It was based on reviewing the literature published in the last 10 years (2000–2010).

Methods Searches were made electronically through various search engines and health-related databases, and manually through journals, reports, and conference proceedings. The references used in the introduction of part 1 were mainly WHO reports, textbooks, and nonserial publications.

Results In part 2, the literature published in 2011 was added to the yield and the results and conclusions are based on the updated search. In this literature search, 69 research articles (epidemiologic, experimental, cellular, and animal studies), 17 systemic or meta-analysis review studies, and four reports were included.

Conclusion The evidence presented in these peer-reviewed publications did not provide a consistent pattern that exposure to mobile phones is detrimental to health. Only studies associating mobile phone use during driving with road traffic accidents and those investigating electromagnetic interference with personal or hospital medical electronic devices showed consistent results. Regarding children, there are currently little data on cell phone use and health effects, including the risk of cancer. Further experimental and epidemiologic studies are needed to seek explanations for the controversies in studies on mobile phones so far. These studies should apply sound methodology for exposure assessment of mobile phone radiation and should focus on the effects of long-term use (more than 10 years). Cohort studies, in particular, should be established to investigate the long-term effects of mobile phone use on brain cancer as well as to investigate the possible health effects among children.

Department of Environmental Health, High Institute of Public Health, Alexandria University, Alexandria, Egypt

Correspondence to Dr Mayada M.R. Moussa, Department of Environmental Health, High Institute of Public Health, Alexandria University, 165, Horreya Road, Alexandria, Egypt Tel: +20 342 855 75/+20 342 855 76; fax: +20342 884 36; e-mail: mayadareda@hotmail.com

Received August 13, 2011

Accepted August 22, 2011

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Results

Potentially eligible articles, reports, and further publications identified amounted to 772. After selection and processing, only 87 studies (69 research articles and 18 reviews) were retained for analysis. Other publications, including four reports (peer-reviewed and published by national or international research programs) and three press releases, were also included in this review.

The scientific literature reviewed in this study are categorized into:

  • Experimental or laboratory studies:
    • In-vitro studies conducted on isolated components of biological systems such as solutions of DNA or cell cultures.
    • In-vivo animal studies that use experimental animals.
    • Human experimental studies that depend on human volunteers.
    • Studies investigating electromagnetic interference (EMI) with electronic devices.
  • Epidemiological studies of health effects associated with exposure to radiofrequency radiation (RFR) of frequencies used in mobile phones (MPhs).
    • (a) Cancer-related epidemiological studies.
    • (b) Noncancer epidemiological studies.
  • Studies on MPh exposure in children.
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Experimental studies

In-vitro studies

These are important for determining the possible mechanisms by which RFR interacts with biological systems. The results obtained from these studies should help in identifying end points for research in in-vivo studies 1.

The majority of the in-vitro studies carried out were concerned with the acute effects of RFR rather than the long-term effects. An American study, 2, found no evidence of chromosomal aberrations on assessing cytogenic damage in human lymphocytes that were exposed for 24 h to 835 MHz RFR at specific absorption rate (SAR) values of 4.4–5 W/kg, which are higher than those observed in human tissues exposed to MPhs. In another American study, 3 RFR mimicking that of MPhs in frequency (835–847 MHz), modulation, and power (leading to SAR of 0.6 W/kg) was used for a longer duration (42 days) on human fibroblasts. However, no detectable DNA damage was found.

In contrast, an Austrian study 4 found DNA breaks in human fibroblasts and rat granulosa cells that were exposed to MPh signals at 1800 MHz, SAR of 1.2 or 2 W/kg, and at different modulations. The cells were exposed for 4, 16, and 24 h (both intermittently at 5 min on/10 min off and continuously). The exposure induced DNA single-strand and double-strand breaks as measured by the comet assay. Effects occurred after 16 h of exposure (or more) in both cell types. The same study conditions were used later in an Italian study 5 and the same results and conclusions were attained. It was noted, however, that trophoblast cells recovered from DNA damage within 2 h after cessation of RFR exposure and their viability was not altered. Nevertheless, the consistency of the findings in both studies suggests that the radiation emitted by MPhs may potentially affect the DNA integrity.

In an American meta-analysis study, 6 the extent of genotoxicity in cells exposed to MPhs RFR compared with sham-exposed/unexposed control cells was assessed for various end points, including single-strand and double-strand breaks in the DNA, incidence of chromosomal aberrations, micronuclei, and sister chromatid exchanges. The overall data indicated that under certain exposure conditions, there were statistically significant increases in genotoxicity for some end points; however, the mean indices for chromosomal aberrations and micronuclei in the exposed and sham/unexposed controls were within the spontaneous levels reported in the historical database.

Nongenotoxic effects of MPh radiation were also investigated in a number of studies exploring the possibility of MPhs involvement in tumor promotion through an increase in the rate of cell proliferation or through other mechanisms. An Egyptian study 7 looking into the effects of RFR on plasma lipid peroxide and antioxidase activities in human erythrocytes reported that acute exposure (2–4 h) to MPhs could significantly increase free radicals and reduce the antioxidative activity of the cells, thus leading to ‘oxidative stress.’ A Finnish study by the Bio-Non-Ionizing Radiation Group 8 confirmed the role of the MPh type of radiation in the induction of a cellular stress response in human endothelial cells through the increase of ‘heat shock proteins (hsp-27).’ These stress proteins could be responsible for the increase in blood–brain barrier (BBB) permeability to noxious materials.

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In-vivo animal studies

Two broad types of these studies were conducted: cancer-related and non-cancer-related studies.

Cancer-related in-vivo animal studies: According to a very recent review on RFR genotoxicity studies, 9 to date, most studies of rodents exposed to RFR provide no clear or consistent evidence that this type of radiation causes cancer or that it enhances the carcinogenicity of known chemical carcinogens.

An Australian study 10 reported that transgenic and nontransgenic wild-type female mice were exposed for 1 h every morning, except on weekends (1 h/day, 5 days/week), to a MPh signal (at 898.4 MHz) at four SAR dose groups (0.25, 1, 2, and 4 W/kg). Transgenic mice are genetically engineered animals that are made to render them at a high risk for cancer. The study also included a sham-exposed group and another (negative) cage control group. The mice were kept under standard laboratory conditions for a maximum study period of 24 months and were then killed, and their organs and tissues were histopathologically examined for tumor tissues. Compared with sham-exposed and control animals, the statistical evaluation of the exposed transgenic mice or wild-type females (in terms of the survival rate, body weight development, clinical health, and the examined tissues) showed no special effects of MPh exposure.

In a much more recent German study 11, mice were exposed to universal mobile telecommunications system (UMTS) electromagnetic fields (EMF), the new high data speed MPh technology, with intensities of 4.8 and 48 W/m2. The low-dose group (4.8 W/m2) was subjected to an additional prenatal treatment of the carcinogen ethylnitrosourea (40 mg/kg body weight) to render them at a high risk for cancer. The study also included a negative sham-exposed group (no exposure to radiation or the carcinogen), a positive sham-exposed group (exposure to the carcinogen only), and another cage control group. The ethylnitrosourea-treated group UMTS exposed at 4.8 W/m2 was the only group displaying an enhanced lung tumor rate and an increased incidence of lung carcinomas as compared with all the other groups, especially the controls treated only with ethylnitrosourea.

If the findings in the latter study could be replicated, then this would mean that MPh radiation may have the ‘epigenetic’ potential to promote cancer formation in already susceptible organisms. This effect would clearly depend on the strength of the ‘original’ carcinogens apart from the radiation dosimetry parameters themselves.

To this end, the National Toxicology Program (NTP) headquartered at the National Institute of Environmental Health Sciences in North Carolina, USA, initiated the largest laboratory rodent study to date on cell phone radiofrequency (RF). The NTP toxicology and carcinogenicity studies are designed to mimic human exposure and are based on the frequencies and modulations currently in use in the United States. Cell phone radiation will be administered in 10-min on/off cycles for approximately 20 h/day. The NTP anticipates the completion and reporting of all phases of the studies by 2014 12.

Non-cancer-related in-vivo animal studies: A large number of studies have researched the noncancer effects of RFR similar to that used in MPhs on many body organs and systems in animals, with varying results.

Effects on brain, cognitive functions, and behavior: A Swedish study 13 investigated the possibility of albumin leakage across the BBB. Three groups of rats were exposed for 2 h to a MPh radiating at 915 MHz with SAR values of 0.002, 0.02, and 0.2 W/kg, respectively. A fourth group of nonexposed rats was included as a control. Fifty days later, the rats were sacrificed and their brains were examined. The brains of exposed animals showed foci of albumin in the central parts and the hypothalamus, confirming the leakage across the BBB. In addition, a significant positive relation was found between the SAR values and the amount of pathological neurons. However, a number of study groups 14–16 attempted to repeat the Salford et al.13 research, but did not achieve the same results, which could indicate that the original observations are losing credibility.

In terms of cognitive functions, a very recent Greek study 17, using three different exposure protocols [90 min/day for 3 days (acute exposure), 17 days (chronic exposure-I), or 31 days (chronic exposure-II)] at an SAR value of 0.22 W/kg, showed that a nonspatial memory task (Object Recognition Task) in mice was affected by MPh radiation. The results suggested a possible severe interaction of EMF with the consolidation phase of recognition memory processes. Conversely, in an earlier study by Dubreuil et al.18 on rats that were exposed once for 45 min to MPh radiation producing a local SAR in the head of 1–3.5 W/kg, no effects on memory or learning tasks were reported.

This variation in the results may suggest that long-term exposure to MPh radiation was more detrimental to memory than to short-term exposure.

Effects on reproduction and development: Many recent studies have addressed RF field effects on prenatal development in animals and male infertility, but without reaching a consensus on whether or not MPhs can exert adverse effects at the nonthermal exposure levels they produce.

The Greek study by Pyrpasopoulou et al.19, showed a statistically significant change in certain major proteins involved in renal development in the kidneys of newborn rats that were exposed in the prenatal period to RFR of mobile telecommunications. These changes led to a delay in the development of the kidneys. Also, a statistically significant derangement of chicken embryo retinal differentiation in response to MPh exposure was shown in a recent study 20 in Pakistan.

A recent Turkish study 21 investigated the effects of cellular phones on ovaries in rats. Female pregnant rats in the study group (43 rats) were exposed to MPhs during the entire period of pregnancy, whereas those in the control group (39 rats) were not. Analysis revealed that in the study group, the number of follicles was significantly lower than that in the control group, which suggests that intrauterine exposure to MPhs may have negative effects on ovaries.

Nevertheless, in a review study by Heynick and Merritt 22, it was concluded that RFR of a low intensity used in mobile telephony presents no teratogenic risk, as long as the exposure does not exceed permissible guidelines. The only adverse reproductive effects that could be related to MPh radiation were a decrease in the fetal mass of experimental animals, lower birth weights, and slower growth rates.

In terms of the effects of MPh emissions on rat sperm cells and male rat infertility, some studies showed a number of negative effects, for example in the form of decreased motility 23,24, hypospermatogenesis and spermatozoa maturation arrest, 25 or a decrease in protein kinase C enzyme activity and total sperm count 26. However, most could be considered as inadequate because of the small number of exposed animals in the study, the low statistical power, and/or the methodological problems regarding exposure parameters in the experiment.

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Experimental studies on human volunteers

This type of research is particularly important in assessing the short-term effects of MPh RFR on the brain and nervous system, EEG recordings, attention and cognitive functions, hearing, driving performance, some endocrine parameters, and the cardiovascular system 27.

Effects on the brain and the neurological system: The effects of MPh use on the neurological system in humans have been the subject of a large number of experimental studies in recent years. There is some evidence of an effect on the EEG, as shown by changes in the EEG α and/or β bands in single-blind or double-blind studies 28–31.

In the Italian study by Vecchio et al.30, the results also revealed that, compared with sham exposure, MPh exposure modulated the interhemispheric coupling of frontal and temporal α wave rhythms, indicating that prolonged MPh emission could affect brain physiology, probably by impinging on the interhemispheric synchronization of signals. The same Italian group tested, in a later study 32, the hypothesis that this effect can vary with physiological aging. The study revealed that, indeed, compared with the young participants, the elderly participants showed a statistically significant increase in the interhemispheric coherence of frontal and temporal EEG α rhythms during MPh exposure.

There is also some evidence that there may be an effect of exposure to MPh signals on sleep EEG. A Russian study 33 found several changes in EEG recordings of humans exposed for 8 h during sleep to a MPh. Moreover, two independent study groups, a Swiss group 34 and an Australian group 35, reported significant changes in some sleep EEG parameters when human volunteers were exposed to MPhs for a period of only 30 min before sleep, showing that the changes in brain function induced by the cellular phones’ EMF outlast the exposure period. It should be noted that none of the detected effects on brain activity have been found to relate to any adverse health effects.

Another set of experimental studies investigated the effects of MPhs on evoked or event-related potentials (ERPs) in the brain. ERP represents the brain activity associated with certain stimuli (e.g. visual, auditory, and memory tasks). In some studies, 36–39 changes in the ERPs in response to certain auditory, memory, and cognitive tasks performed during exposure to MPhs were detected. However, the positive findings in some of the studies exploring the effects of MPhs on ERPs were hard to replicate 40, which indicates that those effects could have been accidental or that the exposure parameters and study methodology were not strong enough to yield consistent results.

Besides the effects of cell phones on electrical brain activity, some studies investigated the effects on cerebral blood flow and brain metabolism. For instance, in a Swiss study 41, an increase in the relative cerebral blood flow in the dorsolateral prefrontal cortex of the brain was observed on the side of exposure to a MPh after 30 min of exposure. On the contrary, a Finnish study group 42 observed a relative decrease in regional cerebral blood flow bilaterally in the auditory cortex, and reported that the findings could be a result of an auditory signal from the active MPh. This latter group explored the discrepancy in the results further, and found out in a later study 43 that a MPh in operation induces a local decrease in regional cerebral blood flow beneath the antenna in the inferior temporal cortex and an increase more distantly in the prefrontal cortex. These findings generally indicate that MPh exposure has some effects on brain physiology and activity.

A very recent American study 44 investigated this concept further by evaluating whether acute cell phone exposure affects brain glucose metabolism as a marker of brain activity. It was found that whole-brain metabolism did not differ between exposure and nonexposure conditions; however, metabolism in the region closest to the antenna (orbitofrontal cortex and temporal pole) was significantly higher during exposure to MPhs. This increase was, moreover, significantly correlated with the estimated EMF amplitudes from the MPhs.

Effects on cognitive performance: A large number of experimental studies also explored the neurobehavioral effects of MPhs and their possible impacts on cognitive performance, but the results have been equivocal. A number of systemic review and meta-analysis studies attempted to address the rising concern about the possible adverse effects of RFR exposure from cellular phones on cognitive functions 45–47. The meta-analysis study by Barth et al.45 concluded that MPh EMFs may have a small impact on human attention and working memory after considering 19 experimental studies. Valentini et al.46 included 24 studies in their meta-analysis review study and found some statistically significant differences between exposure and nonexposure to MPhs in certain cognitive tasks. These differences disappeared when a sensitivity analysis was performed. However, the authors observed a significant effect of sponsorship and publication biases, as a considerable number of the studies yielding negative results were funded by the telecommunication industry. The review study by Regel and Achermann 47 considered the lack of a validated tool to reliably assess changes in cognitive performance as the main factor contributing to the current inconsistencies in the study outcomes. The huge variations in the findings may also be due to methodological issues such as differences in sample size, experimental design, exposure setup as well as exposure conditions.

Considering these conclusions, it seems that the scientific question of the pathophysiology of mobile-phone EMFs as reflected in measurements of brain electrical activity remains unanswered. The intervention of a respected and unbiased research body, such as the WHO, is needed for the development of official research standards and guidelines.

Effects on hearing: A number of human experimental studies have attempted to assess potential changes in hearing function as a consequence of short-term (10–20 min) exposure to EMFs produced by MPhs, but found no significant effects 48–50. This could be because of their low statistical power, as the number of participants in each study did not exceed 30 volunteers.

When the number of participants examined for hearing function increased, like in a Turkish study 51 involving 60 participants, some negative effects of MPhs were detected. The participants were divided into three exposure groups: (a) 20 men who have used a MPh frequently and spoken approximately 2 h/day for 4 years; (b) 20 men who have used a MPh for 10–20 min/day for 4 years; and (c) 20 men who have never used a MPh (control group). The results revealed no significant difference between the exposure groups, except that the detection thresholds in those who talked approximately 2 h/day were significantly higher than those in moderate users or control participants. This could indicate that a higher degree of hearing loss is associated with a long-term and intensive use of MPhs.

A recent large-scale European study 52 reporting results from the EMFnEAR project (Exposure at UMTS Electromagnetic Fields: Study on Potential Adverse Effects on Hearing) concluded that short-term exposure to MPhs, even at the maximum output, does not exert measurable immediate effects on the human auditory system. UMTS is the universal mobile telecommunication system or the third generation of mobile communication systems using frequencies between 1900 and 2170 MHz.

This European study, despite involving 134 participants who were tested across different European laboratories, disregarded MPhs operating at lower frequencies, tested for the effects of short-term exposure only (up to 20 min), and not all participants were subjected to all audiological tests. These shortcomings should be avoided in further studies in order to reach definitive conclusions.

Effects of mobile phones on driving: The impact of cell phone use on various aspects of driving performance has been investigated in a sizeable number of experimental studies, with consistent results. Some studies investigated performance on laboratory tasks similar to driving, some were carried out in a driving simulator, and others used real cars and road situations 27.

A number of studies 53–57 showed that the time taken to react to an imperative stimulus or a potentially dangerous road situation was perilously prolonged when the driver was using a MPh. In general, driving performance measured in terms of traffic violations (e.g. speeding, running stop signs), driving maintenance (e.g. standard deviation of lane position), attention lapses (e.g. stops at green lights, failure to visually scan for intersection traffic), and/or response time (e.g. time to step on brake in response to a pop-up event) was significantly impacted when drivers were concurrently talking on a MPh, whether hand-held or hands-free. These studies lend further empirical support to the dangers of drivers being distracted by cell phone conversations.

Even text messaging while driving was shown to have a negative impact on driving performance. This negative impact appears to exceed the impact of conversing on a cell phone while driving 58.

A meta-analysis review study 59 evaluated 33 experimental studies and found that the reaction time to events and stimuli while talking produced the largest performance decrements, and found no difference between hand-held and hands-free phones regarding the increase in the reaction time. The same conclusion was reached in another review study 60 assessing the scientific literature exploring the effects of those two types of cell phone use on driving and driving-related performance.

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Electromagnetic interference of electronic devices with mobile phones

The interference caused by MPh use with personal medical devices was tested extensively, particularly for cardiac pacemakers.

A recent review study 61 evaluated the scientific literature on the effects of MPhs on implantable pacemakers, and concluded that older pacemakers had a higher rate of being affected by MPhs when compared with newer ones. This is probably due to the fact that the newer generation pacemakers are more protected against EMFs, being equipped with RF feedthrough filters incorporated into their internal circuitry.

Another review 62 assessed studies on EMI of hearing aids with MPhs. It was concluded that some older models of body-worn processors are highly susceptible to EMI problems, whereas the newer and smaller behind-the-ear hearing aids or cochlear implants have better performing signal processing features, and show less EMI with MPhs.

Cellular telephones can also interfere with electronic devices used in hospitals. This could be a serious problem with medical equipment in critical care units and operating theaters. For instance, Fung et al.63 measured the EMF strengths around MPhs of different types at various distances from medical equipment in the emergency department and noted some interference with certain devices. However, a review study by Saraf 64 reported that the recommended safe distance of 1 m from electronic appliances in hospitals is more than enough to prevent EMI, and that the newer generation MPhs (operating predominantly in the 1800 MHz band) might be used much closer to electronic equipment than their predecessors.

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Epidemiological studies

Cancer-related epidemiological studies

By far, the greatest public concern has been that exposure to the low-level RFR emitted from MPhs and their base stations may cause cancer. Although cellular telephone use is comparatively new, since the 1990s, quite a large number of studies have investigated cancer occurrence among cell phone users. However, initial epidemiological studies on brain tumor risk had insufficiently long latency periods to yield a meaningful interpretation of the long-term risk. Only during recent years have a number of studies been published that enable the evaluation of risk related to 10 years or more latency period.

A Swedish group 65 conducted, during 1997–2003, two case–control studies on brain tumors including assessment of the use of MPhs and cordless phones. The anatomical area in the brain where the tumor was located was assessed and related to the side of the head used for both types of wireless phones. The study reported significant risks for astrocytoma [odds ratio (OR)=3.3, 95% confidence interval (CI)=2.0–5.4) and acoustic neuroma (OR=3.0, 95% CI=1.4–6.2) with ipsilateral MPh use in the group using cell phones for more than 10 years. The risk was the highest for cases with first use below 20 years of age, with OR=5.2 (95% CI=2.2–12) for astrocytoma and OR=5.0 (95% CI=1.5–16) for acoustic neuroma.

Another case–control study 66 investigated the relationship between MPh use and the risk of glioma. The study found an increased OR of statistical significance (OR=1.39, 95% CI 1.01, 1.92) for glioma related to MPh use for more than 10 years on the side of the head where the tumor was located.

Moreover, a population-based case–control study carried out in three regions of Germany as part of the INTERPHONE study 67 reported no significant increase in the risk of glioma and meningioma, except among persons who had used cellular phones for 10 or more years, where the risk for glioma was OR=2.20 (95% CI 0.94, 5.11). The study reached the conclusion that for long-term cellular phone users, results need to be confirmed before firm conclusions can be drawn.

This pattern of a significantly elevated risk in relation to prolonged MPh use has been further solidified by a number of recent meta-analysis studies carried out by research groups in Sweden 68, Australia 69, and Korea 70. All three studies reported no significant increase in brain tumors (glioma, acoustic neuroma, or meningioma) in relation to the overall use of cell phones. However, the use of MPhs for 10 or more years was shown to lead to an increased risk for acoustic neuroma and glioma. The risk was highest and significant for ipsilateral exposure. One study 68 yielded an ORs of 2.4 (95% CI 1.1–5.3) for acoustic neuroma and 2.0 (95% CI 1.2–3.4) for glioma, whereas another study 70 yielded an overall OR of 1.18 (95% CI 1.04–1.34) for all types of brain tumors in relation to ipsilateral and prolonged MPh use.

In 2010, the results of the international multicenter INTERPHONE study carried out from 2000 to 2004 were published 71. The INTERPHONE study was initiated as an international set of case–control studies focusing on four types of tumors in tissues that most absorb RF energy emitted by MPhs: tumors of the brain (glioma and meningioma), acoustic nerve (schwannoma), and the parotid gland. Sixteen study centers from 13 countries (Australia, Canada, Denmark, Finland, France, Germany, Israel, Italy, Japan, New Zealand, Norway, Sweden, and the United Kingdom) were included, and 2708 glioma and 2409 meningioma cases and matched controls were interviewed. Overall, no increase in the risk of glioma or meningioma was observed with the use of MPhs; still, an increased and significant risk of glioma (OR=1.40, 95% CI 1.03–1.89) was observed at the highest exposure levels. Nevertheless, the study group concluded that biases and error prevent a causal interpretation, and recommended further investigation of the possible effects of long-term heavy use of MPhs.

The INTERPHONE study, despite being a large-scale multicenter study, was criticized on the grounds that it shares the same limitations as all case–control studies previously carried out on MPhs and cancer, namely that it can investigate only a short period of observation since first exposure to MPhs. As the cancer cases in the study were diagnosed between 2000 and 2004, only a small percent of cases (<5% of the meningioma cases and <9% of the glioma cases) occurred more than 10 years since the start of MPh use. The brief exposure in most of the cases leaves only a limited incubation time for an exposure-related cancer to develop. Thus, observing no increase in risk would be reassuring but only to a limited extent 72.

To overcome the problems in the current body of evidence regarding MPh use and cancer, well-designed prospective cohort studies would be best. However, to date, only one retrospective cohort study involving MPh subscribers has been conducted in Denmark 73. All users of cellular telephones who first subscribed during the period from 1982 through 1995 (420 095 users) were included. Cancer incidence was determined by linkage with the Danish Cancer Registry. The results published in 2001 showed no excesses for cancers of the brain, nervous system, or salivary glands. The risk for these cancers also did not vary by the duration of cellular telephone use, time since first subscription, age at first subscription, or type of cellular telephone (analog or digital). Analysis of brain and nervous system tumors showed no statistically significant standardized incidence ratios for any subtype or anatomic location 73.

In a very recent study published online in June 2011, another Danish study group 74 used two Danish nationwide cohorts: the original cohort of all MPh subscribers in 1982–1995, which was used in the study by Johansen et al.73, and a cohort group in which the association between sociodemographic factors and cancer risk was investigated. The participants included in both cohorts were followed for the occurrence of vestibular schwannoma (a brain tumor) up to 2006 inclusively. It was observed that a long-term MPh subscription of 11 years or more was not related to an increased risk of vestibular schwannoma. However, the authors indicated that because of the usually slow growth of vestibular schwannoma and a possible diagnostic delay, further surveillance is needed.

The results from these cohort studies should be interpreted with caution, as both show obvious methodological shortcomings. The main problem is that they ignored the various exposure parameters related to MPhs, like different phone models, different frequencies, call frequency, and durations (intensity of MPh use in general), use of hands-free devices, whether calls were made from rural or urban locations, etc. Another problem is that the cell phone subscribers identified in the studies through the subscriber lists from the Danish operating companies may not be the primary or the only users of the cell phones.

Kundi 75 summarized the controversy in the studies on brain tumors and MPhs in his review study. He concluded that in most studies, no evidence-based exposure metric was available and the observed duration of MPh use was generally still too low. These problems precluded the detection of reliable risk estimates. Furthermore, in some studies, selection bias, misclassification bias, and effects of the disease on MPh use could have reduced risk estimates, whereas in other studies, recall bias may have led to spuriously increased risks. He reasoned that the overall evidence was in favor of an increased risk, but its magnitude cannot be assessed properly at present.

To date, the body of literature indicating no increased risk of cancer in conjunction with cell phone use is larger and more diverse than the results of existing studies indicating an increased risk of cancer. Nevertheless, in response to public and governmental concern, WHO will conduct a formal risk assessment of all studied health outcomes from RF fields’ exposure by 2012 76.

In addition, the International Agency for Research on Cancer (IARC), a WHO specialized agency, has reviewed the carcinogenic potential of RF fields from MPhs in May 2011 and now considers them ‘possibly carcinogenic to humans (Group 2B).’ The reviewed evidence included exposure data, studies of cancer in humans, studies of cancer in experimental animals, and mechanistic and other relevant data. The press release of the IARC working group indicated that the evidence, while still accumulating, is strong enough to support the 2B classification. This conclusion means that there could be some risk, and that further research is still needed 77.

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Noncancer epidemiological studies

A variety of nonspecific self-reported symptoms (e.g. headache, fatigue, sleep disturbances, dizziness, concentration difficulties, burning and tingling sensations in the skin of the head, and tachycardia) have been suggested to be triggered by exposure to RF fields from MPhs (and sometimes also base stations). Some individuals attribute their health problems to an increased sensitivity to EMFs. The term ‘electromagnetic hypersensitivity’ has been used to describe such cases of nonspecific medically unexplained health problems attributed to EMFs. A number of review studies 78–80 evaluated epidemiological evidence from studies reporting such nonspecific symptoms experienced by MPh users during and after its use. It was generally noted that nearly all of these symptoms can also be attributed to stress and that current research cannot corroborate that these effects are caused by MPh use.

Regarding effects on hearing, a large-scale epidemiological study 81 aiming to assess the effects of chronic exposure (more than 1 year) to MPhs on auditory functions found no significant difference between users and controls for any of the audiologic parameters tested. However, trends for audiologic abnormalities were observed in the group of MPh users with an increase in the duration of MPh use (>4 years), excessive use of MPhs (>60 min/day), and age more than 30 years. The presence of tinnitus or ear warmth during MPh use was also observed in this group. The study concluded that long-term and intensive MPh use could cause inner ear damage.

The same conclusion was reached by an Austrian study group 82 investigating the link between MPh use and tinnitus in a case–control study. It was found that only the subgroup of ipsilateral use for 4 years and longer showed a statistically significant increased risk for MPh use and tinnitus (OR 1.95, 95% CI 1.00–3.80), whereas no such risk was observed among the other subgroups.

Other health effects were investigated in relation to MPh use. A Danish study group 83 conducted a large nationwide cohort study of 420 095 persons whose first cellular telephone subscription was between 1982 and 1995, following them through 2003 for hospitalization for a CNS disorder. The investigated diseases included neurodegenerative diseases like Alzheimer disease, dementia, and Parkinson disease; epilepsy; migraine; and vertigo. Only the standardized hospitalization ratios for migraine and vertigo were significantly increased.

With regard to the effects of MPh use on driving, the findings of experimental studies have been addressed previously 27,53–60. Epidemiological studies also point to a very strong association between cellular telephone use while driving and an increased risk of involvement in road traffic crash accidents.

A Canadian study 84 carried out on two large cohorts of users and nonusers of MPhs reported that the relative risk of all accidents was 38% higher for users of MPhs than for nonusers. The most significant finding was a dose–response relationship between the frequency of MPh use and crash risks. The adjusted relative risks for heavy users were at least two times higher than that for those making minimal use of the MPhs. In another study on college students in the United States 85, it was found that of the 762 reported accidents or near-accidents, 21% involved at least one of the drivers talking on the MPh while driving. Statistical analysis showed that the frequency of calls while driving was strongly related to accidents.

A review by the Royal Society for Prevention of Accidents 86 considered the physical and cognitive distraction by MPhs as the main reasons for the strong association between the use of MPhs during driving and the likelihood of a serious traffic accident. The review study also found no difference between hand-held and hands-free MPhs in terms of the increased risk of accidents.

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Mobile phones and children

Concerns about the potential vulnerability of children to RF fields of MPhs have been raised because of the potentially greater susceptibility of their developing nervous system. In addition, their brain tissue is more conductive than that of adults as it has a higher water content and ion concentration, RF penetration is greater relative to head size, and they have a greater absorption of RF energy in the tissues of the head at mobile telephone frequencies. Besides, although the anatomical development of the nervous system is completed around 2 years of age, functional development continues up to adult age and could be, hypothetically, disturbed by RF fields. Finally, children will have a longer lifetime exposure than adults, considering that the use of MPhs by children and adolescents has been increasing in recent years, with the onset of use starting very early in life 87. Nonetheless, only a few relevant epidemiological or laboratory studies have addressed the possible effects of MPh exposure on children.

In 2005, two double-blind experimental studies 88,89 were published in which children (10–14 years) were exposed to 902 MHz GSM signals, while their cognitive functions were assessed through a number of cognitive tests. Neither study reported any significant differences between the MPh off and on conditions over all tests or in any single test. However, both studies have some experimental weaknesses that restrict their interpretation, such as low exposure, limited statistical power due to the very small number of children involved, and the high variability of the tests of cognitive function.

A more recent cross-sectional study 90 was conducted in Germany to investigate the possible association of exposure to RF fields from MPhs and behavioral problems in 1498 children (8–12 years) and 1524 adolescents (13–17 years). Mental health behavior was assessed using the German version of the Strengths and Difficulties Questionnaire and radiofrequency EMF exposure profiles were also obtained for all participants using a personal dosimeter over 24 h. The results showed that only exposure to RF fields in the highest quartile was significantly associated with overall behavioral problems for adolescents (OR=2.2, 95% CI 1.1–4.5) but not for children (OR=1.3, 95% CI 0.7–2.6). Further analysis of the behavior subgroups showed that the association was the highest in terms of conduct problems for both adolescents (OR=3.7, 95% CI 1.6–8.4) and children (OR=2.9, 95% CI 1.4–5.9) in the highest exposure quartile.

The association of cell phone use during pregnancy and during early childhood with behavioral problems in children was further investigated in two birth cohort groups in Denmark 91,92. Prenatal and postnatal exposure to MPhs was assessed by a questionnaire to mothers, and the behavioral problems in the 7-year-old children were assessed using the Strengths and Difficulties Questionnaire. The results showed positive associations between cell phone use and behavioral problems in young children, even after adjusting for several confounders (in the second study). The highest ORs for behavioral problems were for children who had both prenatal and postnatal exposure to cell phones compared with children not exposed during either time period (OR=1.5, 95% CI 1.4–1.7).

Despite the fact that these studies included a very large number of children (more than 28 000), relying on the mothers’ recall of MPh use during and after pregnancy limits their value due to recall bias. To overcome this problem, questionnaires on cell phone use were administered to the women in the 32nd week of pregnancy in the Spanish cohort study 93 investigating the relationship between the use of MPhs during pregnancy and the mental and psychomotor development of children. The neurodevelopment of their children was later tested at age 14 months using the Bayley Scales of Infant Development. The study reported only small differences in the neurodevelopment scores between the children of cell phone users and nonusers. There was also no observed trend with the amount of cell phone use within the user group.

Although the few studies relevant to children that have been conducted to date do not seem to indicate a substantial increase in risk, a definitive answer to the question of whether children are more at risk from MPhs than adults is not possible and more consistent research is definitely needed.

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Conclusion

The widespread use of MPhs, together with the rise of use and exposure to other wireless technologies and electronic devices that increase the exposure to RFR, has raised the question of possible health effects, mainly effects on brain electrical activity, BBB permeability, cognitive function, hearing, genotoxicity, and various brain diseases including brain tumors.

In this literature survey, 69 research articles (epidemiologic, experimental, cellular, and animal studies), 17 systemic or meta-analysis review studies, and four reports were included. The evidence presented in these peer-reviewed publications did not provide a consistent pattern indicating that exposure to MPhs is detrimental to health. Only studies associating MPh use during driving with road traffic accidents and those investigating EMI with personal or hospital medical electronic devices showed consistent results.

In terms of in-vitro and in-vivo studies, although some of them showed positive findings, in the sense that RFR of MPhs could induce or promote mutagenicity, carcinogenicity, or teratogenicity, the evidence for such low-level genotoxic effects remains very weak. The inconsistency in the findings could generally be attributed to the different exposure metrics used in the different studies. As any effect of MPhs has to depend on the RFR energy absorbed by the biological entity (whether cell culture or living organisms), frequency, radiation intensity, exposure duration, and the number of exposure episodes can affect the response, and these factors can interact with each other to produce different effects.

The review of experimental and provocation studies in humans showed that a large number of studies were carried out to investigate various effects of MPh exposure, mainly cognitive and neurological effects. These studies have the same methodological limitations related to exposure assessment as the in-vitro and in-vivo studies, and also low statistical power, as they are usually conducted on a very limited number of volunteers. Furthermore, they can only assess the effects of short-term exposure, and most studies reporting positive associations between MPhs and health effects have found that only long-term and intense MPh use can be significantly related to adverse effects. As a result, most experimental studies need independent replication with improved methodology before any firm conclusions can be drawn from them.

As regards the epidemiologic evidence on MPh use and the risk of brain and other tumors of the head in adults, it is noted that the scientific evidence has grown in volume, geographic diversity of study settings, and the amount of data on longer-term users. However, some key methodological problems remain, mainly the lack of proper exposure metrics, dose–response relationships, and methods to overcome bias and confounding. Case–control studies in particular have selective nonresponse and inaccuracy and bias in the recall of phone use. Overall, the studies published to date do not demonstrate an increased risk within approximately 10 years of use for any brain tumor. Only a long latency period (more than 10 years) and long-term MPh use have been significantly associated with glioma in some studies. For slower growing tumors such as meningioma and acoustic neuroma, the absence of an association reported thus far does not exclude its possibility, because the observation period has been too short. This argument was probably one of the deciding factors that led the IARC to classify RFR of MPh frequency and power as ‘a possible carcinogen.’

The best way to address the uncertainties of epidemiological studies so far is to carry out a large prospective cohort study of MPh users. One such study (the ‘Cosmos’ study) 94 has already begun recruiting 250 000 men and women aged 18+ years in five European countries: Denmark, Finland, Sweden, The Netherlands, and United Kingdom. MPh users will be followed up for 25 years. Information on MPh use will be collected prospectively through questionnaires and objective data from network operators, and associations with disease risks will be studied by linking cohort members to existing disease registries, whereas changes in symptoms such as headache and sleep quality will be assessed by baseline and follow-up questionnaires.

Regarding children, there are currently little data on cell phone use and health effects, including the risk of cancer, despite the fact that cell phone use by children and adolescents is increasing rapidly. Children could be at a higher risk than adults, as they may be more susceptible to the harmful effects of RFR from MPhs because of their physiological vulnerabilities and because they are likely to accumulate many more years of exposure during their lives than adults or the elderly.

To investigate the relationship between communication technologies including MPhs factors and brain cancer in young people, an international multicenter case–control study ‘MOBI-KIDS’ 95 was initiated in 2009. Over a study period of 5 years, nearly 2000 young people between 10 and 24 years with brain tumors and a similar number of young people without a brain tumor will be invited to participate in the study. Research groups from the following 12 countries are involved in the study: Australia, Austria, Canada, France, Germany, Greece, Israel, Italy, New Zealand, Spain, Taiwan, and The Netherlands. The study is coordinated by the Centre for Research in Environmental Epidemiology in Barcelona, Spain.

Further experimental and epidemiologic studies are needed to seek explanations for the controversies in studies on MPhs so far. These studies should apply sound methodology for exposure assessment of MPh radiation and should focus on the effects of long-term use (more than 10 years). Cohort studies, in particular, should be established to investigate the long-term effects of MPh use on brain cancer and possibly on other diseases, like Alzheimer’s and Parkinson’s disease, as well as to investigate the possible health effects among children. Other areas that merit further research are the possible effects on brain functions and hearing.

In conclusion, as uncertainty regarding the serious health effects of MPhs remains, precautionary measures are best adopted by all concerned parties, namely governments, MPh companies, and the public.

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Acknowledgements

Conflicts of interest

There are no conflicts of interest.

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Keywords:

cell phones; electromagnetic fields; exposure; health effects; mobile phones; radiofrequency fields/radiation; risk

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