RESEARCH
Systematic review on the health effects of exposure to radiofrequency electromagnetic fields from mobile phone base stations
Évaluation systématique des effets sanitaires de l'exposition aux champs électromagnétiques de fréquence radio des stations de base de la téléphonie mobile
Revisión sistemática sobre cómo afecta a la salud la exposición a los campos electromagnéticos de radiofrecuencia de las estaciones base de telefonía móvil
Martin Röösli*; Patrizia Frei; Evelyn Mohler; Kerstin Hug
Swiss Tropical and Public Health Institute and University of Basel, Socinstrasse 59, Basel, CH-4002, Switzerland
ABSTRACT
OBJECTIVE: To review and evaluate the recent literature on the health effects of exposure to mobile phone base station (MPBS) radiation.
METHODS: We performed a systematic review of randomized human trials conducted in laboratory settings and of epidemiological studies that investigated the health effects of MPBS radiation in the everyday environment.
FINDINGS: We included in the analysis 17 articles that met our basic quality criteria: 5 randomized human laboratory trials and 12 epidemiological studies. The majority of the papers (14) examined self-reported non-specific symptoms of ill-health. Most of the randomized trials did not detect any association between MPBS radiation and the development of acute symptoms during or shortly after exposure. The sporadically observed associations did not show a consistent pattern with regard to symptoms or types of exposure. We also found that the more sophisticated the exposure assessment, the less likely it was that an effect would be reported. Studies on health effects other than non-specific symptoms and studies on MPBS exposure in children were scarce.
CONCLUSION: The evidence for a missing relationship between MPBS exposure up to 10 volts per metre and acute symptom development can be considered strong because it is based on randomized, blinded human laboratory trials. At present, there is insufficient data to draw firm conclusions about health effects from long-term low-level exposure typically occurring in the everyday environment.
RESUMÉ
OBJECTIF: Étudier et évaluer la documentation récente sur les effets sur la santé de l'exposition aux radiations des stations de base des téléphones portables.
MÉTHODES: Nous avons réalisé une évaluation systématique des essais aléatoires menés en laboratoire sur des sujets humains et des études épidémiologiques examinant les effets sur la santé des radiations des stations de base de la téléphonie mobile dans l'environnement quotidien.
RÉSULTATS: Nous avons inclus dans l'analyse 17 articles qui répondaient à nos critères de qualité élémentaires : 5 essais aléatoires en laboratoire réalisés sur l'Homme et 12 études épidémiologiques. La majorité des articles (14) examinaient les symptômes non spécifiques autodéclarés d'un mauvais état de santé. La plupart des essais aléatoires ne détectaient aucune association entre les radiations des stations de base des téléphones portables et le développement de symptômes aigus au cours de l'exposition ou peu de temps après. Les associations observées de façon sporadique ne montraient aucun modèle cohérent concernant les symptômes ou les types d'exposition. Nous avons également constaté que plus l'évaluation de l'exposition était sophistiquée, moins la probabilité de signalement d'un effet était importante. Les études sur les effets sanitaires autres que les symptômes non spécifiques et les études sur l'exposition aux stations de base des téléphones portables chez les enfants étaient peu nombreuses.
CONCLUSION: La preuve d'absence de relation entre l'exposition aux stations de base de la téléphonie mobile jusqu'à 10 Volts/mètre et le développement de symptômes aigus peut être considérée comme solide car elle repose sur des essais aléatoires menés sur des sujets humains et à l'aveugle en laboratoire. Actuellement, nous ne disposons pas de données suffisantes pour tirer des conclusions définitives sur les effets sur la santé de l'exposition de faible intensité à long terme qui est présente dans l'environnement quotidien.
RESUMEN
OBJETIVO: Revisar y analizar la bibliografía reciente sobre cómo afecta a la salud la exposición a la radiación de las estaciones base de telefonía móvil (EBTM).
MÉTODOS: Se realizó una revisión sistemática de los ensayos aleatorizados en humanos realizados en laboratorio, así como de los estudios epidemiológicos que investigaron los efectos sobre la salud de la radiación EBTM en el entorno cotidiano.
RESULTADOS: En el análisis se incluyeron 17 artículos que cumplían nuestros criterios básicos de calidad: 5 ensayos de laboratorio aleatorizados y realizados en humanos y 12 estudios epidemiológicos. La mayoría de los artículos (14) examinados informaron sobre síntomas no específicos de enfermedad. La mayoría de los ensayos aleatorizados no detectó relación alguna entre la radiación EBTM y la aparición de síntomas agudos durante o poco después de la exposición. Las asociaciones observadas ocasionalmente no mostraron un patrón homogéneo en lo que respecta a los síntomas o a los tipos de exposición. También observamos que cuanto más compleja era la evaluación de la exposición, menos probable era que se constatara algún efecto. Se han realizado pocos estudios sobre los efectos en la salud más allá de los síntomas no específicos y sobre la exposición de los niños a las EBTM.
CONCLUSIÓN: Los resultados sobre la ausencia de una relación entre la exposición a las EBTM de hasta 10 voltios por metro y la aparición de síntomas agudos se pueden considerar consistentes, ya que se basan en ensayos de laboratorio llevados a cabo en humanos, aleatorizados y enmascarados. En la actualidad no hay datos suficientes para extraer conclusiones en firme acerca de los efectos sobre la salud de la exposición de baja intensidad y a largo plazo en el entorno cotidiano.
Introduction
The introduction in the 1990s of mobile phones using the digital Global System for Mobile Communications (GSM) with bandwidths of 900 and 1800 megahertz and the subsequent introduction of the Universal Mobile Telecommunications System (UMTS) have led to widespread use of this technology and to a substantial increase in the number of mobile phone base stations (MPBS) all over the world. This development has raised public concerns and substantial controversy about the potential health effects of the radiofrequency electromagnetic field emissions of this technology.1-3 A small proportion of the population attributes non-specific symptoms of ill-health, such as sleep disturbances or headache,2,4 to exposure to electromagnetic fields. This phenomenon is described as electromagnetic hypersensitivity or "idiopathic environmental intolerance with attribution to electromagnetic fields."5-8 Additionally, individuals who are hypersensitive to electromagnetic fields often claim to be able to perceive radiofrequency electromagnetic fields in their daily life.6
People are generally exposed to MPBS radiation under far-field conditions, i.e. radiation from a source located at a distance of more than one wavelength. This results in relatively homogenous whole-body exposure. MPBS exposure can occur continuously but the levels are considerably lower than the local maximum levels that occur when someone uses a mobile phone handset.9 A recent study that measured personal exposure to radiofrequency electromagnetic fields in a Swiss population sample demonstrated that the average exposure contribution from MPBSs is relevant for cumulative long-term whole-body exposure to radiofrequency electromagnetic fields. However, as expected, it is of minor importance for cumulative exposure to the head of regular mobile phone users.10(Personal exposure measurements assess the total radiation absorbed by the whole body, whereas spot measurements quantify short-term exposure in a single place, usually the bedroom.)
In 2005, the World Health Organization (WHO) organized a workshop on exposure to radiation from MPBSs and its health consequences and subsequently published a paper summarizing the state of knowledge on the matter.11 At that time, studies about the health impact of MPBS emissions were scarce and of low quality because most of the previous research on the health effects of radiofrequency electromagnetic fields had focused on exposure to mobile phone handsets and on effects related to head exposure, such as brain tumours or changes in brain physiology. In the last four years, research efforts have increased in response to public complaints and to a Dutch study describing decreased well-being associated with UMTS base station exposure.12 Acute effects have been investigated in healthy volunteers and in individuals with hypersensitivity to electromagnetic fields using randomized, blinded laboratory trials and field intervention studies. Further epidemiological research has been stimulated by the recent availability of personal exposure metres. The aim of this paper is to present a systematic review of the scientific literature concerning all the health effects of MPBS radiation that have been investigated to date.
Methods
Literature search
We conducted a systematic search of Medline, EMBASE, ISI Web of Knowledge and the Cochrane Library in March 2009 to identify all relevant peer-reviewed papers published before that date. Key and free-text words included "cellular phone," "cellular," "phone," "mobile" and "mobile phone" in combination with "base station(s)." In addition, we examined references from the specialist databases ELMAR (http://www.elmar.unibas.ch) and EMF-Portal (http://www.emf-portal.de), reference lists in relevant publications and published reports from national electromagnetic field and mobile phone research programmes.
Inclusion and exclusion criteria
We included human laboratory trials and epidemiological studies, and we considered all the health effects that have been addressed so far. These include self-reported non-specific symptoms (e.g. headache, sleep disturbances, concentration difficulties), physiological measures (e.g. hormone levels, brain activity), cognitive functions, genotoxicity, cancer and various chronic diseases. In addition, we included randomized double-blind trials evaluating whether study participants were able to perceive radiofrequency electromagnetic fields. For a study to be eligible, far-field exposure from MPBSs had to be investigated - i.e. a relatively homogenous whole-body field in the GSM 900, GSM 1800 or UMTS frequency range - and the relationship between exposure and outcome had to be statistically quantified. In addition, basic quality criteria had to be fulfilled. Trials had to apply at least two different exposure conditions in a randomized and blinded manner. Epidemiological studies had to quantify exposure using objective measures (such as distance to the nearest MPBS, spot or personal exposure measurements, or modelling), possible confounders had to be considered and the selection of the study population had to be clearly free of bias in terms of exposure and outcomes
Data extraction
The data from each study were extracted independently by two researchers and recorded on one of two standardized forms. These forms, one for randomized trials and one for epidemiological studies, were developed using the CONSORT statement13 for trials and the STROBE statement14 for epidemiological studies. Extracted data included information about study participants, selection procedure, study design, exposure, analytic methods, results and quality aspects. Differences concerning data extraction were resolved by consensus.
Meta-analysis
All reported outcomes were checked for meta-analysis suitability. The only outcome with a sufficient number of comparable studies was the ability to perceive radiofrequency electromagnetic field exposure. To combine these study outcomes, for each study we calculated the difference between the number of observed correct answers (O) and the number of correct answers expected by chance (E), normalized by the number of correct answers expected by chance ([O-E]/E). Exact 95% confidence intervals (CIs) were calculated on the basis of binomial or Poisson data distribution, depending on the experimental design. In the absence of heterogeneity between studies (I2 = 0.0%; P = 0.99), we used fixed-effect models for pooling the study estimates. The detailed method is described in Röösli, 2008.6
Evidence rating
To rate the evidence for detrimental health effects from MPBSs, we assessed the risks of various types of bias for all included studies as proposed by the Cochrane handbook.15 The final evidence rating was obtained according to the Grading of Recommendations Assessment, Development and Evaluation (GRADE) approach.16
Results
Selection of studies
In total, 134 potentially relevant publications were identified; 117 articles were excluded as they did not meet our inclusion criteria (Fig. 1). Of the 17 articles included in the analyses, 5 were randomized trials and 12 were epidemiological or field intervention studies. The majority of the studies examined non-specific symptoms.
Non-specific symptoms of ill-health
Acute effects of MPBS exposure on self-reported non-specific symptoms were investigated in four randomized double-blind human laboratory trials. The details of these studies are summarized in Table 1 (available at: http://www.who.int/bul letin/volumes/88/12/09-071852). Three trials used a UMTS antenna to create controlled exposure circumstances 17, 19, 20 and one study evaluated all three mobile phone frequency bands.18 In total, 282 healthy adults, 40 healthy adolescents and 88 individuals with hypersensitivity to electromagnetic fields were included in these four studies. Exposure levels varied between 0.9 and 10 volts per metre (V/m).
We identified 10 epidemiological studies that investigated the effect of MPBS exposure in terms of self-reported non-specific symptoms (Table 2, avail able at: http://www.who.int/bulletin/volumes/88/12/09-071852). Most of these studies were cross-sectional, and the magnitude of the exposure was based on the distance between place of residence and the nearest MPBS,1,27 or on spot measurements of MPBS radiation in the bedroom,24,35 or on personal measurements of exposure to radiofrequency electromagnetic fields over a 24-hour period.31,39 Four epidemiological studies applied an experimental approach (field intervention) in which exposure was modified either by turning on and off an MPBS28,29 or by using shielding curtains.30,33 Sample size ranged from 43 to 26 039 participants. The cut-off values differentiating exposed from unexposed persons varied between 0.1 and 0.43 V/m.
Of all non-specific symptoms, headache was most often investigated (Table 3). Two epidemiological studies24,27 reported a statistically significant positive correlation between exposure level and headache score. In a Danish laboratory trial, when the data from 40 adults and 40 adolescents were pooled, a larger change in headache score was found under UMTS exposure than under sham exposure.19 However, further analysis indicated that this change was due to a lower baseline score before UMTS exposure rather than to a higher score after exposure. The remaining four epidemiological studies28,31,35,39 and one laboratory trial17 did not indicate any association between MPBS exposure and headache.
With respect to self-reported sleep measures, only an Egyptian study27 reported greater daytime fatigue in exposed individuals. None of the other studies found any association between MPBS exposure and fatigue or self-reported sleep disturbances (Table 4).20,24,29-31,35,39
Many other non-specific symptoms have been evaluated, such as concentration difficulties or dizziness. Generally, no association with exposure was observed (Table 1 and Table 2). One of the few exceptions was a laboratory trial that showed an increased arousal score among individuals with hypersensitivity to electromagnetic fields during UMTS exposure, which might be explained in part by the effect of order of exposure rather than by exposure itself.18 One field intervention study observed a small increase in calmness under unshielded conditions compared with shielded conditions, but no effect on mood or alertness.33 In an observational study from Egypt, several symptoms were more prevalent in 85 inhabitants or employees of a house near an MPBS compared with 80 employees considered unexposed.27 In an Austrian study with 365 participants, a statistically significant association was found between 3 out of 14 symptoms (headache, cold hands and feet, concentration difficulties) and MPBS exposure.24
Some studies evaluated overall symptom scores obtained from standardized questionnaires such as the SF-36 Health Survey,37 the Von Zerssen list25 and the Frick symptom score38 (Table 5). In a survey of 26 039 German residents, the Frick symptom score was significantly elevated for people living less than 500 m from an MPBS compared with those living further away.1 However, subsequent improved dosimetric evaluations in 1326 randomly selected volunteers from this survey did not confirm a relationship between symptoms and measured MPBS radiation.35 Three additional studies also failed to find any association between exposure and symptom scores.17,18,28
In summary, when data from all the randomized trials and epidemiological studies were considered together, no single symptom or symptom pattern was found to be consistently related to exposure. The cross-sectional epidemiological studies, however, showed a noteworthy pattern: studies with crude exposure assessments based on distance showed health effects, whereas studies based on more sophisticated exposure measurements rarely indicated any association.
Field perception
Four randomized double-blind trials addressed the ability to perceive the presence of a radiofrequency electromagnetic field. None of these trials17-20 revealed a correct field detection rate better than expected by chance (Fig. 2) and there was no evidence that individuals who were hypersensitive to electromagnetic fields were more likely to determine correctly the presence or absence of exposure than individuals who were not hypersensitive (P = 0.66). In a German field intervention study,28 a newly installed MPBS on top of an office building was randomly turned on and off over a period of 70 working days, and 95 employees assessed its operation status every evening. The most successful participant achieved 69% correct answers in 42 assessments. The likelihood of achieving a performance score that is good or better by chance is 1% for a given individual, but for one of 95 study participants to have achieved it can be explained by chance alone.
Cognitive functions
Exposure effects on cognitive functions were investigated in three trials17,19,20 and two epidemiological studies.24,27 All three trials investigated the effect of UMTS base station exposure but found no effect in a variety of cognitive tests. One epidemiological study produced inconsistent results,27 whereas the other showed no exposure effects in several cognitive tests.24
Physiological measures
Three laboratory studies investigated different physiological responses. In one trial, no significant changes in blood volume pulse, skin conductance and heart rate were observed in 44 individuals with hypersensitivity to electromagnetic fields or in 115 individuals who were not hypersensitive after exposure to GSM 900, GSM 1800 or UMTS base station fields.18 Likewise, autonomic nervous functions as measured by skin surface temperature, heart rate and local blood flow in the finger tip were not altered by UMTS base station exposure in a Japanese study.20 In a third trial, polysomnographic electroencephalography (EEG) recordings from 13 study participants exposed to a GSM 1800 base station field for two nights did not differ significantly from recordings from two nights of sham exposure (Table 2).41 In two field intervention studies, polysomnographic measures were not related to exposure.29,30
Chronic diseases
We identified no study that investigated an association between chronic diseases other than cancer and MPBS exposure. One observational study addressed the genotoxic effects of MPBS radiation. The investigators compared blood samples from 49 individuals employed by two Belgian mobile phone companies (38 radio field engineers and 11 administrative workers exposed at their workplace to radiofrequency antennas from surrounding buildings) with samples from 25 subjects who were unrelated to the operators, had occupations that excluded exposure to sources of radiofrequency electromagnetic fields and did not use a mobile phone.42 Overall, no differences were found among the three groups in chromosomal aberrations, DNA damage or sister chromatid exchange frequency. There was a tendency towards increased chromatid breaks for field engineers compared with administrative workers and controls.
An ecological study compared the cancer incidence among 177 428 persons living in 48 municipalities in Bavaria between 2002 and 2003 in relation to MPBS coverage.43 Municipalities were classified on a crude three-level exposure scale based on the transmission duration of each MPBS and the proportion of the population living within 400 m of an MPBS. No indication of an overall increase in cancer incidence was found in municipalities belonging to the highest exposure class. The number of cases was too small for tumour-specific analysis.
Discussion
In response to public concerns, most studies dealing with exposure to electromagnetic fields from MPBSs have investigated non-specific symptoms of ill-health, including self-reported sleep disturbances. The majority of these studies have not shown any occurrence of acute symptoms after exposure to GSM 900, GSM 1800 or UMTS fields from MPBSs. The sporadically observed associations in randomized laboratory trials did not show a consistent pattern in terms of symptoms or types of exposure. In our review of epidemiological studies we found that the more sophisticated the exposure assessment, the less likely it was that an effect would be reported. We also found no evidence that individuals who are hypersensitive to electromagnetic fields are more susceptible to MPBS radiation than the rest of the population.
Our findings corroborate previous reviews on exposure to radiofrequency electromagnetic fields and self-reported non-specific symptoms,6,7,11,44,45 while we included several more sophisticated recently published studies. Table 6 (avail able at: http://www.who.int/bulletin/volumes/88/12/09-071852) shows the risks of various types of bias for all studies included in the review. In general, the risk of bias was rare in double-blind randomized trials applying controlled exposure conditions in a laboratory. In epidemiological studies, exposure assessment is a challenge and random exposure misclassification is likely to have occurred in these studies. The corresponding bias probably diluted any exposure-response association, if one existed. None of the studies applied long-term exposure measurements. Cross-sectional studies may reveal effects of prolonged MPBS exposure if the applied measures do in fact represent the exposure level over a longer time period, which was reported to be the case in a Swiss study that measured personal exposure to radiofrequency electromagnetic fields.10 Nevertheless, cross-sectional studies are by design limited in their ability to elucidate causal relationships. For self-reported outcomes, information bias could create spurious exposure-outcome associations if study participants are aware of their exposure status, which is to be expected if exposure is assessed on the basis of distance to a visible transmitter. Selection bias is also of concern, since people who believe that they can feel exposure may be more likely to participate in a study. In fact, objectively measured distance to an MPBS is only weakly correlated with actual exposure from that MPBS.46,47 Interestingly, our review found the strongest symptomatic effects in two studies using measured distance,1,27 which makes these findings arguable as well.
We excluded three epidemiological studies suggesting a link between cancer incidence and proximity to MPBSs48-50 and three studies indicating an association with non-specific symptoms51-53 because they did not fulfil our quality criteria. Data collection48-50 or selection of study participants51 was obviously related to exposure and outcome and therefore biased. Two studies used self-estimated distance, not objective distance, as an exposure measure,52,53 which is problematic because it is likely to introduce bias, especially in combination with self-reported symptoms.
Exposure levels in human laboratory studies varied between 1 and 10 V/m. A homogeneous UMTS field of 1 V/m is estimated to yield an average whole-body specific absorption rate of 6 microwatts per kilogram (µW/kg) and a 1 gram (g) peak specific absorption rate in the brain of 73 µW/kg.17 This is considerably lower than peak specific absorption rates caused by mobile phone handsets (about 1 to 2 W/kg).54 Thus, a finding of acute brain-related effects (e.g. headaches or changes in brain physiology) would be expected in studies of mobile phone handset exposure rather than in studies mimicking MPBS exposure. Studies on mobile phone exposure suggest effects on EEG α-band activity during sleep,55 with some evidence for a dose-response relationship,56 but the results are inconsistent with regard to cognitive functions57 and mostly negative for headache.58,59
Interestingly, persons classified as highly exposed in the epidemiological studies were actually exposed to rather low field levels. Exposure cut-off points for the highest exposed groups were below 0.5 V/m in all studies. This is much lower than the reference levels established by the International Commission on Non-Ionizing Radiation Protection, which range between 41 and 61 V/m for the frequency bands of MPBSs.60 Since population exposure seems to be considerably lower than the reference levels, it is currently difficult to investigate the long-term health effects of exposure close to those levels.
In conclusion, our review does not indicate an association between any health outcome and radiofrequency electromagnetic field exposure from MPBSs at levels typically encountered in people's everyday environment. The evidence that no relationship exists between MPBS exposure and acute symptom development can be considered strong according to the GRADE approach16 because it is based on randomized trials applying controlled exposure conditions in a laboratory. Regarding long-term effects, data are scarce and the evidence for the absence of long-term effects is limited. Moreover, very little information on effects in children and adolescents is available and the question of potential risk for these age groups remains unresolved.
Where data are scarce, the absence of evidence of harm should not necessarily be interpreted as evidence that no harm exists. Further research should focus on long-term effects and should include children and adolescents. Additional cross-sectional studies would be of limited value, so future studies should apply a longitudinal design. Because there is no evidence that potential health effects would be restricted to MPBS frequency bands,9 such studies should include an assessment of exposure to other sources of radiofrequency electromagnetic fields in daily life, such as mobile and cordless phones and wireless local area networks.61
Acknowledgements
Many thanks go to Emilie van Deventer for her helpful feedback on the manuscript draft.
Funding: This review was funded by the World Health Organization. Kerstin Hug is supported by the Swiss Federal Office for the Environment (FOEN), Patrizia Frei and Evelyn Mohler by the Swiss National Science Foundation (Grant 405740-113595). Martin Röösli is supported by the Swiss School of Public Health + (SSPH+).
Competing interests: None declared.
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(Submitted: 10 September 2009 - Revised version received: 6 May 2010 - Accepted: 7 May 2010 - Published online: 5 October 2010)
* Correspondence to Martin Röösli (e-mail: martin.roosli@unibas.ch).