Effects of Electromagnetic Radiation of Mobile phones on the central nervous system

Effects of Electromagnetic Radiation of Mobile phones on the central nervous system

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Effectsof Electromagnetic Radiationof Mobile Phonesonthe Central NervousSystem

K.-A. Hossmann* and D.M. Hermann

Max-Planck-InstituteforNeurologicalResearch, DepartmentofExperimentalNeurology, Cologne,Germany

With the increasing use of mobile communication, concerns have been expressed about the possible interactions of electromagnetic radiation with the human organism and, in particular, the brain. The effects on neuronal electrical activity, energy metabolism, genomic responses, neurotransmitter balance, blood–brain barrier permeability, cognitive function, sleep, and various brain diseases including brain tumors are reviewed. Most of the reported effects are small as long as the radiation intensity remains in thenonthermal range, and noneof the research reviewed givesan indication of the mechanisms involved at this range. However, health risks may evolve from indirect consequences of mobile telephony, such as the sharply increased incidence rate of traffic accidents caused by telephony during driving, and possibly also by stress reactions which annoyed bystanders may experience when cellular phones are used in public places. These indirect health effects presumably outweigh the direct biological perturbations and should be investigated in more detail in the future. Bioelectromagnetics 24:49–62, 2003. 2002 Wiley-Liss, Inc.

Key words: radio frequency radiation; mobile communication; brain; health risk; review; RF

During recent years, mobile communication systems have experienced wide and rapidly growing use all over the world. Ever since, considerable concerns have been expressed about possible health risks to the human organism and, in particular, the brain. Mobile phones work with carrier frequencies in the mega- and gigaHertzrange.Thesecondgenerationsystems,which are mostly used at present, employ the time division multiple access (TDMA) technique, in which each user hasfullpowerononlyindefinedtimeslots.Intheglobal system for mobile communication (GSM) standard, the carrier signal is pulsed at 217 Hz with bursts of 577 ms pulsewidth, evoking electromagnetic fields both in the radio frequency and in the extremely low frequency (ELF) range. Third generation systems, to which the universal mobile telecommunication system (UMTS) standardbelongs,makeuseofthecodedivisionmultiple access (CDMA) technique, in which all data are continuously transported at the same time, being differentiated by individual codes which are emitted by the transmittersandreceivers.ByusingCMDAandalarger bandwidth (5 MHz instead of 200 kHz), the data transmission rate is considerably increased.

Duetothecloseproximityofthemobiletelephone devicetothehead,thebrainisexposedtorelativelyhigh specific absorption rates (SAR), compared with the rest of the body. The absorption characteristics of mobile telephone handsets havebeen examined with phantoms of the human head[Taki et al., 1996; Kuster et al., 1997; Van Leeuwen et al., 1999; Hurt et al., 2000]. Numerical measurements during normal operation for GSM communication devices in the 900 MHz range have shown that, averaged over any 10 g of tissue, a maximum spatial SAR of 0.525 W/kg is reached in the head, given that the time averaged handset power is 0.25 W [Dimbylow and Mann, 1994; ICNIRP, 1996]. For devices in the 1.8 GHz range, slightly lower peak SAR (0.375 W/kg) are achieved, taking into account a typical average handset power of 0.125 W (DCS system) [Dimbylow and Mann, 1994]. Yet, atypical antennas andoperationconditionsofthetransceiver,forexample, in front of the eye, as well as heterogeneities of energy absorptioninsidetheheadmayleadtohigherlocalSAR


—————— *Correspondence to: K.-A. Hossmann, MD, PhD, Department of Experimental Neurology, Max-Planck-Institute for Neurological Research, Gleueler Str. 50, D-50931 Cologne, Germany. E-mail: hossmann@mpin-koeln.mpg.de

Received for review 8 May 2001; Final revision received 24 June 2002

DOI 10.1002/bem.10068 Published online in Wiley InterScience(w.interscience.wiley.com).

values in the brain tissue. Therefore, some studies suggestthatmaximumspatialSARmaybeupto2W/kg [Dimbylow and Mann, 1994; Burkhardt et al., 1997] or even higher [Bernardi et al., 2000].

Due to the heterogeneous power dissipation the estimated SAR values are influenced by the averaging mass [Hombach et al., 1996], which in different studies varies between 0.1 and 100 g. In European recommendations and standards the averaging mass for the calculationoflocalpeakSARis10g[CENELEC,2001].The ANSI/IEEE standard [IEEE, 1992] specifies averaging over 1 g of tissue. This difference has major biological consequences because, at the same nominal SAR, the local pulse energy absorption may greatly differ, depending on the degree of heterogeneity of the microwave field. Other averaging techniques reported in the literature refer to individual organs (e.g., brain or skin) and, therefore, render it difficult to compare the results from different studies.

Whole body averaged SAR measurements are of importance to predict elevations of the core body temperature. Experimental studies suggest that core bodytemperaturerisessignificantlyatwholebodyaverage SAR above 1–4 W/kg [Elder and Cahill, 1984; Gordon et al., 1986; IEEE, 1992]. At this level, behavioral responses related to thermoregulatory effects (i.e.,changesinbodypostureorlocomotion)areobserved[AdairandAdams,1983;IEEE,1992;UNEP/WHO/ IRPA,1993]. Based on the thermoregulatorythresholds and an additional safety margin, whole body averaged SARof0.4 and0.08W/kgarewidelyacceptedaslimits for occupational and general public exposure, respectively [IRPA/INIRC, 1988; IEEE, 1992; UNEP/WHO/ IRPA, 1993; ICNIRP, 1996; CENELEC, 2001]. These values are well above the whole body absorption rates that are typically induced by cellular phones, but due to the heterogeneity of local energy absorption, focal brainSARmaybemuchhigher.However,mostauthors agree that even in such instances the thermostabilizing effect of brain perfusion prevents temperature increase by more than 0.03–0.198C [Anderson and Joyner, 1995; Van Leeuwen et al., 1999; Wang and Fujiwara, 1999; Bernardi et al., 2000; Wainwright, 2000; Gandhi et al., 2001].

Apart from temperature effects, microwave radiation may produce direct perturbations of the central nervoussystem,asdiscussedinseveralliteraturereviews before[Adey, 1992; Blackman,1994; Lai,1994; Vander Vorst and Duhamel, 1996; Hermann and Hossmann, 1997; McKinlay, 1997; Valberg, 1997; Juutilainen and Deseze, 1998; Repacholi, 1998; Rothman, 2000; Santini et al., 2000]. The present article is an update of an earlier publication [Hermann and Hossmann, 1997] in which the effects of microwave exposure on the electrophysiology, biochemistry, morphology, and neuropathology of the central nervous system have been reviewed with special emphasis on the frequency and intensity ranges used in current mobile communication systems.

At high radiation dose (SAR 6.8–100 W/kg) isolated neurons respond to both continuous and pulsed microwaves (2.45 GHz) with a decrease in spontaneous activity, an increase in membrane conductance, a prolongation of the refractory period following depolarization and a decrease of the survival time [Wachtel et al., 1975;SeamanandWachtel,1978;McReeandWachtel, 1980; Arber and Lin, 1984; Arber and Lin, 1985; McRee and Wachtel, 1986]. In Helix aspersa neurons, the electrophysiological effects are abolished following Ca2þ chelation with EDTA, suggesting that changes in calciumhomeostasismightbe involved [ArberandLin, 1984, 1985].

In another study, in which synaptosomes prepared from rat cerebral cortex were exposed to pulsed 2.8 GHz microwaves, an increase in 32P incorporation into phosphoinositides has been described at mean SAR 10 W/kg but not at lower absorption rates, suggestingathermalstimulationofinositolmetabolism [Gandhi and Ross, 1989]. Since phosphoinositides are involved in the mobilization of calcium from nonmitochondrial storage sites[Berridge and Irvine,1984], increased calcium mobilization could lead to increased calcium efflux rates, as observed in synaptosomes [Lin-Lui and Adey, 1982]. The elevated extracellular calcium concentration might, in turn, stabilize neuronal membranes via surface charge screening, explaining the observed electrophysiological disturbances.

Under constant temperature conditions, exposure of peripheral nerve tissue to continuous and pulsed 2.45 GHz microwaves failed to show any effects on the amplitude and conductionvelocity of compound action potentials over a wide power range [Chou and Guy, 1978]. Only at very high absorption rates (1500 W/kg) was a slight increase of the conduction velocity observed, but this effect also occurred when the temperature of the bathing solution was elevated by just 18C [Chou and Guy, 1978]. In agreement with this observation, continuous microwave exposure (2.45 GHz) at constant tissue temperature did not influence the electrophysiological properties of cultured dorsal root ganglion cells, even when sensitive patch clamp techniques were used [Wang et al., 1991].

Several studies revealed that in vitro microwave effects may be critically affected by ELF amplitude modulation. Acute exposure of chick brain tissue

50 Hossmann and Hermann to microwaves (147 MHz) sinusoidally amplitude modulated at frequencies between 6 and 20 Hz (0.5–2 mW/cm2), led to the release of calcium ions into the extracellular compartment [Bawin et al., 1975; Blackman et al., 1979]. Exposure of avian and feline cultured neuroblastoma cells to amplitude modulated microwaves (147 and 915 MHz/16 Hz, 0.005– 0.05 W/kg) also increased calcium release [Dutta et al., 1984, 1989], but the irradiation of rat brain tissue with square wave (16–32 Hz) modulated 1 and 2.45 GHz (0.3–2.9 W/kg) had no effect when temperature was kept constant [Shelton and Merritt, 1981; Merritt et al., 1982]. Some studies proposed that increased calcium efflux occurs only in certain power density windows [Blackman et al., 1979, 1980; Sheppard et al., 1979; Shelton and Merritt, 1981; Merritt et al., 1982; Dutta et al., 1989], which is difficult to explain by conventional thermodynamics. However, Thompson et al. [2000] proposed a cooperative lattice membrane model which may account for this phenomenon.

Taken together, these investigations suggest that nonthermal microwave exposure affects cellular function mainly at ELF modulation frequencies in the 6–20 Hz range. These frequencies are in the range of EEG activity and may explain that ELF magnetic fields can evoke hippocampal rhythmical theta activity [Bawin et al., 1984, 1986, 1996]. At present, there is not much information available whether higher modulation frequencies used in TDMA and CDMA mobile communication systems might also disturb neuronal function. However, as alterations of calcium efflux have previously been reported in distinct ELF frequency windows up to 510 Hz [Blackman et al., 1988], further studies should be carried out to clarify whether such windows are of relevance also for mobile communication.

Rabbits exposed to electromagnetic fields of 1– 30 MHz (15–60 Hz modulation) at up to 1 kV/m produced a shift of EEG frequency pattern during chronic, but not during acute irradiation [Takashima et al., 1979]. Exposure of rats to continuous microwave radiation (2.45 GHz) for 10 min led to an increase in the total spectral EEG power [Thuroczy et al., 1994]. The increase was noticed only at very high power, i.e., brain averaged SAR of 25 W/kg, but not at 8.4 W/kg, which suggests that thermogenic effects were involved. In a second experiment of the same group, 16 Hz amplitude modulated microwave (4 GHz) increased EEG beta activity already at SAR 8.4 W/kg, [Thuroczy et al., 1994], but as this intensity is still above the thermal threshold, arousal effects cannot be excluded. In a joint project in the USA and the former Soviet Union, EEG power spectra were recorded in rats submitted to continuous 2.45 GHz microwaves for 7 h (whole body SAR 2.7 W/kg) [Mitchell et al., 1989]. Although both groups reported incidences of statistically significant effects, changes did not affect the same frequency bands and, therefore, were considered to be unreliable [Mitchell et al., 1989]. These data suggest that in animal experiments EEG activity changes little as long as microwave exposure remains in the nonthermal range.

In humans, recent studies also agree that spectral powers of conventional EEG bands are not influenced by microwaves emitted by digital mobile phones (900 or 1800 MHz/217 Hz), at least under normal resting conditions [Hietanen et al., 2000; Krause et al., 2000]. This is in contrast to earlier investigations where incrementsinthepowerorsynchronyofhighfrequency bands have been described [Reiser et al., 1995; von Klitzing, 1995].

Interestingly, EEG power spectra may be modulated by microwaves during cognitive processing, i.e., after confrontation with complex memory tasks. Inthisparadigm,anincreaseinthespectralpowerofthe 8–10Hzbandwasrecordedafterexposureto900MHz/ 217 Hz microwaves [Krause et al., 2000]. The alterations of EEG activity were associated with changes in simultaneously measured cognitive response times, suggesting compromise of complex memory functions. Mobile communication may also influence other complex EEG features, such as the spectral hemispheric asymmetry [Vorobyov et al., 1997], EEG coherence [Lebedeva et al., 2000], or reinforcement of spontaneous EEG rhythms [Bawin et al., 1973]. However, further rigorously controlled studies are required to confirm these findings.

Microwave associated modulations of evoked brain activity were mainly investigated in the auditory system. Evoked auditory responses were induced in animals by exposure to 918 MHz or 2.45 GHz microwaves [Taylor and Ashleman, 1974; Seaman and Wachtel, 1978; Chou and Guy, 1979; Chou et al., 1982, 1985; Seaman and Lebowitz, 1989]. In one of these studies, the evoked responses were eliminated after destructionofthecochlea,indicatingthatthispartofthe auditory system was sensitive to microwave exposure [Taylor and Ashleman, 1974].

The response characteristics of neurons in the cochlear nucleus to microwave pulses were similar to the responses to acoustic stimuli [Seaman and Wachtel, 1978; Seaman and Lebowitz, 1989]. Apparently, the incidentenergyperpulseandthepeakpulsepowerwere critical factors influencing evoked auditory responses,

EffectofMobile Phonesonthe Brain 51 with an energy threshold at 0.9–1.8 mJ/g/pulse [Chou et al., 1985]. In contrast, the pulse duration did not seem to have an influence on the evoked auditory response [Chou et al., 1985]. Therefore, evoked responses might be elicited by miniscule pressure waves set up when microwave pulses are converted into thermal energy [Chou et al., 1982, 1985]. It is conceivable that these mechanisms are responsible for the phenomenon of ‘‘microwave hearing’’ [Kellenyi et al., 1999], but the precise interpretation of this phenomenon has to await further analysis.

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