Professional Documents
Culture Documents
Leeka Kheifets, Michael Repacholi, Rick Saunders and Emilie van Deventer
Pediatrics 2005;116;303-313
DOI: 10.1542/peds.2004-2541
The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://www.pediatrics.org/cgi/content/full/116/2/e303
Leeka Kheifets, PhD*; Michael Repacholi, PhD; Rick Saunders, PhD; and Emilie van Deventer, PhD
C
ABSTRACT. In todays world, technologic develop- hildren in both industrialized and developing
ments bring social and economic benefits to large sec- countries are exposed to a large variety of
tions of society; however, the health consequences of environmental agents including indoor and
these developments can be difficult to predict and man- outdoor air pollution, water and food contaminants,
age. With rapid advances in electromagnetic field (EMF) chemicals (eg, pesticides, lead, mercury), and physi-
technologies and communications, children are increas-
ingly exposed to EMFs at earlier and earlier ages. Con-
cal agents such as ultraviolet radiation and excessive
sistent epidemiologic evidence of an association between noise. Changes in exposure to these agents are being
childhood leukemia and exposure to extremely low fre- linked to real or perceived increases in the incidence
quency (ELF) magnetic fields has led to their classifica- of certain childhood diseases, such as asthma, leuke-
tion by the International Agency for Research on Cancer mia, and brain cancer, and in some behavioral and
as a possible human carcinogen. Concerns about the learning disabilities. Environmental exposures can
potential vulnerability of children to radio frequency be particularly harmful to children because of their
(RF) fields have been raised because of the potentially special vulnerability during periods of development
greater susceptibility of their developing nervous sys- before and after birth.
tems; in addition, their brain tissue is more conductive, Exposure to electric and magnetic fields from 0 to
RF penetration is greater relative to head size, and they
will have a longer lifetime of exposure than adults. To
300 GHz has been increasing greatly as countries
evaluate information relevant to childrens sensitivity to increase their capacity to generate and distribute
both ELF and RF EMFs and to identify research needs, electricity and take advantage of the many new tech-
the World Health Organization held an expert workshop nologies, such as telecommunications, to improve
in Istanbul, Turkey, in June 2004. This article is based on lifestyle and work efficiency (Fig 1). Evidence of an
discussions from the workshop and provides back- association between childhood leukemia and expo-
ground information on the development of the embryo, sure to extremely low frequency (ELF) magnetic
fetus, and child, with particular attention to the develop- fields has led to their classification by the Interna-
ing brain; an outline of childhood susceptibility to envi- tional Agency for Research on Cancer (IARC) as a
ronmental toxicants and childhood diseases implicated
possible human carcinogen1 based on consistent
in EMF studies; and a review of childhood exposure to
EMFs. It also includes an assessment of the potential epidemiologic data and lack of support by laboratory
susceptibility of children to EMFs and concludes with a studies in animals and cells. The reason why the
recommendation for additional research and the devel- results of the childhood leukemia studies are consis-
opment of precautionary policies in the face of scientific tent is still being investigated, but one possibility is
uncertainty. Pediatrics 2005;116:e303e313. URL: www. that children may be more sensitive to radiation in
pediatrics.org/cgi/doi/10.1542/peds.2004-2541; children, some or all parts of the electromagnetic spectrum.
environmental risk, policies, sensitive periods, mobile Concerns about the potential vulnerability of chil-
phones, electromagnetic fields, power lines. dren to radio frequency (RF) fields from mobile te-
lephony were first raised by an expert group in the
ABBREVIATIONS. ELF, extremely low frequency; IARC, Interna- United Kingdom2 on the grounds that children have
tional Agency for Research on Cancer; RF, radio frequency; EMF, a longer lifetime of exposure than adults, and from a
electromagnetic field; WHO, World Health Organization; CNS, physiologic point of view, they have a developing
central nervous system; ALL, acute lymphoblastic leukemia;
AML, acute myeloblastic leukemia; SAR, specific absorption rate.
nervous system, their brain tissue is more conductive
than that of adults because it has a higher water
content and ion concentration, and they have greater
absorption of RF energy in the tissues of the head at
From the *Department of Epidemiology, University of California School of mobile telephone frequencies. This topic was dis-
Public Health, Los Angeles, California; and Radiation and Environmental
Health, World Health Organization, Geneva, Switzerland.
cussed further at a European Cooperation in the
Accepted for publication Feb 2, 2005. Field of Scientific and Technical Research (COST) 281
doi:10.1542/peds.2004-2541 workshop,3 in a report of the Health Council of the
The opinions in this paper are the sole responsibility of the authors and do Netherlands,4 and in a recent report from the United
not represent the position of the World Health Organization.
Kingdoms National Radiological Protection Board.5
Conflict of interest: Dr Kheifets worked and consulted for Electric Power
Research Institute and Utilities (Palo Alto, CA), and Dr Saunders worked To evaluate the available information relevant to
for the National Radiation Protection Board (Oxfordshire, United King- childrens sensitivity to electromagnetic fields
dom). (EMFs) and to identify research needs, the World
Address correspondence to Leeka Kheifets, PhD, Department of Epidemi- Health Organization (WHO) held an expert work-
ology, UCLA School of Public Health, 73-284 CHS, 50 Charles E. Young Dr
S, Los Angeles, CA 90095-1772. E-mail: kheifets@ucla.edu
shop in Istanbul, Turkey, in June 2004. This article is
PEDIATRICS (ISSN 0031 4005). Copyright 2005 by the American Acad- based on discussions and recommendations from the
emy of Pediatrics. workshop and provides background information on
the development of the embryo, fetus, and child, ity can vary quite rapidly during the prenatal period,
with particular attention to the developing brain; an whereas slower changes occur postnatally.6
outline of childhood susceptibility to environmental During the first 2 weeks of embryonic develop-
toxicants, childhood diseases implicated in EMF ment (known as the all-or-none period), the em-
studies, and exposure to ELF and RF fields, with a bryo is very sensitive to the lethal effects of toxic
focus on children. After a brief presentation of the agents and much less sensitive to the induction of
EMF science most pertinent to effects on children malformation. Many of the cells are still omnipoten-
and a review of several proposed mechanisms, the tial stem cells, and if the embryo survives a toxic
potential sensitivity of children to EMFs is discussed. exposure it can recuperate without an increased risk
Finally, recommendations are outlined on the pro- of birth defects or growth retardation. During the
tection of children through the development of pre- next 6 to 8 weeks of development, major organogenic
cautionary approaches in the face of scientific uncer- events occur and toxic agents with teratogenic po-
tainty. tential can cause major malformations of the visceral
organs, the CNS, the face, and the limbs. From the
FROM EMBRYO TO ADOLESCENCE 8th to the 15th week, neuron proliferation, differen-
Embryo, Fetal, and Childhood Development tiation, and migration in the CNS are particularly
Development proceeds from conception to adult- vulnerable.7 Genitourinary and other malformations,
hood through a number of different stages in which gonad cell depletion, and neurodevelopmental prob-
the developmental processes are markedly different, lems may occur if the thresholds for these effects are
and their susceptibility to environmental teratogens exceeded. During the late fetal period, effects on
varies. The prenatal period of development is di- growth of the fetus and susceptible organs such as
vided roughly into 3 periods: the preimplantation the CNS diminish, but vulnerability to deleterious
period, extending from fertilization to the settling of effects remains high compared with adults.
the embryo into the uterine wall; a period of orga- Development continues after birth, but now this
nogenesis, characterized by the formation of the process largely entails the maturation of existing or-
main body structures; and the fetal period, during gan systems, although growth is still occurring. Neu-
which growth of the structures already formed takes robiologists long believed that neurogenesis in the
place. Additional developmental changes take place human ends during the first months of postnatal life,
after birth. Postnatal changes are characterized by but recent rodent and primate studies demonstrate
slower growth and maturation of existing organ sys- that there is lifelong neuron production in some
tems, notably the central nervous system (CNS), the parts of the CNS.8 However, with some particular
hemopoietic and immune systems, the endocrine exceptions, most adult neurons are already produced
and reproductive systems, and the skeletal system. by birth. The number of connections (synapses) be-
The completion of sexual development at the end of tween neurons in the human brain peaks at 2 years
the second or the beginning of the third decade of and decreases by 40% to the adult number during
human life marks the completion of this period of adolescence8 as experience is acquired and redun-
growth and maturation. Essentially, however, the dant connections lost. This reflects the balance be-
nature of the toxicant and the timing and magnitude tween the formation of new synapses (synaptogen-
of exposure determine the risk of any adverse effects esis) and synapse elimination, a pruning back of
in terms of both severity and occurrence. Vulnerabil- excess synapses between neurons, which are key
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phologic types are acute lymphoblastic leukemia CNS tumors (0 14 years) vary between developed
(ALL) and acute myeloblastic leukemia (AML). and developing nations, with the higher rates ob-
The rate of leukemia for children 15 years old has served in most Westernized countries reaching 3 per
been estimated to be 4 per 100 000 per year in the 100 000 per year compared with 1 to 2 per 100 000 in
developed world and 2.5 per 100 000 per year in the other parts of the world.19 Over recent decades,
developing world.14 In developed countries, the in- steady rises in the incidence of childhood CNS tu-
cidence of leukemia rises rapidly after birth, peaking mors have been observed in several populations of
at 3 years of age before declining and then rising the United Kingdom, the United States, Japan, and
steadily again throughout life. Thus, unlike many Australia. The debate continues over whether these
cancers, it has a short latency and a peak incidence increases are real or an artifact of improved diag-
early in life15 that has resulted in many etiologic nostic practice and case finding by cancer registries.
hypotheses, most notably those involving exposure The causes of CNS cancers are largely unknown,
to infections.16 although up to 5% may be explained by genetic
Subtypes of AML and ALL are frequently charac- predisposition, associated with disorders such as
terized by genetic alterations, including changes in neurofibromatosis type I.20,21 Having a parent or sib-
chromosome number (hyperdiploidy or hypodip- ling with a CNS tumor also increases the risk. The
loidy) and chromosomal translocations that may in- identification of environmental risk factors for CNS
volve chimeric or fusion genes.17,18 These genes in- tumors has generally been inconsistent.20,21 Again,
clude MLL, TEL, and AML1, all of which can fuse ionizing radiation given in therapeutic doses is one
with many other genes and, in the case of TEL and of the few known risk factors for CNS tumors.
AML1, with each other. There is strong evidence that
this rearrangement may originate in utero, sup- CHILDRENS EXPOSURE TO RF AND ELF FIELDS
ported by data obtained from studies of identical In evaluating the potential role of environmental
twins or children with concordant ALL. Screening of exposures in the development of childhood diseases,
newborn blood samples suggests that 1% have the it is important to consider not only the fact that
TEL-AML1 gene fusion, 100 times the proportion of childhood exposures can be different from exposures
children that will develop ALL with a TEL-AML1 during adulthood but also the fact that they can be
gene fusion before the age of 15 years. This implies highly age dependent. Exposures of interest during
that the conversion of the preleukemic clone to overt the preconception and gestation periods include res-
disease is low and that development of childhood idential and parental exposures to ELF and RF fields,
ALL is a multistep process requiring at least 1 pre- including mothers exposure from use of domestic
natal event in combination with additional prenatal appliances and mobile phones. Infants and toddlers
and/or postnatal events. Although the first hit, the are exposed mostly at home or at day care facilities.
initiating in utero event, is believed to be common, Among preteens, exposure sources expand to in-
the second hit, possibly occurring postnatally, is clude mobile-phone use and sources at school, with
rare and therefore acts as the rate-determining step an increased use of mobile phones in adolescence.
in development of the disease. Here we focus on 2 major exposure scenarios: resi-
As with most other cancers, the mechanism by dential ELF and RF exposures and exposure from
which leukemia arises is likely to involve gene-envi- mobile phones.
ronment interactions, the environmental exposures
being derived from both endogenous and exogenous Residential Exposure
sources. Accordingly, it is important to identify ex- Everyone is exposed to ELF electric and magnetic
posures that either cause DNA damage and induce fields at home.22 High-voltage power lines are a ma-
chromosome breaks that are repaired inadequately jor source of exposure for children who live near
or act as promoters and/or progressers, ultimately them; however, only 1% of children live in close
leading to the overt expression of the disease. Expo- proximity to high-voltage lines. For most children,
sures acting before birth and early in life have long exposure to low-level fields from primary and sec-
been thought to be important determinants of leuke- ondary distribution wiring is continuous; short-du-
mia; it is unfortunate that the evidence regarding the ration and intermittent exposure to higher fields re-
majority of suggested exposures is limited and often sults from proximity to domestic appliances. ELF
contradictory. Ionizing radiation given at large doses exposure also occurs at school, during transport, and
is one of the few known risk factors for leukemia. even during mobile-phone use. Typical average
magnetic fields in homes seem to be 0.05 to 0.1 T.
Brain Cancer Generally, magnetic fields in homes vary from coun-
CNS tumors account for 20% of all malignancies try to country; geometric-mean fields are 35 nT in
in children 15 years old19 but account for 2% of the United Kingdom and 70 nT in the United States.
cancers in adults. CNS cancers in children occur in This difference results from the supply voltage used
tissues of mesodermal or embryonic origin, but in in the United States (110 V) being approximately half
adults they occur in epithelial tissues. Another dif- that used in the United Kingdom (220 V), leading to
ference between childhood and adult tumors is that approximately twice the electric current and mag-
adult tumors tend to occur in the cerebral hemi- netic field exposure. The fraction of homes with av-
spheres, whereas the majority of pediatric tumors are erage fields above certain thresholds likewise varies;
brainstem gliomas. for example, 1% to 2% of homes in the United King-
The international incidence rates of childhood dom and 10% in the United States have fields of 0.2
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nificantly higher internal field strengths and current the scientific literature. They include studies investi-
densities from contact currents than do adults. Dose gating the use of video display terminals, electric
computations using anatomically correct models of blankets, or heated waterbeds, as well as studies of
children30 reveal that modest, imperceptible current parental occupational exposure. Most studies have
into the hand (10 A) produces 50 mV m1 aver- found no effects, but these studies have been limited
aged across the lower-arm marrow of a small child in exposure assessment and lacked the power to
and approximately 130 mV m1 in 5% of that examine high exposure levels. Two studies have in-
tissue. During pregnancy, the magnitude and distri- cluded personal measurements of ELF exposure and
bution of induced electric fields and currents in the reported effects on spontaneous abortion in relation
mother will be different because of changes in body to maximum measured magnetic fields.33,34 The pos-
shape and will not have been assessed in the embryo sibility of exposure assessment bias in these studies
or fetus. These factors, along with differences in di- has been discussed, and results need to be confirmed
electric properties, need to be taken into account in in additional studies before firm conclusions can be
assessing health risks to children from ELF EMFs. drawn.
The guidance cited above was based on a consid- The potential cancer risks to children of exposure
eration of laboratory evidence, including evidence to ELF EMF, estimated from residential proximity to
from volunteer studies of magnetic phosphenes, and power sources and from measured fields, have been
more recently on evidence from voltage-gated ion investigated in relation to in utero and postnatal time
channel and neural-network behavior.29 Neurobe- periods and to paternal exposure. No consistent as-
havioral studies in volunteers and in animals, mostly sociations have been observed for childhood CNS
in adults, have not reported robust responses to ELF tumors.35 One recent study36 found an increased risk
exposure31; overall, any changes seen have been sub- of childhood leukemia with high maternal occupa-
tle, transient, and reversible. Workshop participants tional exposure during pregnancy.
thought that there is no reason to suppose a greater An increased risk of childhood leukemia has been
sensitivity of CNS neural networks and ion channels found to be consistently associated with exposure to
to induced electric fields in children or in the embryo environmental levels of power-frequency magnetic
or fetus. Reduced myelination seen in childhood and fields at levels very much below present guidance.
early adolescence was not thought likely to increase Initial studies used a surrogate for magnetic fields
sensitivity either. It is not clear what the impact (known as wire codes) that was based on distance
would be of an overabundance of synaptic connec- and thickness of power lines near the residence.37 As
tions seen in infants and early childhood, but any instruments became available, the focus shifted to
increased sensitivity was considered to be covered measured or calculated magnetic fields. Results of
by the more restrictive guidance on public exposure. dozens of increasingly sophisticated studies and the
The evidence that induced electric fields might 2 pooled analyses have reported a doubling of risk
affect development of the nervous system and other for children exposed to magnetic fields 0.3 to 0.4
tissue was discussed at the workshop in some detail. T compared with children exposed to fields 0.1
Evidence was presented that endogenous direct-cur- T.38,39 Although a number of factors, including so-
rent electric fields of 10 to 100 V m1 played a role cioeconomic status, have been evaluated as con-
in prenatal development. There is little evidence re- founders, substantial confounding has not been iden-
garding susceptibility to ELF electric fields, although tified. However, because of limited knowledge of the
it was thought that there is no reason to suppose etiology of childhood leukemia, it is difficult to ex-
greater sensitivity. It was noted that the direct-cur- clude the possibility of some yet-to-be-identified con-
rent electric fields were several orders of magnitude founder or of confounding by a combination of fac-
above present guidance values. However, the possi- tors. Nevertheless, substantial confounding of the
ble influence of such fields on synaptogenesis observed association, it seems to us, is unlikely. Al-
and/or synapse elimination is not known. though these results are also not likely to be a result
Results from several independent research groups of chance, bias cannot be ruled out.40 An epidemio-
suggest that exposure to ELF magnetic fields at mi- logically detectable risk of leukemia for children, but
crotesla levels may disturb early development of not for adults, might result from either better expo-
bird embryos. However, replication attempts have sure assessment for children or from greater suscep-
been unsuccessful in some laboratories. Results from tibility in children.
experiments with other nonmammalian experimen- At present there is no experimental evidence that
tal models (fish, sea urchins, and insects) have also supports the view that this relationship is causal;
suggested subtle effects on developmental stability.32 however, few animal studies have been conducted
In mammals, prenatal exposure to ELF magnetic or using animal models of the predominant form of
electric fields does not result in strong adverse effects childhood leukemia, and most carcinogenesis bioas-
on development. Some effects of magnetic (or com- says begin when animals are sexually mature. In
bined electric and magnetic) fields on postnatal de- addition, there is no biophysical explanation for bi-
velopment have been reported, but evaluation of the ologically significant interactions at these low field
consistency of the findings is difficult because of the values, so if the association is causal, then there is
varying methods and approaches used in different currently no scientific explanation. Two hypotheses
studies. for such effects were discussed at the workshop.
Numerous epidemiologic studies of various preg- One hypothesis discussed at the workshop pro-
nancy outcomes in relation to EMFs are available in posed that the association of power-frequency mag-
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ligands such as Ca2 to cell receptor proteins, also All the studies have reported negative results for
resulting in changed receptor function, (3) absorp- carcinogenicity in normal animals at SARs compati-
tion of RF energy by the vibrational states of biolog- ble with mobile telephony,55 although controversy
ical components such as microtubules, (4) enhanced still exists about the carcinogenic effects of RF radi-
attraction between cells (the pearl-chain effect), and ation in a transgenic mouse model.56 Two studies in
(5) demodulation of a modulated RF signal, produc- particular reported the lack of an effect of perinatal
ing ELF electric fields. Generally, it was considered RF exposure, continuing for 24 months, on sponta-
that such interactions are unlikely to be biologically neous and chemically induced brain tumors in
significant at RF levels below guidance values. rats.57,58
In addition, there is evidence concerning RF inter- Several ecological studies5966 have examined can-
actions with magnetite affecting nearby ion channel cer risk, including risk of childhood leukemia,
function by exerting a torque. Possible RF magnetic among populations living in proximity to radio and
field effects include (1) interaction with magnetite television broadcast towers. Often driven by a pre-
particles in biological tissue and (2) radical pair viously identified cluster, these analyses are based
interactions, potentially increasing free-radical con- simply on distance from the source and often include
centrations, thereby leading to an increased risk of an extremely small number of cases. Such studies
oxidative damage. Although these interaction mech- have been uninformative. More rigorous investiga-
anisms are also considered unlikely to be of biolog- tions might be feasible with development of new
ical significance at RF levels below guidance values, instruments capable of capturing personal RF expo-
given the link between free radicals and disease, RF sure.
effects on free-radical concentrations via radical-pair Few relevant epidemiologic or laboratory studies
interactions are considered worth exploring. have addressed the possible effects of RF exposure
For infant, childhood, and adolescent exposure, on children. Because of widespread use of mobile
the maturation of the CNS has been raised as poten- phones among children and adolescents and rela-
tially susceptible. In this context, the major changes tively high exposures to the brain, investigation of
to the CNS during this period comprise a maturation the potential effects of RF fields on the development
of the hard-wiring (namely, increased myelination), of childhood brain tumors is warranted. The impor-
facilitating the transmission of information, which tance of longer lifetime exposure has been empha-
occurs rapidly over the first 2 years but extends into sized by a recent study67 in which acoustic neuroma
the second decade of life, and remodeling of the occurred only after 10-year use of mobile phones.
synaptic connections between neurons8 after the first The type of mobile-phone use among children (eg,
2 years and into adolescence, mostly by synapse text messaging), their potential biological vulnerabil-
elimination as redundant connections are lost. With ity, and longer lifetime exposure make extrapolation
regard to synaptogenesis, spontaneous and stimu- from adult studies problematic. Such scientific un-
lus-evoked electrical activity in the CNS is believed certainty can be addressed through both the applica-
to play a crucial role in local competition between tion of precautionary policies and through additional
growing nerve axons and the distribution of their research.
synaptic boutons on target cells.52 Whether RF fields
could affect these processes is not known. Neurobe- DEVELOPING POLICY FOR CHILDREN AND
havioral studies in volunteers and in animals, mostly PREGNANT WOMEN
adults, have not reported robust responses to RF In todays world, technologic developments bring
exposure, particularly that associated with mobile both social and economic benefits to large sections of
phones.31 society; however, the health consequences of these
Numerous studies have evaluated developmental developments can be difficult to predict and manage.
effects of RF fields on mammals, birds, and other Nevertheless, even if the effects are small, a wide-
nonmammalian species.53,54 These studies have spread exposure can have large public health conse-
shown clearly that RF fields are teratogenic at expo- quences. When risks are complex, an established
sure levels that are high enough to cause significant cause-effect relationship is absent, or the scientific
increases in temperature. There is no consistent evi- findings are not robustly quantifiable, the need for
dence of effects at nonthermal exposure levels, al- timely preventive action makes a precautionary ap-
though only a few studies have evaluated possible proach an essential part of policy making. Many
effects on postnatal development using sensitive end societies believe that this is particularly true regard-
points such as behavioral effects. ing children (including the unborn child): they rep-
Several studies of maternal occupational RF expo- resent the future of the society, have the potential for
sure, primarily to physiotherapists, have reported an longer exposure than adults, and yet are less able to
increased risk of congenital malformations. How- manage their own risk.
ever, no specific type of malformation has been con- International guidance on occupational and public
sistently reported, and there is a potential for recall exposure to EMFs, described above, is based on
bias in these studies. Exposure to the fetus from a avoiding risks to health that are well understood and
mobile phone kept in a pocket, handbag, or belt by for which there is good scientific evidence. However,
the hip when a pregnant woman is using hands-free with regard to childhood exposure to EMFs (and
equipment has been mentioned. Thus far, no studies exposure during pregnancy), several factors argue
are available on pregnancy outcomes related to mo- for the adoption of precautionary measures, includ-
bile telephony. ing the possibility that EMFs might affect children;
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that has been widely adopted at frequencies above simetry. Epidemiology. 1996;7:151155
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ACKNOWLEDGMENTS ing exposure, and predictors for the occurrence of magnetic fields above
background level. Radiat Environ Biophys. 2000;39:233240
The workshop was funded by the World Health Organization, 24. Cardis E, Kilkenny M. International case-control study of adult brain,
Electric Power Research Institute, the European programs EMF- head and neck tumours: results of the feasibility study. Radiat Prot
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We are grateful to all participants of the expert group (see 25. Christensen HC, Schuz J, Kosteljanetz M, Poulsen HS, Thomsen J,
www.who.int/peh-emf/research/rf03/en for a list of invited ex- Johansen C. Cellular telephone use and risk of acoustic neuroma. Am J
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Riti Shimkhada for all organizational aspects. 26. Schuz J. Mobile phone exposures in children. Bioelectromagnetics. 2005;
In press
27. Bohler E, Schuz J. Cellular telephone use among primary school chil-
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Part 1: Static and Extremely Low-Frequency Electric and Magnetic Fields. Guidelines for limiting exposure to time-varying electric, magnetic, and
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The Sensitivity of Children to Electromagnetic Fields
Leeka Kheifets, Michael Repacholi, Rick Saunders and Emilie van Deventer
Pediatrics 2005;116;303-313
DOI: 10.1542/peds.2004-2541
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