The Chernobyl Disaster: Cancer following the Accident at the Chernobyl
Nuclear Power Plant
M. Hatch1, E. Ron1, A. Bouville1, L. Zablotska2, and G. Howe2
1National Cancer Institute, Radiation Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National
Institutes of Health, Department of Health and Human Services, Rockville, MD.
2Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY.
Received for publication March 20, 2005; accepted for publication March 30, 2005.
The Chernobyl nuclear power plant, located in Ukraine
about 130 km north of the capital of Kiev and about 10 km
south of the border with Belarus, was the scene of the most
of unit 4 of the power plant and the roof of the building,
resulting in a series of fires and in massive releases of
radioactive materials into the atmosphere. The releases
consisted of gases, aerosols, and finely fragmented nuclear
fuel particles. From the radiologic point of view, iodine-131
(131I) and cesium-137 (137Cs) are the most important radio-
nuclides to consider (1, 2). During the 10 days of massive
releases, the wind direction changed frequently, so that all
areas surrounding the reactor received some fallout at one
time or another. In addition, rainfall occurred in an irregular
pattern, causing varying degrees of deposition. The releases
of radioactive materials were such that contamination of the
ground was found to some extent in every country in the
Northern Hemisphere (3). However, the most contaminated
areas were in Belarus, Russia, and Ukraine (table 1).
Several categories of people were affected by the
accident: 1) workers, who can be divided into two groups:
a) the approximately 600 persons involved in emergency
measures during the first day of the accident (the so-called
emergency workers), and b) the hundreds of thousands of
people who, from 1986 to 1989, were sent in to the power
station or the zone surrounding it for decontamination work,
sarcophagus construction, and other cleanup operations; this
second group of workers is usually referred to as cleanup
workers or liquidators; and 2) members of the general
public, including a) the evacuees, mainly from the area
within 30 km of the damaged reactor; about 100,000 persons
were evacuated within 2 weeks of the accident and 16,000
more before the autumn of 1986, for a total of 116,000
persons, and b) the approximately 5 million residents of the
contaminated areas in Belarus, Ukraine, and Russia (2).
The most important exposures for emergency workers
were due to external irradiation. Because all of the dosim-
eters worn by the workers were overexposed, they could
not be used to estimate doses. Estimates were obtained by
means of biologic dosimetry for the treated workers.
Short-term health effects
A number of the emergency workers, who dealt with the
fires and other emergency situations within hours of the
accident, developed radiation sickness, that is, health effects
due to massive cell damage and cell death, regarded as a
deterministic event. A total of 134 workers were treated
clinically for radiation sickness (2). Of these, all had bone
marrow symptoms and some demonstrated symptoms related
to other organs such as the intestines, lung, and eye.
The clinical treatment was generally successful for those
who received whole-body doses of less than 4 Gy and was
moderately successful for those who received doses of 4–6
Gy, but the fatality rate for doses above 6 Gy was very high.
Twenty-two workers received whole-body doses of external
irradiation in excess of 4 Gy and 21 workers doses in excess
of 6 Gy, with fatality rates of 32 percent and 95 percent,
respectively (2). The experience gained in terms of clinical
treatment of so many persons with severe radiation sickness
should provide valuable information in the event of future
Correspondence to Dr. Maureen Hatch, Chernobyl Research Unit, Radiation Epidemiology Branch, Division of Cancer Epidemiology and
Genetics, National CancerInstitute, National Institutesof Health, 6120 ExecutiveBoulevard, Rockville, MD 20852 (e-mail: firstname.lastname@example.org).
56 Epidemiol Rev 2005;27:56–66
Copyright ª 2005 by the Johns Hopkins Bloomberg School of Public Health
All rights reserved
Vol. 27, 2005
Printed in U.S.A.
by guest on June 13, 2013
The cleanup workers, sent to the Chernobyl power plant
from 1986 through 1989 to mitigate the consequences of
the accident, received radiation exposures primarily due to
external irradiation from gamma-emitting radionuclides.
The highest doses were received by the cleanup workers,
mostly males aged 20–45 years, who were employed in
1986–1987 in the 30-km exclusion zone. Lower doses were
received by the remainder of the cleanup workers who came
to the reactor site in 1988–1989 (a small number of workers
are still involved).
External doses from gamma radiation.
ternal irradiation have been recorded, to the extent feasible,
in national registries. The national registry data for Belarus,
Russia, and Ukraine, presented in table 2, show that the
number of cleanup workers and the average of the doses
recorded decreased from year to year, with mean doses
of about 0.14 Gy in 1986, 0.09 Gy in 1987, and 0.04 Gy in
1988–1989, in accordance with a decrease in the annual
dose limits for most cleanup workers, from 0.25 Gy in 1986,
to 0.1 Gy in 1987, and to 0.05 Gy from 1988 onward.
Within the framework of epidemiologic studies con-
ducted by the National Cancer Institute and the International
Agency for Research on Cancer, efforts have been made to
develop a time-and-motion method of dose assessment that
would be applicable to all subjects (4). Gamma radiation
levels were measured at various points at the reactor site,
and the dose to theworker was estimated as a function of the
location of work and of time spent there. The results will be
validated by using biodosimetry.
Doses from ex-
shorter-lived radioiodines in the environment of the reactor
during the accident, the cleanup workers on site during the
first few weeks after the accident may also have received
substantial thyroid doses from internal irradiation, since the
thyroid gland concentrates radioiodines. Information on the
thyroid doses is very limited and imprecise, however.
Tentative thyroid dose estimates, based on direct thyroid
than 0.15 Gy, 32.9 percent to 0.15–0.74 Gy, 2.6 percent to
0.75–1.4 Gy, and the remaining 0.5 percent to 1.5–3.0 Gy.
The average thyroid dose estimate is about 0.21 Gy.
Because of the abundance of131I and of
The several hundred thousand cleanup workers, drawn
mainly from Belarus, Ukraine, and the Russian Federation,
the emergency workers described above. For the rest of the
Chernobyl workers, the dose was protracted over days,
concern are the long-term stochastic effects such as cancer
All cleanup workers were eligible to be enrolled in
Chernobyl state registries and received free annual medical
examinations. Although not all cleanup workers were reg-
istered, the state registries have been the basis for nearly all
epidemiology studies that have assessed long-term health
effects. However, the ‘‘official doses’’ contained in the state
registries are missing for many (refer to table 2) and are of
uncertain accuracy and precision for others. Secondly,
diagnostic information in the registries may be of question-
able quality and requires further independent confirmation.
Finally, comparisons with external population rates may be
misleading because the cleanup workers who attend the
medical examinations will all generally be screened much
more frequently than the general population. These limi-
tations should be borne in mind in interpreting epidemio-
logic studies that depend on registry data.
and thyroid cancer, given their short minimal latency period
and sensitivity to radiation. In addition, a few studies of the
occurrence of other cancers have been reported (6, 7).
An early cohort study of Estonian cleanup workers
reported no cases of leukemia occurring among 4,742 men
between 1986 and 1993 (7). However, this study was limited
by small numbers and a relatively short follow-up.
A much larger cohort study among 168,000 Russian
liquidators was reported by Ivanov et al. (8). On the basis
of 48 cases of leukemia through 1993 (including chronic
lymphocytic leukemia, generally believed not to be radio-
sensitive), they found a statistically significant standardized
incidence ratio of 1.77 (95 percent confidence interval: 1.22,
2.47) compared with the Russian population for the period
1990–1995. Before 1990, the standardized incidence ratio
was much lower and was not significant. A statistically
following the 1986 Chernobyl nuclear power plant accidenty
Size of contaminated area (km2)
Contaminated areas* of European countries
* Defined as those in which the137Cs deposition density resulting
from the Chernobyl accident was >37 kBq/m2.
y Adapted from Izrael et al. (90).
The Chernobyl Disaster and Cancer57
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
significant excess relative risk of 4.3 per Gy (95 percent
confidence interval: 0.83, 7.75) was observed in the cohort.
This estimate appeared comparable in magnitude to the
leukemia risk estimate for the survivors of atomic bombings
who were older than 20 years of age at the time of the
bombings (excess relative risk 5 3.70 per Gy, averaged over
In a further study of Russian cleanup workers, Ivanov
et al. (9) studied the occurrence of leukemia in a cohort of
71,870 workers engaged in recovery operations within the
30-km zone between 1986 and 1990 and for whom in-
dividual external radiation dose estimates were available
in the Russian National Medical and Dosimetric Registry.
They observed 58 cases of pathologically confirmed leuke-
mia between 1986 and 1998. After excluding chronic lym-
phocytic leukemia (n 5 16), they obtained a standardized
incidence ratio of 2.5 (90 percent confidence interval: 1.3,
3.7) comparing those who received doses of 150–300 mGy
to those whose doses were below 150 mGy and estimated an
excess relative risk at 1 Gy of 6.7 (90 percent confidence
interval: 0.8, 23.5).
Buzunov et al. (10) studied leukemia occurrence among
approximately 175,000 cleanup workers in Ukraine. They
compared the rates of leukemia for those first employed in
1986 with those for workers employed in 1987, when doses
were lower; they found that the rate of leukemia had
approximately doubled among those who first worked in
1986. However, there was no obvious time trend among
those employed in 1986.
To date, the results of one analytic study—a case-control
study nested within a cohort of cleanup workers—have been
reported (11). A total of 36 nonchronic lymphocytic leuke-
mia cases diagnosed between1986and 1993were compared
with controls (case:control ratio of 1:3). The mean dose for
cases was lower than that for the corresponding controls;
nevertheless, an elevated, nonstatistically significant relative
risk was observed with the highest exposures.
In the study of 4,742 Estonian cleanup workers referred to
above, Inskip et al. (12) did not find an excess of thyroid
cancer 9 years after the accident, and subsequent extended
follow-up of this cohort did not show any increase in the risk
of thyroid cancer up to 16 years after the accident. In an
early study of Russian cleanup workers, Ivanov et al. (8, 13)
did find a suggestion of increased risk of thyroid cancer for
early workers, that is, those on site within several weeks of
the accident who had been exposed to radioactive iodines in
addition to the external radiation to which all workers were
A later follow-up study of Russian cleanup workers by
Ivanov et al. (14) reported on thyroid cancer incidence
among 99,024 workers. A total of 58 thyroid cancers were
registries, following the 1986 Chernobyl nuclear power plant accident*
Distribution of doses from external radiation to cleanup workers, as recorded in national
No. of cleanup
Percentage for whom
dose is known
1986 68,0008 60 5393 138
1987 17,00012 281929 54
19884,000 202011 3193
19892,00016 20 1530 42
1986–1989 91,0009 46 2570 125
198669,000 51 169194 220250
198753,000 7192 92 100208
1988 20,5008334 26 4594
1989 6,000 7332304852
1989 11,0008635 2842 107
* Data are from Cardis et al. (91), Kenigsberg and Kruk (92), and the Ministry of Health of Ukraine (93).
58Hatch et al.
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
detected between 1986 and 1998, which yielded a standard-
ized incidence ratio of 4.33 (95 percent confidence interval:
3.29, 5.60) compared with Russian population rates for men.
There was no significant association with risk of thyroid
cancer when considering internal comparisons within the
lack of data on internal doses and the possibility ofincreased
detection because of the regular medical examinations.
In general, there are very few data related to other
individual cancer risks among cleanup workers. There have
been reports, however, of an increase in all solid cancers
combined occurring among Russian cleanup workers (15,
16). In a cohort of approximately 56,000 such workers, who
received doses of up to 300 mGy, 1,370 cancers were ob-
served between 1991 and 2001 (16). There was a suggestion
of an association with radiation dose that was not significant
either in an internal analysis or in comparison with Russian
population rates. Similar results were obtained in a much
smaller cohort of Russian cleanup workers (15).
the general population, studies of such workers potentially
have greater statistical power to measure effects. The use of
registry-based cohorts offer the best chance for estimating
doses by means of reconstruction techniques and also offer
the potential for determining possible confounders or effect
To date, the available data support a measurable increase
in risk of leukemia among cleanup workers; the evidence
with regard to thyroid cancer is more equivocal, which may
be due to the difficulty in estimating internal doses to the
thyroid among the early emergency workers who potentially
are at the greatest risk. For other solid cancers, little can be
said, presumablybecauseof a longerminimal latencyperiod
and lower risks per dose. It is hoped that future studies of
cleanup workers will clarify information in all these areas.
RESIDENTS OF CONTAMINATED AREAS
of contaminated regions were found to be external exposure
from radionuclides deposited on the ground and internal
exposure resulting from ingesting milk and other foodstuffs
contaminated with131I,134Cs, and137Cs. In the first few
months, because of the significant release of the short-lived
131I,the thyroidwas the mostexposedorgan. The mainroute
of internal exposure for thyroid dose was the pasture-cow-
milk pathway, with a secondary component from inhalation.
After a few months, when131I had decayed away, the most
important contributors to the doses to all organs and tissues
were137Cs and, to a lesser degree,134Cs.
on measurements of external gamma radiation performed by
means of radiation detectors placed against the neck. Within
a few weeks following the accident, approximately 350,000
of these measurements were made in Belarus, Ukraine, and
Russia (17–19). The thyroid dose estimates obtained in this
manner for the approximately 25,000 subjects of two
epidemiologic cohort studies conducted in Belarus and in
Ukraine are presented in table 3 (20); the distribution of
the thyroid doses is similar in the two countries, with me-
dians of about 0.3 Gy and a substantial fraction of doses
exceeding 1 Gy.
For the persons whose exposure was not measured but
who lived in areas where many persons had been measured,
the thyroid doses are reconstructed on the basis of the
statistical distribution of the thyroid doses estimated for the
people for whom measurements are available, together with
knowledge of the dietary habits of the persons considered.
Finally, the thyroid doses for people who lived in areas with
very few or no direct thyroid measurements within a few
weeks after the accident are reconstructed by means of
associations using available data on131I or137Cs deposition,
exposure rates, or concentrations of131I in milk (2). Cata-
logues of thyroid dose estimates are available for the
exposed populations of Belarus, Russia, and Ukraine
(18, 21, 22).
Bone marrow doses.
Bone marrow doses also have been
estimated for the approximately 5 million residents of the
contaminated areas who were not evacuated. Following the
first few weeks of the accident, when131I was the main
contributor, doses relatively homogeneous over all organs
137Cs and134Cs, so the bone marrow doses are generally
assumed to be equal to the whole-body doses. The average
accident are estimated to be about 0.01 Gy (table 4).
The assessment of thyroid doses is based
As described earlier, the principal component of the
massive releases of radioactive materials into the environ-
ment from the Chernobyl accident was131I, which is pri-
marily absorbed by the thyroid gland. Because of the small
subjects according to the geometric mean of their thyroid
doses following the 1986 Chernobyl nuclear power plant
Distribution of the Ukrainian and Belarusian cohort
Relative percentage of subjects
0–0.3 57 43
* Adapted from Likhtarev et al. (20).
The Chernobyl Disaster and Cancer 59
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
size of the gland in children and their high intake of milk,
much of which was contaminated, children generally
received the highest thyroid doses (3, 17).
Thyroid cancer among those exposed in childhood.
thyroid gland in children is especially radiosensitive, and
childhood exposure to relatively low doses of external
radiation (approximately 0.1 Gy) is known to significantly
increase the risk of thyroid tumors (2, 23–25). Thus, one of
the main health concerns related to the Chernobyl disaster
was the risk of developing radiation-related thyroid dis-
eases, particularly neoplasms. Five years after the accident,
the first report of an unusually high occurrence of childhood
thyroid cancer in the contaminated regions of Ukraine was
published (26). Shortly afterward, a high incidence of
thyroid cancer in children also was observed in Belarus
(27–30) and later in the contaminated area of Russia (31,
32). Between 1990 and 1998, it has been estimated that
close to 2,000 thyroid cancers were diagnosed in the
contaminated regions of the three countries (Belarus,
Ukraine, and the Russian Federation) among persons less
than 18 years of age (2). In Belarus, the enormous rise in
pediatric thyroid cancers was especially notable. Compared
with the usual incidence rate of about 1 case per million
children per year, the rate in Belarus was nearly 30 times
higher less than 10 years after the accident (33). Between
1992 and 2000, about 4,000 thyroid cancers were diag-
nosed in the contaminated regions of Belarus, Russia, and
Early on, it was thought that better reporting and
screening might be partly responsible for the large number
of thyroid cancers diagnosed so soon after the accident (35–
37). However, more recent epidemiologic data have dem-
onstrated that the enhanced risk is associated with the
radioiodine exposure (38–50).
While it is now unquestionable that radiation exposure
from the Chernobyl accident has resulted in a substantially
elevated incidence of thyroid cancer among persons ex-
posed at young ages, most studies to date have been de-
scriptive and few have quantified risks or have evaluated
factors that may modify risk. Several ecologic studies have
been conducted in the three countries most affected (39–42,
51). On the basis of collective dose, Jacob et al. (41)
reported a linear dose response for the three countries and
an excess absolute risk per 10,000 person-year-Gy of 2.3
(95 percent confidence interval: 1.4, 3.8). In a later study
(51), performed in Belarus and the Bryansk region of
Russia, results were very similar. The excess absolute risk
per 10,000 person-year-Gy was 2.1 (95 percent confidence
interval: 1.0, 4.5), and the excess relative risk per Gy was 23
(95 percent confidence interval: 8.6, 82). The risk was
statistically significantly elevated even in the lowest dose
group, which received an average of only 0.05 Gy.
The first population-based case-control study of thyroid
thyroid cancer cases and double the number of controls, was
conducted in Belarus (38). This study was unique because it
tried to account for possible ascertainment bias by choosing
one general control group and another control group
comprising persons who had an opportunity to be diagnosed
with thyroid cancer similar to that of the cases. Doses were
calculated based on the mean doses estimated for adults
living in the same villages or towns, taking into account the
strong association between thyroid cancer and estimated
subgroups of controls were used as the comparison popula-
accident, has recently been completed in Russia. It demon-
strated a strong dose response (one-sided p < 0.01) (48).
As has been clearly shown for external radiation (2, 23–
25), the risk of developing thyroid cancer related to
Chernobyl exposure appears to increase with decreasing
age at exposure (33, 42–45, 52–54). Comparing the number
of thyroid cancer cases reported in Belarus and three oblasts
(territorial subdivisions) in Russia with cases in the United
Kingdom, Cardis et al. (55) estimated that the risk for
children less than 1 year of age at the time of the accident
was about five times larger than for those aged 5 years at
exposure, and about 40 times greater than for children aged
10 years at exposure. Other studies have also reported
greater risks for younger children compared with older
children, but the magnitude of the difference was consider-
ably smaller (45). In a new evaluation of time trends in the
exposed regions in Ukraine, the absolute risk for developing
radiation-related thyroid cancer was similar for children
up to age 15 years at the time of the accident (56).
Information is lacking about thyroid cancer risks associ-
ated with in utero exposure. Since, in early childhood, the
thyroid is very sensitive to radiation, the fetus might also be
expected to be extremely vulnerable. However, almost 20
years after the accident, there is little evidence to support the
notion that in utero exposure is particularly dangerous to the
thyroid. On the basis of the finding of only two thyroid
cancers diagnosed before 1999 among persons exposed in
utero, it has been postulated that the thyroid gland of the
fetus is protected by the mother’s physiology (57). Further-
more, the two cases were born a few weeks after the
accident, when they would have received some environ-
mental contamination postnatally. Fetal thyroid risk from
131I has also been examined in 400 subjects from the Utah
fallout study who were exposed in utero (58); no thyroid
(excluding thyroid doses) to populations of areas contaminated
by the Chernobyl nuclear power plant accident (1986–1995)*
Summary of estimated average bone marrow doses
Estimated arithmetic mean
bone marrow dose (mGy)
Russian Federation4 2.56.5
* Information in this table was based on Bennett et al. (94).
60Hatch et al.
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
cancers were found, but benign thyroid disease was
observed. However, before drawing firm conclusions about
the sensitivity of the fetal thyroid, it should be noted that the
power to observe excess risks in persons exposed in utero is
very limited compared with those exposed as children (aged
Thyroid cancer among those exposed as adults.
have been few investigations of radiation-related thyroid
cancer among adults living in the exposed areas (52). Early
on, reports suggested an association between thyroid cancer
and adult exposure in Ukraine (26) and in Russia (13). A
recent dose-response analysis of thyroid cancer in persons
exposed in Bryansk between ages 15 and 69 years found no
association with dose (59). On the basis of the current data,
the role of adult radioiodine exposure in the etiology of
thyroid cancer remains to be clarified. The role of adult
external radiation exposure is equally unclear.
A radiation-associated increase in
thyroid cancer incidence has been shown for both women
and men, with women often having a somewhat higher
excess relative risk (45, 48). It is of note, however, that in
Belarus, there is little evidence of women having a greater
susceptibility than men (39). This difference may be partly
due to thevery early age at diagnosis for many of the thyroid
cancers, that is, at ages when there is little difference in the
sex ratio of spontaneous thyroid cancers.
It has been suggested that radiation exposure in the
presence of iodine deficiency might make people more
susceptible to developing benign thyroid diseases and
thyroid cancer (54, 60). This susceptibility may occur
because the iodine deficiency results in greater radioiodine
uptake and therefore dose, as well as hypothyroidism and
increased thyroid-stimulating hormone. Elevated levels of
thyroid-stimulating hormone are related to thyroid growth
and possibly thyroid cancer (61, 62). In the Bryansk region
of Russia, a twofold risk of childhood thyroid cancer was
observed in highly deficient areas compared with regions
that had normal iodine levels (63).
From the few studies that have reported quantified risks
associated with Chernobyl exposure, the shape of the dose-
response curve, the magnitude of the risks, and the patterns
of modifying effects are consistent with those demonstrated
for external radiation exposure. The excess absolute risks
estimated from ecologic studies (42, 51) were about 50
percent lower than in the pooled analysis of childhood
exposure to external radiation (25), but the differences were
not significant. In contrast, the excess relative risk was about
2.5 times higher than that reported for the pooled analysis,
but again it was not significantly different (42). From these
risk estimates, the authors concluded that the carcinogenic
effectiveness of131I relative to external X- or gamma ra-
diation was less than unity based on an absolute risk model
but above unity based on a relative risk model.
Clinical and molecular features.
molecular features of the thyroid cancers that developed
following Chernobyl are unique. As expected for radiogenic
thyroid cancers, the great majority of the cancers that
occurred in children or young adults were papillary carcino-
mas; however, many had an unusual subtype that has a large
solid component. The thyroid cancers also appeared to grow
Both the clinical and
rapidly and had high rates of local and distant metastasis
(64–67). Although many of the cancers were aggressive,
survival has been excellent. In Belarus, the survival rate was
99 percent for patients diagnosed between 1986 and 2002,
with eight (0.7 percent) patients dying from the thyroid
course of the Chernobyl-related cancers is unusual or
whether some of the findings represent a more general
it occurs in conjunction with iodine deficiency, or very
shortly after radiation exposure (2, 67, 68).
Chernobyl childhood papillary thyroid cancers (69–71). The
PTC3 type is particularly common and has been associated
with the solid variant of papillary cancer. Whether the PTC3
rearrangements are due toradiation exposureor to theyoung
age of the patients or early latency has not yet been
established (67, 72). In a study of 67 Ukrainian patients,
the frequency of rearrangements was about the same for
young thyroid cancer patients whether they were exposed to
Chernobyl or were born after the accident (72). Point
cancers (73, 74); however, unlike RET rearrangements, they
occur most frequently in adult papillary carcinoma and are
infrequent inchildhoodthyroid cancers (72,75,76).Todate,
no radiation ‘‘footprint’’ has been identified, and what once
appeared to be radiation-related mutations may actually be
Although there is still an excess of thyroid
cancers in the territories near Chernobyl, the long-term time
trends are not yet known. Of particular interest is whether
thevery rapid increase in incidence seen 5–10 years after the
accident will continue. When an excess absolute risk model
was used, there was no evidence of a downturn in risk
between 1989 and 1998 (56). Learning more about time
since exposure is important in trying to predict the future
level of risk. Cardis et al. (55) predicted the lifetime number
of thyroid cancers that would develop among children in
Belarus less than age 5 years at the time of the accident.
Depending on what statistical model was used, between
17,710 and 66,198 cases were estimated. The number of
cases predicted is considerably larger than the approxi-
mately 12,000 predicted by Jacob et al. (51) to occur
between 1997 and 2036.
In most assessments, both internal and external exposures
appeared to be especially carcinogenic to the very young
thyroid, and neither type of radiation has been clearly linked
to adult exposure. As observed for external radiation,
females generally have higher risks than males, but the
differences are not statistically significant. A particularly
short latency period has been demonstrated in Chernobyl,
but this finding may be due to the large number of exposed
persons and the early detection resulting from screening
rather than to a true biologic difference. Further follow-up is
needed to learn whether risks persist over time.
Although thyroid cancer was a primary concern in the
aftermath of the Chernobyl accident, attention has also been
The Chernobyl Disaster and Cancer61
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
paid to a potential increased risk of leukemia due to the
exposure to external radiation. Several ecologic studies have
examined this possibility by using comparisons by time
period (pre-/postaccident) or extent of contamination.
Leukemia among those exposed in utero.
mentioned above, there is little evidence concerning thyroid
cancer among those exposed to Chernobyl radiation in
utero, a series of studies have been carried out to examine
leukemia risk in this population, stimulated by an initial
report from Greece, which received some fallout from the
accident (table 1) (77). The Greek study compared rates for
cohorts born during ‘‘exposed’’ and ‘‘unexposed’’ periods
and found a 2.6-fold increase (95 percent confidence
interval: 1.4, 5.1) in leukemia risk among those in utero at
the time of the accident. Elevated rates were also reported
for those born in regions of Greece with higher levels of
radioactive fallout (<6 kBq/m2, 6–10 kBq/m2, >10 kBq/
m2). However, the numbers of cases in each exposure
category were small, and the results were not confirmed
when a similar approach comparing areas with the same
categories of contamination was applied to analyzing data
from the German Childhood Cancer Registry (78).
In a study in Belarus (79), where levels of contamination
less, the highest annual incidence rate was in 1987, the year
after the accident, and although numbers are small and the
95 percent confidence interval: 0.63, 3.61) was found in
the two most contaminated regions of Belarus (Gomel and
A small study published by Noshchenko et al. (80)
compares leukemia incidence during 1986–1996 among
Ukrainian children born in 1986 and thus exposed in utero in
the contaminated oblast of Zhitomir with children born in
Poltava, a supposedly uncontaminated oblast. The reported
risk ratios based on cumulative incidence show significant
increases for all leukemia (rate ratio 5 2.7, 95 percent
confidence interval: 1.9, 3.8) and for acute lymphoblastic
leukemia (rate ratio 5 3.4, 95 percent confidence interval:
1.1, 10.4). The number of total cases was relatively small,
however (21 in Zhitomir, eight in Poltava).
Leukemia among those exposed in childhood.
registry-based studies (81–83) focused on possible risk
among children in Belarus. None of the three studies, each
with a different length of follow-up, reported excess rates of
acute or other types of childhood leukemias in the post-
accident period, either overall or in the most severely
To our knowledge, only one analytic study of childhood
leukemia (84) has been reported. The case-control study
was based in two contaminated oblasts in Ukraine. Cases,
diagnosed between 1987 and 1997, were under age 20 years
at the time of the accident. Controls were randomly selected
from the same oblast as the case and were matched on age at
exposure, gender, and type of settlement (urban, rural).
Although significant results are reported for subgroups in
two time periods—acute leukemias among males who
received doses of more than 10 mGy and were diagnosed
between 1993 and 1997 and acute myeloid leukemia in the
period 1987–1992—the analysis was restricted to a small
subset of the total cases, with no description of how they
One of the largest studies to date is the European
Childhood Leukemia-Lymphoma Incidence Study (ECLIS),
which examined rates of childhood leukemia in Belarus,
Russia, and 33 other regions of Europe in relation to
an estimated region- or country-specific exposure to Cher-
nobyl fallout (85). Estimated doses had been calculated by
the United Nations Scientific Committee on the Effects of
Atomic Radiation (3) using models based on direct mea-
surements carried out in the year after the accident (86).
Rates of childhood leukemia were higher in the postaccident
period, but there was no trend with radiation dose. However,
the study design treating both dose and cancer rates at the
regional or national level had only limited power to detect
a small effect if there were one, given the misclassification
inherent in such a metric.
Leukemia among those exposed as adults.
studies have been conducted examining leukemia incidence
in adult residents of exposed areas. Age-specific leukemia
incidence rates in three contaminated regions of Ukraine
(87) were examined by year of diagnosis, before and after
the accident (through 1990). Increases were seen only in the
age group 65 years or older, suggesting heightened medical
surveillance rather than an effect of exposure.
Time trends were also examined in the Kaluga oblast of
the Russian Federation 10 years postaccident (47). Rate
ratios were similar before and after the accident or steadily
increased with time, and no increase in leukemia occurred in
the most contaminated areas of the oblast. In Ukraine (88),
incidence rates increased postaccident from 5.1 per 100,000
to 11.0 per 100,000, but rates were not higher in the more
To date, the available evidence does not
indicate an effect of Chernobyl fallout on leukemia risk
among residents of contaminated areas exposed either as
children or as adults. The great majority of studies have
relied on available data from registries. Although ecologic
studies do not have much power to detect small effects, if
increases were occurring of the same magnitude as those for
thyroid cancer in children, they would likely have been
picked up by now.
There is a suggestion that leukemia risk may be raised for
persons exposed in utero. The hypothesis that low-dose fetal
irradiation may damage hematopoietic processes may merit
further consideration but primarily on the basis of biologic
assumptions about susceptibility and evidence from external
radiation rather than the results of studies of Chernobyl
fallout, which are conflicting.
Only a few
Scant evidence exists concerning risk of solid tumors,
other than thyroid cancer, among residents of contaminated
areas. What evidence there is is difficult to interpret since
follow-up periods are generally shorter than the latency
periods for these cancers, and the ecologic study designs
used to date have not generally permitted adjustment for
potential confounding variables.
62Hatch et al.
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
One of the series of reports by Ivanov et al. (47) analyzed
time trends and relative population risks among adults in
a contaminated oblast in the Russian Federation. Data came
from a computerized cancer registry, part of the Russian
National Medical and Dosimetric Registry, and included
approximately 10 years of follow-up postaccident. Aver-
age137Cs contamination densities were based on models of
the composition of the fallout and atmospheric transport.
Standardized incidence and mortality ratios were similar
the respiratory organs among women from the contaminated
areas were raised, but the increase was not significant.
Breast cancer is of interest because of its sensitivity to
external radiation and because lactating women receive
higher doses of radioiodines. We know of no descriptive or
analytic studies concerning breast cancer risk in exposed
populations that have been published in peer-reviewed
journals. However, a monograph report (89) has shown an
increase in premenopausal breast cancer in women from
contaminated areas of Ukraine close to Chernobyl compared
ratio 5 1.50, 95 percent confidence interval: 1.27, 1.73).
As the length of time since the accident increases to
almost 20 years, there is interest in pursuing the lead with
respect to breast cancer as well as in examining patterns
with other solid tumors.
Considerationofnoncancer endpointsisbeyondthe scope
of this review. However, research is being conducted in
a number of different areas, including nonmalignant thyroid
outcomes, psychological and cognitive status of children,
and mental health and well-being of the population. AWorld
Health Organizationreportofthe ChernobylForum’sExpert
Group Health summarizes this work (34).
Because of the magnitude and extent of the radioactive
releases and the size of the exposed population, the
Chernobyl accident is a man-made, nuclear disaster of
unparalleled proportions. From the Chernobyl disaster,
however, we have learned a great deal about childhood
exposure to131I. In general, there appears to be much in
common between the role of external and internal radiation
in the development of thyroid cancer. Given all of the
uncertainties in dose estimates, the role of screening in case
ascertainment, and the small numbers for some of the
observations, the magnitude of the excess risks is consistent.
Following either internal or external radiation, the thyroid of
young children is more vulnerable to radiation carcinogen-
esis than that of adults, radiation-related risks may be
somewhat higher for females than males, and excess risks
are still observed 18 years after the accident. Gaps still need
to be filled, however. Of particular interest is whether some
of the findings to date are related to Chernobyl specifically
or to the characteristics of thyroid cancer in very young
children or the very short latency period between radiation
exposure and the development of thyroid cancer. Little is
known about the potential modifying effects of prior thyroid
disease, hormonal and reproductive factors, diet, or ethnic
differences. Finally, because the Chernobyl-related thyroid
cancers are known to be caused by radiation, these cancers
are a unique resource for studying the molecular biology of
radiation- and non-radiation-induced thyroid cancer. This
field is continuing to advance and should increase our
understanding of thyroid cancer in general.
With respect to adults, it appears that although risks of
thyroid cancer and leukemia are not elevated among
residents of contaminated areas, increases in leukemia are
being observed in those exposed to external radiation during
cleanup operations. There is also a suggestion of heightened
risk among those exposed in utero. (Refer to table 5 for
Although we have not covered the topic of disaster
preparedness in this review, the Chernobyl accident has
provided valuable experience in this area, particularly with
regard to the administration of potassium iodide as a pre-
ventive measure. Furthermore, the accidental exposure of
children to radioiodines has generated information that will
be relevant in evaluating the use of131I in treating children
with hyperthyroidism. The opportunity to compare out-
comes in different population subgroups, such as workers or
residents exposed as children or as adults, contributes to our
understanding of dose-response relations and moderating
factors and, in the case of cleanup workers, should provide
input for formulating guidelines to protect the health of
1. NEA. Nuclear Energy Agency. Chernobyl: assessment of
radiological and health impacts. 2002 update of Chernobyl:
ten years on. Paris, France: OECD Publications, 2002.
2. UNSCEAR. United Nations Scientific Committee on the
Effects of Atomic Radiation. Sources and effects of ionizing
radiation. UNSCEAR 2000 report to the General Assembly,
with scientific annexes. New York, NY: United Nations, 2000.
(United Nations sales publication no. E.00.IX.4).
3. UNSCEAR. United Nations Scientific Committee on the
Effects of Atomic Radiation. Sources, effects and risks of
ionizing radiation. 1988 Report to the General Assembly,
and cancer risk following the 1986 nuclear power plant accident
Summary of findings* to date on Chernobyl fallout
Children1 1 1–0
In utero01 ?0
* 1, positive; –, no association; 0, data lacking; ?, equivocal.
The Chernobyl Disaster and Cancer 63
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
with annexes. New York, NY: United Nations, 1988. (United
Nations sales publication no. E.88.IX.7).
4. Bouville A, Chumak VV, Inskip PD, et al. Chornobyl accident:
estimation of radiation doses received by the Baltic and
Ukrainian clean-up workers. Radiat Res (in press).
5. Khrouch VT, Gavrilin YI, Konstantinov YO, et al. Character-
istics of the radionuclides inhalation intake. In: Medical
aspects of the Chernobyl accident at the ChNPP. Proceedings
of the International Conference, Kiev, Ukraine, May 11–13,
1988. Kiev, Ukraine: Zdorovie Publishing House, 1988:76–87.
6. Ivanov VK, Rastopchin EM, Gorsky AI, et al. Cancer incidence
among liquidators of the Chernobyl accident: solid tumors,
1986–1995. Health Phys 1998;74:309–15.
7. Rahu M, Tekkel M, Veidebaum T, et al. The Estonian study
of Chernobyl cleanup workers: II. Incidence of cancer and
mortality. Radiat Res 1997;147:653–7.
8. Ivanov VK, Tsyb AF, Gorsky AI, et al. Leukaemia and thyroid
cancer in emergency workers of the Chernobyl accident:
estimation of radiation risks (1986–1995). Radiat Environ
9. Ivanov VK, Tsyb AF, Gorsky AI, et al. Elevated leukemia rates
in Chernobyl accident liquidators. BMJ, Rapid Responses,
April 15, 2003. (available at www.bmj.bmjjournals.com/cgi/
10. Buzunov V, Omelyanetz N, Strapko N, et al. Chernobyl
NPP accident consequences cleaning up participants in
Ukraine—health status epidemiologic study—main results.
In: Karaoglou A, Desmet G, Kelly GN, et al, eds. The radio-
logical consequences of the Chernobyl accident. Luxembourg,
Belgium: Office for Official Publications of the European
11. Konogorov AP, Ivanov VK, Chekin SY, et al. A case-
control analysis of leukemia in accident emergency workers
of Chernobyl. J Environ Pathol Toxicol Oncol 2000;19:
12. Inskip PD, Hartshorne MF, Tekkel M, et al. Thyroid nodularity
and cancer among Chernobyl cleanup workers from Estonia.
Radiat Res 1997;147:225–35.
13. Ivanov VK, Tsyb AF, Gorsky AI, et al. Thyroid cancer among
‘‘liquidators’’ of the Chernobyl accident. Br J Radiol 1997;
14. Ivanov VK, Tsyb AF, Petrov AV, et al. Thyroid cancer inci-
dence among liquidators of the Chernobyl accident. Absence
of dependence of radiation risks on external radiation dose.
Radiat Environ Biophys 2002;41:195–8.
15. Ivanov V, Ilyin L, Gorski A, et al. Radiation and epidemio-
logical analysis for solid cancer incidence among nuclear
workers who participated in recovery operations following
the accident at the Chernobyl NPP. J Radiat Res (Tokyo)
16. Ivanov VK, Gorski AI, Tsyb AF, et al. Solid cancer incidence
among the Chernobyl emergency workers residing in Russia:
estimation of radiation risks. Radiat Environ Biophys 2004;
17. Gavrilin YI, Khrouch VT, Shinkarev SM, et al. Chernobyl
accident: reconstruction of thyroid dose for inhabitants of
the Republic of Belarus. Health Physics 1999;76:105–18.
18. Likhtarev IL, Kovgan L, Vavilov M, et al. Post-Chornobyl
thyroid cancers in Ukraine. Report 1: estimation of thyroid
doses. Radiat Res 2005;163:125–36.
19. Zvonova IA, Balonov MI. Radioiodine dosimetry and pre-
diction of consequences of thyroid exposure of the Russian
population following the Chernobyl accident. In: Merwin SE,
Balonow MI, eds. Doses to the Soviet population and early
health effects studies. Vol I. Richland, WA: Research Enter-
prises Inc, 1993:71–125.
20. Likhtarev IV, Minenko V, Khrouch VT, et al. Uncertainties in
the thyroid dose reconstruction after Chernobyl. Radiat Prot
21. Balonov MI, Zvonova IA, Bratilova AA, et al. Thyroid dose
reconstruction of radioactive iodine exposure in thyroids of
inhabitants living in settlements of the Russian Federation
that were radioactively contaminated due to the accident at the
Chernobyl NPP in 1986. Moscow, Russia: Russian Ministry
of Public Health, 2001. (Publication MU 22.214.171.1240-00).
22. Kenigsberg JE, Kruk JE. Iodine-131 exposure of thyroid of
Belarus population cancer due to Chernobyl accident. In:
Proceedings of the 2nd International Scientific and Practical
Conference ‘‘Mitigation of the Consequences of the Catas-
trophe at the Chernobyl NPP: State and Perspectives,’’ Gomel,
Belarus, April 26–27, 2004.
23. Shore RE. Issues and epidemiological evidence regarding
radiation-induced thyroid cancer. Radiat Res 1992;131:
24. Thompson D, Mabuchi K, Ron E, et al. Cancer incidence
in atomic bomb survivors. Part II: solid tumors, 1958–87.
Radiat Res 1994;137:S17–S67.
25. Ron E, Lubin J, Shore R, et al. Thyroid cancer after expo-
sure to external radiation: a pooled analysis of seven studies.
Radiat Res 1995;141:259–77.
26. Prisyazhiuk A, Pjatak OA, Buzanov VA, et al. Cancer in the
Ukraine, post-Chernobyl. Lancet 1991;338:1334–5.
27. Kazakov VS, Demidchik EP, Astakhova LN. Thyroid cancer
after Chernobyl. (Letter). Nature 1992;359:21.
28. Baverstock K, Egloff B, Pinchera A, et al. Thyroid cancer
after Chernobyl. (Letter). Nature 1992;359:21–2.
29. Commission of the European Communities (CEC). Thyroid
cancer in children living near Chernobyl. Expert panel re-
port on the consequences of the Chernobyl accident. Brussels,
Belgium: CEC, 1993. (Publication EUR 15248EN).
30. Abelin T, Egger M, Ruchti C. Fallout from Chernobyl. Belarus
increase was probably caused by Chernobyl. (Letter). BMJ
31. Stsjazhko VA, Tsyb AF, Tronko ND, et al. Childhood thy-
roid cancer since accident at Chernobyl. (Letter). BMJ 1995;
32. Tsyb AF, Parshkov EM, Ivanov VK, et al. Disease indices of
thyroid and the dose dependence in children and adolescents
affected as a result of the Chernobyl accident. In: Nagataki S,
ed. Nagasaki Symposium on Chernobyl: update and future.
Amsterdam, the Netherlands: Elsevier Science, 1994:31–46.
33. Williams D. Cancer after nuclear fallout: lessons from the
Chernobyl accident. Nat Rev Cancer 2002;2:543–9.
34. World Health Organization (WHO). Health effects of the
Chernobyl accident: report of the Chernobyl Forum’s Expert
Group ‘‘Health.’’ Geneva, Switzerland: WHO (in press).
35. Ron E, Lubin J, Schneider AB. Thyroid cancer incidence.
(Letter). Nature 1992;360:113.
36. Beral V, Reeves G. Childhood thyroid cancer in Belarus.
(Letter). Nature 1992;359:680–1.
37. Shigematsu I, Thiessen JW. Childhood thyroid cancer in
Belarus. (Letter). Nature 1992;359:681.
38. Astakhova LN, Anspaugh LR, Beebe GW, et al. Chernobyl-
related thyroid cancer in children of Belarus: a case-control
study. Radiat Res 1998;150:349–56.
39. Buglova EE, Kenigsberg JE, Sergeeva NV. Cancer risk
estimation in Belarusian children due to thyroid irradiation
as a consequence of the Chernobyl nuclear accident. Health
64 Hatch et al.
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
40. Sobolev B, Heidenreich WF, Kairo I, et al. Thyroid cancer
incidence in the Ukraine after the Chernobyl accident: com-
parison with spontaneous incidences. Radiat Environ Biophys
41. Jacob P, Goulko G, Heidenreich WF, et al. Thyroid cancer
risk to children calculated. (Letter). Nature 1998;392:31–2.
42. Jacob P, Kenigsberg Y, Goulko G, et al. Thyroid cancer risk
in Belarus after the Chernobyl accident: comparison with
external exposures. Radiat Environ Biophys 2000;1:25–31.
43. Tronko M, Bogdanova T, Komissarenko I, et al. Thyroid
carcinoma in children and adolescents in Ukraine after the
Chernobyl nuclear accident: statistical data and clinico-
morphologic characteristics. Cancer 1999;86:149–56.
44. Tronko ND, Bogdanova TI, Epstein OV, et al. Thyroid
cancer in children and adolescents of Ukraine having been
exposed as a result of the Chernobyl accident (15-year
expertise of investigations). Int J Radiat Med 2002;4:
45. Heidenreich WF, Kenigsberg J, Jacob P, et al. Time trends
of thyroid cancer incidence in Belarus after the Chernobyl
accident. Radiat Res 1999;151:617–25.
46. Kenigsberg J, Buglova E, Kruk J, et al. Thyroid cancer among
children and adolescents of Belarus exposed due to the Cher-
nobyl accident: dose and risk assessment. In: Yamashita S,
Shibata Y, Hoshi M, et al, eds. Chernobyl: message for the 21st
century. Amsterdam, the Netherlands: 2002:293–300. (Inter-
national Congress series 1234).
47. Ivanov VK, Tsyb AF, Nilova EV, et al. Cancer risks in the
Kaluga oblast of the Russian Federation 10 years after the
Chernobyl accident. Radiat Environ Biophys 1997;36:161–7.
48. Davis S, Stepanenko V, Rivkind N, et al. Risk of thyroid
cancer in the Bryansk Oblast of the Russian Federation after
the Chernobyl Power Station accident. Radiat Res 2004;162:
49. Demidchik E, Mrochek A, Demidchik Y, et al. Thyroid cancer
promoted by radiation in young people of Belarus (clinical and
epidemiological features). In: Thomas G, Karaoglou A,
Williams ED, eds. Radiation and thyroid cancer. Singapore:
World Scientific Publishing Co, 1999.
50. Shibata Y, Yamashita S, Masyakin V, et al. 15 years after
Chernobyl: new evidence of thyroid cancer. Lancet 2001;
51. Jacob P, Kenigsberg Y, Zvonova I, et al. Childhood exposure
due to the Chernobyl accident and thyroid cancer risk in
contaminated areas of Belarus and Russia. Br J Cancer 1999;
52. Moysich K, Menezes R, Michalek A. Chernobyl-related ion-
ising radiation exposure and cancer risk: an epidemiological
review. Lancet Oncol 2002;5:269–79.
53. Mahoney MC, Lawvere S, Falkner KL, et al. Thyroid can-
cer incidence trends in Belarus: examining the impact of
Chernobyl. Int J Epidemiol 2004;33:1025–33.
54. Nikiforov Y, Gnepp DR, Fagin JA. Thyroid lesions in
children and adolescents after the Chernobyl disaster:
implications for the study of radiation tumorigenesis. J Clin
Endocrinol Metab 1996;81:9–14.
55. Cardis E, Amoros E, Kesminiene A. Observed and predicted
thyroid cancer incidence following the Chernobyl accident:
evidence for factors influencing susceptibility to radiation
induced thyroid cancer. In: Thomas G, Karaoglou A, Williams
ED, eds. Radiation and thyroid cancer. Singapore: World
Scientific Publishing Co, 1999:395–404.
56. Heidenreich WF, Bogdanova TI, Biryukov AG, et al. Time
trends of thyroid cancer incidence in Ukraine after the
Chernobyl accident. J Radiol Prot 2004;24:283–93.
57. Parshkov EM. Pathogenesis of radiation-induced thyroid
cancer in children affected as a result of the Chernobyl
accident. Int J Radiat Med 1999;3–4:67–75.
58. Lloyd RD, Tripp DA, Kerber RA. Limits of fetal thyroid
risk from radioiodine exposure. Health Physics 1996;70:
59. Ivanov VK, Gorski AI, Maksioutov MA, et al. Thyroid cancer
incidence among adolescents and adults in the Bryansk region
of Russia following the Chernobyl accident. Health Phys
60. Gembicki M, Stozharov AN, Arinchin AN, et al. Iodine
deficiency in Belarusian children as a possible factor stimu-
lating the irradiation of the thyroid gland during the Chernobyl
catastrophe. Environ Health Perspect 1997;105:1487–90.
61. Derwahl M, Broecker M, Karaiem Z. Clinical review 101:
thyrotropin may not be the dominant growth factor in be-
nign and malignant thyroid tumors. J Clin Endocrinol Metab
62. Williams ED. TSH and thyroid cancer. Horm Metab Res
63. Shakhtarin VV, Tsyb AF, Stepanenko VF, et al. Iodine defi-
ciency, radiation dose, and the risk of thyroid cancer among
children and adolescents in the Bryansk region of Russia
following the Chernobyl power station accident. Int J Epi-
64. Farahati J, Demidchik E, Biko J, et al. Inverse association
between age at the time of radiation exposure and extent of
disease in cases of radiation-induced childhood thyroid
carcinoma in Belarus. Cancer 2000;6:1470–6.
65. Nikiforov YE, Gnepp DR. Pediatric thyroid cancer after the
Chernobyl disaster. Pathomorphologic study of 84 cases
(1991–1992) from the Republic of Belarus. Cancer 1994;74:
66. Nikiforov YE, Rowland JM, Bove KE, et al. Distinct pattern of
ret oncogene rearrangements in morphological variants of
radiation-induced and sporadic thyroid papillary carcinomas
in children. Cancer Res 1997;57:1690–4.
67. Williams ED, Abrosimov A, Bogdanova T, et al. Thyroid
carcinoma after Chernobyl latent period, morphology and
aggressiveness. Br J Cancer 2004;90:2219–24.
68. Pacini F, Vorontsova T, Demidchik EP, et al. Post-Chernobyl
thyroid carcinoma in Belarus children and adolescents: com-
parison with naturally occurring thyroid carcinoma in Italy
and France. J Clin Endocrinol Metab 1997;82:3563–9.
69. Klugbauer S, Lengfelder E, Demidchik EP, et al. High preva-
lence of RET rearrangement in thyroid tumors of children
from Belarus after the Chernobyl reactor accident. Oncogene
70. Smida J, Salassidis K, Hieber L, et al. Distinct frequency of
ret rearrangements in papillary thyroid carcinomas of child-
ren and adults from Belarus. Int J Cancer 1999;80:32–8.
71. Thomas GA, Bunnell H, Cook HA, et al. High prevalence of
RET/PTC rearrangements in Ukrainian and Belarusian post-
Chernobyl thyroid papillary carcinomas: a strong correlation
between RET/PTC3 and the solid-follicular variant. J Clin
Endocrinol Metab 1999;84:4232–8.
72. Powell N, Jeremiah S, Morishita M, et al. Frequency of
BRAF T1796A mutation in papillary thyroid carcinoma relates
to age of patient at diagnosis and not to radiation exposure.
J Pathol 2005;205:558–64.
73. Cohen Y, Xing M, Mambo E, et al. BRAF mutation in
papillary thyroid carcinoma. J Natl Cancer Inst 2003;95:
74. Kimura ET, Nikiforova MN, Zhu Z, et al. High prevalence of
BRAF mutations in thyroid cancer: genetic evidence for
The Chernobyl Disaster and Cancer 65
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013
constitutive activation of the RET/PTC-RAS-BRAF signaling Download full-text
pathway in papillary thyroid carcinoma. Cancer Res 2003;63:
75. Kumagai A, Namba H, Saenko VA, et al. Low frequency of
BRAFT1796A mutations in childhood thyroid carcinomas.
J Clin Endocrinol Metab 2004;89:4280–4.
76. Lima J, Trovisco V, Soares P, et al. BRAF mutations are not
a major event in post-Chernobyl childhood thyroid carcino-
mas. J Clin Endocrinol Metab 2004;89:4267–71.
77. Petridou E, Trichopoulos D, Dessypris N, et al. Infant leu-
kaemia after in utero exposure to radiation from Chernobyl.
78. Steiner M, Burkart W, Grosche B, et al. Trends in infant
leukaemia in West Germany in relation to in utero exposure
due to the Chernobyl accident. Radiat Environ Biophys
79. Ivanov EP, Tolochko GV, Shuvaeva LP, et al. Infant leuke-
mia in Belarus after the Chernobyl accident. Radiat Environ
80. Noshchenko AG, Moysich KB, Bondar A, et al. Patterns of
acute leukaemia occurrence among children in the Chernobyl
region. Intl J Epidemiol 2001;30:125–9.
81. Ivanov EP, Tolochko G, Lazarev VS, et al. Child leukaemia
after Chernobyl. (Letter). Nature 1993;365:702.
82. Ivanov EP, Tolochko GV, Shuvaeva LP, et al. Childhood
leukemia in Belarus before and after the Chernobyl accident.
Radiat Environ Biophys 1996;35:75–80.
83. Gapanovich VN, Iaroshevich RF, Shuvaeva LP, et al. Child-
hood leukemia in Belarus before and after the Chernobyl
accident: continued follow-up. Radiat Environ Biophys 2001;
84. Noshchenko AG, Zamostyan PV, Bondar OY, et al.
Radiation-induced leukemia risk among those aged 0–20
at the time of the Chernobyl accident: a case-control study
in the Ukraine. Intl J Cancer 2002;99:609–18.
85. Parkin DM, Clayton D, Black RJ, et al. Childhood leukaemia
in Europe after Chernobyl: 5 year follow-up. Br J Cancer
86. Parkin DM, Cardis E, Masuyer E, et al. Childhood leukaemia
following the Chernobyl accident: the European childhood
leukaemia–lymphoma incidence study (ECLIS). Eur J Cancer
87. Prisyazhiuk A, Pjatak OA, Buzanov VA, et al. Cancer in the
Ukraine, post-Chernobyl. Lancet 1991;338:1334–5.
88. Bebeshko V, Kovalenk A, Bely D, et al. Health effects of the
Chernobyl accident uranium and nuclear energy. Proceedings
of the 20th International Symposium, the Uranium Institute.
London, United Kingdom, September 1995:69–73.
89. Prysyazhnyuk AYe, Gulak LO, Gristchyenko VG, et al. Cancer
incidence in Ukraine after the Chernobyl accident. In:
Chernobyl: message for the 21st century. Proceedings of the
Sixth Chernobyl Sasakawa Medical Cooperation Symposium.
New York, NY: Elsevier, 2002.
90. Izrael YA, De Cort M, Jones AR, et al. The atlas of
caesium-137 contamination of Europe after the Chernobyl
accident. In: Karaoglou A, Desmet G, Kelly GN, et al, eds.
The radiological consequences of the Chernobyl acci-
dent. Proceedings of the First International Conference,
Minsk, Belarus, March 18–22, 1996. (Publication EUR
91. Cardis EL, Anspaugh L, Ivanov VK, et al. Estimated long
term health effects of the Chernobyl accident. In: Proceedings
summing up the consequences of the accident. Vienna,
Austria: International Atomic Energy Agency, 1996:241–79.
92. Kenigsberg JE, Kruk JE. Exposure of Belarus participants of
liquidation of consequences of the Chernobyl accident and
possibilities of revealing of stochastic effects. In: Proceedings
of 2nd International Scientific and Practical Conference
‘‘Mitigation of the Consequences of the Catastrophe at the
Chernobyl NPP: State and Perspectives,’’ Gomel, Belarus,
April 26–27, 2004:62–5.
93. Chernobyl state registry data. Kiev, Ukraine: Ministry of
Health of Ukraine, 1999.
94. Bennett B, Bouville A, Hall P, et al. Chernobyl accident
exposures and effects. Paper T-12-1 in the proceedings of the
10th International Congress of the International Radiation
Protection Association, Hiroshima, Japan, May 14–19, 2000.
66 Hatch et al.
Epidemiol Rev 2005;27:56–66
by guest on June 13, 2013