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Risk of Thyroid Cancer among Chernobyl Liquidators

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After the Chernobyl accident in 1986, the "liquidators" or clean-up workers were among those who received the highest radiation doses to the thyroid from external radiation. Some were also exposed to radioiodines through inhalation or ingestion. A collaborative case-control study nested within cohorts of Belarusian, Russian and Baltic liquidators was conducted to evaluate the radiation-induced risk of thyroid cancer. The study included 107 cases and 423 controls. Individual doses to the thyroid from external radiation and from iodine-131 (¹³¹I) were estimated for each subject. Most subjects received low doses (median 69 mGy). A statistically significant dose-response relationship was found with total thyroid dose. The Excess Relative Risk (ERR) per 100 mGy was 0.38 [95% confidence interval (CI): 0.10,1.09]. The risk estimates were similar when doses from ¹³¹I and external radiation were considered separately, although for external radiation the ERR was not statistically significantly elevated. The ERR was similar for micro carcinomas and larger size tumors, and for tumors with and without lymph node involvement. Although recall bias and uncertainties in doses could have affected the magnitude of the risk estimates, the findings of this study contribute to a better characterization the risk of thyroid cancer after radiation exposure in adulthood.
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RADIATION RESEARCH 178, 425–436 (2012)
0033-7587/12 $15.00
Ó2012 by Radiation Research Society.
All rights of reproduction in any form reserved.
DOI: 10.1667/RR2975.1
Risk of Thyroid Cancer among Chernobyl Liquidators
Ausrele Kesminiene,
a,1
Anne-Sophie Evrard,
a,2
Viktor K. Ivanov,
b
Irina V. Malakhova,
c
Juozas Kurtinaitise,
d,3
Aivars Stengrevics,
e
Mare Tekkel,
f
Sergei Chekin,
b
Vladimir Drozdovitch,
a
Yuri Gavrilin,
g
Ivan Golovanov,
g
Viktor P. Kryuchkov,
g
Evaldas Maceika,
h
Anatoly K. Mirkhaidarov,
i
Semion Polyakov,
c
Vanessa Tenet,
a
Aleksandr R. Tukov,
g
Graham Byrnes
a
and Elisabeth Cardis
a,4, 5,6
a
International Agency for Research on Cancer,Lyon,France;
b
Medical Radiological Research Centre of Russian Academy of Medical Sciences
(MRRC RAMC),Obninsk,the Russian Federation;
c
Republican Scientific and Practical Center for Medical Technologies,Informatization,
Administration and Management of Health (RSPC MT),Minsk,Belarus;
d
Institute of Oncology,Vilnius University,Vilnius,Lithuania;
e
Latvian
Centre of Oncology,Riga,Latvia;
f
National Institute for Health Development,Tallinn,Estonia;
g
Federal Medical Biological Agency,Burnasyan
Federal Medical Biophysical Centre,Moscow,the Russian Federation;
h
State Scientific Research Institute Center for Physical Sciences and
Technology, Vilnius, Lithuania;
i
Republican Scientific Centre of Radiation Medicine and Human Ecology, Gomel, Belarus;
Kesminiene, A., Evrard, A-S., Ivanov, V. K., Malakhova, I. V.,
Kurtinaitis, J., Stengrevics, A., Tekkel, M., Chekin, S., Drozdo-
vitch, V., Gavrilin, Y., Golovanov, I., Kryuchkov, V. P., Maceika,
E., Mirkhaidarov, A. K., Polyakov, S., Tenet, V., Tukov, A. R.,
Byrnes, G. and Cardis, E. Risk of Thyroid Cancer among
Chernobyl Liquidators. Radiat. Res. 178, 425–436 (2012).
After the Chernobyl accident in 1986, the ‘‘liquidators’’ or
clean-up workers were among those who received the highest
radiation doses to the thyroid from external radiation. Some
were also exposed to radioiodines through inhalation or
ingestion. A collaborative case-control study nested within
cohorts of Belarusian, Russian and Baltic liquidators was
conducted to evaluate the radiation-induced risk of thyroid
cancer. The study included 107 cases and 423 controls.
Individual doses to the thyroid from external radiation and
from iodine-131 (
131
I) were estimated for each subject. Most
subjects received low doses (median 69 mGy). A statistically
significant dose-response relationship was found with total
thyroid dose. The Excess Relative Risk (ERR) per 100 mGy
was 0.38 [95% confidence interval (CI): 0.10, 1.09]. The risk
estimates were similar when doses from
131
I and external
radiation were considered separately, although for external
radiation the ERR was not statistically significantly elevated.
The ERR was similar for micro carcinomas and larger size
tumors, and for tumors with and without lymph node
involvement. Although recall bias and uncertainties in doses
could have affected the magnitude of the risk estimates, the
findings of this study contribute to a better characterization
the risk of thyroid cancer after radiation exposure in
adulthood. Ó2012 by Radiation Research Society
INTRODUCTION
Over the last 25 years, there have been many reports of
increased incidence of cancer and of other health effects
attributed to the Chernobyl accident (1–4). Until now,
however, only the dramatic increase in thyroid cancer
incidence among those exposed in childhood and adoles-
cence has been clearly demonstrated to be related to
radiation from the accident (1–8) and, more recently, an
increased risk of leukemia and lymphoma among Chernobyl
liquidators (9, 10).
While it is well established that exposure to ionizing
radiation in childhood and adolescence increases the risk of
thyroid cancer, the effects of exposure in adults remains
ambiguous. For external radiation, results from the Japanese
atomic-bomb survivors study suggest that the excess risk of
thyroid cancer after exposure to external radiation at
younger adult ages is smaller than that at age 10 but is
still elevated, especially, if the exposure occurs before age
30 (11, 12). Studies of exposure to
131
I in adults, in cohorts
of patients with therapeutic and diagnostic exposures, have
not provided firm evidence for a radiation-related increase
in thyroid cancer, as previously reviewed [see ref. (13) for a
review].
A possible association between Chernobyl radiation and
risk of thyroid cancer for those exposed as adults was
studied in the residents of highly contaminated areas and in
liquidators (clean-up workers). No dose-response relation-
ship was found in a study that assessed the risk for adults
living in the contaminated areas of the Bryansk region of
Russia (14). An early study conducted in the contaminated
1
Address for correspondence: International Agency for Research
on Cancer, 150 Cours A. Thomas, 69372 Lyon Cedex 08, France; e-
mail: kesminiene@iarc.fr.
2
Current address: Epidemiological Research & Surveillance Unit in
Transport, Occupation and Environment (UMRESTTE), Joint
Research Unit of INRETS (French Research Institute on Transport
& Safety), Claude Bernard University of Lyon, and National Institute
for Public Health Surveillance, Bron, France.
3
Deceased.
4
Current address: Center for Research in Environmental Epidemi-
ology (CREAL), Barcelona, Spain.
5
Municipal Institute of Medical Research (IMIM Hospital del Mar),
Barcelona, Spain.
5
CIBER Epidemiologia y Salud Pu´blica (CIBERESP), Barcelona,
Spain.
425
regions of Ukraine found no relationship between exposure
and increase in thyroid cancer incidence in the exposed
adults (15). More recent analyses of thyroid cancer
incidence rates in Ukraine from 1989 through 2008 showed
some indication of an excess in thyroid cancer cases in
residents of highly contaminated areas who were exposed as
adults, in particular in females (16). These studies, however,
suffer from a number of limitations, including lack of
adequate dosimetry, ecological biases and limitations, and
their findings are difficult to interpret with certainty. Among
liquidators, an increased incidence of thyroid cancer has
been reported in a number of cohorts from Belarus, Russia
and Ukraine (17–19) compared to the general population of
these countries. Most recently, based on a small number of
cases, an increase was also reported in a combined cohort of
liquidators from Estonia and Latvia (20). Because Cher-
nobyl liquidators tend to undergo a more intensive medical
surveillance than the general population (21, 22), it is
unclear whether these increases reflect a real association
related to radiation exposure or an artifact due to a
surveillance bias. In a study of 99,024 liquidators from 6
regions in Russia (23), the risk of thyroid cancer was
evaluated by the level of radiation dose, thus reducing the
impact of a potential surveillance bias. No association
between radiation dose and risk of thyroid cancer was found
in the study in which officially recorded external radiation
dose estimates were used. These dose estimates, however,
are known to be inaccurate (2, 24). Additionally, no
information on dose from other radiation types was
available.
Liquidators were mainly exposed to external penetrating c
radiation. Internal exposure due to ingestion was less
important, though inhaled radioiodines may have contrib-
uted to the dose for a small proportion of those who worked
in the first weeks after the accident. In the first few days
after the accident, dose rates were extremely heterogeneous
and the liquidators who worked on the industrial site of the
Chernobyl nuclear power plant, as well as those who
resided in the most contaminated areas of Belarus, could
have received very high doses (up to several Gy) (2).
We therefore conducted a collaborative study among
liquidators from Belarus, Russia, Estonia, Latvia and
Lithuania with the objective of evaluating more precisely
the relationship between the dose to the adult thyroid from
both external cradiation and internally incorporated
radioiodines and risk of thyroid cancer. A secondary
objective was to assess the role of screening in the observed
increased thyroid cancer incidence among Chernobyl
liquidators.
MATERIALS AND METHODS
Study Design and Collection of Information
The study was designed as a case-control study nested within
cohorts of liquidators who worked on the industrial site and in the
most contaminated areas around the Chernobyl nuclear power plant
between April 26, 1986 and December 31, 1987. As described in
detail elsewhere (9), the study population consisted of approximately
66,000 Belarusian, 65,000 Russian and 15,000 Baltic country
liquidators identified through the national Chernobyl Registries in
Belarus and Russia, and through the rosters of the established Baltic
liquidator cohorts. The cohorts of Baltic liquidators were established
in the 1990s and verified for completeness using several sources (28).
Although there are concerns about the completeness and accuracy of
registration of liquidators in the Chernobyl registries of Belarus and
Russia, and further information should be collected in case-control
studies to verify the status of the liquidators, these registries provide a
reasonable roster for more detailed studies of long-term health effects
of the Chernobyl accident (3).
In the Belarusian cohort and the Russian sub-cohort of professional
radiation workers, the proportion of women liquidators was quite
substantial. Because the background thyroid cancer incidence among
women is higher than among men (25), and because any potential
modifying effect of gender on the radiation-induced thyroid cancer
risk is not very clear (4), we decided to include both men and women
from these cohorts.
The cases were defined as all histologically verified cases of
papillary or follicular carcinoma diagnosed in the study population
during the study period: 1993–1998 for Russia; 1993–2000 for
Belarus; and 1990–2000 for Baltic countries. Cases were ascertained
retrospectively from the national population based cancer registries in
Belarus, Estonia, Latvia and Lithuania (26), and from the National
Medical Dosimetry Registry (NMDR) in Russia. The population-
based cancer registries in Belarus and the Baltic countries have existed
since the 1970s, but individual patient records became available since
the 1980s. The registries contributed cancer incidence data to the
Cancer Incidence in Five Continents starting from volume VI (27).
This facilitated verification of completeness of case ascertainment. In
Russia, a computerized cancer registration system, the National
Medical Dosimetry Cancer sub-registry, was established in the 1990s
for the groups of populations affected by the Chernobyl accident
including liquidators and residents of the most contaminated regions.
It collects personalized information on incident cancer cases among
liquidators (28).
From 1997, shortly after the current study started, prospective case
ascertainment was conducted in Belarus and Russia through the major
endocrinological and/or surgical departments of the oblast (adminis-
trative region) and central hospitals in Minsk (Belarus), St. Petersburg
and Moscow (Russia) where all patients with preliminary diagnosis of
thyroid cancer are referred for confirmation and treatment. Collabo-
ration was established with these treatment institutions for the purpose
of the current study to ensure rapid reporting to the national study
coordinators about newly diagnosed cases of thyroid cancer in
liquidators.
To maximize statistical power, four controls were selected, using a
random number generator from the roster of the study population in
each country (i.e., from the Chernobyl Registries in Belarus and
Russia, and from electronic lists of the established cohorts in Baltic
countries). They were matched on age, sex and region of residence at
the time of the accident in Belarus and Russia, and on age and country
in Baltic countries.
A trained interviewer collected information on the history and
conditions of work as a liquidator (places, dates, duration, protective
means, type of activities and residence) during a face-to-face interview
with the study subject. The detailed questionnaire also contained
questions about demographic factors, history of occupational and
medical radiation exposures, personal and family history of cancer and
of thyroid diseases, smoking and alcohol consumption.
Verification of Diagnoses
An international panel comprised of Belarusian, Russian and
Finnish pathologists reviewed histological slides of the case patients
426 KESMINIENE ET AL.
included in the study. For logistical reasons, slides were not available
for review for 22% of cases. Since the proportion of cases for which
the original diagnosis was contradicted by the international panel was
very small (1%), the main analyses included all of the cases, whether
or not their diagnosis could be verified. Sensitivity analyses were also
conducted and were used to exclude cases with unverified diagnoses.
Radiation Dose Estimation
For each study subject, individual doses to the thyroid were
reconstructed by considering the following pathways of exposure: (1)
external irradiation from c-ray-emitting radionuclides; and (2) internal
irradiation arising from the intake of
131
I via inhalation of
contaminated air or ingestion of contaminated foodstuffs.
To estimate external doses received by the liquidators during their
clean-up missions, a method entitled RADRUE (Realistic Analytical
Dose Reconstruction with Uncertainty Estimation) was developed and
validated by a multinational group of dosimetrists and epidemiologists
(29). Results of exposure rate and nuclide deposition measurements
were embedded in RADRUE and were used to derive exposure-rates
at places where liquidators lived and worked, and thus to calculate
external dose to the thyroid according to the liquidators’ itineraries.
Liquidators’ routes were reconstructed by dosimetry experts familiar
with the organization and conditions of work in the 30-km zone based
on information obtained through the study questionnaire. The method
is described in detail elsewhere (29).
Internal doses to the thyroid due to the intake of
131
I via inhalation
during the period of work as a liquidator were calculated for the six
study subjects who worked on the industrial site during the first 2
weeks after the accident. The approach was based on the
measurements of concentration of
131
I in air in the settlements in the
30-km zone (30). It was assumed that activity of
131
I inhaled by the
liquidators who worked at the Chernobyl NPP site, as well as inside
buildings of the Chernobyl NPP, correlated with the dynamics of
concentration of
131
I at locations close to the Chernobyl NPP. This
approach was validated by measurements of the dose-rate near the
neck taken, April 30, 1986 through May 5, 1986 in a group of 624
early liquidators. For this purpose, values of
131
I activity in the thyroids
were calculated with the approach used in our study and then
compared with those derived from the direct thyroid measurements
taken in 1986. The mean of ratios of those measured to calculated
activities was found to be 0.8 61.1 and the median of ratios was 0.5.
The modeled doses from
131
I inhalation for the study subjects were
then calibrated against the median of ratios of those measured to
calculated
131
I activity in the thyroids of the group of 624 liquidators.
In addition to the dose received during their work, liquidators who
were residents of contaminated settlements of Gomel and Mogilev
oblasts of Belarus and were returning home every evening or after
weekly shift-work may also have received substantial dose to the
thyroid from
131
I through consumption of locally produced contam-
inated milk and/or vegetables, and also from external irradiation from
ground deposits of gamma-ray-emitting radionuclides. For these
liquidators, ‘‘residential’’ doses from
131
I were estimated up to June
20, 1986 and from external irradiation—for the entire period of work
as a liquidator using models previously developed for calculating
average doses to the thyroid in contaminated settlements of Belarus
(31, 32). No information was collected in our study about individual
consumption of milk and leafy vegetables around the time of the
accident. The estimated residential component of the total dose
therefore represents average doses in each subject’s settlement of
residence. Some of the study subjects from Belarus lived in 42
settlements where direct measurements of
131
I activity in the thyroids
of residents were performed in May and early June of 1986. We
compared the residential thyroid doses reconstructed within our study
with the mean thyroid doses in the settlements of residence derived
from direct thyroid activity measurements. The mean of ratios of
thyroid dose from
131
I intake estimated using the model to that
estimated from the direct thyroid measurement was 1.8 61.2 and the
median of ratios was 1.5.
Residential doses were not calculated for Russian and Baltic
liquidators as they were thought to have consumed foodstuffs that
were produced in and imported from uncontaminated areas during
their work in the Chernobyl area, and as levels of
131
I in their original
places of residence were substantially lower than in the most
contaminated districts of the Gomel and Mogilev regions in Belarus.
Intake of short-lived radioactive iodine isotopes was considered to
be negligible for all except one study subject, who started to work on
April 26, 1986 on the industrial site of the Chernobyl nuclear power
plant. For that liquidator thyroid dose was estimated to be mainly due
to the inhalation of
131
I, with a contribution from short-lived
radioiodines and
132
Te [estimated using the approach developed for
the population of the 30-km zone around the Chernobyl nuclear power
plant (32)], not exceeding 35% of the total thyroid dose.
For the purpose of the current study, the total radiation dose to the
thyroid was estimated in mGy as the sum of the doses from external
exposure and from intake of
131
I, short-lived radioiodines, and
132
Te
during their clean-up mission for Russian and Baltic liquidators.
Residential doses from
131
I and external radiation were added for their
Belarusian counterparts.
Uncertainties in radiation dose estimates were evaluated as a part of
the dose reconstruction process. The major sources of errors were
found to be the errors related to the parameters of the dosimetry model
and to the information obtained by questionnaire through the personal
interviews (29). Errors from these sources were characterized and
quantified. By the application of Monte Carlo simulations, a set of
10,000 approximately log-normally distributed dose estimates was
obtained for each subject and for the major dose components (external
dose and residential
131
I dose). The geometric standard deviation
(GSD) of the external doses varied from 1.1 to 5.8 with a median equal
to 1.8, while for the residential doses from
131
I intake GSD varied from
1.9 to 2.5 with a median of 2.0.
The assumption was made that doses from external radiation and
131
I were independent as the approach used to estimate these differed
considerably and because little correlation was found between central
dose estimates from both sources (Pearson correlation coefficient:
0.052. Spearman rank correlation coefficient: 0.035). For Belarusian
liquidators who also received residential doses, shared errors within
the same mission and within the same settlement of residence were
also evaluated, but not across missions or residences.
Consent and Approval
Written informed consent to participate in the study was obtained
from each study subject, as appropriate. The study was approved by
the IARC Ethical Review Committee, the Belarus Coordinating
Council for Studies of the Medical Consequences of the Chernobyl
Accident, the Ethical Committee of the Medical Radiological
Research Centre of the Russian Academy of Medical Sciences,
Obninsk, the Ethical Review Board of the Institute of Oncology,
Vilnius, Lithuania, the Ethical Review Committee of Latvian
Oncology Center, and the Tallinn Medical Research Ethics Commit-
tee. The procedures followed were in accordance with the ethical
standards of the responsible committee on human experimentation
(institutional or regional) and with the Helsinki Declaration of 1975,
as revised in 1983.
Statistical Methods
Data were analyzed by conditional logistic regression using the
PECAN module within the EPICURE software package (33). Two
different risk models were fitted as follows. The primary risk model
used was the linear Excess Relative Risk (ERR) model, which is the
model most commonly used in radiation epidemiology (34). The odds
ratio (OR) at a dose dapproximates the estimate of the relative risk
THYROID CANCER AMONG CHERNOBYL LIQUIDATORS 427
(RR) for rare diseases such as thyroid cancer and is expressed as
OR(d)¼1þbdþcd
2
þ. . . , where band cdenote, respectively, the
slope coefficients of the linear and quadratic dose terms in the model.
Analyses were also carried out with the model most generally used in
occupational and environmental epidemiology (35), the log-linear risk
model, in which the odds ratio at a dose dis expressed as OR(d)¼
exp(bdþcd
2
þ. . . ). As can be seen below, within the range of
doses in the data set, both risk models yielded very similar risk
estimates. However, the ERR model is frequently unstable for the
estimation of relatively small risks associated with relatively low
doses, particularly when the number of subjects is small. Thus,
convergence problems are sometimes encountered in fitting this
model. Consequently, the log-linear risk model was used for the
exploration of interactions, especially when looking at effect
modification.
The main analyses included dose as a continuous variable.
Departures from linearity of risk were explored by fitting polynomial
equations in dose. In addition, departures from a constant relative risk
model were explored by carrying out analyses that addressed the
possible modifying effects of other variables (including country,
gender, age at exposure, time since exposure, attained age and dose-
rate) by the introduction of interaction terms between the factor
considered and the radiation dose in the log-linear risk model. The
statistical significance of model parameters was tested with the
likelihood ratio test. All statistical tests were two-sided.
The effect of potential confounders (including education, occupa-
tion at the time of the Chernobyl accident, organization that sent the
liquidator to Chernobyl and other known or suspected risk factors for
which information was collected in the questionnaire) was tested by
introducing them in the statistical analyses. A factor was taken to be a
confounder of the association between radiation dose and the risk of
thyroid cancer if it modified the OR by 10% or more.
Analyses were also conducted using dose as a categorical variable
in six distinct categories (0, 68.8, 100, 200, 300 and 400 mGy). The
reference category included all subjects whose dose was below the
median of the dose distribution, and the upper categories were chosen
to span the width of this skewed distribution. Estimated odds ratios
and confidence intervals were calculated for the mean of each dose
class.
In the main analyses, we included only the liquidators whose dose
was estimated with RADRUE from the interview completed by the
liquidator himself or by a colleague proxy (these were more accurate
than those completed by a relative proxy). We also excluded from the
main data set four cases (and their respective controls) of medullary
thyroid carcinoma that was considered unlikely to be caused by
radiation and a follicular tumor with an uncertain grade of malignancy
as defined by the International Panel. Sensitivity analyses were
conducted to evaluate the robustness of the findings to these analytical
choices.
Effect of Uncertainties in the Dose Estimates
The dose-response estimate and its confidence limits were estimated
using a maximum likelihood approach incorporating the uncertainty of
the assigned doses. The likelihood for any given set of doses can be
evaluated by standard methods. However, to account for the
uncertainty of the dose estimates it is necessary to integrate over all
possible dose assignments, weighted by their probabilities and given a
hypothetical true dose assignment (36). This process was approxi-
mated by making 10,000 draws from a Bayesian posterior distribution
of the doses, using the Monte Carlo Maximum Likelihood approach
(37, 38). Although the null distribution of the likelihood ratio (LR)
statistic does not necessarily have the standard v
2
distribution, we
conducted simulations to validate the process for the range of doses in
the present study. The central estimate of the dose-response was then
obtained by maximizing this Monte Carlo likelihood with respect to
the dose-response parameters. Conceptually, this is the same as in
standard maximum likelihood estimation, although the numerical
computation is somewhat more involved. The confidence set is
defined as all dose-response curves that would not be rejected as a
significantly worse fit than the maximum likelihood estimate, using
the LR test. We identified the upper and lower envelope of a sample of
these curves as the confidence set boundaries.
RESULTS
Descriptive Analyses
A total of 127 eligible case patients were ascertained
retrospectively and prospectively. Four cases were diag-
nosed with medullary carcinoma and 122 as papillary
carcinomas. For the remaining case, the International Panel
of pathologists suspected a diagnosis of follicular carcino-
ma, but could not confirm this with certainty due to poor
quality of pathological material. As explained above, this
case and the four cases of medullary carcinoma and their
controls were excluded from the main analyses.
Ten case patients or proxies of deceased patients refused
to participate in the study; two patients could not be traced
and interviewed. Participation rates were generally high
among cases—78% in Baltic countries, 94% in Russia, 89%
in Belarus and were somewhat lower among controls—65%
in Baltic countries, 91% in Russia and 82% in Belarus.
Overall, 107 case patients and 423 control subjects were
included in the study after exclusion of 3 deceased cases
whose dose was estimated based on the interview completed
by a relative less familiar with the liquidator’s work in
Chernobyl than would have been a proxy who was a
colleague. The majority of case patients (85) were from
Belarus, the rest (15 and 7, respectively) were from Russia
and the Baltic countries (Table 1).
Overall, the median age at the moment of first exposure
was 37 years old and at the time of diagnosis was 45 years
old (Table 1). There were more cases diagnosed with
thyroid cancer at 50 years old and older in the more recent
period (after 1996) compared to the earlier period.
Belarusian study subjects differed substantially from the
Russian and Baltic subjects (Table 2). The proportions of
men (53%) and women (47%) were similar in Belarus,
while most liquidators in Russia (94%), and all liquidators
in Baltic countries were men. Ninety percent of Belarus
liquidators were sent on clean-up missions by civilian
organizations (while Russian and Baltic liquidators were
mainly military reservists), 39% did not work in the 30-km
zone (5% and 3%, respectively, among Russians and Baltic
liquidators), only 2.1% reported having worked on the
industrial site of the Chernobyl power plant (68% and 73%,
respectively, among Russians and Baltic liquidators), and
23% were sent on two missions or more (only one Russian
case patient had more than one mission). Only 6% of
Russian liquidators started work before May 10, 1986,
compared to 35% in Belarus and 15% in Baltic countries.
No difference in the distribution of date of start of mission
between cases and controls was seen, although in all
428 KESMINIENE ET AL.
countries the median date of start of case patients was earlier
than that of controls (Table 2). The median number of
working days for all missions was shorter (Table 2) in
Belarus than elsewhere (21.5 days in Belarus, 61.0 in Russia
and 75.0 in Baltic countries). Case patients and controls did
not differ notably in median number of working days,
except in the Baltic countries where controls tended to have
more active days (days spent in the Chernobyl zone
excluding resting periods) (median: 83.0) than case patients
(median: 65.0).
No differences in the distribution of the potentially
confounding factors, such as education level, family status,
TABLE 1
Characteristics and Distribution of Study Case Patients by Country
Characteristic
Total Belarus Russia Baltic countries
n¼107 n¼85 n¼15 n¼7
Number %Number %Number %Number %
By gender
Male 66 62 45 53 14 93 7100
Female 41 38 40 47 170
By age at exposure
,35 45 42 37 44 747 114
35–49 49 46 35 41 853 686
50þ13 12 13 15 0000
Median 37 37 36 39
Range 17–60 17–60 19–45 32–44
By age at diagnosis
,35 11 10 910 213 00
35–49 52 49 38 45 10 67 457
50þ44 41 38 45 320 343
Median 45 46 43 48
Range 27–72 27–72 28–53 44–57
TABLE 2
Distribution of Cases and Controls by Characteristics of Mission
Characteristic
Total Belarus Russia Baltic countries
Cases Controls Cases Controls Cases Controls Cases Controls
Did the subject work in the 30-km zone?
Yes (inside) 73 289 52 205 14 59 7 25
%68 68 61 61 93 95 100 96
No (outside) 34 134 33 130 1 3 0 1
%32 32 39 39 7 5 0 4
P-homogeneity
a
1.00 1.00 1.00 1.00
Date of beginning of mission
Before June 20, 1986 63 224 55 203 3 11 5 10
%59 53 65 61 20 18 71 38
June 20–August 31, 1986 19 63 17 52 2 6 0 5
%18 15 20 16 13 10 0 19
September1, 1986–December 31, 1987 25 136 13 80 10 45 2 11
%23 32 15 24 67 73 29 42
P-homogeneity
a
0.19 0.19 0.72 0.31
Median 25/05/86 11/06/86 15/05/86 03/06/86 22/12/86 06/01/87 12/05/86 11/07/86
Number of active working days for all missions in Chernobyl
,12 days 26 104 25 102 1 2 0 0
%24 25 29 30 7 3 0 0
12–30 days 23 108 21 102 2 6 0 0
%21 26 25 30 13 10 0 0
31–86 days 30 105 17 57 8 35 5 13
%28 25 20 17 53 56 71 50
86 days þ28 106 22 74 4 19 2 13
%26 25 26 22 27 31 29 50
P-homogeneity
a
0.81 0.67 0.74 0.41
Median (days) 32 30 25 21 62 61 65 83
a
Fisher’s exact test.
THYROID CANCER AMONG CHERNOBYL LIQUIDATORS 429
past occupational exposure to radiation, history of cancer,
smoking and alcohol consumption, were observed between
case patients and controls (Table 3). However, case patients
significantly differ from controls in respect to the past
medical radiation exposure, history of thyroid diseases and
stable iodine prophylaxis (Table 3). Case patients more
frequently reported having thyroid disease in the past or
undertaken stable iodine prophylaxis, but were less frequent-
ly exposed to medical radiation compared to controls.
The distribution of total thyroid radiation doses was
skewed for all subjects (Fig. 1). The median radiation dose
from all radiation types was estimated to be 70.4 mGy in
Belarus, 63.0 mGy in Russia and 55.5 mGy in Baltic
countries; the range of doses was, however, much wider in
Belarus. The median doses received by female liquidators
who were mainly Belarusian were higher (196.1 mGy) than
those received by males (63.8 mGy). The major contribu-
tion to the total thyroid dose for Belarusian liquidators was
from exposure to
131
I in their place of residence.
The median radiation dose from all radiation types tended
to be higher among case patients than among controls
overall in Belarus and in the Baltic countries (Table 4), but
not in Russia. The median thyroid dose from exposure to
131
I was much higher for Belarusian liquidators (Table 4)
than in other countries, mainly reflected doses received at
their places of residence from consuming contaminated milk
and leafy vegetables, while the median dose to the thyroid
from external exposure was much lower (6.53 mGy in
Belarus, 63.0 mGy in Russia and 55.1 mGy in Baltic
countries). In Belarus, doses from external exposure tended
to be similar among men and women (median: 6.34 vs. 8.63
mGy, respectively) while average doses from
131
I were
much higher among women than among men (median:
260.9 vs. 72.0 mGy), most likely because women were
staying at the site only during the day in the Chernobyl
zone. They were returning home in the evening where they
received higher residential doses from ingestion of contam-
inated foods compared to the small doses received by male
liquidators closer to the rector site through inhalation. In
contrast, in Russia, doses from external exposure received
by male liquidators were considerably higher than those
received by the few female liquidators whose activities were
limited to the tasks performed in less contaminated places
(canteens, medical aid stations, etc.) (Table 4).
All study subjects received their doses at low dose-rates:
only 5 subjects had dose-rates above 25 mGy/day and 7
subjects had dose-rates between 10–25 mGy/day at some
point during their mission.
Risk Analyses
Figure 2 shows the variation in the odds ratio as a
function of dose level. A statistically significant dose-
response relationship was observed (P¼0.0008). The
increase was statistically significant in the penultimate
(300–399 mGy: OR 4.20, 95% CI 1.62, 10.9) and highest
(400þmGy OR 2.63, 95% CI 1.36, 5.09) categories.
The ERR/100 mGy was 0.38 (95% CI 0.10, 1.09) overall
(Table 5), corresponding to an RR of 1.38 at 100 mGy.
There was no evidence of heterogeneity of risk across
countries. The ERR/100 mGy was significantly elevated
overall and especially in Belarus (0.37, 95% CI 0.08, 1.21).
The corresponding estimates using the log-linear model
were lower, except in Russia, and were significantly
elevated overall and in Belarus.
TABLE 3
Distribution by Potentially Confounding Factors and by
Case-Control Status (all Countries)
Characteristic
Cases Controls
n%n%
Family status
Married 89 83 327 77
Single 4 413 3
Widowed 9 837 9
Divorced 5 546 11
P-homogeneity
a
0.24
Education level
Eight class or less 18 17 81 19
High school 26 24 138 33
Special high school 38 36 131 31
Higher school 25 23 72 17
Missing 0 010
P-homogeneity
a
0.28
Past occupational exposure to radiation
Yes 10 922 5
No 97 91 399 94
Missing 0 020
P-homogeneity
a
0.2
Past medical radiation exposure
Yes 84 79 353 83
No 19 18 67 16
Missing 4 431
P-homogeneity
a
0.05
Past history of thyroid diseases
Yes 59 55 100 24
No 45 42 319 75
Missing 3 341
P-homogeneity
a
,0.001
Stable iodine prophylaxis
Yes 29 27 77 18
No 68 64 325 77
Missing 10 921 5
P-homogeneity
a
0.02
Smoking status
b
Current 33 31 173 41
Past 10 938 9
Non smoker 64 60 212 50
P-homogeneity
a
0.15
Alcohol consumption
Yes 79 74 344 81
No 28 26 77 18
Missing 0 020
P-homogeneity
a
0.13
a
Fisher’s exact test.
b
Subjects who were smokers and for whom it was not possible to
determine whether they had quit smoking before the reference date are
included as current smoker in this analysis—results including these
subjects as ex-smokers are very similar.
430 KESMINIENE ET AL.
The ERR/100 mGy for females was higher (Table 5) than
it was for males, although the difference was not significant.
However, the corresponding estimates using the log-linear
model were very similar.
Analyses by tumor diameter (,10 mm vs. 10 mm or
more) gave similar risk estimates as did analyses with or
without lymph node involvement.
Risk estimates by type of radiation dose are also shown in
Table 5. Risk estimates were similar for
131
I and for external
exposure, though the increase was significant only for total
dose and dose from
131
I. There was little correlation between
internal and external doses (not shown). Adjusting for doses
from external radiation had no effect on the
131
I risk
estimate. Adjusting for
131
I exposure somewhat reduced the
risk estimate from external radiation when using the linear
ERR, but not when using the log-linear model.
Higher risk estimates were seen among subjects with
dose-rates of 10 mGy/day or more compared to lower dose-
rates, although based on small numbers of subjects.
Results of Sensitivity Analyses
We conducted sensitivity analyses to evaluate the
robustness of the overall risk estimates to different analytic
FIG. 1. Distribution of total thyroid dose among study subjects (overall, by country and by case-control status).
THYROID CANCER AMONG CHERNOBYL LIQUIDATORS 431
strategies and to different dose estimates. The results of log-
linear analyses were generally similar to those reported
above; as were results using the linear ERR model.
Restricting analyses to subjects who worked in the 30-km
zone, using doses without application of dose-limitation
procedure or unconditional logistic regression yielded
lower, but statistically significantly elevated risk estimates
(not shown). Modeling uncertainties in external dose
estimates had little effect on the risk estimate, although it
increased the width of the confidence interval (Table 5).
Age at exposure and time since exposure did not appear to
modify the association between radiation dose and risk of
thyroid cancer (not shown).
None of the other factors studied such as date of start of
mission, work on roof of reactor, stable iodine prophylaxis,
past medical exposures to radiation, smoking and alcohol
consumption, as well as organization that sent the
liquidators to Chernobyl, number of working days for all
missions, personal monitoring of dose, use of protective
measures, education, marital status, history of cancer or of
thyroid diseases (not shown) appeared to play a role either
as a confounder or as a modifier of the association between
radiation dose and risk.
DISCUSSION
This study is the first study of thyroid cancer in
Chernobyl liquidators in which careful individual thyroid
dose reconstruction was attempted and in which information
was sought on a number of potential risk factors. Overall,
107 case patients and 423 controls from Belarus, Russia and
Baltic countries were included in these analyses. A
significant dose-response relationship was observed be-
tween radiation dose to the thyroid received in adulthood
and the risk of subsequent thyroid cancer, with a
significantly increased risk at doses of 300 mGy or above.
Are the findings of our study unexpected? Table 6 shows
a comparison of the risk estimates in this study with those
derived from analyses of adult atomic bomb survivors (39,
40), from the 15-country nuclear industry study (41) and
from the third analysis of the UK NRRW (42), as well as
from studies of exposure to
131
I in children and adults (5,
43–46). Risk estimates from the current study are higher
than those seen in other populations exposed in adulthood,
except in the UK NRRW study, but are lower than
comparable estimates derived from studies of thyroid cancer
in young people after the Chernobyl accident (5). However,
one should be careful when comparing the magnitude of
risk from exposure to ionizing radiation between popula-
tions that differ in respect to genetic background or
environmental factors, such as stable iodine intake. Iodine
deficiency was present at the time of the Chernobyl accident
in many areas of the former Soviet Union, particularly in
TABLE 4
Distribution of Doses to the Thyroid by Country, by Sex and by Case/Control Status
Total Belarus
Cases Controls Cases Controls
Median and range of total dose to the thyroid (mGy)
Overall 103 (0.18–3308) 66 (0.13–1643) 153 (0.95–3308) 68 (0.29–1643)
Male 69 (0.18–3308) 63 (0.29–924) 69 (3.34–3308) 64 (0.29–924)
Female 303 (0.95–1547) 139 (0.13–1643) 306 (0.95–1547) 156 (0.29–1643)
Median and range of external dose to the thyroid (mGy)
Overall 13 (0.18–496) 9 (0.11–508) 9 (0.39–142) 6 (0.11–454)
Male 22 (0.18–496) 11 (0.11–508) 9 (0.39–142) 6 (0.11–454)
Female 9 (0.71–64) 6 (0.11–91) 9 (0.71–64) 6 (0.11–91)
Median and range of internal dose to the thyroid from
131
I (mGy)
Overall 62 (0–3253) 62 (0–1552) 131 (0.24–3253) 62 (0–1552)
Male 18 (0–3253) 8 (0–902) 62 (1–3253) 57 (0–902)
Female 287 (0–1517) 123 (0–1552) 291 (0.24–1517) 143 (0–1552)
By source
Mission 0.72 (0–3198) 0.05 (0–1552) 4.27 (0–3198) 1.27 (0–1552)
Residence 43 (0–725) 37 (0–734) 62 (0–725) 56 (0–734)
FIG. 2. Comparison of odds ratios (ORs) predicted by different risk
models with categorical odds ratios estimated in six dose categories:
(u) OR and 95% CI; (), (heavy line) Log-linear model–linear dose-
response; (—) (light line) Excess relative risk (ERR) model–linear
dose-response.
432 KESMINIENE ET AL.
Belarus (47) and might have modified the effect of radiation
on the risk of thyroid cancer (4).
Uncertainties in thyroid dose estimates and possible
biases resulting from screening, selection, recall, confound-
ing, or effect modifiers must be considered carefully in
evaluating the results of this study.
Within this project, considerable efforts were made to
evaluate, quantify and take into account the uncertainties in
thyroid dose estimates. As indicated above, adjustment for
dosimetric uncertainties had little impact on the risk
estimates in this study. However, residential
131
I doses for
Belarusian liquidators were estimated crudely and were
based on average doses in the settlement of residence,
because no information had been collected in the question-
naire about consumption of milk and leafy vegetables
around the time of the accident. It is therefore likely that
there is some misclassification of residential
131
I doses, but
this should not be differential between cases and controls.
Non-differential misclassification would tend to bias risk
estimates toward the null (48).
A higher risk (although not statistically significantly
different) was observed in female liquidators from Belarus
who were residents of the contaminated villages. Women
received higher doses to the thyroid from
131
I compared to
their male colleagues through the ingestion of contaminated
food consumed every day after returning home from work.
Male liquidators who were the residents of contaminated
villages in Belarus were often sent for clean-up activities
during weekdays and returned home only on weekends or
after two-week shifts. During weekdays, they consumed
TABLE 4
Extended
Russia Baltic countries
Cases Controls Cases Controls
61 (0.18–496) 66 (0.13–508) 69 (22–323) 41 (1.91–488)
79 (0.18–496) 77 (1.94–508) 69 (22–323) 41 (1.91–488)
34 (34–34) 3.08 (0.13–4.22) 0 0
61 (0.18–496) 66 (0.13–508) 68 (22–322) 41 (1.91–488)
79 (0.18–496) 77 (1.94–508) 68 (22–322) 41 (1.91–488)
34 (34–34) 3.08 (0.13–4.22) 0 0
0 (0–1.6) 0 (0–11) 0.39 (0–1.09) 0 (0–1.39)
0 (0–1.6) 0 (0–11) 0.39 (0–1.09) 0 (0–1.39)
0 (0–0) 0 (0–0)
0 (0–1.6) 0 (0–11) 0.39 (0–1.09) 0 (0–1.39)
TABLE 5
Risk Estimates of Thyroid Cancer, from the Linear ERR and Log-Linear Models
Cases/controls
Linear ERR model Log-linear model
ERR/100 mGy 95%CI RR at 100 mGy RR at 100 mGy 95%CI
Overall 107/423 0.38 0.10 1.09 1.38 1.17 1.06 1.29
Country-specific
Belarus 85/335 0.37 0.08 1.21 1.37 1.16 1.05 1.29
Russia 15/62 0.47 –0.12 5.61 1.47 1.44 0.86 2.47
Baltic countries 7/26 0.25 nd
a
nd
a
1.25 1.12 0.45 2.22
P-homogeneity between countries
b
0.98 0.70
Gender-specific
Male 66/261 0.29 0.02 1.08 1.29 1.16 1.02 1.37
Female 41/162 0.61 0.06 31.5 1.61 1.17 1.03 1.34
P-homogeneity between gender
b
0.55 0.93
Tumor size (diameter)
10 mm or less 17/65 0.36 nd
a
5.73 1.36 1.12 0.78 1.58
.10 mm 68/268 0.43 0.08 1.74 1.43 1.16 1.05 1.31
Lymph node involvement
No lymph node involved 68/269 0.43 0.07 1.66 1.43 1.19 1.06 1.37
Spread to lymph nodes 32/125 0.47 0.00 3.04 1.47 1.25 1.01 1.56
Radiation type
Dose from
131
I alone 107/423 0.45 0.10 1.61 1.45 1.17 1.06 1.31
Dose from external exposure alone 107/423 0.38 –0.11 2.07 1.38 1.23 0.87 1.71
Model with both
131
I and dose from external exposure
Dose from
131
I, adjusted for external exposure 107/423 0.45 0.10 1.64 1.45 1.17 1.05 1.31
Dose from external exposure, adjusted for
131
I 107/423 0.21 –0.14 1.42 1.21 1.16 0.80 1.63
Level of dose-rate (mGy/day)
,10 103/415 0.34 0.10 0.86 1.34 1.15 1.07 1.26
10þ4/8 0.86 0.05 3.57 1.86 1.43 1.06 2.05
P-homogeneity between categories
b
0.42 0.24
Modeling dose uncertainties 107/423 Not available 1.20 1.07 1.43
a
Not defined.
b
Fisher’s exact test.
THYROID CANCER AMONG CHERNOBYL LIQUIDATORS 433
clean food supplied from outside the contaminated
territories.
The overall risk estimates were compatible for
131
I and for
external exposure, and we observed the statistically
significant risk only for total dose and for dose from
131
I.
Screening for thyroid cancer, either through formal
screening campaigns or through closer attention by medical
professionals has clearly occurred among Chernobyl
liquidators. The increased risk estimates in our study could
be attributable to a screening related selection bias, if
screening was, for some reason, more intensive among
groups with higher radiation exposure from the Chernobyl
accident. We have no evidence that, within the group of
liquidators, the level of screening is related to the level of
dose. All liquidators in Belarus and the Russian Federation
should undergo regular health examinations. However,
physicians are not aware of the doses they received during
clean up activities. To evaluate the possible impact of
screening, we conducted analyses by tumor size and by the
fact of lymph node involvement. The majority of tumors
reviewed by the International Panel (64%) were carcinomas
bigger than 10 mm in diameter, which were likely to be
diagnosed even in the absence of screening. When analyses
were restricted to such tumors, risk estimates were similar to
those obtained for micro carcinomas, i.e., tumors less than
10 mm. Similarly, there was little difference in risk of
tumors with and without lymph node involvement. Further,
past history of thyroid diseases (which could lead to
increased screening of individuals) was not associated with
increased radiation dose [RR at 100 mGy of thyroid cancer
in subjects with history of thyroid disease was 1.00 (95% CI
0.89, 1.12) compared to subjects with no such history]. The
higher proportion of the cases with older attained age in
1996–2000 could be explained due to increased surveillance
that has taken place in more recent years. However, when
time since exposure and attained age were included in the
model, they did not modify the association between
radiation dose and risk of thyroid cancer. Taken together,
these results suggest that screening is unlikely to fully
explain the increased risk in this study.
As interviews were carried out with case patients and
control subjects years after the Chernobyl accident, the
possibility that recall bias may have played a role in the
magnitude of the increased risk estimates of thyroid cancer,
observed in the present study cannot be excluded. The case
patient, aware of his/her disease status, could report
conditions of work as a liquidator, which would lead to
higher doses. It is difficult to precisely quantify the effects
of different possible recall errors. It should be noted,
however, that details of work in Chernobyl reported by the
liquidator were verified independently by two dosimetry
experts familiar with the clean-up practices, dates, places
TABLE 6
Comparison of Risk Estimates (and 95%Confidence Intervals) with Comparable Estimates from the Atomic Bomb Survivors,
Nuclear Workers and Those Exposed to
131
I in Childhood
Number of cases ERR/100 mSv 95%CI RR at 100 mSv 95%CI
External exposures
Atomic-bomb survivors (15)
Linear dose-response
a
Age at exposure
,20 years 105 0.39 0.26 0.58 1.39
20–40 years 87 0.10 0.03 0.19 1.10
.40 years 73 0.03 ,0
b
0.10 1.03
Women, .20 years at exposure (40)
a
241 0.07 0.02 0.15 1.07
Men, .20 years at exposure (40)
a
55 –0.03 ,0 0.03 0.97
15-country nuclear workers study (41)
Linear ERR model 17 ,0
b
nd
a
nd
c
Log-linear model
a
17 0.91 0.12 2.84
Third follow-up of UK NRRW study (42)
54 0.32 –0.05 1.75 1.32
Internal exposures
Exposure to
131
I in childhood, case-control study (5)
Linear ERR model up to 2 Gy 276 0.55 0.22 0.88 1.55
Swedish diagnostic
131
I(43, 44)
105 Not shown: no increase shown
German diagnostic
131
I
b
(45)
13,896 0.03 0.00 0.14 1.03
Chernobyl liquidators (current study)
Linear ERR model 107 0.38 0.10 1.09 1.38
Log-linear model 107 1.17 1.06 1.29
a
90% confidence interval for ERR/100mSv.
b
Central risk estimate or lower confidence bound is on boundary of parameter space (1/max dose).
c
Not defined.
d
90% confidence interval for RR/100 mSv.
434 KESMINIENE ET AL.
and conditions of these activities, and who were blind to the
disease status of each study subject (29). Random errors in
reporting conditions of work as a liquidator could induce a
bias toward the null, if there was a true association between
radiation exposure and thyroid cancer. At the same time,
however, if a differential recall bias existed between case
patients and controls, this could have produced a spurious
positive association. Analyses of individual factors that
study subjects may consider as being important determi-
nants of radiation dose (including duration of mission,
specific type of activities on the industrial site, work on the
roof of the reactor) did not show any association between
these factors and the risk of thyroid cancer. This would be
expected if recall bias were responsible for the increased
risk in this study. It appears unlikely that recall bias had a
strong impact on the results of the present study.
Information was collected by questionnaire on a number
of different risk factors for thyroid cancer and cancer in
general. These included socio-economic status (measured
by education and by occupation at the time of the Chernobyl
accident), other sources of radiation exposure (medical and
occupational), history of cancer or of thyroid diseases,
smoking and alcohol consumption. Adjustment for these
factors in the estimation of thyroid cancer risk did not,
however, materially affect the risk estimates. These factors
are therefore unlikely to be strong confounding factors for
these diseases.
CONCLUSION
The Chernobyl accident has provided a unique opportunity
to estimate the magnitude of the risk of thyroid cancer after
exposure to external radiation and to
131
I. We report here results
of a multinational case-control study of thyroid cancer risk
among Chernobyl liquidators in which considerable efforts
were made to reconstruct and validate individual dose
estimates. Most risk estimates were statistically significantly
elevated. They appear to be related to both
131
I exposure and to
external radiation. Risk estimates observed in our study were
higher than those estimated from most studies of other
populations exposed as adults. Although considerable efforts
were made to reconstruct and validate individual dose
estimates, uncertainties in doses and recall bias could have
affected the magnitude of the risk estimates in this study.
The findings of our study contribute to the better
characterization of the risk of thyroid cancer after radiation
exposure in adulthood. Further studies of populations exposed
as adults, including those exposed after the Chernobyl
accident, are needed to better understand this risk.
ACKNOWLEDGMENTS
This study was supported by contracts F14C-CT96-0011 and ERBIC15-
CT96-0317 from the European Union (Nuclear Fission Safety and INCO-
CopernicusProgrammes) and DHSS contract no. IROI/CC/ROI5763-01from
the U.S. National Institute for Environmental Health Sciences. The authors
would like to thank the late Professor Geoffrey Howe for helpful discussions
during the course of the study. The authors also wish to thank the interviewers
who collected the data (Belarus: Kunitski Dzmitry, Bondarovitch Pavel;
Estonia: Vello Jaakmees;Latvia: Kojalo Una; Lithuania: Stankevic Audrone;
Russia: Deniwenko Aleksandr, Frolov Gennadiy, Ganina Tatiana, Istomina
Svetlana, Shantyr Igor, Tishkovec Tatiana; the personnel of the regional
centers of the National Radiation and Epidemiological Registry in Northwest,
Volgo-Vyatsky, Central-Chernozem, North-Caucasus and Urals who
participated in the organization of the work and collection of data in the
regions; the Chernobyl Movement of Lithuania, the Latvian Association
‘‘Chernobyl’’ and the Center for Occupational Diseases and Radiation
Pathology (head physician Dr. E. Tchurbakova) atthe RSU Clinical Hospital,
Latvia, for assistance in the tracing, recruitment and establishment of contact
with the study subjects; the members of the panels of pathologists and
hematologists who carried out the review of the diagnoses: Dr. Kaarle
Franssila, former Head of Oncological Pathology at the Department of
Pathology at the Helsinki University Hospital, Finland; Prof. Eugeny F.
Lushnikov and Dr. Aleksandr Abrosimov at the Medical Radiological
ResearchCentre, Obninsk,the Russian Federation;Dr. Yuryi D. Sidorovat the
Minsk City Bureau of P athology, Belarus; Dr. Mikhail Fridma n, at Minsk City
Oncological Dispensary, Belarus; Dr. Andre Bouville at the National Cancer
Institute, U.S., for advice on dose reconstruction issues.
Received: February 22, 2012; accepted: June 14, 2012; published online:
September 21, 2012
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436 KESMINIENE ET AL.
... Between 250,000 and 600,000 military and civilians were later brought in as salvage workers, known as 'liquidators', to clean up the detritus of the blast, with aversive health effects [6][7][8]. Most of the 135,000 persons living within the 30-km. ...
... Eye disorders, endocrine/metabolic/nutritional causes, and respiratory causes of hospitalization were higher among the low exposure group but not in comparison to other FSU immigrants. Overall, the findings reflect some types of morbidity associated with exposure to the Chernobyl accident in studies from FSU, Europe and earlier studies from Israel [1,3,7,8,10,11,30,34,37,53,54]. Thus, we accept the hypothesis that there is a Chernobyl exposure association for some diagnostic groups, both in comparison to FSU immigrants, other immigrants and to native-born Israelis. ...
Article
Full-text available
On April 26th, 1986 the nuclear reactor at Chernobyl, Ukraine exploded, causing the worst radiation disaster in history. The aim was to estimate hospitalization rates among exposed civilians who later immigrated to Israel. We conducted a historical follow-up study, among persons exposed to Chernobyl (n = 1128) using linked hospitalization records from Soroka University Medical Center (SUMC), compared with immigrants from other areas of the Former Soviet Union (FSU) (n = 11,574), immigrants not from FSU (n = 11,742) and native-born Israelis (n = 8351), matched on age and gender (N = 32,795). Hospitalizations for specific ICD-10 coded diagnostic groups were analyzed by exposure and comparison groups by gender and age at accident. In addition, the rate of hospitalization, and the duration of hospital days and the number of hospitalizations for these selected diagnostic groups was also calculated. Hospitalizations for specific ICD-10 coded diagnostic groups and for any hospitalization in these diagnostic groups in general were analyzed by exposure and comparison groups and by covariates (gender and age at accident). The rate of any hospitalization for the selected diagnostic groups was elevated in the low exposure Chernobyl group (51.1%), which was significantly higher than the immigrant (41.6%) and the Israel-born comparison group (35.1%) (p < .01) but did not differ from either the high exposure group (46.9%) or the FSU comparison group (46.4%), according to the post-hoc tests. The total number of hospitalizations in the low exposure Chernobyl group (2.35) differed from the immigrant (1.73) and Israel comparison group (1.26) (p < .01) but did not differ from the FSU comparison group (1.73) or the high exposure group (2.10). Low exposure women showed higher rates of circulatory hospitalizations (33.8%) compared to immigrants (22.8%) and Israeli born (16.5%), while high exposure women (27.5%) only differed from Israelis (p < .01). Neither exposure group differed from FSU immigrant women on the rate of circulatory hospitalizations. Post-hoc tests showed that among women in the low exposure group, there was a significant difference in rate of hospitalizations for neoplasms (28.6%) compared to the three comparison groups; FSU (18.6%), immigrants (15.7%) and Israel (13.1) (p < .01). Those among the low exposure group who were over the age of 20 at the time of the accident showed the higher rates of circulatory (51.2%) and neoplasm hospitalizations (33.3%), compared to the other immigrant groups (p < .01). When controlling for both age at accident and gender, hospitalizations for neoplasms were higher among Chernobyl-exposed populations (RR = 1.65, RR = 1.77 for high and low-exposure groups, respectively) compared to other FSU immigrants (RR = 1.31) other immigrants (RR = 1.11) and Israeli born (RR = 1.0) after controlling for gender and age at accident. High RRs attributable to Chernobyl exposure were also found for circulatory diseases compared to other immigrants and Israeli born (RRs = 1.50, 1.47 for high and low exposure compared to 1.11. and 1.0, other immigrants and Israeli born, respectively). Endocrine problems and disorders of the eye also showed elevated RR compared to the immigrant comparison groups. Respiratory and mental disorders did not show any consistent association with Chernobyl exposure. The findings support unique Chernobyl morbidity associations only in some diagnostic groups, particularly for low exposure women. General immigration effects on hospitalizations compared to the Israeli born population were found on all diagnostic groups. There is a need to improve the services and medical follow-up for these Chernobyl exposed groups in specific diagnostic groups.
... Between 250,000 and 600,000 military and civilians were later brought in as salvage workers, known as 'liquidators', to clean up the detritus of the blast, with aversive health effects [6][7][8]. Most of the 135,000 persons living within the 30-km. ...
... Eye disorders, endocrine/metabolic/nutritional causes, and respiratory causes of hospitalization were higher among the low exposure group but not in comparison to other FSU immigrants. Overall, the findings reflect some types of morbidity associated with exposure to the Chernobyl accident in studies from FSU, Europe and earlier studies from Israel [1,3,7,8,10,11,30,34,37,53,54]. Thus, we accept the hypothesis that there is a Chernobyl exposure association for some diagnostic groups, both in comparison to FSU immigrants, other immigrants and to native-born Israelis. ...
Article
Full-text available
On April 26th, 1986 the nuclear reactor at Chernobyl, Ukraine exploded, causing the worst radiation disaster in history. The aim was to estimate hospitalization rates among exposed civilians who later immigrated to Israel. We conducted a historical follow-up study, among persons exposed to Chernobyl (n = 1128) using linked hospitalization records from Soroka University Medical Center (SUMC), compared with immigrants from other areas of the Former Soviet Union (FSU) (n = 11,574), immigrants not from FSU (n = 11,742) and native-born Israelis (n = 8351), matched on age and gender (N = 32,795). Hospitalizations for specific ICD-10 coded diagnostic groups were analyzed by exposure and comparison groups by gender and age at accident. In addition, the rate of hospitalization, and the duration of hospital days and the number of hospitalizations for these selected diagnostic groups was also calculated. Hospitalizations for specific ICD-10 coded diagnostic groups and for any hospitalization in these diagnostic groups in general were analyzed by exposure and comparison groups and by covariates (gender and age at accident). The rate of any hospitalization for the selected diagnostic groups was elevated in the low exposure Chernobyl group (51.1%), which was significantly higher than the immigrant (41.6%) and the Israel-born comparison group (35.1%) (p < .01) but did not differ from either the high exposure group (46.9%) or the FSU comparison group (46.4%), according to the post-hoc tests. The total number of hospitalizations in the low exposure Chernobyl group (2.35) differed from the immigrant (1.73) and Israel comparison group (1.26) (p < .01) but did not differ from the FSU comparison group (1.73) or the high exposure group (2.10). Low exposure women showed higher rates of circulatory hospitalizations (33.8%) compared to immigrants (22.8%) and Israeli born (16.5%), while high exposure women (27.5%) only differed from Israelis (p < .01). Neither exposure group differed from FSU immigrant women on the rate of circulatory hospitalizations. Post-hoc tests showed that among women in the low exposure group, there was a significant difference in rate of hospitalizations for neoplasms (28.6%) compared to the three comparison groups; FSU (18.6%), immigrants (15.7%) and Israel (13.1) (p < .01). Those among the low exposure group who were over the age of 20 at the time of the accident showed the higher rates of circulatory (51.2%) and neoplasm hospitalizations (33.3%), compared to the other immigrant groups (p < .01). When controlling for both age at accident and gender, hospitalizations for neoplasms were higher among Chernobyl-exposed populations (RR = 1.65, RR = 1.77 for high and low-exposure groups, respectively) compared to other FSU immigrants (RR = 1.31) other immigrants (RR = 1.11) and Israeli born (RR = 1.0) after controlling for gender and age at accident. High RRs attributable to Chernobyl exposure were also found for circulatory diseases compared to other immigrants and Israeli born (RRs = 1.50, 1.47 for high and low exposure compared to 1.11. and 1.0, other immigrants and Israeli born, respectively). Endocrine problems and disorders of the eye also showed elevated RR compared to the immigrant comparison groups. Respiratory and mental disorders did not show any consistent association with Chernobyl exposure. The findings support unique Chernobyl morbidity associations only in some diagnostic groups, particularly for low exposure women. General immigration effects on hospitalizations compared to the Israeli born population were found on all diagnostic groups. There is a need to improve the services and medical follow-up for these Chernobyl exposed groups in specific diagnostic groups.
... According to the Life Span Study [2], which consisted of ABS in Japan, atomic bomb radiation was significantly associated with increased solid cancer incidence [3], including salivary gland, esophageal, and stomach cancers [4]. Other evidence regarding radiation exposure unrelated to medical purposes and its health effects was obtained from studies after the Chernobyl disaster [5,6]. ...
Article
In 1945, atomic bombs were dropped on Hiroshima and Nagasaki. Approximately 70 000 Koreans are estimated to have been exposed to radiation from atomic bombs at that time. After Korea’s Liberation Day, approximately 23 000 of these people returned to Korea. To investigate the long-term health and hereditary effects of atomic bomb exposure on the offspring, cohort studies have been conducted on atomic bomb survivors in Japan. This study is an ongoing cohort study to determine the health status of Korean atomic bomb survivors and investigate whether any health effects were inherited by their offspring. Atomic bomb survivors are defined by the Special Act On the Support for Korean Atomic Bomb Victims, and their offspring are identified by participating atomic bomb survivors. As of 2024, we plan to recruit 1500 atomic bomb survivors and their offspring, including 200 trios with more than 300 people. Questionnaires regarding socio-demographic factors, health behaviors, past medical history, laboratory tests, and pedigree information comprise the data collected to minimize survival bias. For the 200 trios, whole-genome analysis is planned to identify de novo mutations in atomic bomb survivors and to compare the prevalence of de novo mutations with trios in the general population. Active follow-up based on telephone surveys and passive follow-up with linkage to the Korean Red Cross, National Health Insurance Service, death registry, and Korea Central Cancer Registry data are ongoing. By combining pedigree information with the findings of trio-based whole-genome analysis, the results will elucidate the hereditary health effects of atomic bomb exposure.
... The absorbed dose to the thyroid is a primary determinant of the effect, regardless of external or internal exposure. According to an epidemiological study of Chernobyl liquidators, the excess relative risk per 100 mGy was 0.38, and a significantly increased risk was observed at doses of 300 mGy or above, suggesting the necessity of long-term follow-up for nuclear workers who received nearly or more than 300 mGy to their thyroid glands [1]. Furthermore, the effective and prompt implementation of iodine thyroid blocking (ITB) is important and should be considered before and during the release of radioactive iodine. ...
Article
Full-text available
Seven emergency nuclear workers, who had internal exposure due to an intake of radionuclides, mainly I-131, during the emergency response operation in March 2011, after the accident at the Tokyo Electric Power Company (TEPCO) Fukushima Daiichi Nuclear Power Plant (FDNPP), visited the National Institute of Radiological Sciences (NIRS) outpatient clinic for medical evaluation. They were followed up after their first visit for 10 years. The estimated committed equivalent doses to the thyroid were distributed between 3.2 to 1.2 × 10 Sv. This group thought to be received highest exposure at the accident. None of the workers had symptoms related to abnormal thyroid function. The examinations, including thyroid function tests and ultrasound, detected no abnormalities related to radiation exposure. However, there is a need for continuous monitoring of their thyroid status for longer periods in the future.
... Late health effects in cleanup workers following the chernobyl accident (D. Bazyka) Studies performed in the three most highly exposed republics, specifically Ukraine, Russia and Belarus, of the former USSR after the Chernobyl accident have demonstrated numerous types of late health effects associated with radiation exposure in the cleanup workers (formerly termed liquidators) residing there (Ivanov et al. 2006;2008;Kesminiene et al. 2012;Zablotska et al. 2013;Kashcheev et al. 2015;2016;. ...
... Although the exact mechanism linking these diseases is not clear, there are currently three main hypotheses: 1) HT is a precancerous lesion of PTC; 2,23 2) the hypothesis of chronic inflammation; and 3) HT and PTC have common causes, potentially including immune factors (both thyroid globulin antibody and microsomal antibody have been found in the blood of HT and PTC patients), [24][25][26] endocrine factors (HT can cause hypothyroidism and increase reactive thyrotropin, which can in turn cause carcinogenesis), [27][28][29][30][31] and radioactive factors (exposure to X-rays can lead to thyroid inflammation and carcinogenesis, via the same mechanism). [32][33][34][35][36][37] In this study, we explored the possible relationships among HT, HTB, HTC, and PTC by focusing on their US characteristics and expression of IL-17 and VEGF. We showed that blood flow PSV, blood flow RI, rate of microcalcification, a thyroid nodule aspect ratio >1, low thyroid echo ratio, and rate of suspicious abnormal lymph nodes in the neck were all significantly increased in thyroid US manifestations in patients with HTC compared with HTB. ...
Article
Full-text available
Objective The incidences of papillary thyroid carcinoma (PTC) and Hashimoto’s thyroiditis (HT) have shown increasing trends. Numerous studies have shown a close relationship between the two diseases, but the exact mechanism linking PTC with HT is still unclear. Interleukin-17 (IL-17) plays an important role in the development of malignant tumors. However, information on the association between IL-17 and thyroid disease is lacking. Methods Tissue samples were collected from patients with thyroid diseases admitted to the thyroid surgery department of our hospital between May 2015 and December 2017. The characteristics of the thyroid were observed by ultrasonography, hematoxylin-eosin staining, enzyme-linked immunosorbent assays, and immunohistochemistry. Results We found that HT with carcinoma (HTC) showed unique characteristics in two-dimensional ultrasound images. Moreover, IL-17 and vascular endothelial growth factor (VEGF) levels showed gradually increasing trends during the process of HT malignant transformation, with a significant positive correlation between the two cytokines. Serum IL-17 and VEGF levels could distinguish between HTC and HT with benign adenoma. Conclusion Our data suggest that serum IL-17 and VEGF levels may represent novel biomarkers for the diagnosis of HT malignant nodules.
... Des augmentations de l'incidence du cancer de la thyroïde ont été observées parmi les liquidateurs russes [12], baltes [13] et ukrainiens [14], en particulier parmi ceux ayant travaillé dans les premiers mois après l'accident (lorsque l'exposition à l'iode radioactif était la plus élevée), mais ces études ne prenaient pas en compte la dose individuelle de rayonnements. Une étude sur les liquidateurs biélorusses, russes et baltes [15], utilisant une reconstruction de doses individuelles, a trouvé une augmentation du risque de cancer de la thyroïde avec la dose : le risque était multiplié par cinq pour une dose de 1 Gy reçue à la thyroïde et, d'après les auteurs, cette augmentation ne pouvait s'expliquer uniquement par les campagnes de dépistage thyroïdien et l'attention accrue des professionnels de santé vis-à-vis de ce type de cancer chez les liquidateurs. Une autre étude sur les adultes résidant en territoire contaminé a également observé un excès de cancer thyroïdien dans les régions contaminées par rapport aux régions non contaminées [16]. ...
... Публікації Для оцінки радіаційно-спричиненого ризику розвитку раку ЩЗ було проведено спільне дослідження співвідношення «випадок-контроль» у когорті білоруських, російських та прибалтійських УЛНА, яке включало 107 випадків та 423 контроля [31]. Було встановлено статистично значущий взаємозв'язок «дозавідгук» із загальною дозою опромінення ЩЗ. ...
Article
26 квітня 1986 р. на четвертому реакторі Чорнобильської атомної електростанції (ЧАЕС) сталася найбільш масштабна техногенна аварія в історії людства. Мета — представити інформацію про клінічні дослідження медичних наслідків аварії на ЧАЕС. Результати. Станом на 31 березня 2020 р. на сайті ClinicalTrials.gov була розміщена інформація про 6 клінічних досліджень із медичних наслідків аварії на ЧАЕС. Середня тривалість досліджень становить 15 років і 9 місяців, а 2/3 із них виконуються понад 20 років. Поточний статус досліджень: «завершено» — 3 дослідження, «набір», «активний, без набору» і «призупинено» — по 1 дослідженню. 4 клінічних дослідження проводяться в Україні: 3 — на базі ДУ «Національний науковий центр радіаційної медицини НАМН України» і 1 — на базі ДУ «Інститут ендокринології та обміну речовин ім. В.П. Комісаренка НАМН України»; 1 дослідження проводиться в Республіці Білорусь на базі Республіканського науково-практичного центру радіаційної медицини та екології людини (м. Гомель), а 1 завершене дослідження проводилося в Спо- лучених Штатах Америки на базі Національного інституту раку (National Cancer Institute). У всіх дослідженнях головний дослідник є співробітником National Cancer Institute (США). Спонсором усіх досліджень є National Cancer Institute (США). Загальна кількість учасників клінічних досліджень становила 51 051 особу (мінімальна — 673, максимальна — 23 143, середня — 8 508). Тип дослідження у всіх випадках був обсерваційний. За моделлю дослідження розподіл наступний: когортне дослідження — 2 дослідження, дослідження «випадок-контроль» — 2 дослідження, дослідження сімей — 1 дослідження (для одного дослідження інформація відсутня). За часовою перспективою дослідження були ретроспективними — 3 дослідження, проспективними і поперечними — по 1 дослідженню (для одного дослідження інформація відсутня). За методом вибірки клінічні дослідження були випадковими (2 дослідження) і невипадковими (3 дослідження); для одного дослідженняінформація відсутня. Представлено огляд 20 публікацій за результатами 5 клінічних досліджень. Висновок. На сайті ClinicalTrials.gov зареєстрована вкрай мала кількість клінічних досліджень медичних наслідків аварії на ЧАЕС.
... It is estimated that thyroid gland received an average 131 I dose of 650 mGy in Ukraine and 560 mGy in Belarus Zablotska et al., 2011). About 600 workers were involved in the emergency response immediately after the accident; 134 developed acute radiation syndrome resulting in 28 deaths (Kesminiene et al., 2012;Zablotska et al., 2013). Thyroid cancer was high in children aged 0e5 years at exposure, but no such increase was detected in adults. ...
Chapter
Humans are constantly being exposed to one or the other kinds of radiation, either from natural sources such as sunlight or from human-made inventions. Ionizing radiation plays an important role in daily life of human life such as the sources used in medical diagnosis—X-rays and computed tomography scans, for example. Most of the hospitals around the world use radiation for either diagnosis or for cancer therapy. Industrial uses of ionizing radiation such as food irradiation and sterilization of medical and other equipment have major implications in our daily life. International Atomic Energy Agency estimates that at least 10% world's electricity is produced from nuclear power plants. Moreover, we all live in an environment where radiation-emitting devices are abundant, and it appears that radiation exposure is practically unavoidable. Historically, humankind has witnessed few nuclear accidents/incidents such as the Hiroshima and Nagasaki bombing (1945), Chernobyl (1986), Goiânia (1987), and Fukushima (2011) where unintended exposures have occurred. Humans are exposed to cosmic radiation from space exploration and air travel. Thus, obviously, it is important to understand the biological effects of various types of radiation. While high doses of ionizing radiation ha ve shown to be harmful to the exposed individuals, low doses of radiation may have long-term consequences. Immediately after the discovery of X-rays by Wilhelm Roentgen in 1895, health effects of ionizing radiation started to appear. Ionizing radiations have found to be detrimental and carcinogenic. In this chapter, we summarize the various health impacts of ionizing radiation to humans.
Article
This original study aims to quantify the human factor uncertainties in radiation doses for Chernobyl cleanup workers that are associated with errors in direct or proxy personal interviews due to poor memory recall a long time after exposure. Two types of doses due to external irradiation during cleanup mission were calculated independently. First, a “reference” dose, that was calculated using the historical description of cleanup activities reported by 47 cleanup workers shortly after the completion of the cleanup mission. Second, a “current” dose that was calculated using information reported by 47 cleanup workers and respective 24 proxies (colleagues) nominated by cleanup workers during a personal interview conducted more recently, as part of this study, i.e., 25–30 years after their cleanup missions. The Jaccard similarity coefficient for reference and current doses was moderate: the arithmetic mean ± standard deviation was 0.29 ± 0.18 (median = 0.31) and 0.23 ± 0.18 (median = 0.22) for the cleanup worker's and proxy's interviews, respectively. The agreement between two doses was better if the cleanup worker was interviewed rather than his proxy: the median ratio of current to reference dose was 1.0 and 0.56 for cleanup workers and proxies, respectively. The present study has shown that human factor uncertainties lead to underestimation or overestimation of the “true” reference dose for most cleanup workers up to 3 times. In turn, the potential impact of these errors on radiation-related risk estimates should be assessed.
Article
Full-text available
This report from HPA Radiation Protection Division reflects understanding and evaluation of the current scientific evidence as presented and referenced in this document. ABSTRACT Mortality and cancer incidence have been studied in a cohort of about 175,000 persons on the National Registry for Radiation Workers (NRRW) who were followed until the end of 2001. This analysis is based on a larger cohort and nine years' further follow-up compared with the 2 nd NRRW analysis, and includes cancer registration data for the first time. As in previous NRRW analyses, total mortality and mortality from major causes were less than would be expected based on rates for England and Wales; the Standardised Mortality Ratio (SMR) for all causes was 81, whilst the SMR for all malignant neoplasms was 84. This "healthy worker effect" was still present after adjustment for social class. The only cause for which mortality was statistically significantly greater than expected from national rates was pleural cancer, probably reflecting exposure to asbestos. Within the cohort, there was borderline evidence of an increasing trend in total mortality with increasing external radiation dose. Much of the evidence for this trend related to cancer. Mortality and incidence from both leukaemia excluding chronic lymphatic leukaemia and the grouping of all malignant neoplasms other than leukaemia increased to a statistically significant extent with increasing dose. The corresponding central estimates of the trend in risk with dose were similar to those for the survivors of the atomic bombings of Hiroshima and Nagasaki, whilst the 90% confidence intervals for the NRRW trends excluded values more than about 2-3 times greater than the A-bomb risk estimates as well as values of zero or less. Whilst there was some evidence of an increasing trend with dose in mortality from all circulatory diseases combined, the irregular pattern in risk with dose and similarities with the corresponding pattern for lung cancer suggest that this finding may, at least in part, be due to confounding by smoking.
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relationship was observed up to 1.5 - 2 Gy. The risk of radiation-related thyroid cancer was three times higher in iodine-defi cient areas (relative risk (RR)= 3.2, 95% CI = 1.9 to 5.5) than elsewhere. Administration of potassium iodide as a dietary supplement reduced this risk of radiation-related thyroid cancer by a factor of 3 (RR = 0.34, 95% CI = 0.1 to 0.9, for consumption of potassium iodide versus no consump- tion). Conclusion: Exposure to 131 I in childhood is associated with an increased risk of thyroid cancer. Both iodine defi ciency and iodine supplementation appear to modify this risk. These results have important public health implications: stable iodine supplementation in iodine-defi cient populations may substantially reduce the risk of thyroid cancer related to radioactive iodines in case of exposure to radioactive iodines in childhood that may occur after radiation accidents or during medical diagnostic and therapeutic procedures. (J Natl Cancer Inst 2005;97:724 - 32)
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Variation of the stable iodine supply was evaluated in the soils of around more than 700 settlements in the regions (oblasts) of Belarus and the Russian Federation contaminated after the Chernobyl accident. It involved the use of regional information on iodine content in different types of soil cover, biogeochemical criteria of iodine deficiency in food chains, and the available soil maps.The proposed method enabled to create overview maps that differentiated study areas by iodine supply level and to rank rural settlements according to iodine content in soil cover. The area-weighted concentration of stable iodine in the soil cover used for farming was estimated. Median iodine concentration was found to be highest in the settlements of Orel and Tula oblasts (3.6mg/kg), lower in Gomel and Mogilev oblasts (3.0 and 2.3mg/kg, respectively) and lowest in Bryansk and Kaluga oblasts (1.3mg/kg). Estimates of iodine availability from different types of soils were corrected for volumetric weight and adjusted for the type of settlement in order to assign the stable iodine status for each subject in a case–control study of thyroid cancer risk following the Chernobyl accident. The epidemiological study found a significant modifying effect of iodine deficiency on the risk of thyroid cancer following exposure to radioiodines.