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Cancer Epidemiology 37 (2013) 585592

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Cancer Epidemiology
The International Journal of Cancer Epidemiology, Detection, and Prevention

journal homepage: www.cancerepidemiology.net

Fallout from the Chernobyl accident and overall cancer incidence in Finland
Paivi Kurttio a,*, Karri Seppa b,c, Kari Pasanen d,e, Toni Patama b, Anssi Auvinen a,f,
Eero Pukkala b,f, Sirpa Heinavaara a, Hannu Arvela a, Timo Hakulinen b
Environmental Radiation Surveillance, Radiation and Nuclear Safety Authority, Laippatie 4, FI-00881 Helsinki, Finland
Finnish Cancer Registry, Institute for Statistical and Epidemiological Cancer Research, Pieni Roobertinkatu 9, FI-00130 Helsinki, Finland
Department of Mathematical Sciences, FI-90014 University of Oulu, Finland
Department of Environmental Health, National Institute for Health and Welfare, Neulaniementie 4, FI-70210 Kuopio, Finland
University of Eastern Finland, P.O. Box 1627, FI-70211 Kuopio, Finland
Department of Epidemiology, FI-33014 University of Tampere, Finland


Article history: Aim: We studied whether incidence of all cancer sites combined was associated with the radiation
Received 27 December 2012 exposure due to fallout from the Chernobyl accident in Finland. An emphasis was on the rst decade after
Received in revised form 10 April 2013 the accident to assess the suggested promotion effect. Methods: The segment of Finnish population
Accepted 23 May 2013
with a stable residence in the rst post-Chernobyl year (2 million people) was studied. The analyses were
Available online 22 June 2013
based on a 250 m  250 m grid squares covering all of Finland and all cancer cases except cancers of the
breast, prostate and lung. Cancer incidence in four exposure areas (based on rst-year dose due to
external exposure <0.1 mSv, 0.11.3, 0.30.5, or 0.5 mSv) was compared before the Chernobyl accident
Chernobyl nuclear accident
(19811985) and after it (19882007) taking into account cancer incidence trends for a longer period
Cancer prior to the accident (since 1966). Results: There were no systematic differences in the cancer incidence
Finland in relation to radiation exposure in any calendar period, or any subgroup by sex or age at accident.
Ionizing radiation Conclusion: The current large and comprehensive cohort analysis of the relatively low levels of the
Registries Chernobyl fallout in Finland did not observe a cancer promotion effect.
2013 Elsevier Ltd. All rights reserved.

1. Introduction compared to the lowest exposure areas within 5 years after the
accident [5,6]. This increase in cancer incidence after a short
Outside of the most affected three countries adjacent to the latency was interpreted by the authors as a cancer promoting effect
damaged nuclear reactor, Ukraine, Belarus and parts of the Russian of low-dose radiation.
Federation, Finland was among the countries most heavily affected The validity of extrapolation from acute high external doses to
by the radioactive fallout after the Chernobyl accident in April low doses and dose rates of combined external and internal
1986 [1]. radiation remains under debate, and more studies have been
Studies in Finland following the Chernobyl accident have not requested on health effects of low doses [7]. This is important
indicated increased risks of childhood leukaemia [2] or thyroid since most of the collective radiation exposure is received as
cancer in children and adolescents [3], which are considered to be chronic or repeated low doses. Therefore, if low-dose exposures
the most readily radiation induced cancer sites. Several studies in carry a higher or lower risk than that predicted from a linear
other countries outside of the three most affected countries have extrapolation from acute higher doses, it would have substantial
also failed to show an effect [4]. It was therefore surprising that implications for the fundamental radiation protection principles
overall cancer incidence was found to be 1020% higher in the and practices.
population with the highest radiation exposure in Central Sweden The aim of the study was to analyze the overall cancer incidence
(excluding cancers in breast, lung and prostate) in relation to the
estimated radiation dose from the Chernobyl accident in the

Finnish Cancer Organizations supported the study. No other external support Finnish population. An emphasis was on assessing whether an
was received. early increase in the overall cancer incidence following the
* Corresponding author at: Environmental Radiation Surveillance, Radiation and
Chernobyl accident can be demonstrated in accordance with
Nuclear Safety Authority, P.O. Box 14, FI-00881 Helsinki, Finland.
Tel.: +358 9 759 88 554; fax: +358 9 859 88 498. the hypothesized cancer-promoting effect with a short latency
E-mail address: paivi.kurttio@stuk. (P. Kurttio). [5,6], i.e., in the rst decade following the accident.

1877-7821/$ see front matter 2013 Elsevier Ltd. All rights reserved.
586 P. Kurttio et al. / Cancer Epidemiology 37 (2013) 585592

2. Materials and methods (April 1986March 1987). The dose estimates were based on a
mobile survey carried out from May 1986 to August 1987 [9].
2.1. Study design, inclusion criteria Continuous measurements were carried out using a germanium
spectrometer, Geiger-Muller (GM)-tubes and a high pressure
The data were based on 250 m  250 m map grid squares ionization chamber (HPIC). Average dose rates and fallout levels of
covering the whole Finland and Finnish population with a stable each section of the route were calculated. The dose rate calibration
residence i.e., those who had lived in a same address during the rst was based on point source calibrations of the HPIC. The mobile
post-Chernobyl year (the time period when most of the radiation survey covered 19,000 km through the mainland. The SAS G3GRID
exposure was received). The registry data on age, sex, residential (SAS Institute Inc., Cary, North Carolina, 1985) procedure was used
history, and house type on population in the 250 m  250 m map for interpolating values from an irregularly spaced set of 1050
grid squares were obtained from Statistics Finland. observations to generate a map with a 8 km  8 km grid (Fig. 1).
The data were restricted to detached, semidetached or terraced The dose rate estimates were based on both dose rate
houses and are called as single family houses later on. The measurements with GM-tubes and spectrometric measurements
population in single family houses was assumed to have received of caesium-137 (137Cs) and caesium-134 (134Cs). The contribution
higher external radiation doses than people living in apartments as of all relevant short lived nuclides was determined from
the shielding of the building is substantially lower in single family spectrometric results. The effect of delay in the measurements
houses than in blocks of ats. Therefore, a higher exposure contrast was eliminated by using a back-calculation technique that takes
was attainable by limiting the analysis to single family houses. A into account both the radioactive decay and the washout effect.
single family house must have existed on a map grid square The inuence of fallout from atomic bomb tests in the 1950s and
already in the beginning of the pre-Chernobyl period. In order to 1960s was avoided by calculating the calibration factor on the
restrict the analyses on areas of single family houses (and to basis of 134Cs deposition [10]. The population doses were mainly
maintain comparability of incidence rates with time), a map grid caused by 137Cs and other volatile nuclides [9].
square was excluded if there was one or more block of ats (high- House structures reduce the gamma exposure indoors due to
rise residential buildings) on a grid square in the end of 1980 or shielding and distribution of fallout in the building area. A
1990. In addition, a map grid square was excluded if there was no shielding factor of 0.37 for single family houses was adopted from a
populated single family house in 1980. The number of the eligible Swedish study [11]. Application of these factors has been assessed
250 m  250 m map grid squares used in the study (inhabited and in a Finnish study [10]. From data provided by Statistics Finland it
with single family houses only) was 267,936 which is 5% of the all was estimated that people stayed indoors 80% of a day. The
map grid squares (5,461,215) covering the area of Finland and 94% occupancy-weighted shielding factor was thus 0.50. The nal
of inhabited map grid squares in Finland. This is an indication of conversion factor of the deposition (kBq/m2) to the rst year dose
the sparse population density of the country. after the accident (mSv) for occupants in the single family houses
For the statistical analyses, aggregated small area level data was 0.0108. The exposure estimation was expressed as effective
(250 m  250 m map grid squares) on cancer cases and person dose (mSv) instead of whole body absorbed dose (mGy) which are
years for two cross-sectional population cohorts were used. comparable (0.7  mGy = mSv).
Aggregation of cancer cases and person years was based on the The country was divided into four exposure areas based on the
address location in the beginning of follow up. Aggregated data on estimated effective radiation dose due to external exposure from
population and the linkage of house type with coordinates for the Chernobyl accident fallout during the rst year after the
cancer cases were obtained from Statistics Finland. In addition, accident. The exposure areas were dened using convenient and
small area level data on number of residences (by house type) in equidistant cut-points as follows:
1980 and 1990 were obtained from Statistics Finland.
The study cohort included persons of all ages who lived in the Exposure Estimated dose during the Corresponds
same address in a grid square including only single family houses area rst year after the to 137Cs fallout
from May 1986 through April 1987. A follow-up time of a person Chernobyl accident (mSv) (kBq/m2)
was censored after the rst emigration. The study cohort consists
of 2,095,822 persons, i.e., approximately 40% of the total Finnish 1 <0.1 <9
population in 1987. The cohort denition was based on the data on 2 0.1<0.3 9<28
the continuously updated national population register which
3 0.3<0.5 28<46
contains individual level information on residential history since
1981. In Finland the quality of data on address locations is high [8]. 4 0.5 46
A pre-Chernobyl cohort was formed to compare cancer incidence
in the study cohort with the cancer incidence in the same areas
before the accident. The pre-Chernobyl cohort included persons
who lived in the grid squares containing only single family houses The radioactive fallout was considered reasonably homogenous
at the end of 1980 with the follow-up from the beginning of 1981 within each 8 km  8 km map grids. The level of exposure from the
until the end of 1985. Cancer incidence during the pre-Chernobyl 8 km  8 km map grid square was assigned to the overlapping
period of 19811985 was thus used as a baseline. This period 250 m  250 m map squares using ArcGIS 9.2 geographical
reects the underlying differences in the cancer incidences information system (Environmental Systems Research Institute
between the exposure areas. Furthermore, it represents the Inc., Redlands, CA, USA). Finally, 250 m  250 m grids that contain
aggregated effect of confounding factors, i.e., other risk factors single family houses only were extracted and used to select study
for cancers. From the pre-Chernobyl cohort the expected incidence populations for each exposure areas both from the pre-Chernobyl
rates could be estimated. and the study cohorts.
The effect of other sources of radiation exposure, such as natural
2.2. Exposure assessment background radiation (from terrestrial and cosmic sources), indoor
radon, and medical uses of radiation, was assumed to have
Radiation exposure was estimated as the cumulative remained similar or changed similarly in different areas after the
external dose over the rst year after the Chernobyl accident Chernobyl accident.
P. Kurttio et al. / Cancer Epidemiology 37 (2013) 585592 587

Fig. 1. Exposure areas based on the estimated 1st year dose from external gamma radiation from the Chernobyl accident in populated 8 km  8 km map grids in Finland
among people living in single family houses. White squares indicate uninhabited areas.

2.3. Outcome assessment then used anonymous aggregated cancer incidence data (from 1988
to 2007) for 250 m  250 m map grid squares, with numbers of
The data of individual cancer cases data were obtained from the person-years by the four exposure areas, ve -year groups of
Finnish Cancer Registry for the period from 1981 to 2007. Cancer attained age, age at the Chernobyl accident (059 and 60+ years),
cases were linked to 250 m  250 m map grid squares based on their and sex. Cancer cases and person-years of a person were excluded
stable one-year residence in 19861987 and the house type using from the study cohort (19882007) after the rst emigration.
personal ID numbers. The nal dataset was compiled by Statistics The pre-Chernobyl cohort was divided into the same four areas
Finland by linking the cancer cases data to the exposure data. We as the post-Chernobyl cohort according to persons address of
588 P. Kurttio et al. / Cancer Epidemiology 37 (2013) 585592

residence at the end of 1980. The pre-Chernobyl cohort is the In order to examine the overall cancer incidence trends in the
closed cohort like the study cohort i.e., it did not include births or four exposure areas prior to the accident, the whole Cancer
immigration after the end of 1980. Cancer cases were excluded Registry data during 19661985 were used at municipality level.
from the cohort after the rst emigration. The numbers of person- The municipalities were classied for the exposure areas according
years in 19811985 by the four exposure areas, ve-year groups of to the majority of the map grid squares. Only the municipalities in
attained age and sex were estimated from the population counts of which at least 2/3 of the households were single family houses in
the pre-Chernobyl cohort in 1980 and 1985. The population counts 1980 were included in the analysis (383 municipalities out of 445;
in 1985 were estimated from those in 1980 and the numbers of 151, 156, 53, and 23 municipalities in the exposure area 1, 2, 3, and
deaths in 19811985 that were stratied by the four exposure 4, respectively). The exclusions of the cancer sites of overall cancer
areas, ve-year age groups (dened by age at the end of year 1980) incidence were the same as in the main analysis.
and sex. Emigration rate (0.16% in the whole population of Finland
during 19811985) was not taken into account. 2.4. Statistical analysis
Overall cancer incidence excluding cancers in breast, prostate
and lung was analyzed. Breast and prostate cancers were excluded Incidence rates were calculated for males and females in 5-year
because potential differences in the cancer screening activities calendar periods (the pre-Chernobyl period 19811985, and post-
between exposure areas. Lung cancer was excluded due different Chernobyl periods 19881992, 19931997, 19982002, and 2003
trends in smoking habits in various parts of the country. Basal cell 2007) and were standardized by attained age using person-years of
carcinomas of the skin were not included in the analysis due to each calendar period as weights. This was done in order to make
incomplete registration of the disease. Thyroid cancer was incidence rates comparable between the exposure areas within
included as no differences in screening activities was expected each 5-year period. The years 19861987 were excluded from the
[3]. The cancer site specic analysis will be presented in another analysis, because the eligibility criteria of the cohort (persons had
paper (Auvinen et al. submitted for publication). to live in the same address in 1986 and in 1987). To estimate
The numbers of person-years and cancer cases potential for the exposure area-specic incidence rate ratios (RRs) between the pre-
analyses are shown in Table 1 according to age at accident. The pre- and a post-Chernobyl period, each of the post-Chernobyl periods
Chernobyl cohort is larger than the post-Chernobyl cohort as the was analyzed together with the baseline period 19811985 using
criteria of one-year permanent residency following the accident Poisson regression where the logarithm of the incidence rate l was
cannot be applied. modelled as a linear function of the 5-year group of attained age i
Cancer sites were classied by the association with radiation (from 04 to 8084, and an open-ended age group 85+ years) and
[12,13] into sub-groups for some ancillary analyses described in exposure area e (e = 1, 2, 3, 4). In addition, an interaction between
the Supplementary material (Table S1). Leukaemia, ovary, oesoph- exposure area e and calendar period p was included in the model.
agus, colon, bladder, stomach, and thyroid were cancer sites Thus in the model
strongly associated with radiation; Hodgkin, non-Hodgkin, rectum,
and pancreas were cancers rarely associated with radiation. The lnlie p ai ee be I p
third sub-group, other, included all but cancer sites strongly or
rarely associated with radiation and breast, prostate, lung and where indicator Ip equals 1 for the post-Chernobyl periods and 0
basal cell carcinomas. otherwise. In the model, RRe = exp(be) is the RR in the exposure

Table 1
Numbers of person-years and cancer cases by age at the time of the Chernobyl accident in four exposure areas dened based on the 1st year dose from external radiation from
the accident (mSv) in ve calendar periods.

Males Females
19811985 19881992 19931997 19982002 20032007 19811985 19881992 19931997 19982002 20032007

059 years at accident
<0.1 mSv 2,160,707 1,952,799 1,905,526 1,845,858 1,777,880 1,941,082 1,773,867 1,748,932 1,717,401 1,681,226
0.1<0.3 1,459,151 1,317,979 1,287,451 1,249,984 1,205,894 1,319,488 1,200,343 1,183,166 1,162,537 1,138,853
0.3<0.5 696,416 530,687 517,509 500,719 481,564 624,136 477,953 471,104 462,880 453,088
0.5 243,141 213,724 208,828 202,242 194,632 218,952 195,625 192,912 189,643 185,712
Total 4,559,414 4,015,189 3,919,315 3,798,804 3,659,970 4,103,659 3,647,788 3,596,113 3,532,461 3,458,878
60+ years at accident
<0.1 mSv 470,681 251,111 184,968 124,915 77,414 605,539 344,724 276,314 205,174 140,311
0.1<0.3 367,595 207,606 152,341 103,318 64,496 494,037 294,739 236,407 176,109 121,488
0.3<0.5 185,157 88,376 64,226 43,069 26,764 250,400 127,138 101,572 75,027 50,969
0.5 64,067 33,118 24,232 16,344 10,056 86,421 47,623 37,952 27,994 19,220
Total 1,087,501 580,211 425,768 287,647 178,730 1,436,397 814,224 652,245 484,303 331,988

Cancer cases
059 years at accident
<0.1 mSv 1365 2046 2956 4009 5487 1259 1896 2855 3606 4814
0.1<0.3 939 1428 2028 2896 3843 964 1301 2039 2737 3376
0.3<0.5 452 600 888 1215 1575 434 551 810 1095 1468
0.5 137 229 350 473 631 148 215 327 409 577
Total 2893 4303 6222 8593 11,536 2805 3963 6031 7847 10,235
60+ years at accident
<0.1 mSv 3807 2769 2600 2066 1446 4120 3070 2859 2400 1845
0.1<0.3 3039 2374 2171 1715 1172 3466 2788 2714 2191 1735
0.3<0.5 1492 1017 915 654 508 1771 1204 1116 971 762
0.5 519 361 321 267 191 590 447 422 355 270
Total 8857 6521 6007 4702 3317 9947 7509 7111 5917 4612
Inclusion criterion on one-year permanent residency was not implied in the pre-Chernobyl period, therefore the cohort is larger.
P. Kurttio et al. / Cancer Epidemiology 37 (2013) 585592 589

Table 2
Overall cancer incidence rate ratios (RR, exposure-specic incidence rates in 19811985 as reference) and excess incidence RR (ERR, %, the lowest exposure area as reference)
by age at accident in males and females and calendar periods. ERR per incremental exposure unit (multiplicative ERR, %) indicates a potential trend.a

Calendar period Exposure 059 years at accident 60+ years at accident

RR 95% CIb ERR 95% CI Pc RR 95% CI ERR 95% CI P

19881992 <0.1 1.00 0.93, 1.09 0.0 0.651 1.04 0.99, 1.12 0.0 0.625
0.1<0.3 1.01 0.93, 1.11 0.9 10.1, 13.3 1.07 1.01, 1.13 3.0 4.3, 11.0
0.3<0.5 1.01 0.88, 1.15 0.3 13.9, 16.8 1.10 1.02, 1.20 6.2 3.4, 16.8
0.5 1.17 0.93, 1.47 16.6 8.1, 48.0 1.04 0.91, 1.19 0.3 13.3, 16.0
Multiplicative ERR 2.4 3.3, 8.5 1.7 2.0, 5.5
19931997 <0.1 1.03 0.96, 1.09 0.0 0.296 1.08 1.02, 1.17 0.0 0.492
0.1<0.3 1.01 0.93, 1.11 2.1 12.8, 9.8 1.11 1.05, 1.18 3.1 4.7, 11.6
0.3<0.5 1.05 0.92, 1.20 1.9 12.4, 18.5 1.14 1.04, 1.24 5.8 4.5, 17.2
0.5 1.28 1.02, 1.59 23.3 2.4, 55.8 1.02 0.88, 1.18 5.7 19.3, 10.2
Multiplicative ERR 3.4 2.3, 9.5 0.6 3.2, 4.6
19982002 <0.1 1.03 0.96, 1.14 0.0 0.520 1.07 1.01, 1.19 0.0 0.417
0.1<0.3 1.06 0.97, 1.16 2.9 8.2, 15.4 1.12 1.05, 1.20 4.6 4.5, 14.4
0.3<0.5 1.06 0.92, 1.21 2.8 11.7, 19.6 1.01 0.91, 1.12 5.6 16.1, 6.2
0.5 1.23 0.98, 1.54 19.5 5.6, 51.2 1.08 0.92, 1.28 1.1 15.1, 20.5
Multiplicative ERR 3.6 2.2, 9.7 0.8 5.1, 3.7
20032007 <0.1 1.08 1.00, 1.17 0.0 0.236 1.06 0.98, 1.18 0.0 0.952
0.1<0.3 1.09 0.99, 1.19 0.6 10.3, 12.9 1.09 1.00, 1.19 2.6 8.3, 14.8
0.3<0.5 1.20 1.05, 1.37 11.0 4.5, 29.0 1.05 0.93, 1.18 1.3 14.3, 13.7
0.5 1.32 1.05, 1.65 21.6 4.0, 54.1 1.06 0.86, 1.29 0.7 19.7, 23.0
Multiplicative ERR 5.5 0.4, 11.7 0.3 5.5, 5.3

19881992 <0.1 1.10 1.02, 1.03 0.0 0.114 1.04 0.99, 1.13 0.0 0.657
0.1<0.3 0.96 0.87, 1.05 12.9 22.5, 2.1 1.07 1.02, 1.13 3.7 3.3, 11.1
0.3<0.5 1.07 0.93, 1.23 2.5 16.5, 13.9 1.08 1.00, 1.16 4.0 4.8, 13.6
0.5 1.12 0.90, 1.40 2.1 19.2, 29.0 1.09 0.97, 1.24 5.7 7.5, 20.8
Multiplicative ERR 1.5 7.1, 4.4 2.0 1.4, 5.5
19931997 <0.1 1.26 1.17, 1.19 0.0 0.164 1.00 0.95, 1.14 0.0 0.247
0.1<0.3 1.11 1.01, 1.21 12.0 21.4, 1.5 1.08 1.02, 1.14 7.9 0.3, 16.0
0.3<0.5 1.16 1.02, 1.33 7.4 20.5, 7.8 1.04 0.96, 1.13 4.0 5.2, 14.2
0.5 1.23 0.99, 1.53 2.2 22.2, 22.9 1.04 0.91, 1.18 3.5 9.9, 19.0
Multiplicative ERR 3.2 8.6, 2.4 1.9 1.7, 5.6
19982002 <0.1 1.16 1.07, 1.19 0.0 0.834 0.95 0.90, 1.05 0.0 0.333
0.1<0.3 1.10 1.01, 1.20 4.9 15.1, 6.6 0.99 0.93, 1.05 3.7 4.4, 12.5
0.3<0.5 1.14 0.99, 1.30 2.0 16.0, 14.2 1.05 0.96, 1.14 10.1 0.7, 22.0
0.5 1.18 0.95, 1.47 2.0 19.0, 28.5 0.99 0.86, 1.15 4.3 10.6, 21.6
Multiplicative ERR 0.6 6.2, 5.3 3.1 0.8, 7.3
20032007 <0.1 1.19 1.11, 1.15 0.0 0.087 0.92 0.86, 1.03 0.0 0.081
0.1<0.3 1.06 0.97, 1.16 11.2 20.9, 0.2 0.96 0.90, 1.03 5.3 4.3, 15.7
0.3<0.5 1.26 1.11, 1.44 5.8 9.2, 23.2 1.07 0.97, 1.19 17.3 3.9, 32.3
0.5 1.25 1.01, 1.55 4.6 16.9, 31.7 0.95 0.80, 1.12 3.6 13.5, 24.2
Multiplicative ERR 1.0 4.7, 6.9 4.7 0.1, 9.6
ERR per incremental exposure unit when numerical values for exposure areas are: 1, if exposure area (exp) < 0.1; 2, if 0.1  exp < 0.3; 3, if 0.3  exp < 0.5; 4, if
exp  0.5 mSv/1st year.
95% condence interval.
P-value for H0: same RR in every exposure area.

area e in a post-Chernobyl period using the incidence rate in the periods were excluded (see Supplementary Fig. S1). With this
corresponding area in the pre-Chernobyl period 19811985 as the restriction of the data the ageing of the cohort was properly taken
reference. The heterogeneity in the RRs was tested with the into account by including the 5-year groups of attained age in the
likelihood ratio test. The excess RR (ERR) in exposure area e relative model. Therefore, the increase in cancer incidence due to the
to the RR in the exposure area 1 is written as ERRe = exp(be  b1)  1, ageing of the cohorts (Fig. 2) does not affect the RRs and ERRs
1, i.e., RRe is (ERRe + 1)-fold compared to RR1. (Table 2). In the municipality level analysis incidence rate ratios
To test for the trend in the exposure area -specic RRs the effect between the four exposure areas in period 19661985 were
of the increasing exposure was modelled using a numerical estimated using Poisson regression. In addition to the main effect
exposure variable e such that be = b + (e  1)g. In the model with of exposure area, the effects of the combinations of 5-year age
the numerical exposure variable, ERR = exp(g)  1 is the excess RR groups (the same groups as in the main analysis) and 5-year
per incremental exposure unit (multiplicative ERR), i.e., the RRs in calendar periods (19661971, . . ., 19811985) were included in
exposure areas 24 are exp(g), exp(2g) and exp(3g)-fold, the regression model.
respectively, compared to the RR in exposure area 1 (reference). R environment for statistical computing and graphics [14] was
Two age groups at the time of the accident (059 and 60+ years, used in the analyses. The Poisson regression models were tted
also referred as younger and older) by sex were analyzed using the glm function in R.
separately. The pre-Chernobyl cohort was divided into these age
groups according to persons potential age at accident (see 2.5. Ethical issues
Supplementary material for further details). To obtain the most
unbiased estimates the analysis of RRs was restricted to the pre- No condentiality issues arose, as no individual-level data were
Chernobyl and the study cohort within the same birth cohort and used in the analyses and the units of observation were too large for
the 5-year groups of attained age that do not exist in the both identifying individuals. A permission to use the Cancer Registry
590 P. Kurttio et al. / Cancer Epidemiology 37 (2013) 585592

per 100 000 Males
2000 Chernobyl
accident (1986)

1st year dose
500 (mSv)
< 0.1
0.1 < 0.3
200 0.3 < 0.5


1981 1988 1993 1998 2003
1985 1992 1997 2002 2007
per 100 000 Females
2000 Chernobyl
accident (1986)

1st year dose
500 (mSv)
< 0.1
0.1 < 0.3
200 0.3 < 0.5


1981 1988 1993 1998 2003
1985 1992 1997 2002 2007
Fig. 2. Age-standardized incidence rates of overall cancer in four exposure areas in ve 5-year calendar periods for males and females. Lower bars in front represent 059 years
olds at accident and taller bars behind represent 60+ years olds at accident. Increase in cancer incidences reects ageing of the cohorts. Bars in 19811985 represent the
baseline incidence rates of the pre-Chernobyl cohort in the corresponding exposure areas.

data was issued by the National Institute for Health and Welfare. A low background cancer incidence in 19811985 among
The in-house ethical committee at Radiation and Nuclear Safety younger men (aged 059 years at the time of the accident) was
Authority was notied of the study protocol. According to the observed in the highest exposure area (Fig. 2). In the municipality
Finnish regulations registry based studies are exempt from ethical level analysis on extended pre-Chernobyl accident period, from
committee review. Good research practice was followed in data 1966 to 1985, the incidence rate among these younger men in the
management and analyses to ensure data protection. municipalities in the highest exposure area was 7% (95% CI 7 to
18%) lower than that in the other municipalities on average
3. Results (Results not shown). After the accident, the incidence rates of the
younger men in all exposure areas, and especially in the highest
The age-standardized overall cancer incidence (excluding exposure area, tended to be higher than before the accident, but
breast, prostate and lung cancers) in the calendar periods before the RRs did not differ statistically signicantly by exposure area
and after the Chernobyl accident by exposure area is shown in (Table 2). Among the younger males in the latest calendar period of
Fig. 2. The increased cancer incidence by calendar time reects 20032007, the multiplicative ERR per exposure area was elevated
mainly the ageing of the cohorts. Tests for heterogeneity indicated with a borderline statistical signicance (ERR 5.5%, 95% CI 0.4 to
that the age-standardized RRs did not differ signicantly between 11.7%). This elevation was due to the group of other cancer sites
exposure areas in the rst two calendar periods (i.e., decade after and not found for those strongly or rarely associated with radiation
the accident) or any other post-Chernobyl calendar period, or in (Supplementary Table S1).
either sex or within any age group (Table 2). Furthermore, the ERRs Among the younger females the RRs after the accident in all
with the lowest exposure area as reference did not indicate exposure areas tended to be higher than before the accident, but no
statistically signicant changes per incremental exposure unit. statistically signicant trend by exposure was observed (Table 2).
P. Kurttio et al. / Cancer Epidemiology 37 (2013) 585592 591

Among the older females the multiplicative ERR per incremen- short latency claimed for the increase in cancer in the Chernobyl
tal exposure unit during the last calendar period of 20032007 was affected regions of Sweden, this mechanism would most likely
marginally elevated (ERR 4.7%, 95% CI 0.1 to 9.6%), but the RRs account for the effect. However, the somatic mutation theory has
were consistently lower than during the pre-Chernobyl period increasingly been questioned on the grounds of the accumulating
(Table 2). A similar pattern was also seen in a sub-analysis on the evidence that epigenetic process play a role in carcinogenesis
radiation-related cancer sites (Supplementary Table S1). [17,18]. Genomic instability would appear to be equally likely a
driver of radiation-induced cancer as mutation and indeed a model
4. Discussion has been proposed [19]. If genomic instability is the driver of
carcinogenesis, then a promotional effect, if any, might be expected
The aim in the current study was to examine a potential to be weak.
promoting effect (rapid increase in cancer incidence) of the fallout Since no complete retrospective individual dose measurements
from the Chernobyl accident, particularly in the initial 10 years for the population of this size could have been arranged we had to
following the accident (19881997). A promoting effect would rely on the other source of information on exposure. In the Swedish
bring forward cancer that may occur later in life and thus increase study [5,6], the exposure areas were classied based on deposition
the incidence in the early post-exposure period. No consistent (kBq/m2) and dose rate (nGy/h) while in the current study, we
indication of a promotion effect was observed in the comprehen- estimated external dose during the rst year after the accident
sive analysis using the pre-Chernobyl incidence rates or the lowest (mSv) taking into account average time spent indoors, shielding
exposure area as references. and washout of the radionuclides in different surroundings. The
The borderline statistical signicant association between two exposure indicators are correlated, but our approach is more
cancer incidence and radiation exposure was observed among rened and likely to provide a more valid measure of the relevant
younger males for the latest calendar period (20032007). This exposure (by virtue of restricting the analysis to single family
was interpreted as reecting the low pre-Chernobyl cancer houses only).
incidence among young men in the highest exposure area The exposure indicator was a proxy for the committed dose
increased after the accident and reached that of the other areas. from the Chernobyl fallout. The rst-year external dose used in the
This increase was due to other cancer sites, not those previously current study can be estimated to represent about 64% of the total
associated with radiation. It is not known why younger men had rst-year dose including internal and external doses and 37% of the
low cancer incidence prior to the accident in the areas, which total dose received during the rst ten years [20]. We limited the
received the highest fallout. current analysis to detached, semidetached and terraced houses
In the main analysis we divided the study population into two only, due to different shielding factors applicable to different house
groups based on age at accident, because radiation can have types. In the urban areas including mainly blocks of ats, building
different effects depending on age. Similar age group of younger materials shield better against gamma radiation and radioactivity
than 60 years olds were used in Tondel et al. study [6]. Radiation- is washed out from surroundings more efciently than in suburban
related promotional processes, i.e., promotion of pre-existing and rural areas. The exposure was estimated using the location of
premalignant cells, have been suggested especially for older ages at the residence, and no data on work places or other relevant
exposure [15]. In the current study, no such effect was observed. In locations such as summer houses were available and could not be
the current study, a short latency period between the accident and considered. We do not have information on whether the
cancer incidence was focused in, exposure levels were low, and population living in the single family houses is similar as regards
small cancer effect was expected. Therefore, it was not feasible to their habits and intake of wild mushrooms, berries, sh and game
analyze data on only children at the time of the accident because of meat, which are the major route on internal dose of radionuclides
low number of cancer cases among young people. from the Chernobyl fallout. No small area geographical data on
The current study does not support the hypothesis regarding a internal exposure due to food contaminated with the Chernobyl
promotion effect of cancers due to low doses from the Chernobyl fallout were available. However, internal and external doses due to
fallout. Thus, we could not conrm the ndings of the Swedish the fallout are correlated [21]. The exposure estimation in the
study, in which the overall cancer incidence was associated with current study is thus a surrogate of the actual exposure from the
the radiation exposure within a few years after the accident [5,6]. Chernobyl fallout because internal exposure could not be
Some warranty still remains as the highest deposit category estimated at the small area level. The dose estimation is prone
(46 kBq 137Cs/m2) in the current study was lower than that in the to underestimation and misclassication. Therefore, the quantita-
Swedish study (80120 kBq 137Cs/m2). Furthermore, even with our tive risk estimates incorporate substantial uncertainty and
large and comprehensive data of Finnish population we may lack quantitative risk estimation was not performed.
the power of detecting such effect. Due to the relatively low radiation doses received from the
According to the current theoretical understanding of the fallout, the effect of the Chernobyl accident in Finland was
effects of radiation, the induction of mutations at the time of expected to be small. Therefore, it was essential to use a large study
exposure is the primary radiation-related event leading to cancer. population and obtain accurate exposure estimates. Finland
However, as carcinogenesis is a multi-stage process, other later provided an excellent opportunity for such a study because of
occurring events contribute to the process, which typically for solid the reliable national population-based registers. We restricted the
cancers takes up to several decades. The dominant theory of analysis to the population with a stable residence with the highest
carcinogenesis is the so-called somatic mutation theory [16], exposure and included data on around 2,000,000 persons in the
which, in the case of an acute exposure to radiation, would current study.
envisage the spontaneous acquisition of mutations as constituting Due to the multi-factorial aetiology of cancers and high
the later stages of the process. Under this model, ambient radiation potential for confounding, control for other risk factors for cancer
during the development of a cancer would act as an additional was recognized as essential. For this purpose, the underlying
source of mutations and thus promote the carcinogenic process, differences in cancer incidence rates before the accident were
bringing the diagnosis forward in time. As in any population there assessed in the areas with contrasting levels of radiation exposure.
will be a substantial prevalence of subclinical cancers (mostly They represent the aggregate effect of confounding factors and
unrelated to radiation), a promoting effect of ambient radiation provide expected incidence rates in the absence of fallout. The
would lead to an apparent increase in cancer incidence. Given the baseline comparison of pre-existing geographical differences was
592 P. Kurttio et al. / Cancer Epidemiology 37 (2013) 585592

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