RADIATION RESEARCH 182, 599–606 (2014)0033-7587/14 $15.00
Ó2014 by Radiation Research Society.
All rights of reproduction in any form reserved.
DOI: 10.1667/RR13822.1

Long-Term Effects of the Rain Exposure Shortly after the Atomic Bombings
in Hiroshima and Nagasaki
Ritsu Sakata,a,1 Eric J. Grant,a Kyoji Furukawa,b Munechika Misumi,b Harry Cullings,b Kotaro Ozasaa and Roy E.
Shoreca

Department of Epidemiology, b Department of Statistics and c Vice Chairman and Chief of Research, Radiation Effects Research Foundation,
Hiroshima, Japan

uncertainties regarding exposures and missing individual
data, so cautious interpretation is advised. Ó 2014 by Radiation

Sakata, R., Grant, E. J., Furukawa, K., Misumi, M.,
Cullings, H., Ozasa, K. and Shore, R. E. Long-Term Effectsof the Rain Exposure Shortly after the Atomic Bombings
in Hiroshima and Nagasaki. Radiat. Res. 182, 599–606(2014).

Research Society

The ‘‘black rain’’ that fell after the atomic bombings ofHiroshima and Nagasaki has been generally believed tocontain radioactive materials. During 1949–1961 theAtomic Bomb Casualty Commission conducted surveys
that included a query about exposure to the rain that fell ashort time after the bombings. This article presents thefirst report of those data in relation to possible adverse
health outcomes. This study looked at Life Span Study
subjects who were in either city at the time of bombing andhad an estimated direct radiation dose from the bombs (n¼ 86,609). The mortality data from 1950–2005 and cancer
incidence data from 1958–2005 were used. Excess relative
risks (ERRs) of subjects who were exposed to raincompared to those who reported no rain exposure were
calculated using a Poisson regression model. In Hiroshima
11,661 subjects (20%) reported that they were exposed torain, while in Nagasaki only 733 subjects (2.6%) reported
rain exposure. To avoid outcome dependent biases (i.e.,
recall of exposure after a health outcome has alreadyoccurred), the primary analyses were based on events that
occurred during 1962–2005. No significant risks due to rain
exposure were observed for death due to all causes, allsolid cancer or leukemia in Hiroshima. In Nagasaki there
was no significantly elevated rain exposure-associated risks
for 1962–2005, however, for 1950–2005 there was a weakassociation for all-cause mortality (ERR ¼ 0.08; 95%
confidence interval 0.00006, 0.17; P ¼ 0.05). For incidenceof solid cancer and leukemia, no significantly elevated rain
exposure risks were observed in either city. These results
failed to show deleterious health effects from rain
exposure. While these data represent the most extensive
set of systematically collected data on rain exposure of theatomic bomb survivors, they are limited by substantial

INTRODUCTION

Shortly after the atomic bombings in Hiroshima andNagasaki, it was reported that rain fell widely in the cities
out to areas several kilometers from the hypocenter. Sincemuch of the rain was dirty with soot and ash, it was called‘‘black rain’’. The rain likely originated from the ascending
air currents of both the fireball from the atomic bomb
explosion and the widespread fires that burned throughout
the cities after the bombings. It has been generally believedthat this rain contained radioactive materials, though thedegree of radioactivity probably varied considerably
depending on how much the rain was associated with theradioactive plume. Increased amounts of ground level
radioactivity due to rain fallout were observed: a small
increase (;45 lR/h) at Koi-Takasu in western Hiroshima
and a large increase (;1.8 mR/h) at Nishiyama in eastern
Nagasaki (1), though rainfall was widely reported in theother areas, especially Hiroshima (2–4). Although measurements made within a few months after the bombing did notindicate that rain contained significant radioactivity in areas
other than Koi-Takasu and Nishiyama (1), the public
perception has been that all black rain was highly
radioactive, and therefore its health effects have long beena public concern.
Information about ‘‘fallout rain’’ exposure was gatheredfrom several surveys conducted by the Atomic Bomb
Casualty Commission (ABCC), the predecessor of the
Radiation Effects Research Foundation (RERF), in the early
period after the bombings. However, these data were
thought to be inadequate for quantitative risk analyses
because it was not possible to estimate individual doses,
given the dichotomous nature of the exposure information,
absence of location-specific data on the radioactivity
concentration of the rain, lack of information on the

Editor’s note. The online version of this article (DOI: 10.1667/
RR13822.1) contains supplementary information that is available to
all authorized users.
1 Address for correspondence: Department of Epidemiology,
Radiation Effects Research Foundation, 5-2 Hijiyama-park, Minami-ku, Hiroshima, 732-0815, Japan; e-mail: rsakata@rerf.or.jp.
599

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SAKATA ET AL.

evacuation routes used by most subjects and paucity of
individual information regarding shielding from fallout
radiation and/or ingestion of radioactive substances present
in the rain. The data were further limited because no
information on exposure to fallout rain was available for aconsiderable proportion of the subjects, and for those who
responded that they had been exposed, the location at which
exposure occurred was often unavailable. From a dosimetricperspective, it is also unclear whether survivors whoreported that they were exposed to the rain were actuallyin contact with rainwater or were merely in an area whererain fell, and there was no information on the extent of bodysurface area, duration of skin contact with the rainwater,
protective effect of clothing, or other factors related to either
internal or short-range external exposure to radiation fromany radioactive material that might have been in the rain.
However, upon reconsideration and re-evaluation of the
ABCC/RERF records on fallout rain exposure along with
the RERF mortality and cancer incidence data, it was
decided this information may be of interest in light of publicconcerns. Therefore, we investigated whether subjects whoreported exposure to fallout rain have higher long-term
health risks compared to those whose survey response
indicated that they had not been exposed to rain.
METHODS
The ABCC/RERF Life Span Study (LSS) is a prospective study of a
fixed cohort of atomic bomb survivors followed since 1950. The
ABCC conducted several baseline surveys to document the survivors’situations at the time of bombing and shortly thereafter with various
primary objectives and inclusion criteria between 1949–1961.
Questions about exposure to the rain were included in the two majorinterview surveys: the Migration Questionnaire (MQ), conducted in
1955–1956, and the Master Sample Questionnaire (MSQ), conducted
in 1956–1961. The MQ questions were, ‘‘Was the person caught inFallout Rain?’’ (Yes or No) plus ‘‘Where’’ and ‘‘Time’’ with boxes forfree-form description. The MSQ questions were, ‘‘Was the person
caught in Fallout Rain?’’ (Yes, No or Unknown) and ‘‘Where’’ with abox for a free-form description. The words ‘‘Fallout Rain’’ were usedin the questions written in English. However, a more accuratetranslation of the question as asked in Japanese was ‘‘Were you caught
in rain just after the atomic bombing?’’ The rain exposure status ofsubjects was classified as ‘‘yes’’, ‘‘no’’ or ‘‘unknown’’ based on thequestionnaires. If the reported rain exposure status was inconsistent
between the MQ and MSQ, the exposure status recorded in the MSQ
was given higher priority because the MSQ was conducted for more
subjects and is considered the most reliable baseline survey. Questions
regarding exposure to the rain were not included in any of the otherbaseline surveys: the Radiation Census, the Radiation Questionnaire,
and the Nonmedical Radiation History, which were conducted in
1949–1953, 1953–1955 and 1951–1954, respectively. However,infrequently information about exposure to the rain was described in
the margins of these surveys. For subjects who did not participate ineither the MQ or MSQ (10% of the subjects in this study), if
information about rain exposure was obtained from another survey
conducted by the ABCC, that information was used. Subjects whose
questionnaires were left blank for questions regarding fallout rain
[Hiroshima; 16,442 (28%), Nagasaki; 3,053 (11%)] were included inthe ‘‘unknown’’ category, although reasons for leaving these questions
blank remain unclear. Eligible subjects for this study were defined as

LSS cohort members who were in either city at the time of thebombing and had an estimated DS02 (5) radiation dose (n ¼ 86,609).
The date of entry for the mortality study was 1 October 1950, which isalso the date that comprehensive mortality follow-up was initiated.
The date of entry into the cancer incidence study was 1 January 1958,
which is the date that population-based tumor registries were
established in Hiroshima and Nagasaki. Follow-up data on mortality
and cancer incidence until 31 December 2005 were used in theanalysis. Mortality data were derived from Japan’s mandatory family
registry system (koseki), while cancer incidence was derived from theHiroshima and Nagasaki population-based cancer registries. Analyses
for solid cancer and leukemia incidence were adjusted to allow for
migration. Detailed descriptions about the definition of the study
population, follow-up of vital status, cause of death, cancer incidence
and migration rate adjustments have been reported elsewhere (6–8).
Mortality and cancer incidence follow-up data overlapped with thetime the fallout exposure data were being gathered (late 1940s to1961). Furthermore, the computerized data do not contain the dates
that the questionnaire information was ascertained or who supplied theprimary information. Therefore, it could not be determined whether
those who were incapacitated by cancer or other severe disease, or
who died before 1962, may have been more likely to have missing
data or have unknown/inaccurate responses from surrogates. Thus,
two sets of analyses were performed, one for the entire follow-up
period (potentially influenced by concurrent data acquisition,
particularly by surrogates) and the other beginning in 1962 after allquestionnaires had been completed. We consider the analyses for theperiod beginning in 1962 to be the primary analyses; the results fromthe analyses using the entire follow-up period are shown forcomparison with results from other LSS reports.
The effects of exposure to rain were estimated by city because
meteorological conditions and fallout materials contained in the rain
were assumed to be different between Hiroshima and Nagasaki. The
dependent variables examined were mortality rate (all cause, all solidcancer and leukemia) and cancer incidence rate (all solid cancer andleukemia). Using a Poisson rate regression, we modeled the rate ofeach end point by the form,k0 ðc; s; b; aÞ½1 þ ðb1 d þ crainhiro yes þ drainnaga yes Þ expðse þ tlnðaÞÞ  rs þ erainhiro unk þ frainnaga unk :This model estimates excess relative risk (ERR) above the baselinerisks (k0), which are described nonparametrically using stratification
by city (c), sex (s), birth year (b) with 10-year categories and attainedage (a) with 10-year categories. We included the effects of caught-inrain status (rainhiro_yes, rainnaga_yes, rainhiro_unk, rainnaga_unk) as an addition
to the model of the direct radiation dose (d), where the effect of total
radiation (both direct and rain) could be modified by age at exposure(e), sex and attained age.
As in previous reports (6, 7), we used the linear model (b1d) for the
direct radiation dose response in all but analyses for leukemia
outcomes. A linear-quadratic model for direct radiation dose (b1d þb2d2) was used for both leukemia mortality and incidence, because
previous LSS reports indicated that a linear-quadratic model is more
appropriate for leukemia among the LSS subjects.
In the above model, both direct and fallout exposures are treated ina biologically consistent manner, i.e., as potentially additive radiation
doses with parallel modification by age at exposure, attained age andsex (‘‘common effect modification model’’). In addition, we tested
another model assuming that the rain effects did not vary with sex, age
at exposure and attained age (‘‘no rain effect modification model’’).
For leukemia incidence, estimates based on the no rain effectmodification model are shown in Table 2, because the common effectmodification model did not converge. Full results from supplemental
analyses using the no effect modification model (‘‘direct exposure
only model’’) are available in the supplementary materials (http://dx.
doi.org/10.1667/RR13822.1.S1).

601

EFFECTS OF RAIN EXPOSURE SHORTLY AFTER A-BOMBINGSTABLE 1
Distribution of Subjects by Caught-in-Fallout Rain Status
Caught in fallout rain?
No
Items

Yes

n

(%)

n

Unknown
(%)

n

Total
(%)

n

(%)

Hiroshima
29,254Sex
Male
11,835
Female17,419Age at the time of bombing (years)
0–9
5,354
10–19
5,686
20–29
3,748
30–39
4,548
40–49
5,005
Over 50
4,913
Mean age
29.84(SD)(18.82)
Weighted absorbed colon dose (Gy)0–0.004
13,6460.005–0.09
10,908
0.1–0.4
3,436
0.5–0.9770
1–494
Nagasaki
23,664
Sex
Male
9,799
Female13,865Age at the time of bombing (years)
0–9
6,069
10–19
5,353
20–29
2,752
30–39
2,808
40–49
3,253
Over 50
3,429
Mean age27.88(SD)(18.02)
Weighted absorbed colon dose (Gy)0–0.004
14,6550.005–0.09
6,065
0.1–0.4
1,694
0.5–0.9712
1–
538

11,661

17,57758,492(40.5)(59.5)

4,606
7,055

(39.5)(60.5)

7,523
10,054(42.8)(57.2)

23,96434,528(41.0)(59.0)(18.3)(19.4)(12.8)(15.5)(17.1)(16.8)

2,213
2,091
1,580
1,951
1,983
1,843
29.49
(18.48)(19.0)(17.9)(13.5)(16.7)(17.0)(15.8)

3,420
3,146
2,246
2,466
2,738
3,561
29.29
(18.79)(19.5)(17.9)(12.8)(14.0)(15.6)(20.3)

10,987
10,923
7,574
8,965
9,726
10,317
29.54(18.70)(18.8)(18.7)(12.9)(15.3)(16.6)(17.6)(46.6)(37.3)(11.7)
(2.6)
(1.7)

2,869
4,706
2,851
794
441

(24.6)(40.4)(24.4)
(6.8)
(3.8)

5,181
7,118
3,817
809
652

(29.5)(40.5)(21.7)(4.6)(3.7)

21,696
22,732
10,1042,373
1,587(37.1)(38.9)(17.3)
(4.1)
(2.7)

733

3,720

28,117(41.4)(58.6)

299
434(40.8)(59.2)

1625
2095(43.7)(56.3)

11,723
16,394(41.7)(58.3)(25.6)(22.6)(11.6)(11.9)(13.7)(14.5)

165
233
92
85
91
67
22.91
(15.93)(22.5)(31.8)(12.6)(11.6)(12.4)
(9.1)

610
1,055
473
411
434
737
25.68
(17.51)(16.4)(28.4)(12.7)(11.0)(11.7)(19.8)

6,844
6,641
3,317
3,304
3,778
4,233
26.23
(17.58)(24.3)(23.6)(11.8)(11.8)(13.4)(15.1)(61.9)(25.6)
(7.2)
(3.0)
(2.3)

351
210
85
57
30

(47.9)(28.6)(11.6)
(7.8)
(4.1)

1,806
953
447
282
232

(48.5)(25.6)(12.0)(7.6)(6.2)

16,812
7,228
2,226
1,051
800

(59.8)(25.7)
(7.9)
(3.7)
(2.8)

Model fits were compared based on the likelihood ratio tests (atsignificance level a ¼ 0.05) for nested models or the Akaike
Information Criteria (AIC) (9) for non-nested models. The ERRs ofrain exposure were estimated as the increase in the relative risk
compared to those who were not exposed to rain but had the same
estimated direct radiation dose. Parameter estimation and testing were
performed using the Epicure program (10).

RESULTS

Among the 86,609 eligible LSS subjects, 42,050 (72%)
subjects in Hiroshima and 25,064 (89%) subjects in
Nagasaki had ‘‘yes’’, ‘‘no’’ or ‘‘unknown’’ rain exposure
information available from the baseline surveys (the balance
had missing information). In Hiroshima, 11,661 subjects(20%) reported that they were exposed to rain, while only

733 subjects (2.6%) in Nagasaki reported rain exposure(Table 1). The distribution of subjects by age at the time of
the bombings was relatively similar in Hiroshima. In
Nagasaki, the distribution was skewed, where 48% of the
respondents were less than 20 years old at the time of thebombing. In Hiroshima, the proportion of survivors whoreported rain exposure was nearly the same in all age groups
while teens in Nagasaki had the highest proportion ofreported rain exposure (3.5% vs. the city average of 2.6%).
The percentage of subjects whose rain exposure was
unknown was relatively high among the teenage group in
Nagasaki, as well as those over 50 years old in both cities.
Subjects who reported no rain exposure tended to havelower direct radiation doses (i.e., they were more distally
located at the time of the bombing).

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SAKATA ET AL.

TABLE 2
Excess Relative Risks for Exposure to Fallout Rain with 95% Confidence Intervals for All Causes of Death, Solid Cancer
Death, Leukemia Death, Solid Cancer Incidence and Leukemia Incidence
Outcomes
1962–2005
All cause of death
Solid cancer death
Leukemia death
Solid cancer incidence
Leukemia incidence#
1950–2005
All cause of death
Solid cancer death
Leukemia death
1958–2005
Solid cancer incidence#
Leukemia incidence#

Hiroshima

Nagasaki

Fallout rainstatusNo. of cases

ERRa

95% CIb

No. of cases

ERR

95% CINo
Yes
UnknownNo
Yes
UnknownNo
Yes
UnknownNo
Yes
UnknownNo
Yes
Unknown

15,997
6,381
7,941
3,573
1,483
1,892
89
49
47
5,653
2,283
3,026
79
46
45

0.00
–0.03
0.004
0.00
–0.04
–0.01
0.00
0.05
–0.13
0.00
–0.06
–0.02
0.00
0.26
–0.03

Reference group(0.06, 0.01)(0.02, 0.03)
Reference group(0.08, 0.01)(0.07, 0.05)
Reference group(0.36*, 0.56)(0.44, 0.30)
Reference group(0.10, 0.03)(0.07, 0.03)
Reference group(0.21, 1.05)(0.39, 0.47)

10,865
349
1,348
2,654
106
353
65
2
13
3,849
106
459
46
1
11

0.00
0.08
0.02
0.00
0.15
–0.03
0.00
–0.18
0.35
0.00
–0.09
–0.19
0.00
–0.79
0.48

Reference group(0.008, 0.18)(0.04, 0.08)
Reference group(0.003, 0.36)(0.15, 0.09)
Reference group(1.39,* 1.02*)(0.40, 1.63)
Reference group(0.19,* 0.03)(0.27, 0.10*)
Reference group(1.71, 2.03)(0.44, 2.15)

No
Yes
UnknownNo
Yes
UnknownNo
Yes
Unknown

18,322
7,294
11,315
3,970
1,633
2,460
111
69
68

0.00
0.01
0.26
0.00
–0.02
0.19
0.00
0.06
–0.13

Reference group(0.02, 0.04)(0.23, 0.29)
Reference group(0.06, 0.04)(0.13, 0.25)
Reference group(0.15,* 0.32)(0.41, 0.24)

13,060
394
2,289
2,937
109
451
79
3
20

0.00
0.08
0.43
0.00
0.14
0.15
0.00
–0.03
0.74

Reference group(0.00, 0.17)(0.36, 0.49)
Reference group(0.01, 0.33)(0.03, 0.27)
Reference group(0.07,* 0.02*)(0.10, 2.05)

No
Yes
UnknownNo
Yes
Unknown

5,982
2,430
3,196
91
51
50

0.00
–0.03
–0.006
0.00
0.11
–0.10

Reference group(0.08, 0.02)(0.05, 0.04)
Reference group(0.30, 0.70)(0.42, 0.36)

4,045
106
475
53
1
12

0.00
–0.21
–0.19
0.00
–0.90
0.35

Reference group(0.36, 0.04)(0.27, 0.10)
Reference group(1.53,* 1.63)(0.49, 1.85)

aExcess relative risk.
95% confidence interval.
* Likelihood-based estimation algorithm failed to identify an interval. A Wald-type confidence interval was calculated.
#
Estimates are based on the no effect modification for rain model, because the common effect modification model did not converge.
bFIG. 1. Sex-averaged mortality rate adjusted for birth year bycalendar year and caught-in-rain status.

Sex-averaged mortality rates adjusted for birth cohort (10year birth cohorts) by caught-in-rain status and calendar
year are shown in Fig. 1. This figure shows standardizedmortality rates calculated for calendar years 1950–1980.
After 1980, standardized rates became unstable due tosparse data for the earliest birth cohorts. Among those withunknown rain exposure, the mortality rate was considerably
higher in the years during which the baseline surveys wereconducted (1950–1961) but it was similar to those of otherrain status groups thereafter. This suggests that surrogate
interviewees probably were more likely to report unknown
rain exposure at the time of the survey if the actual bomb
survivor had already died.
Table 2 shows, by rain exposure status, the estimates of
all-cause mortality and both mortality from and incidence
for all solid cancer and leukemia. The number of leukemia
incidence cases was smaller than those of leukemia death

603

EFFECTS OF RAIN EXPOSURE SHORTLY AFTER A-BOMBINGSTABLE 3
Excess Relative Risks for Exposure to Fallout Rain with 95% Confidence Intervals for All Causes of Death, Solid Cancer
Death and Leukemia Death among Subjects Who Have Less than 5 mGy Weighted Absorbed Colon Dose
Cause of death
1962–2005
All causes of death
Solid cancer
Leukemia
1950–2005
All causes of death
Solid cancer
Leukemia

Hiroshima

Nagasaki

Fallout rainstatusNo. of deaths

ERRa

95% CIb

No. of deaths

ERR

95% CINo
Yes
UnknownNo
Yes
UnknownNo
Yes
Unknown

7,498
1,584
2,204
1,644
378
517
36
5
17

0.00
–0.03
0.03
0.00
–0.001
0.02
0.00
–0.36
0.47

Reference group(0.09, 0.02)(0.02, 0.08)
Reference group(0.00,* 0.00*)(0.07, 0.12)
Reference group(0.78, 0.48)(0.19, 1.32*)

6,640
161
621
1,557
43
155
15
0
5

0.00
0.01
0.08
0.00
0.05
0.02
0.00

Reference group(0.07,* 0.15)(0.01, 0.17)
Reference group(0.11,* 0.20*)(0.14, 0.20)
Reference groupNA(0.60, 2.43)

No
Yes
UnknownNo
Yes
UnknownNo
Yes
Unknown

8,573
1,795
3,442
1,822
409
710
42
9
19

0.00
–0.02
0.38
0.00
–0.001
0.27
0.00
–0.01
0.41

Reference group(0.04,* 0.01*)(0.33, 0.43)
Reference group(0.01,* 0.00*)(0.16, 0.38)
Reference group(0.54, 0.71*)(0.20, 1.17*)

8,085
182
1,114
1,730
44
203
34
0
7

0.00
–0.01
0.54
0.00
0.05
0.21
0.00

0.35

1.08

Reference group(0.04,* 0.02*)(0.45, 0.64)
Reference group(0.10,* 0.21*)(0.04, 0.39)
Reference groupNA(0.16, 3.44)

aExcess relative risk.
95% confidence interval.
* Likelihood-based estimation algorithm failed to identify an interval. A Wald-type confidence interval was calculated.
bcases for 1962–2005. This is driven by differences in theascertainment of events: deaths and cause of death are
obtained throughout Japan, while cancer incidence information is obtained only from Hiroshima and Nagasaki
tumor registry catchment areas.
In Hiroshima, no significantly increased risks from rain
exposure were observed for death due to all causes, all solidcancers or leukemia, or for the incidence of all solid cancers
or leukemia. This was true for both the 1962–2005 and1950–2005 analyses.
In Nagasaki, rain exposure showed no significantly
increased risk for any of the cancer outcomes or for allcause mortality for the 1962–2005 period. Although the risk
estimate for leukemia incidence could not be calculated
properly due to the small number of cases among persons
exposed to rain in Nagasaki, the number of cases did notappear to be elevated. For 1950–2005 a marginal association was suggested for death due to all causes (ERR ¼
0.08; 95% CI 0.00006, 0.17; P ¼ 0.05) (Table 2 andSupplementary Table S1; http://dx.doi.org/10.1667/
RR13822.1.S1). The magnitudes of the risk estimates due
to direct radiation were equivalent to previously publishedanalyses (6, 7).
To determine whether the rain exposure effect may havebeen masked by the direct radiation effects, analyses limited
to subjects with estimated weighted absorbed colon doseless than 5 mGy were carried out (Table 3). The direct
radiation term was omitted from these low-dose analyses.
All subjects were more than 2.2 km from the hypocenter at

the time of the bombing. No significantly increased risks for
persons exposed to rain were observed for deaths due to allcauses, all solid cancer or leukemia in either city.
Significant increased risks were observed for all-cause andsolid cancer death among those with unknown rain
exposure during 1950–2005.
Parameter estimates and model fit summary information
based on the models with and without variables of rain
exposure are shown in Supplementary Tables S1–S5 (http://dx.doi.org/10.1667/RR13822.1.S1). Over the full observation period, model fits for all-cause mortality, solid cancer
mortality and solid cancer incidence were significantly
improved by adding variables of rain exposure (P , 0.001).
However, the improved fits for the entire follow-up period
did not result from significant increases of risk for thosewith rain exposure; rather, those with unknown rain
exposure had significantly higher risks of death (6, 7).
The ERRs for death due to all causes and solid cancer
significantly increased among those with unknown rain
exposure in the full follow-up period. However, these risks
were not significant when the analysis period was limited to
the years after 1961. This tendency was observed in bothcities. Thus, the improvements of model fit for the entire
follow-up period and the elevated risk of death before 1962
appear to be related to the adjustment of those dying in theearliest period who predominantly had unknown/missing
rain exposure status.
In summary, in the period 1962–2005, which represents
estimates from data with suspected biases removed, there

604

SAKATA ET AL.

were no statistically significant increased risks associatedwith rain exposure for any of the outcomes examined: allcause mortality, all solid cancer mortality, leukemia
mortality, all solid cancer incidence or leukemia incidence.
For the period 1950–2005 (or 1958–2005 for cancer
incidence), all-cause mortality showed a marginal excess
in Nagasaki.
DISCUSSION

This is the first report that addresses the possibility of thelong-term risks of mortality and cancer incidence among
LSS cohort members due to the rain that fell in the cities
shortly after the atomic bombings.
In Hiroshima, the results consistently indicated that
exposure to rain was not significantly associated withincreased mortality or incidence for any end points: total
mortality, cancer mortality, solid cancer incidence orleukemia incidence. Conversely, increased ERRs for rain
exposure were observed in Nagasaki for all-cause death in
1950–2005 (Table 2 and Supplementary Table S1; http://dx.doi.org/10.1667/RR13822.1.S1) and for all solid cancer
death in 1962–2005 in the analysis using a model which
ignores effect modification (by sex, age at exposure andattained age) for rain effects [ERR ¼ 0.25; 95% CI: 0.01,
0.53; P ¼ 0.038 (Supplementary Table S2)], but thesefindings were inconsistent between models as well as
observation periods. There are several reasons that thepositive finding may be spurious. First, only 733 subjects(2.6%) in Nagasaki reported that they had been ‘‘caught inrain’’, which may be too few to provide reliable statisticalinference. Note that no positive association of rain
exposure with any outcome was observed in Hiroshima,
which had far greater statistical power to detect possible
effects because of the much larger number who indicatedrain exposure. Second, the association of direct radiation
exposure with cancer death is much stronger than that of
noncancer death (7) and many other studies have had
similar findings. Therefore, one would expect the risk ofrain exposure would be higher for cancer death comparedto all-cause deaths, yet they were similar (Table 2). Third,
radiation is known to elevate risks of both cancer mortality
and incidence, yet there was no increased risk of cancer
incidence after rain exposure in any model or city (Table2). Finally, leukemia is often taken to be a ‘‘sentinel’’indicator of radiation effects, but neither mortality nor
incidence of leukemia was significantly elevated in either
city.
Elevated risks of leukemia and cancer due to direct
radiation exposure were evident in this study and thoseeffects were consistent between the results for mortality andincidence outcomes (Supplementary Tables S1–S5; http://dx.doi.org/10.1667/RR13822.1.S1). The parameter estimates of the risk of direct radiation did not vary after
inclusion of the rain exposure term for any of the examinedmodels, which indicates no important confounding of direct
radiation dose for reported rain exposure.
Using the three available rain exposure categorizations,the risks of mortality for all causes and solid cancer weresignificantly higher during 1950–2005 among the people
who had unknown rain exposure information compared tothose who reported no rain exposure in both cities.
However, no such elevated ERRs were observed foranalyses limited to the years 1962–2005 (Table 2). The
MQ and MSQ surveys that provided the information on rain
exposure were conducted from 1955–1961. Hence, subjects
who died before the survey may often have had their survey
conducted by proxy, which may have raised their apparent
risks due to recall bias. The fact that the mortality rate of the‘‘unknown’’ group decreased after the baseline surveys
finished and later increased in parallel with the other rain
exposure groups as the cohort aged supports this supposition of an outcome-dependent bias; i.e., ‘‘reverse causation’’.
While the questionnaires were the same in both cities,
there is evidence that the procedures may have beendifferent between cities, as the percentage of the subjects
who left the question for rain exposure blank was higher in
Hiroshima compared with Nagasaki. Unfortunately, questions about the intensity of rainfall (heavy or light) or
quantitative evaluation of exposure to rain were notgenerally asked. Although more detailed information on
rainfall was recorded during 1954–1958, the questions were
presented to only a small fraction of the cohort and theanswers were narrative rather than quantitative (11). Since
there are no records remaining on the methods by which thesurveys were conducted, it is not possible to determine theexact way in which investigators asked survivors about theirrain exposure status. The MSQ records suggest an English
translation of the question could be written as follows:‘‘Were you caught in the rain just after the atomic
bombing?’’ Unfortunately, the definition of ‘‘just after’’ isnot clear, so it is not possible to determine how individual
survivors interpreted the question. Although the most likelyinterpretation of ‘‘the rain just after’’ would be rain that fell
several minutes to several hours after the bombing, subjects
might have reported rain that fell up to several days later.
Throughout this article, we used reported exposure to rainthat fell just after each bombing as a simple surrogate forradiation dose. While estimated doses may be preferable,
they are difficult to derive for a number of reasons, which
include: 1. lack of location-specific data on the radioactivity
concentration of the rain; 2. spatial discrepancy between thesurvivor’s location at the time of bombing and the location
where they may have had any reported exposure to the rain,
which is poorly documented; and 3. lack of individual
information about variables that would relate the radioactivity content of the rain at a given location to the external
and internal radiation doses that a survivor would havereceived. Each of these points is discussed briefly.

EFFECTS OF RAIN EXPOSURE SHORTLY AFTER A-BOMBINGSFirst, it is theoretically possible to estimate the total
radionuclide inventory that was deposited on the ground in
the known fallout areas of Koi-Takasu in Hiroshima andNishiyama in Nagasaki by making assumptions about thefractionation of the bomb debris and using the gamma-ray
exposure-rate measurements of early surveys that were donein 1945 (12). However, the lack of data on the amount of
rainfall precludes a calculation of the radioactivity concentration of the rain. The few direct measurements of black
rain from preserved stained walls in Hiroshima do notprovide sufficient information to estimate the radioactivity
concentration of the rain (13).
Second, the nomenclature ‘‘fallout rain’’ has been usedvery generally, and while rain fell in many areas throughout
the cities, documented radioactive fallout was concentrated
in a few geographic locations. Hence, there is confusion
about the distinction between ‘‘black rain’’ and rain that
truly contained fallout. Because the areas of known fallout
in Koi-Takasu and Nishiyama are both around 3 km fromtheir respective hypocenters, it may be possible forcalculations of approximate dose to be made for people
who were in those areas at the times of the bombings andexposed to the rain, assuming that they either did notevacuate or received the majority of dose before theyevacuated (1), however, that would not be possible for thoseat other locations.
Third, if the radioactivity content of the rain were known,
calculations of close-range external exposure to gamma rays
and beta particles from rain itself would be possible only if
additional information were available, including individual
information about posture, clothing and whether any
material adhered to skin or clothing. Calculation of dosefrom internal exposure would require assumptions about
routes of entry into the body. Due to this limited
information, it is not possible to accurately estimate
radiation dose due to rain exposure.
The purpose of this study was to establish whether or notthere was a risk from exposure to rain that fell shortly after
the bombings. There were other potential sources of
exposure to residual radioactivity, such as induced radiationfrom activated soil. However, expert consensus indicatesthat additional fallout due to gravitational settling was notpossible in the absence of rain since the residual bombmaterials that condensed in the atmosphere were very small
and would have been dispersed by the winds (14).
Controversy has erupted in recent years over the idea that
there may have been undocumented fallout in distal areas tothe northwest in Hiroshima on the premise that the bomb
debris cloud was moving to the northwest. Early surveys tomeasure residual radiation were not done because the areas
were mountainous and inaccessible. However, no significant levels have been detected there despite new andinnovative efforts to overcome the effects of time andinterference from global fallout in later years (15, 16).
Furthermore, the current cohort is not appropriate for use in605

these studies because there were virtually no members of
the LSS in that sparsely populated area.
Despite the discussed limitations, these data represent themost extensively and systematically collected data on rain
exposure in the atomic bomb survivors and therefore may
help address public concerns about health effects from black
rain exposure. It has been recently reported (17) that those
exposed to black rain have physical/mental health afflictions
similar to those directly exposed to the atomic bombcompared to those who were not exposed to either theatomic bomb or black rain. However, those results werecollected by cross-sectional survey in 2008. The long periodof time between exposure and survey date, the retrospective
nature of the study, as well as the many deaths and outmigration that occurred prior to the survey raise concerns
regarding possible biases from cohort selection and recall.
In contrast, our data were collected during the 1950s andearly 1960s, which indicates that most of the follow-up wasprospective rather than retrospective.
Based on systematically collected data, we failed to finddeleterious health effects from rain exposure, though thedata have limitations. We believe that these results alignwith the claim that health effects induced by fallout rain
exposure are not as great as those observed in survivors who
were directly exposed proximally to the atomic bomb.
However, due to the limitations of the data, deleterious
health effects from rain exposure immediately after theatomic bombing cannot be completely ruled out.
ACKNOWLEDGMENTS
The Radiation Effects Research Foundation (RERF), Hiroshima andNagasaki, Japan is a public interest foundation funded by Japanese
Ministry of Health, Labour and Welfare (MHLW) and the U.S.
Department of Energy (DOE). The research was also funded in partthrough DOE award DE-HS0000031 to the National Academy of
Sciences. This publication was supported by RERF Research Protocol
RP 1–75. The views of the authors do not necessarily reflect those of thetwo governments.
Received: June 9, 2014; accepted: August 6, 2014; published online:
November 17, 2014

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