RADIATION RESEARCH 185, 604–615 (2016)0033-7587/16 $15.00
Ó2016 by Radiation Research Society.
All rights of reproduction in any form reserved.
DOI: 10.1667/RR14038.1

Association of Acute Radiation Syndrome and Rain after the Bombings in
Atomic Bomb Survivors
K. Ozasa,a,1 R. Sakata,a H. M. Cullingsb and E. J. Granta
Departments of a Epidemiology and b Statistics, Radiation Effects Research Foundation, Hiroshima, JapanINTRODUCTION
Ozasa, K., Sakata, R., Cullings, H. M. and Grant, E. J.
Association of Acute Radiation Syndrome and Rain after theBombings in Atomic Bomb Survivors. Radiat. Res. 185, 604–
615 (2016).

Acute radiation syndrome can occur after exposure tohigh doses of radiation (1) and has been reported among
survivors of the atomic bombings in Hiroshima andNagasaki, with a strong relationship to distance from the
hypocenters and therefore, to the direct radiation dose fromthe bombs (2). After the bombings, rain fell over wide areasof Hiroshima and in reportedly limited areas of Nagasaki.
The rain was thought to originate from the ascending air
currents from the heat of the bombs and ensuing fires that
consumed many of the cities’ structures. Combined with thesoot and ash from the fires, it came to be known as ‘‘black
rain’’, and there is evidence that some of this wasradioactive (3). Early survey measurements in the KoiTakasu area in western Hiroshima and the Nishiyama area
in eastern Nagasaki detected localized areas of residual
radiation; both areas are distal from the hypocenter and theelevated measurements of radioactivity were thought tohave been caused by fallout of radioactive bomb debris
contained in rain (4). Some survivors who reported being
exposed to the rain that fell shortly after the bombings, often
during evacuation to areas outside the central parts of thecities, also reported acute radiation symptoms in interviews
conducted by the Atomic Bomb Casualty Commission(ABCC) (5, 6). However, the association has not been
evaluated in an epidemiological study that considers theeffects of the direct dose from the atomic bombs, as well asother factors affecting the likelihood that a survivor reported
particular symptoms in interviews conducted some timeafter the bombings. These factors may depend on both theexistence and severity of the symptoms that occurred andthe accuracy of survivor/surrogate responder recall.
The Life Span Study (LSS) is a prospective study of a
fixed cohort of atomic bomb survivors followed since 1950
(7). The Atomic Bomb Casualty Commission collectedsurveys during the 1950s to early 1960s documenting rain
exposure information along with the occurrence of acute
symptoms and other data that could be used to estimate
radiation dose received directly from the bombs, such as
location and shielding. However, although information on
acute symptoms was used for validation of estimated direct
radiation from the atomic bomb explosions among high-Acute radiation-induced symptoms reported in survivors
after the atomic bombings in Hiroshima and Nagasaki havebeen suspected to be associated with rain that fell after the
explosions, but this association has not been evaluated in an
epidemiological study that considers the effects of the directdose from the atomic bombs and other factors. The aim of
this study was to evaluate this association using informationfrom a fixed cohort, comprised of 93,741 members of the Life
Span Study who were in the city at the time of the bombing.
Information on acute symptoms and exposure to rain wascollected in surveys conducted by interviewers, primarily inthe 1950s. The proportion of survivors developing severe
epilation was around 60% at levels of direct radiation dosesof 3 Gy or higher and less than 0.2% at levels ,0.005 Gy
regardless of reported rain exposure status. The low
prevalence of acute symptoms at low direct doses indicatesthat the reported fallout rain was not homogeneously
radioactive at a level sufficient to cause a substantial
probability of acute symptoms. We observed that the
proportion of reported acute symptoms was slightly higher
among those who reported rain exposure in some subgroups,
however, suggestions that rain was the cause of these reported
symptoms are not supported by analyses specific to the
known areas of radioactive fallout. Misclassification of
exposure and outcome, including symptoms due to othercauses and recall bias, appears to be a more plausible
explanation. However, the insufficient and retrospective
nature of the available data limited our ability to quantify
the attribution to those possible causes. Ó 2016 by Radiation
Research Society

Editor’s note. The online version of this article (DOI: 10.1667/
RR14038.S1) contains supplementary information that is available to
all authorized users.
1 Address for correspondence: Radiation Effects Research Foundation, Department of Epidemiology, 5-2 Hijiyama-koen, Minamiku, Hiroshima, Hiroshima 732-0815, Japan; email: ozasa@rerf.or.jp.
604

ACUTE SYMPTOMS AND RAIN AFTER ATOMIC BOMBINGS

dose survivors, in the 1950s prior to development of the firstreal dosimetry system, it was not evaluated for an
association with exposure to rain. (5, 6, 8–10). This study
is an examination of the association of exposure to rain withthe occurrence of acute symptoms typically associated withradiation exposure, especially epilation.
RESEARCH COHORT AND METHODSThis study was comprised of 93,741 cohort members of
the LSS whose locations at the time of bombings were lessthan 10 km from the hypocenters in Hiroshima andNagasaki. Information on exposure to rain was collectedprimarily in two large-scale surveys across the LSS cohort
with small numbers of reports from some provisional
surveys, which were conducted by interview by ABCC
personnel using the Migration Questionnaire (MQ, 1955–
1956) and the Master Sample Questionnaire (MSQ, 1955–
1961). The MQ questions were: ‘‘Was person caught inFallout Rain?’’ (Yes or No) plus ‘‘Where’’ and ‘‘Time’’with boxes for a free-form description. The MSQ questions
were ‘‘Was person caught in Fallout Rain?’’ (Yes, No or
Unknown) and ‘‘Where’’ with a box for a free-form
description. Rain exposure status was classified as ‘‘yes’’,‘‘no’’ or ‘‘unknown.’’ Blank answers were categorized as‘‘unknown.’’ Survivor responses about their location at thetime of rain exposure were recorded in a variety of ways,
usually indicating some area such as the name of a town
block. The distance and direction of the location from the
hypocenter was determined by the geographic center of thatarea. If information was not sufficient to estimate that point(that is, the response was, for example, ‘‘on the way from X
to Y’’ or ‘‘along the river Z’’, etc.), it was classified‘‘location unknown.’’ A small number of answers thatindicated a distant location from Hiroshima or Nagasaki citywere also classified ‘‘location unknown.’’ The free-form
information on exposure to rain was coded and computerized starting in 2008.
Information on the occurrence and severity of acute
symptoms was also collected during the interviews. In
addition to some provisional surveys, two large-scale
surveys, the Radiation Questionnaire (RQ, conducted in
1953–1955) and the MSQ, included questions on acute
symptoms. Symptom information included date of onset,
severity (mild, moderate, severe, unknown or not stated andnone) and a free-form response field for ‘‘duration orcomment.’’ The types of symptoms included fever, malaise,vomiting, nausea, anorexia, diarrhea (bloody and nonbloody), sore throat, sore mouth, sore gums (gingivitis),
bleeding gums, purpura, other bleeding and epilation. The
MQ questions consisted of check boxes (Yes/No) for
various symptoms, including sore throat, sore mouth, soregums, bleeding gums, purpura and epilation.
For those with multiple questionnaires, discrepantanswers were examined and the answer judged mostreliable (usually based on an earlier response date and/or

605

self-reported rather than surrogate-reported) was identified
by ABCC personnel. Summary variables for epilation,
bleeding and oropharyngeal lesions were coded from thequestionnaires and an integrated database created fromprevious studies (5, 6, 10). As the LSS was expanded withindividuals from the previous studies, the database was
expanded in the same manner and was used in this study.
Epilation that occurred within 60 days was classified byseverity as: none, slight (loss of less than 1/4 of hair on thescalp), moderate (1/4 to less than 2/3), severe (2/3 or more),questionable (including unknown severity and unknown
onset date) and no information (i.e., answer was left blank).
Purpura or bleeding gums that occurred within 6 weeks after
the bombings were summarized as ‘‘bleeding’’ (‘‘Yes’’/‘‘No’’/‘‘Unknown or No Information’’). Sore throat, sore
mouth and sore gums that occurred within 6 weeks after thebombings were summarized as ‘‘oropharyngeal lesions’’
and were coded in the same manner as ‘‘bleeding’’.
Individual doses of direct radiation from the atomic
bombs were estimated using the DS02 dosimetry system
according to the established methods (11, 12). Weighted
absorbed dose (neutron 3 10 þ gamma ray) to the skin wasused for epilation in the analysis, and the dose to the bonemarrow was used for bleeding and oropharyngeal lesions.
Oropharyngeal lesions were thought to indicate severe
inflammation of the mouth and throat mucosa due tolymphocytopenia (2).
The basic analysis strategy was to adjust for thecontributions of direct radiation from the atomic bomb,
along with variation by age and sex, to the likelihood of
epilation or other acute symptoms. Analyses were performed separately by city because meteorological conditions and fallout materials contained in the rain were likely
to have been different. First, the proportion of persons
developing acute symptoms was tabulated by DS02 direct
radiation dose. Next, associations of exposure to rain (yesvs. no) and occurrence of acute symptoms (occur vs. no
symptoms) were examined by odds ratios (OR) using a
conditional logistic regression matched for direct-dose bandwith cutoff points of 0.005, 0.1, 0.25 and every 0.25 Gy up
to 4.0 Gy, and adjusted for sex and age at bombing using
SASt software (SAS Institute Inc., Cary, NC) (13).
Survivors with unknown direct dose (N ¼ 7,070) were
excluded from odds ratio calculations.
Analyses were also conducted by distance and direction
from the hypocenter because reported frequency of
exposure to rain was different in different areas. Thus,
areas were classified by quadrants from true north inHiroshima and east and west semicircles in Nagasaki, basedon the spatial distribution of the frequency of reported rain.
In addition, specific effects of rain were investigated in the
Koi-Takasu area in Hiroshima, which is a known area ofhigh residual radiation around 3.5 km west-southwest of the
hypocenter. Since the effects at Koi-Takasu might be
attributable to either exposure to fallout in the rain or later
integrated dose from fallout in the environment, the west-

606

OZASA ET AL.

FIG. 1. Maps of Hiroshima and Nagasaki. ‘‘3’’ indicates hypocenters. N, E, S and W represent the compass
directions from the hypocenter, respectively.

southwest octant 2 km or more distant from the hypocenter
was analyzed as a separate area. In Nagasaki, the east
sextant (between 608 and 1208 clockwise from true north) 2
km or more distant was analyzed separately to provide a
result specific to the Nishiyama area (around 3.0 km east of
the hypocenter). Consequently, the distant areas beyond 2
km from the hypocenter were divided into five quadrants/
octants in Hiroshima and five sextants/quadrants in
Nagasaki [Fig. 1 and Table 1 (left column)].

Locations where persons encountered rain were only
recorded for those who actually reported rain exposure, so
effects of exposure to rain at a certain area were evaluatedby the interaction between effects of exposure to rain andeffects of area (14, 15). Therefore, coefficients in theconditional logistic regression model are described as:
logit½risk ¼ ln½OR X
X
cj  rain  areaj ;¼ a  sex þbi  agei þ

TABLE 1
Distribution of Survivors Classified by Exposure to Rain and Location at the Time of theBombings

Areaa
Hiroshima
NE quadrant
SE quadrant
SW quadrant
NW quadrant
Total
Limited to 2þ kmb
NE quadrant
SE quadrant
SSW octant
WSW octant
NW quadrant
NagasakiEast semicircle
West semicircle
Total
Limited to 2þ kmb
NE sextant
E sextant
SE sextant
SW quadrant
NW quadrantaExposedto rain

Percentage(%)

Not
exposedto rainUnknown
exposure
to rain

Total

2,418
826
3,708
5,298
12,250

20.7
3.3
24.8
50.2
19.8

5,247
17,0886,610
1,624
30,569

4,004
6,900
4,632
3,629
19,165

11,66924,814
14,95010,551
61,984

1,244
339
276
1,551
2,554

19.7
2.1
7.5
31.6
57.0

3,369
12,216
2,458
2,170
871

1,696
3,328
946
1,184
1,053

6,309
15,883
3,680
4,905
4,478

722
131
853

3.4
1.2
2.7

17,3408,945
26,285

3,131
1,488
4,619

21,193
10,56431,757

86
197
203
62
15

12.7
12.7
1.4
0.9
1.4

506
1,183
12,420
5,866
938

85
168
1,676
652
136

677
1,548
14,2996,580
1,089

Abbreviations indicate the direction from the hypocenter. N, E, S and W represent the compass directions,
respectively.
b
Numbers of these subareas are included in the above areas.

ACUTE SYMPTOMS AND RAIN AFTER ATOMIC BOMBINGSTABLE 2Distribution of Survivors who were Exposed to RainClassified by Location at the Time of the Bombingsand at Exposure to Rain

Areaa
Hiroshima
NE quadrant
SE quadrant
SW quadrant
NW quadrant
Unknown
Total
Limited to 2þ kmb
NE quadrant
SE quadrant
SSW octant
WSW octant
NW quadrant
Total
NagasakiEast semicircle
West semicircle
Unknown
Total
Limited to 2þ km
NE sextant
E sextant
SE sextant
SW quadrant
NW quadrant
Total

At
At time of Percentage exposure Percentage
to rain(%)
bombings
(%)
2,418
826
3,708
5,298
12,250

19.8
6.7
30.3
43.2
100

2,397
440
4,783
4,107
523
12,250

19.6
3.6
39.0
33.5
4.3
100

1,244
339
276
1,551
2,554
5,964

20.9
5.7
4.6
26.0
42.8
100

1,630
217
351
3,268
2,772
8,238

19.8
2.6
4.3
39.7
33.6
100

722
131
853

84.6
15.4
100

544
57
252
853

63.8
6.7
29.5
100

86
197
203
62
15
563

15.3
35.0
36.0
11.0
2.7
100

36
197
80
24
11
348

10.3
56.6
23.0
6.9
3.2
100

a
Abbreviations indicate the direction from the hypocenter. N, E, S
and W represent the compass directions, respectively.
b
Numbers of these subareas are included in the above areas.

a indicates a coefficient for effects of sex, bi indicate that forage class with ten-year interval (0–9, 10–19, . . ., 60 þ) andage class of 40–49 was used for the reference and cj
represents interaction of effects from exposure to rain andspecific location of rain exposure, including the category of
unknown location, respectively. Locations were known only
for those individuals exposed to rain (rain ¼ 1) and there
was no information on areas occupied during and after
evacuation at the times of the ‘‘fallout rain,’’ for those who
were not exposed to rain (rain ¼ 0). Thus, there is no
primary term for effects of rain or area and cj indicates areaspecific effects of exposure to rain compared to nonexposure to rain anywhere. In addition, sex- and age classadjusted odds ratios of the symptoms for direct radiation
categories irrespective of rain exposure were estimated toevaluate the specificity of the symptoms with direct
radiation exposure from the atomic bombs.
RESULTS

Table 1 shows the number of individuals exposed to rain
and their location at the time of the bombings. A total of
about 20% of survivors reported contact with ‘‘fallout’’ rainin Hiroshima (12,250/61,984), about half reported no607

exposure (30,569/61,984) and the remaining 30% (19,165/
61,984) had unknown status. People located in thenorthwest (NW) quadrant at the time of the bombing
reported the highest frequency of exposure to rain (50%),
followed by those in the SW and NE quadrants, while thosein the SE quadrant reported the lowest. Among those whoreported exposure to rain, about 40% reported being in the
SW quadrant at the time of exposure. Among those exposed
who were located beyond 2 km (8,238), the highest
concentration (40%) were exposed in the WSW octant,which includes the Koi-Takasu area (Table 2). In Nagasaki,
only 3% (853/31,757) of individuals reported rain exposure,
83% (26,285/31,757) reported no exposure and 15% (4,619/
31,757) had unknown exposure. People who were located in
the east semicircle from the hypocenter at the bombing
reported a higher frequency of exposure to rain than those in
the other semicircle. About 64% of those exposed to rainreported being in the east semicircle. Beyond 2 km, 197(50%) were exposed in the east sextant, which includes the
Nishiyama area.
For those exposed to the Hiroshima bomb, the proportions and selected numbers of persons reporting acute
symptoms by exposure to rain and radiation dose categories
are shown in Table 3. The proportion of individuals
reporting acute symptoms showed similar tendencies ineach direct-dose category regardless of exposure to rain.
Among those with no exposure to rain, the proportion ofindividuals who reported severe epilation was 57.4% in
those with a direct radiation dose of 3.0 Gy or higher to theskin. This proportion decreased with lower doses ofradiation to less than 1% at ,0.1 Gy and decreased to
0.4% and 0.04% in the lowest two categories, respectively.
Among those who were exposed to rain, the proportion was
also large at the highest dose level (66.5%) and decreased
with decreasing doses, to 0.4% and 0.2% in the lowest two,
respectively. Individuals with unknown exposure to rain
showed a similar tendency.
Table 4 shows the same information for those exposed in
Nagasaki. The maximum values were smaller but the trends
in the proportions by dose group were similar to thoseobserved in Hiroshima. For those not exposed to rain,
severe epilation was reported by 39.8% at the level of 3.0 þ
Gy, and also decreased in proportion to 0.2% and 0.1% at
the lowest two dose categories, respectively. For thosereporting rain exposures, the respective proportions were33.3%, 0.9% and 0.3%. The proportions of individuals whoreported moderate or slight epilation showed similartendencies to those with severe epilation for all but thehighest two dose categories (where values were consistently
higher) in each city.
As for the bleeding category, the proportions were high at
high doses and appeared to reach a plateau at 1.0 Gy or
higher (43–48% at the highest three levels) and decreased to
0.9% at ,0.005 Gy among those with no rain exposure in
Hiroshima. The values ranged from 53–66% at the highest
three levels and 2.3% at the lowest level among those608

OZASA ET AL.

TABLE 3
Proportion of Hiroshima Bomb Survivors Developing Acute Symptoms, Classified by Exposure to Rain and DS02 Direct
Radiation Dose
Epilation
Severebac

Exposure to rain

Dose (Gy)No.

No,0.0050.005–
0.1–
0.5–
1.0–
2.0–
3þ
Unknown
Total,0.0050.005–
0.1–
0.5–
1.0–
2.0–
3þ
Unknown
Total,0.0050.005–
0.1–
0.5–
1.0–
2.0–
3þ
Unknown
Total

5
41
42
20
69
73
109
44
403
6
19
22
14
74
69
109
41
354
6
47
48
27
59
89
172
83
531

Yes

Unknown

Pecentage (%)

Moderateb
Pecentage (%)

Slightb
Pecentage (%)

None
Pecentage (%)

Total

0.04
0.4
1.1
1.8
12.0
38.6
57.4
3.4
1.3
0.2
0.4
0.8
1.4
11.8
44.8
66.5
7.1
2.9
0.1
0.9
1.1
2.6
10.0
35.9
61.4
6.2
3.1

0.2
0.9
2.2
4.8
8.5
13.8
13.2
3.3
1.3
0.9
1.1
1.6
3.4
14.1
14.3
11.0
4.3
2.5
0.4
1.5
2.5
5.1
11.8
18.1
8.9
5.3
2.7

0.4
1.3
2.5
4.9
9.9
5.8
1.6
2.9
1.4
1.0
1.4
3.0
6.3
11.1
12.3
3.7
4.3
2.9
0.5
1.9
3.0
5.9
10.2
7.3
3.2
4.8
2.7

99.2
96.9
92.4
86.1
65.9
38.6
24.2
89.3
95.2
97.6
95.8
93.0
86.8
60.1
25.3
16.5
81.6
90.3
98.4
94.6
91.6
83.8
63.8
33.1
23.2
81.3
90.0

12,944
10,568
3,706
1,099
574
189
190
1,299
30,569
2,472
4,590
2,686
971
630
154
164
583
12,250
4,912
6,078
4,430
1,052
596
249
281
1,567
19,165Note. The denominators of percentage (%) exclude respondents with ‘‘no information’’ on the symptoms from the total number.
a
Weighted absorbed skin dose for epilation and bone marrow dose for bleeding and oropharyngeal lesions.
b
Includes symptoms occurring within 60 days after the bombings for epilation and within 6 weeks for bleeding and oropharyngeal lesions.
cNumber of respondents.

individuals with rain exposure. In Nagasaki, the values
ranged from 39–54% at the highest three levels and 0.6% at
the lowest level among those not reporting rain exposure,and 45.7% at 1.0 to ,2.0 Gy and 63% at the combined levelof 2.0 Gy or higher in those exposed to rain, and 2.6% at,0.005 Gy. Oropharyngeal lesions also showed similarvalues by dose category and exposure status to rain (Tables
3 and 4).
The point estimates of proportions of the cohort
developing acute symptoms were higher in the rainexposed group than the non-exposed group at many levelsof direct radiation dose in both cities. Odds ratios ofdeveloping acute symptoms by location of rain exposure
are shown in Fig. 2 and the cross tables for calculating theodds ratios are shown in Table 5. The odds ratio of severe
epilation for the rain-exposed group was .1 but notstatistically significant at the 0.05 level [1.20, 95%
confidence interval (CI): 0.97, 1.47] in Hiroshima. The
odds ratio in the SE quadrant and at unknown location
were significantly higher than 1, but the odds ratio at
WSW octant beyond 2 km (including the Koi-Takasu area
which had measureable fallout) was not significantly

higher. In Nagasaki, the odds ratio was 1.76 (95% CI:
0.86, 3.57), and the odds ratio for rain-exposed at the west
semicircle was nominally higher than that at the east
semicircle, but not statistically significant. The odds ratio
for the east sextant at distances greater than 2 km(including the Nishiyama area which had considerable
fallout) was not available because there were no reports ofsevere epilation in this area.
When the outcome of epilation included all grades (severe
to slight), the odds ratio was 1.23 (95% CI: 1.11, 1.37) for
all individuals in Hiroshima and 2.10 (95% CI: 1.54, 2.86)
in Nagasaki. The odds ratio was significantly high for rainexposed persons in the NE and SE quadrants of all distances
and at unknown locations in Hiroshima, and was also highfor those exposed in both semicircles and in some distantsubareas in Nagasaki. However, for the WSW octant
beyond 2 km in Hiroshima the odds ratio was not high,and at the east sextant beyond 2 km in Nagasaki it wascomparatively low. (Fig. 2).
As for bleeding, the overall odds ratio after exposure torain was 1.48 (95% CI: 1.33, 1.64) in Hiroshima and 2.01
(95% CI: 1.45, 2.78) in Nagasaki. The odds ratios were609

ACUTE SYMPTOMS AND RAIN AFTER ATOMIC BOMBINGSTABLE 3Extended.
Bleeding
Occurrencesb

Oropharyngeal lesions
Occurrencesb

No.

Pecentage (%)

None
Pecentage (%)

No.

Pecentage (%)

None
Pecentage (%)

Total

119
280
180
138
190
76
16
116
1,115
61
153
180
195
215
68
31
72
975
55
221
239
196
217
119
36
196
1,279

0.9
2.6
5.1
14.9
45.7
48.4
43.2
9.0
3.7
2.3
3.3
6.3
22.3
53.0
62.4
66.0
12.5
8.0
1.3
3.7
6.0
21.9
44.9
58.9
40.0
14.6
7.5

98.8
96.9
93.1
81.3
49.0
42.7
45.9
89.4
95.5
96.9
95.1
91.8
74.1
42.9
34.9
34.0
83.8
90.2
98.1
94.8
92.2
74.8
49.5
36.6
48.9
82.7
90.8

78
172
123
74
130
61
12
57
707
42
114
114
103
145
54
19
46
637
44
158
138
104
132
76
21
110
783

0.6
1.6
3.5
8.0
31.3
38.9
32.4
4.4
2.3
1.6
2.5
4.0
11.8
35.7
49.5
40.4
8.0
5.2
1.0
2.7
3.5
11.6
27.3
37.6
23.3
8.2
4.6

99.2
97.8
95.2
90.4
66.6
55.4
62.2
94.3
97.1
97.8
96.3
94.7
86.1
62.8
46.8
57.4
89.0
93.4
98.3
96.1
95.2
85.8
68.5
57.9
66.7
89.3
94.0

13,31910,843
3,568
930
416
157
37
1,299
30,569
2,695
4,686
2,846
878
406
109
47
583
12,250
5,062
6,722
4,124
910
487
202
91
1,567
19,165consistently high for all quadrants of rain exposure in
Hiroshima and both semicircles in Nagasaki regardless of
distance from the hypocenters, and also high in many ofthe distant subareas. The odds ratio was the highest for theSE quadrant at all distances and beyond 2 km in
Hiroshima and higher for the west semicircle in Nagasaki
in which rain was not frequently reported, except for
location unknown, respectively. The odds ratio wassignificantly high for the WSW octant beyond 2 km in
Hiroshima, but was not higher than the overall odds ratioor the odds ratios for other areas. The odds ratio was nothigh for the east sextant beyond 2 km in Nagasaki. The
overall odds ratio of oropharyngeal lesions was 1.47 (95%
CI: 1.29, 1.67) in Hiroshima and 2.46 (95% CI: 1.80,
3.36) in Nagasaki and the odds ratios showed similartendencies to those for epilation or bleeding The odds
ratios of those outcomes were heterogeneous between theareas and tended to be higher in areas where rain was notfrequently reported (i.e., SE quadrant at all distances andbeyond 2 km in Hiroshima and the west semicircle in
Nagasaki). The odds ratios for the areas including KoiTakasu and Nishiyama, which had known radioactive
fallout, were not higher than the overall risks in Hiroshima
or Nagasaki, respectively.

DISCUSSION

Exposure to high-dose radiation induces acute symptoms
in various organs. Neurological, gastrointestinal andhematopoietic (bone marrow failure) syndromes are induced
in a dose-dependent fashion. Acute tissue reactions also
occur in skin (erythema, abnormal hair growth, epilation,desquamation, and vascular and dermal injury), mucous
membranes in the mouth and throat (inflammation andswelling, with ulceration and necrosis), as well as in othersat various levels of whole-body doses above approximately
1 Gy of X or gamma radiation (1). Unlike systemic
exposure to direct radiation by neutrons and gamma raysfrom the atomic bombs, residual radioactivity would have
involved radioactive material in the surrounding environment of the survivor and would have resulted in different
exposure modalities. Examples include contact skin dosefrom fallout that may have been in rain, or beta dose to skinoccurring after the end of rainfall from fallout on the groundor other surfaces in the environment, or external exposure
from neutron-activated soil materials nearby or adhering toskin (16, 17).
Among the atomic bomb survivors exposed proximally tothe explosion, epilation began abruptly about 2 weeks after
the explosion, primarily at the frontal region and then theoccipital and parietal areas, with temporal and neck areas

610

OZASA ET AL.

TABLE 4
Proportion of Nagasaki Bomb Survivors Developing Acute Symptoms, Classified by Exposure to Rain and DS02 Direct
Radiation Dose
Epilation
Severeb
Exposure to rain

Dose (Gy)No,0.0050.005–
0.1–
0.5–
1.0–
2.0–
3þ
Unknown
Total,0.0050.005–
0.1–
0.5–
1.0–
2.0–
3þ
Unknown
Total,0.0050.005–
0.1–
0.5–
1.0–
2.0–
3þ
Unknown
Total

Yes

UnknownaNo.

Pecentage (%)

Moderateb
Pecentage (%)

13
13
15
9
49
41
41
56
237
1
2
0
1
3
3
2
10
22
3
6
4
8
21
25
27
31
125

0.1
0.2
0.9
1.4
7.7
26.3
39.8
2.2
0.9
0.3
0.9
0.0
2.1
6.7
75.0
33.3
8.7
2.6
0.2
0.7
1.0
3.7
8.8
31.6
42.2
3.8
3.0

0.1
1.0
2.8
5.4
11.5
16.7
10.7
3.3
1.4
0.3
1.4
0.0
6.3
11.1
0.0
0.0
2.6
1.8
0.3
1.4
4.5
3.3
14.6
11.4
4.7
4.5
3.0

c

Slightb
Pecentage (%)

None
Pecentage (%)

Total no.

0.3
1.3
3.4
6.1
11.8
10.9
7.8
4.9
1.7
2.8
4.6
4.1
10.4
31.1
25.0
0.0
13.0
6.8
0.6
1.3
2.6
7.9
12.5
11.4
15.6
6.9
3.6

99.4
96.7
91.4
83.3
65.9
44.2
38.8
87.5
95.3
96.0
91.3
91.8
81.3
51.1
0.0
66.7
72.2
87.2
98.5
93.4
89.3
82.3
59.6
38.0
31.3
81.5
88.1

13,882
6,605
1,636
658
637
157
103
2,607
26,285
333
223
73
49
46
4
6
119
853
1,713
976
429
217
243
81
65
895
4,619

Note. The denominators of percentage (%) exclude respondens with ‘‘no information’’ on the symptoms from the total number.
a
Weighted absorbed skin dose for epilation and bone marrow dose for bleeding and oropharyngeal lesions.
b
Includes symptoms occurring within 60 days after the bombings for epilation and within 6 weeks for bleeding and oropharyngeal lesions.
cNumber of respondents.

spared; very few of these individuals had total epilation. The
onset was delayed as distance from the hypocenter
increased (e.g., mean number of days was 28.1 at about
1.6–1.9 km in Hiroshima). Purpura occurred with a peak
onset 20–30 days after the explosion and the mean time toonset was not greatly changed by the distance from the
hypocenter. Oropharyngeal lesions occurred over a relatively wide time period after the explosion with a mean of
22 days (2). The periods for which we chose to analyze theoccurrence of acute symptoms (60 days for epilation and 6
weeks for bleeding and oropharyngeal lesions) wereconsistent with those findings.
The list of acute symptoms in the ABCC surveys included
prodromal gastrointestinal symptoms, hemorrhagic diathesis(purpura and oropharyngeal lesions) and epilation. Since
gastrointestinal symptoms could be induced by many causes
and are therefore not considered to be specific to radiation
exposure (2), survey data categorization did not use
gastrointestinal symptoms but focused on epilation, bleeding and oropharyngeal lesions, as in previously publishedstudies (5–10).

Two major findings were observed in this study. First, theproportion of those developing acute symptoms was large athigh DS02 dose levels and lower with decreasing doses,with the lowest level reached in the lowest dose category in
all groups regardless of rain exposure. If the reported rain
had been homogenous and highly radioactive, those
exposed to rain should have uniformly higher frequenciesof reported acute effects regardless of their direct radiationdose category. For example, if rain exposure was equivalent
to 0.1 Gy or higher, the proportion of those exposed to raindeveloping severe epilation should be similarly high as
those with direct dose of 0.1–0.5 Gy and no rain exposure(1.1%, 95% CI of 0.8–1.5% based on normal distribution,
Hiroshima). Yet, among those with direct exposures of,0.005 Gy and rain exposure, the proportion was 0.2%
(95% CI: 0.05%, 0.4%). Similar findings were observed forbleeding and oropharyngeal lesions, except for severe
epilation in Nagasaki because of the small number of theindividuals exposed to rain. Therefore, it is unlikely that therain was uniformly highly radioactive.
The second finding was that rain exposure was associatedwith increased frequency of acute symptoms, especially in

611

ACUTE SYMPTOMS AND RAIN AFTER ATOMIC BOMBINGSTABLE 4
Extended.
Bleeding
Occurrencesb

Oropharyngeal lesions
Occurrencesb

No.

Pecentage (%)

None
Pecentage (%)

No.

Pecentage (%)

None
Pecentage (%)

Total no.

85
142
92
136
202
63
12
242
974
9
11
5
14
16
5
0
27
87
15
31
28
48
83
32
2
105
344

0.6
2.2
5.5
19.4
39.2
53.8
46.2
9.3
3.7
2.6
5.3
6.5
27.5
45.7
83.3
0.0
23.3
10.4
1.0
3.5
6.5
18.5
40.5
49.2
15.4
13.0
8.2

99.2
96.9
93.3
77.9
53.6
41.9
53.8
88.7
95.5
96.5
94.3
89.6
66.7
45.7
16.7
100.0
72.4
87.5
98.1
93.6
90.4
78.0
50.7
43.1
69.2
83.6
89.1

104
159
76
87
145
44
5
203
823
17
12
5
8
11
5
0
18
76
19
39
23
34
59
29
3
94
300

0.7
2.5
4.5
12.4
28.2
37.6
19.2
7.8
3.1
5.0
5.7
6.5
15.7
31.4
83.3
0.0
15.7
9.1
1.2
4.4
5.4
13.1
28.8
45.3
23.1
11.8
7.2

99.1
97.0
94.4
85.6
65.6
59.0
76.9
90.8
96.3
93.3
93.3
90.9
84.3
65.7
16.7
100.0
78.3
88.8
98.1
93.1
92.3
82.7
63.4
42.2
69.2
85.2
90.4

14,247
6,393
1,675
703
517
117
26
2,607
26,285
348
213
77
53
35
6
2
119
853
1,757
976
440
264
207
67
13
895
4,619

the survivors who were exposed to rain in distal areas and in
the areas in which rain was not frequently reported. Thisfinding appears to support the deleterious nature of the rain.
There were localized areas of high residual radiation in the
Koi-Takasu area in Hiroshima and the Nishiyama area in
Nagasaki; both areas are distal from the hypocenter andthought to be caused by fallout rain (4). While the increased
odds ratios for acute symptoms among those who were
exposed to rain appeared to be consistent with the effects ofradioactive fallout in the rain, the odds ratio for the westsouthwest octant beyond 2 km in Hiroshima (including the
Koi-Takasu area) did not exceed the odds ratios for theother areas. No individuals developed severe epilation in theeast sextant beyond 2 km in Nagasaki (which includes the
Nishiyama area) and the odds ratios for other acute
symptoms were generally smaller in the east sextant
compared to other sextants. Thus, there was no further
increased risk of exposure to rain for developing acute
symptoms in the areas where radioactive fallout was
actually detected. Therefore, the increased odds ratios ofrain exposure for acute symptoms in distal areas and in theareas in which rain was not frequently reported were notthought to be due to radioactive fallout.
The symptoms recorded in the ABCC surveys were notdirectly observed by the investigators but were reportedby the individuals in interviews approximately ten years
after the bombings, probably reducing the reliability of theinformation for several reasons. First, not all questionnaires were answered directly by the responder but instead
could have been answered by a surrogate who may nothave had firsthand information on either the exposure or
the outcome. Second, individuals could have misjudged
the symptoms since they were not medical specialists. For
some elicited exposure symptoms such as severe epilation, misclassification would be unlikely as the symptoms
were pathognomonic for radiation exposure and easily
apparent. However, other symptoms were less specific toradiation and might have been misreported as radiation
related, such as ‘‘sore throat’’ and ‘‘other bleeding.’’
Third, memories of occurrence could be lost or confusedin the years after the bombing. Finally, both the exposure(rain) and the outcome (acute effects) were asked
retrospectively and on the same survey or on two surveys
that occurred within a short interval. This situation often
can induce the occurrence of ‘‘recall bias’’ whereindividuals who have experienced a disease or adverse
health outcome tend to think about the possible ‘‘causes’’of their illness and are likely to remember their exposure
histories differently from those unaffected by the disease,or more frequently report exposures that did not actually

612

OZASA ET AL.

TABLE 5
Cross Tables Calculating Fig. 1
Severe epilation
Total
Hiroshima
Exposed to rain at any location 11,667
NEa quadrant
2,248
SE quadrant
398
SW quadrant
4,621
NW quadrant
3,922
2þ km, all directions
7,968
2þ km, NE quadrant
1,575
2þ km, SE quadrant213
2þ km, SWS octant
340
2þ km, WSW octant
3,166
2þ km, NW quadrant
2,674
Location unknown
478
Non-exposed to rain
29,270Nagasaki
Exposed to rain at any location
734
East semicircle
465
West semicircle
50
2þ km, all directions329
2þ km, NE sextant
34
2þ km, E sextant
192
2þ km, SE sextant
71
2þ km, SW quadrant23
2þ km, NW quadrant
9
Location unknown
219
Non-exposed to rain
23,678a

Severe to slight epilation

Bleeding

Oropharyngeal lesions

Occurences

None

Occurences

None

Occurences

None

Occurences

None

313
54
27
96
109
110
22
5
8
39
36
27
359

10,527
2,023
315
4,259
3,535
7,449
1,462
184
308
2,992
2,503
386
27,827

914
177
58
303
322
396
85
13
29
136
133
54
1,112

10,527
2,023
315
4,259
3,535
7,449
1,462
184
308
2,992
2,503
386
27,827

903
172
56
312
307
407
92
14
33
140
128
56
999

10,490
2,022
323
4,224
3,536
7,410
1,448
187
301
2,977
2,497
385
27,914

591
98
42
206
212
275
51
12
16
107
89
33
650

10,860
2,111
332
4,350
3,659
7,574
1,498
189
319
3,020
2,548
408
28,326

12
6
2
2
0
0
0
2
0
4
181

647
425
34
312
34
189
65
18
6
188
22,714

66
32
13
10
0
1
3
4
2
21
772

647
425
34
312
34
189
65
18
6
188
22,714

60
32
10
12
1
3
4
3
1
18
732

650
420
39
311
33
187
64
19
8
191
22,746

58
26
8
13
2
2
5
2
2
24
620

652
428
40
307
32
186
62
20
7
184
22,892Abbreviations indicate the direction from the hypocenter. N, E, S and W represent the compass directions, respectively.

FIG. 2. Odds ratios and 95% confidence intervals of exposure to rain for acute symptoms by city and location
at exposure to rain. Odds ratios of exposure to rain (vs. non-exposure) for acute symptoms (vs. no symptoms)
matched for dose (weighted absorbed skin dose for epilation and bone marrow dose for bleeding andoropharyngeal lesions) and adjusted for sex and age at the time of bombing. *Asterisk indicates no odds ratio
because of null cell. (For point values see supplementary materials, http://dx.doi.org/10.1667.RR14038.S1.)

613

ACUTE SYMPTOMS AND RAIN AFTER ATOMIC BOMBINGSTABLE 6
Odds Ratios of Acute Symptoms for Direct Dose Adjusted for Sex and Age at Exposure
Weighted skin dose

City
Hiroshima
Nagasaki

Weighted bone marrow dose

Dose band(mean dose, Gy)

No. ofindividuals

Odds ratioof severe
epilation

Odds ratio of
all grade(severe to slight)
epilation,0.005 (,0.001)
1 to 2 (1.38)
2 to 3 (2.44),0.005 (0.0013)
1 to 2 (1.39)
2 to 3 (2.32)

20,3281,800
592
15,928926
242

1 (ref.)
209.999
1 (ref.)
119
707

1 (ref.)59
225
1 (ref.)
81
216

Dose band(mean dose, Gy)

No. ofindividuals

Odds ratioof bleeding

Odds ratio oforopharyngeal
lesions,0.005 (,0.001)
1 to 2 (1.38)
2 to 3 (2.44),0.005 (0.0012)
1 to 2 (1.34)
2 to 3 (2.55)

21,076
1,309
468
16,352759
190

1 (ref.)91
131
1 (ref.)103
180

1 (ref.)59
93
1 (ref.)46
85

Note. Results of other dose bands are omitted.

occur (18, 19). The responses from surrogates are thought
to have similar tendency although there was no information on surrogate response in the database used in thisstudy.
During the surveys, survivors who had some symptoms
similar to acute radiation syndrome may have soughttangible causes associated with radiation exposure (such as‘‘black rain’’) because direct radiation from the bomb wasinvisible and people could not estimate the dose. The
inverse is also true: people who experienced rain exposure
may have been more likely to think that their symptoms
were caused by radiation. There was no difference in odds
ratios of exposure to rain between the areas in whichradioactive fallout was detected shortly after the bombingsand the other areas. This finding suggests that the increased
frequency of reporting acute symptoms was not associatedwith actual radioactivity, but with exposure to any rain
regardless of radioactivity level. Increased odds ratios forthe answer category of ‘‘location unknown’’ suggests
uncertain memory of rain and symptoms, which is likely
to be affected by recall bias. Increased odds ratios were also
observed in the southeast quadrant in Hiroshima and thewest semicircle in Nagasaki where rain exposure was lessfrequently reported. It would be difficult to conclude thatstrong radioactive fallout rain had fallen on a limited
number of people in those areas, especially since there was
no evidence of residual radiation in early surveys of thoseareas with radiation-measuring instruments (20). Instead, it
is more plausible that recall bias occurred in a small groupof people who reported exposure to rain and produced ahigher odds ratio. A follow-up study indicated no increasein mortality of all cause, cancer or leukemia, or in cancer or
leukemia incidence among the survivors who were exposed
to rain (21). Because cause of death in the vital statistics andcancer incidence collected by population-based registries ismore valid in quality of information compared to selfreported symptoms used in this study, the results of thisfollow-up study are consistent with the interpretation that
increased frequencies of acute symptoms among those
exposed to rain were derived from some systematic
misclassification such as recall bias.

When epilation is defined using any grade of occurrence(severe to slight), it is less specific to radiation exposure
than severe epilation because low-grade epilation is difficult
to recognize and easily misreported. This is evident in thesmaller odds ratios of all-grade epilation compared to thosefor severe epilation at a given dose level irrespective of rain
exposure (Table 6). Bleeding and oropharyngeal lesions
were thought to be even less specific. However, the odds
ratios of fallout rain were not smaller for those lessradiation-specific symptoms. This inconsistency suggeststhat the association of exposure to fallout rain and acute
symptoms was influenced by other factors in addition toradiation effects.
Fission products of nuclear weapons were thought toproduce much more beta dose to exposed skin than gammaray dose to the skin and deeper tissues. For example, betato-gamma dose ratio for bare skin exposure to mixed fission
products in some nuclear tests were around 10 for a heightof 1 m above the source plane and more than 3 times thatvalue at a height of 1 cm (22). Since beta rays originating
outside the body do not penetrate to deep organs through thehuman body (their range in tissue is typically ,1 cm),radiation dose due to external exposure or skin contact
exposure to fallout rain should be much higher to the skinthan to bone marrow. Nevertheless, odds ratios of epilation(due to skin exposure) and those of bleeding andoropharyngeal lesions (due to bone marrow exposure) after
exposure to rain were quite similar. Although we do notknow how high or different the doses to skin and bonemarrow were (beta doses were added to the skin) or how
similar the dose responses of radiation for epilation andbone marrow symptoms were, the similarity seems too
coincidental for the associations to be true. Thus, itsuggested that the association of exposure to fallout rain
and acute symptoms was influenced by other factors.
Radiation dose of external exposure from radioactive
fallout was estimated as 200–400 mGy in the Nishiyama
area in Nagasaki and 10–30 mGy in the Koi-Takasu area in
Hiroshima, but early measurements of soil and air indicatedessentially no fallout in other areas of the cities (4, 20).
Fallout doses in the Nishiyama district of Nagasaki werehigh enough to cause blood disorders among some of the614

OZASA ET AL.

600 residents who lived in areas with the highest
contamination in the months after exposure. A peak inleukocytosis occurred within a few months of the bombing
and then regressed (23). Also, a small sample of Nishiyama
and non-exposed residents were tested for radiological bodyburdens in 1970 and higher 137Cs counts were observed
among the Nishiyama residents.
Radiation dose to the skin from fission fallout andneutron-activated soil has been previously estimated basedon the following assumptions in Hiroshima (16, 17). Endoet al. calculated that if the skin was covered with a 26 lm
thick layer of soil contaminated with a fallout radionuclide
inventory corresponding to an initial ground deposition of 1
kBq/m2–137Cs, the total beta dose to skin would be about 0.5
Sv for continuous exposure over the one-month period after
the explosion (16). Therefore, for the highest initial grounddeposition estimated for the Koi-Takasu area in Hiroshima(0.49 kBq/m2), Shizuma et al. (24) expected the skin dose of
0.25 Sv. As for induced radiation, a thickness on the skin of
about 1 mm of the neutron-activated soil at the hypocenter,
continuously present throughout the first 7 days from thedetonation, would result in a skin exposure of about 0.8 Gy,
but such an exposure condition was not plausible (17).
The findings that distal survivors were not exposed tohigh-dose residual radiation are also supported by studies
using biodosimetry. The frequency of stable chromosome
aberrations among the survivors with individual dose
estimates of ,0.005 Gy was thought to be similar to thatin the general population and the not-in-city group (26).
Another published study, on electron spin resonance of
tooth enamel, did not support claims that a large fraction of
distally-exposed survivors received a large dose (e.g., 1 Gy)of external penetrating radiation resulting from residual
radiation (27).
Using DS02 dose estimates, our data clearly indicate
some increase in severe epilation at doses less than 1 Gy,
shown in Tables 3 and 4 and by Stram, et al. (6), in contrast
to the threshold of 3 Gy suggested by the ICRP (25).
Consideration of dose error based on existing RERF models
would not suggest that this corresponds to a true dose much
above 1 Gy. These considerations are supported by studies
using multiple end points in addition to epilation, including
chromosomal aberrations and leukemia (28, 29). On theother hand, even doses on the order of 1 Gy are
considerably in excess of those that could plausibly result
from known fallout levels, as discussed above. Althoughvery small rates of epilation on the order of a few
percentages are observed at longer distances where DS02
doses are vanishingly small, these are not spatially localized
to the Nishiyama or Koi-Takasu areas or to any otherparticular distal area for that matter, and we consider them
to be artifacts due to non-radiation effects, such as trauma,
poor nutrition and hygiene conditions after the bombings orother unknown causes, including exceptional instances ofhigh radioactive fallout or high radiosensitive persons, ormisreported locations at the time of the bombings or
symptoms.
The number of individuals who reported acute symptoms
in distant areas from the hypocenter (2.0 þ km) was small,but the proportion developing acute symptoms in the lowest
direct dose categories was not nil, although those levels of
exposure were below that required to induce such symptoms(1). There were no conclusive explanations about whether
those symptoms were genuine acute radiation syndromes orabout any misclassifications of location at the time of thebombings or reported symptoms. Another unresolved issue
is the higher proportion of individuals who reported
epilation in Hiroshima compared to Nagasaki (but not forbleeding or oropharyngeal legions). This was previously
observed in reports documenting atomic bomb dosimetry
systems, but no consensus was reached to explain this (5, 6).
The proportion of survivors with no records of rain
(unknown exposure) was higher in Hiroshima than in
Nagasaki, and higher in proximal survivors than in distal
survivors in both cities, but there were no substantial
differences by direction from the hypocenter (Table 1). The
reasons for the city-specific differences in the survey results
are unknown, as no field documentation for survey methods
has been found. The unbalanced proportions between
proximal and distal survivors were adjusted for by matchingon direct dose. Frequencies of occurrence of acute
symptoms among those with unknown rain exposure
generally fell between those of exposed and unexposed
individuals (Tables 3 and 4). It has been suggested that thegroup with unknown exposure was a mixture of exposed
and unexposed individuals. The intermediate values imply
that the considerable proportion of the those with unknown
exposure to rain did not induce a serious systematic bias on
the analysis comparing exposed and unexposed individuals
but likely did decrease the study’s statistical power.
In conclusion, there is no consistent evidence to support
the notion that the reported rain was generally andhomogeneously radioactive at a considerable level, suchthat it would have resulted in cumulative doses over time ofseveral hundred mGy or higher from integrated external
exposure. This accords with ground measurements madesoon after the bombings showing that radioactive fallout
occurred only in a localized area in each city. Only the smalland sparsely populated area just west of the reservoir in
Nishiyama had estimated doses from fallout that approachedseveral hundred mGy. The observed infrequent associations
between reported exposure to rain and reported development of acute symptoms observed in distant areas from the
hypocenter may have occurred due to various but
exceptional reasons. First is the possibility of exposure tohighly radioactive fallout or direct exposures among highly
radiosensitive persons, or an interaction of radiation andpoor health. The second is due to misclassifications or
misreporting of exposure and outcome, such as incorrect
memory of the location at the time of bombing, reporting
symptoms due to other causes or reporting that suffers from

ACUTE SYMPTOMS AND RAIN AFTER ATOMIC BOMBINGS

recall bias that produces an apparent association between
exposures and outcomes. Although there may have beensome individual cases consistent with rare circumstances,
recall bias is a more plausible explanation of the association
between reported exposure to rain and development of acute
symptoms based on this group analysis. However, theinsufficient and retrospective nature of the available data
limits our ability to differentiate attribution of acute effects
to the several possible causes.
ACKNOWLEDGMENTS
The Radiation Effects Research Foundation (RERF), Hiroshima andNagasaki, Japan is a public interest foundation funded by the Japanese
Ministry of Health, Labour and Welfare (MHLW) and the U.S.
Department of Energy (DOE). The research was also funded in part by
the DOE, award no. DE-HS0000031 to the National Academy of Sciences.
This work was supported by RERF Research Protocol 1-75. The views of
the authors do not necessarily reflect those of the two governments.
Received: February 1, 2015; accepted: March 18, 2016; published online:
May 25, 2016

REFERENCES
1. United Nations Scientific Committee on the Effects of Atomic
Radiation (UNSCEAR). Early effects in man of high dose ofradiation. In: UNSCEAR. Sources, Effects and Risks of Ionizing
Radiation, 1988 Report of the General Assembly and Annex G.
New York: United Nations; 1988. paragraphs 1–89.
2. Oughterson AW, Warren S. Clinical observations in Hiroshima
and Nagasaki. In: Oughterson AW, Warren S. editors. Medical
effects of the atomic bomb in Japan. New York: McGraw-Hill;
1956. p. 97–190.
3. Takeda J, Hoshi M, Sawada S, Sakanoue M. Uranium isotopes in
Hiroshima ‘‘black rain’’ soil. J Radiat Res 1983; 24:229–36.
4. Okajima S, Fujita S, Harley JH. Radiation doses from residual
radioactivity. In: Roesch WC, editor. US-Japan joint reassessmentof atomic bomb radiation dosimetry in Hiroshima and Nagasaki,
final report. Hiroshima: Radiation Effects Research Foundation;
1987. p. 205–26.
5. Gilbert ES, Ohara JL. An analysis of various aspects of atomic
bomb dose estimation at RERF using data on acute radiation
symptoms. Radiat Res 1984; 100:124–38.
6. Stram DO, Mizuno S. Analysis of the DS86 atomic bomb radiation
dosimetry methods using data on severe epilation. Radiat Res
1989; 117:93–113.
7. Ishida M, Beebe G. Research plan for joint NIH-ABCC study oflife-span of A-bomb survivors. ABCC Technical Report 4-59.
Hiroshima: Atomic Bomb Casualty Commission; 1959.
8. Jablon S, Ishida M, Yamasaki M. JNIH-ABCC Life Span Study,
Hiroshima and Nagasaki. Report 3, Mortality, October 1950–
September 1960. ABCC Technical Report 15-63. Hiroshima:
Atomic Bomb Casualty Commission; 1963.
9. Noble KB. Shielding survey and radiation dosimetry study plan,
Hiroshima - Nagasaki. ABCC Technical Report 7-67. Hiroshima:
Atomic Bomb Casualty Commission; 1967.
10. Preston D, Mabuchi K, Kodama K, Fujita S. Relationship of
epilation to distance from hypocenter. Nagasaki Igakukai Zasshi(Nagasaki Med J ) 1998; 73:251–3. [Japanese]
11. Young RW, Kerr GD editors. DS02: A revised system for atomic

615

bomb survivor dose estimation. Hiroshima: Radiation Effects
Research Foundation; 2006.
12. Cullings HM, Fujita S, Funamoto S, Grant EJ, Kerr GD, Preston
DL. Dose estimation for atomic bomb survivor studies: Itsevolution and present status. Radiat Res 2006; 166:219–54.
13. SAS Institute. SAS 9.1.3, Cary (NC): SAS Inc.; 2003
14. Greenland S. Introduction to regression models. In: Rothman KJ,
Greenland S, Lash TL, editors. Modern epidemiology, 3rd ed.
Philadelphia: Lippincott Williams & Wilkins; 2008. p. 381–417.
15. Greenland S. Introduction to regression modeling. In: Rothman
KJ, Greenland S, Lash TL, editors. Modern epidemiology, 3rd ed.
Philadelphia: Lippincott Williams & Wilkins; 2008. p. 418–55.
16. Endo S, Tanaka K, Shizuma K, Hoshi M, Imanaka T. Estimationof beta-skin dose from exposure to fission fallout from theHiroshima atomic bomb. Rad Prot Dosm 2012; 149:84–90.
17. Tanaka K, Endo S, Imanaka T, Shizuma, Hasai H, Hoshi M. Skindose from neutron-activated soil for early entrants following the Abomb detonation in Hiroshima: contribution from beta- andgamma-rays. Radiat Environ Biophys 2008; 47:323–30.
18. Rothman KJ, Greenland S, Lash TL. Validity in epidemiologic
studies. In: Rothman KJ, Greenland S, Lash TL, editors. Modern
epidemiology, 3rd ed. Philadelphia: Lippincott Williams &Wilkins; 2008. p. 128–47.
19. Hennekins CH, Buring JE. Analysis of epidemiologic studies:
evaluating the role of bias. In: Epidemiology in medicine. Boston:
Little Brown and Company; 1987. p. 272–86.
20. Arakawa ET. Residual radiation in Hiroshima and Nagasaki.
ABCC Technical Report 2-62. Hiroshima: Atomic Bomb Casualty
Commission; 1962.
21. Sakata R, Grant EJ, Furukawa K, Misumi M, Cullings HM, Ozasa
K, et al. Long-term effects of the rain exposure shortly after theatomic bombings in Hiroshima and Nagasaki. Radiat Res 2014;
182:599–606.
22. Barss NM, Weitz RL. Reconstruction of external dose from beta
radiation sources of nuclear weapon origin. Health Phys 2006;
91:379–89.
23. Okajima S. Dose estimation from residual and fallout radioactivity.
Part 3. Fallout in the Nagasaki–Nishiyama district. J Radiat Res
1975; 16:S35–41.
24. Shizuma K, Iwatani K, Hasai H, Hoshi M, Oka T, Okano M.
137Cs concentration in soil samples from an early survey ofHiroshima atomic bomb and cumulative dose estimation from thefallout. Health Phys 1996; 71:340–6.
25. ICRP. Early and late effects of radiation in normal tissue andorgans – threshold dose for tissue reactions in a radiation
protection context. ICRP publication 118. Ann ICRP 2012;41:152–76.
26. Kodama Y, Pawel D, Nakamura N, Preston D, Honda T, Itoh M, etal. Stable choromosome aberrations in atomic bomb survivors:
results from 25 years of investigation. Radiat Res 2001; 156:337–
46.
27. Hirai Y, Kodama Y, Cullings HM, Miyazawa C, Nakamura N.
Electron spin resonance analysis of tooth enamel does not indicate
exposure to large radiation doses in a large proportion of distallyexposed A-bomb survivors. J Radiat Res 2011; 52:600–8.
28. Sposto R, Stram DO, Awa AA. An estimate of the magnitude ofrandom errors in the DS86 dosimetry from data on chromosome
aberrations and severe epilation. Radiat Res 1991; 128:157–69.
29. Neriishi K, Stram DO, Vaeth M, Mizuno S, Akiba S. The observed
relationship between the occurrence of acute radiation effects andleukemia mortality among A-bomb survivors. Radiat Res 1991;
125:206–13.