RADIATION RESEARCH 174, 146–154 (2010)0033-7587/10 $15.00
g 2010 by Radiation Research Society.
All rights of reproduction in any form reserved.
DOI: 10.1667/RR2044.1

41

Ca in Tooth Enamel. Part II: A Means for Retrospective Biological
Neutron Dosimetry in Atomic Bomb Survivors

W. Rühm,a,b,1 A. Wallner,b,c,d H. Cullings,e S. D. Egbert,f N. El-Faramawy,a,g T. Faestermann,c D. Kaul,f K. Knie,cG. Korschinek,c N. Nakamura,e J. Robertsf and G. Rugelc
Helmholtz Zentrum München, German Research Center for Environmental Health, 85764 Neuherberg, Germany; b Radiobiological Institute,
University of Munich, 80336 Munich, Germany; c Faculty of Physics, Technical University of Munich, 85747 Garching, Germany;; d VERA laboratory, Faculty of Physics, University of Vienna, A-1090 Wien, Austria; e Radiation Effects Research Foundation, Hiroshima, Japan;fScience Applications International Corporation, San Diego, California 92121; and g On leave from Department of Physics, Faculty of Science,
Ain Shams University, 65511 Abbassia, Cairo, Egypta

INTRODUCTION
Rühm, W., Wallner, A., Cullings, H., Egbert, S. D., ElFaramawy, N., Faestermann, T., Kaul, D., Knie, K., Korschinek, G., Nakamura, N., Roberts, J. and Rugel, G. 41Ca in Tooth
Enamel. Part II: A Means for Retrospective Biological Neutron
Dosimetry in Atomic Bomb Survivors. Radiat. Res. 174, 146–
154 (2010).

Neutrons represent a densely ionizing radiation that ismore effective biologically than X or c rays. There aremany occasions where neutrons contribute significantly
to the dose of individuals or groups of individuals. For
example, they are produced continuously in the atmosphere by cosmic radiation and contribute about half ofthe effective dose at flight altitudes (1). Occupational
exposure to neutrons may occur in nuclear installations
or outside the shielding of high-energy accelerators (2),and accidental exposures to large doses of neutrons havebeen reported (3). Fairly substantial exposures have also
been reported as a by-product of proton therapy (4).
Exposures to mixed radiation fields including neutrons
occurred in the atomic bomb survivors of Hiroshima
and Nagasaki (5). Retrospective dose estimation forthese exposed individuals is always a difficult task.
In the past, the obvious need to quantify individual
exposures to ionizing radiation retrospectively led toefforts aimed at finding traces of radiation exposure in
biological materials of those exposed. Biological dosimetry—as it is called—primarily includes two methods;
one is detection of chromosome aberrations (dicentricchromosomes shortly after exposure or translocations
years after exposure) in peripheral blood lymphocytes,
and the other is measurement of carbon radicals in tooth
enamel by means of electron paramagnetic resonance(EPR). Translocation frequencies have been measured ina large number of atomic bomb survivors and carbon
radicals in tooth enamel from several tens of survivors to
substantiate or better understand possible biases inindividual doses estimated physically (6, 7). However, no
method is available to evaluate neutron exposures
separately under mixed exposures, which include c rays.
Despite those difficulties, efforts have been made over
several decades to quantify the radiation doses to thesurvivors given the importance of the atomic bomb
survivor cohort in radiation sciences; atomic bomb

41

Ca is produced mainly by absorption of low-energy neutrons
on stable 40Ca. We used accelerator mass spectrometry (AMS)
to measure 41Ca in enamel of 16 teeth from 13 atomic bomb
survivors who were exposed to the bomb within 1.2 km from the
hypocenter in Hiroshima. In our accompanying paper (Wallner
et al., Radiat. Res. 174, 000–000, 2010), we reported that thebackground-corrected 41Ca/Ca ratio decreased from 19.5 310215 to 2.8 3 10215 with increasing distance from the
hypocenter. Here we show that the measured ratios are in goodcorrelation with c-ray doses assessed by electron paramagnetic
resonance (EPR) in the same enamel samples, and agree wellwith calculated ratios based on either the current Dosimetry
System 2002 (DS02) or more customized dose estimates where
the regression slope as obtained from an errors-in-variables
linear model was about 0.85. The calculated DS02 neutron doseto the survivors was about 10 to 80 mGy. The low-energy
neutrons responsible for 41Ca activation contributed variably tothe total neutron dose depending on the shielding conditions.
Namely, the contribution was smaller (10%) when shielding
conditions were lighter (e.g., outside far away from a single
house) and was larger (26%) when they were heavier (e.g., in or
close to several houses) because of local moderation of neutronsby shielding materials. We conclude that AMS is useful forverifying calculated neutron doses under mixed exposure
conditions with c rays. g 2010 by Radiation Research Society

1 Address for correspondence: German Research Center for
Environmental Health, Institute of Radiation Protection, Ingolstädter Landstr. 1, 85764 Neuherberg, Germany; e-mail: Werner.
ruehm@helmholtz-muenchen.de.

146

41

Ca IN TOOTH ENAMEL. PART II

survivor data that accumulated from 1950 up until
recent years are being used as a basis for setting
radiation safety standards world-wide (8). Regarding
the assessment of neutron doses, a number of different
neutron-induced radioisotopes have been quantified inenvironmental samples from Hiroshima and Nagasaki
to reconstruct the neutron fluence at their locations (5,9–16), while no appropriate methods are available forindividual biological samples [see ref. (17) for more
information]. In the present study, we propose a new
method to estimate individual doses of neutrons using
human teeth.
The proposed method includes measurements of the41
Ca/Ca ratio in tooth enamel. 41Ca (tK 5 103,000 years) is
produced mainly by absorption of low-energy neutrons
on stable 40Ca. In a companion paper (18), we describe themethods used to prepare enamel samples and to detect the
number of 41Ca nuclei by means of accelerator mass
spectrometry (AMS), and we apply it for the first time toenamel samples from atomic bomb survivors. In thepresent paper, we compare the measured 41Ca/Ca ratioswith the c-ray dose measured by EPR and with calculated
41
Ca/Ca ratios based on the DS02 dosimetry system andon more customized simulations.
MATERIALS AND METHODS
Method of Detection
We propose detecting the long-lived radionuclide 41Ca in tooth
enamel in a manner similar to what we have reported previously forenvironmental granite samples (19, 20). In the samples, 41Ca is
produced by absorption of thermal neutrons on stable 40Ca. Thus the41
Ca/Ca ratio in an enamel sample is a direct measure of the neutron
fluence to which the sample was exposed. Because the 41Ca activity ina 100-mg enamel sample, which is typically available from individual
molars, is far too low to detect by decay counting (e.g., the activity isless than 1 mBq), AMS is proposed for the measurement of 41Ca,
which identifies 41Ca by its mass and nuclear charge prior to its decay.
That technique allows detection of 41Ca/Ca levels below 1 3 10215(which would correspond to about 0.1 mBq of 41Ca activity in a 100mg enamel sample). Details of the method are given in the companion
paper (18).
Samples InvestigatedTooth enamel is considered the most suitable human biomaterial
for 41Ca detection because of its high calcium concentration, little if
any metabolism after completion of tooth formation, and applicability of EPR for the assessment of c-ray doses in the same sample (7).
For the present study, 16 tooth enamel samples from 13 donors werechosen, which satisfied the following conditions: (1) he or she was
exposed to the bomb between 0.8 km and 1.2 km from the hypocenter
in Hiroshima; the hypocenter is the vertical projection to the groundof the point of explosion (i.e., the epicenter) that was 600 m above theground (5); (2) a tooth sample was extracted for medical reasons anddonated to the Radiation Effects Research Foundation (RERF); and(3) EPR measurements had already been performed on the samples toquantify the dose of c rays from the bomb (7). Typically, 100 mg ofenamel was available from each tooth, which corresponded to about
36 mg of calcium. Teeth from a control group with low exposure werealso included in the study. See ref. (21) for more details.

147

Simulation of the 41Ca/Ca Ratios in Individual Survivors Based on DS02
In an effort to calculate the 41Ca/Ca ratio expected in tooth enamelof atomic bomb survivors, DS02 (5) was used as a reference. Amongthe organs considered in DS02, the thyroid gland was chosen as asurrogate because its mean depth below the skin is similar to that of
the teeth in the oral cavity. Specifically, the 41Ca/Ca ratio in theenamel samples was calculated for 10 investigated donors bymultiplying the DS02 neutron fluence spectrum in the thyroid withthe energy differential 40Ca absorption cross-section (22) to calculate
neutron-induced 41Ca. DS02 house shielding, body size and individual
orientation with respect to the direction to the epicenter were also
taken into account as well as different possible postures (standing,sitting/kneeling, or lying). There is approximately a 20% systematicand 20% random uncertainty on the calculations. That is based on theassumption that the uncertainty for total and thermal neutron fluenceis similar to that of neutron dose (23). Figure 1 shows, as an example,
the neutron fluence spectra as provided by DS02 at a distance where
survivor D20 was located at the time of bombing. The fluence in eachenergy group is divided by the logarithmic width between the group’s
lower and upper energy bounds and then is normalized to the value
for the thermal energy group. This presentation makes equal areas
below the curve correspond to equal neutron fluence and allows each
spectrum to be represented over a more narrow range for all energies
to highlight differences among spectra. Because survivor D20 was
exposed almost free-in-air, the DS02 neutron spectrum at that
distance calculated free-in-air and 1 m above ground (i.e., without any
disturbing building structures; light gray line in Fig. 1) is not muchchanged when DS02 standard procedures were included to takesurrounding shielding structures into account (dark gray line in
Fig. 1). The DS02 neutron spectrum in the thyroid, however, becomes
more thermalized (black line in Fig. 1) due to moderation of neutrons
in the human body. For comparison, Fig. 2 shows neutron fluence
spectra for survivor E90, who was also exposed in the open but very
close to adjacent buildings. In this case, the DS02 neutron spectrum
that takes shielding into account (dark gray line in Fig. 2) differs
much from the DS02 free-in-air spectrum at that distance (light grayline in Fig. 2) and is much softer. For the thyroid, the DS02 neutron
spectrum (black line in Fig. 2) is still softer. Here, compared tosurvivor D20, the relative contribution of neutrons above say 100 keV,which are important for neutron dose, is reduced, and the role ofthermal neutrons in dose becomes more important (see discussion
below). Note also that the DS02 free-in-air spectrum for survivor D20
appears to be somewhat harder due to the hardening of the neutron
spectrum with increasing distance from the hypocenter [corrected
ground ranges are 1,057 m for D20 and 894 m for E90, respectively(Table 1)]. Given these neutron fluence spectra and the 41Ca
production cross-section, most of the 41Ca nuclei produced in theenamel samples were due to neutrons below 0.4 eV (first bin in Figs. 1
and 2) (18).
DS02 does not calculate each individual’s unique shielding
situation directly but translates the individual’s shielding parameters
to a limited number of model shielding cases. Therefore, in an effort
to improve the DS02 procedure, customized shielding calculations forthe donors in this study were performed (23) by means of the MASH
code (24). For that, the shielding history of each survivor had to bemodeled individually. To achieve that, we used questionnaire
information, which was collected in the early phase of the life spanstudy (LSS) project in the 1950s. It contained locations of survivors at
the time of the bombing with respect to the hypocenter, detailed
shielding conditions by houses or other neighborhood structures, andorientation of the survivor with respect to the epicenter, posture, etc.
The summary information is given in Table 1. Figure 3 gives, as an
example, the environment where the individual who donated sample
D20 survived (as modeled in the present paper for the customized
approach). For comparison, Fig. 4 shows the donor of the E90
sample, who was exposed to radiation close to a cluster of Japanese

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RÜHM ET AL.

FIG. 1. Neutron fluence spectra for survivor D20 (DS02 ground
range: 1,053 m) as provided by DS02. Light gray line: free-in-air 1 m
above ground; dark gray line: including surrounding structures; black
line: within thyroid.
houses, with complicated conditions that require detailed modeling.
With that customized approach, neutron energy spectra were
calculated for the position of the survivor at the time of the bombing.
The customized approach calculated the individual neutron energy
spectra at the survivors’ in-house locations but did not include
calculations of neutron energy spectra within the survivors’ bodies.
Therefore, to obtain a customized 41Ca activation at the position of
the thyroid gland of the donors, the standard DS02 total neutron
fluences in the house (corresponding to the dark gray lines in Figs. 1
and 2) were adjusted to equal the total neutron fluence in the houseobtained by the customized MASH calculations, and the resulting
adjustment factor was used to renormalize the DS02 neutron energy
spectrum in the thyroid gland. This is because 41Ca activation in the
thyroid gland is closely related to the total neutron fluence impinging
on the body (for the adjustment factor, see column 6 of Table 1). In
contrast to those survivors who provided samples I29, B51/53 andL80 and who received adjustment factors of 1.27, 1.27 and 1.23,
respectively, the survivor who provided sample C47 also survived in aschool building but received a much lower adjustment factor of 0.68.
That difference is due to the fact that the former survivors’ schoolbuilding had a side with an unshielded exposure to the bomb, while
the latter survivor had a two-story wing of the building, 12 m in front,
near the line of sight, that blocked half of the incident neutron
fluence. Neither large open classrooms nor building wings were
included in the DS02 neutron calculations for Japanese wooden
houses. The customized thyroid neutron fluence was multiplied by the40
Ca neutron absorption cross section (22) to customize the 41Ca
production in the thyroid.
Re-evaluation of DS02 Ground Ranges by Means of Aerial Photographs
Values for the ground ranges of the survivors studied were initiallytaken from the DS02 database, and the customized shielding
calculations described above were performed based on these values.
The values are based on coordinates that were assigned to survivors in
the 1950s and early 1960s, when survivors’ shielding histories werecreated, using the plane rectangular coordinate system of the U.S.
Army maps of 1945. Recently, in a further customized approach to
improve the individual information available for the investigatedsurvivors, the ground range values were re-evaluated based on
prebombing aerial photographs showing detailed street plans andindividual neighborhood houses, and survivors were located in

FIG. 2. Neutron fluence spectra for survivor E90 (DS02 ground
range: 893 m) as provided by DS02. Light gray line: free-in-air 1 m
above ground; dark gray line: including surrounding structures; black
line: within thyroid.
relation to the estimated locations of the hypocenters using ageographical information system (GIS) and a set of newer and moreaccurate maps (25). From a fit of the DS02 ground ranges as afunction of total neutron fluence free-in-air (wtot,fia,DS02gr), adjustmentsin the total neutron fluence due to the re-evaluation of the ground
ranges were calculated for each survivor. It was assumed that achange in ground range would affect the total neutron fluence but
would not change the neutron energy spectrum appreciably over the
distances corresponding to the differences between each survivor’s
ground range in the RERF database and the more accurate ground
range determined with aerial photographs, which were all ,40 m.
Therefore, the customized neutron spectra were corrected bymultiplying by the wtot,fia,corrected-gr/wtot,fia,DS02-gr ratio (column 5 inTable 1).

RESULTS AND DISCUSSION

For the samples investigated, we obtained gross 41Ca/
Ca ratios varying from 4.0 3 10215 to 23 3 10215. A
background level of (1.72 ± 0.46) 3 10215 was thensubtracted, which was obtained from measurement ofsix control samples from distant survivors whose
estimated c-ray doses are below 0.5 mGy (18). The
resulting net 41Ca/Ca ratios ranged from 2.8 3 10215 to19.5 3 10215 (Table 2). Because of the limited number ofdetected counts, statistical uncertainties dominate theoverall uncertainties (13–24%). The results clearly
demonstrate a systematic decrease of the 41Ca/Ca ratioswith increasing distance from the hypocenter, whichsuggests that A-bomb neutrons are the primary cause of
the measured 41Ca signal (18).
The measured 41Ca/Ca ratios can be compared withthe c-ray doses measured by EPR on the same enamel
samples (7). The results are also included in Table 2 andplotted in Fig. 5. A significant positive correlation isobserved between the measured 41Ca/Ca ratios and thec-ray dose, which is expected because the distance from

41

149

Ca IN TOOTH ENAMEL. PART II

TABLE 1
Basic Information on the Samples Used for the Present Study
Age of donor
at the time ofbombing (years)

DS02
groundrange (m)Customized
groundrange (m)bCorrection factor
for total free-in-air
neutron fluencec

Correction factor forneutron fluence incustomized housed

F04
H43
E90

19
17
14

827
884
893

827f
884f
894

1.0f
1.0f
0.98

-

G91zG65
A72zA34
M93
K67
D20
I29e
B51zB53e
L80e
C47
J66

20
10
17
18
14
19
18
18
33
27

962
942
1,000
1,019
1,053
1,148
1,148
1,153
1,132
1,163

952
956
1,000 f
1,018
1,057
1,108
1,111
1,116
1,124
1,163f

1.08
0.90
1.0f
1.0
0.97
1.34
1.31
1.32
1.05
1.0f

SampleIDa

Type ofshieldingIndividual
position

0.89

2
2
Free-in-air (Fig. 4)

1.02
1.22
0.93
1.19
0.97
1.27
1.27
1.23
0.68
-

Twin house
Triple house
House cluster
House cluster
Free-in-air (Fig. 3)
School building
School building
School building
School building
22
2
In front of and close
to house cluster
First floor
First floor
First floor
First floor
Far away from house
Second floor
First floor
Second floor
First floor
2

Individual
shieldingcalculation
no
no
yes
yes
yes
yes
yes
yes
yes
yes
yes
yes
no

a

Tooth samples G91 and G65, A72 and A34, and B51 and B53 are from the same survivor, respectively.
DS02 ground ranges re-evaluated from aerial photographs when possible.
cBased on the re-evaluated ground ranges.
dI.e., the ratio of total customized MASH neutron fluence at the survivors’ locations to the total DS02 neutron fluence at these locations.
eSurvivors who donated the samples I29, B51zB53 and L80 survived in the same school building.
f
No aerial photograph available to correct for.
bthe hypocenter is the major parameter influencing bothneutron and c-ray doses of individual survivors in
Hiroshima (but the neutron dose decreases faster thanthe c-ray dose in the air with increasing distance fromthe hypocenter). In fact, based on DS02 free-in-air
neutron and c-ray energy spectra (26), the curvilinear
dependence is expected to be similar to that observed inFig. 5. It should be mentioned, however, that shieldingof the survivors (for example by intervening building
material) acts somewhat differently for neutrons and crays, which explains at least part of the scatter seen in
Fig. 5.
Since the measured 41Ca/Ca ratios indicate a close
correlation with both the distance from the hypocenter

FIG. 3. Model of the environment in which the individual who donated sample D20 survived. Gray arrow:survivor location and orientation; solid black arrow: direction to epicenter from house origin; dashed blackarrow: direction to hypocenter from survivor location.

150

RÜHM ET AL.

FIG. 4. Model of a house cluster where the individual who donated sample E90 survived. Gray arrow:survivor location and orientation; solid black arrow: direction to epicenter from house cluster origin; dashedblack arrow: direction to hypocenter from survivor location.

(Table 1) (18) and the measured c-ray dose (Fig. 5), 41Cain enamel can be considered as a biomarker for neutron
exposure. To be a biodosimeter, however, the measured
41
Ca/Ca ratios need to be validated quantitatively. To
address this issue, we calculated the 41Ca/Ca ratio at theposition of the thyroid for 10 donors by means of the
MASH code, which used detailed shielding and incorporated the new information on ground ranges. The
results of those calculations are also included in Table 2
and are compared with the measured 41Ca/Ca ratios in
Fig. 6. The measured ratios are generally proportionallyrelated to the calculated ones, but the mean slope was
0.68, which is somewhat lower than unity (Fig. 6). Theremay be several causes for this.
Based on the uncertainty discussion above, about 20%
systematic and 20% random uncertainty may be
involved in the 41Ca activation calculations due touncertainties, e.g., in survivor location and shielding
conditions. Thus the total uncertainty in the calculated
41
Ca/Ca ratios may not be better than about 30%, which
may explain part of the observed discrepancy. To be
more specific, a slope of 0.68 was obtained by applying a

TABLE 2
Results Obtained on the Investigated Tooth Enamel Samples
SampleIDa

Toothpositionb

EPR c-raydose (Gy)c,dDS02 c-ray dose
for thyroid (Gy)

Net 41Ca/Ca
measured (10215)d41
Ca/Ca for thyroid based on
customized calculation (10215)

Total DS02 neutron
dose for thyroid (mGy)

F04
H43
E90
G91
G65
A72
A34
M93
K67
D20
I29
B51
B53
L80
C47
J66

7
6
1
7
6
2
3
8
6
7
8
4
4
7/8
8
7

3.1 ± 0.1
2.5 ± 0.1
2.3 ± 0.1
3.1 ± 0.1
2.7 ± 0.1
3.6 ± 0.1
3.9 ± 0.1
1.2 ± 0.1
1.2 ± 0.1
2.7 ± 0.1
1.8 ± 0.1
2.4 ± 0.1
2.4 ± 0.1
1.7 ± 0.1
2.8 ± 0.1
1.2 ± 0.1

2.8
2.7
2.3
2.5
2.5
2.8
2.8
2.1
1.2
2.8
1.2
1.1
1.1
1.0
1.7
0.8

19.5 ± 4.0
13.5 ± 2.0
16.9 ± 4.1
11.3 ± 2.3
9.1 ± 2.0
18.2 ± 4.0
18.5 ± 4.0
7.2 ± 2.5
5.0 ± 1.5
8.6 ± 2.7
3.9 ± 2.0
7.4 ± 2.1
7.5 ± 2.4
7.6 ± 2.0
6.0 ± 2.1
2.8 ± 3.0

23.6
19.3
19.3
22.2
22.2
10.1
14.4
13.2
8.7
6.3
6.3
8.0
2.4
-

82
71
50
44
44
45
45
23
29
58
15
9.5
9.5
13
13
11

a

Tooth samples G91 and G65, A72 and A34, and B51 and B53 are from the same survivors.
Positions 1–2: incisor, position 3: canine, positions 4–5: premolar, positions 6–7: molar, position 8: wisdom tooth.
c
Samples E90, A72, A34, B51 and B53, are non-molars, and the EPR c-ray dose may include a contribution from exposure to ultraviolet light(27).
dUncertainties refer to measurement errors including statistics and systematic 1 s uncertainties (for details see text).
b

41

Ca IN TOOTH ENAMEL. PART II

FIG. 5. Plots of 41Ca/Ca ratios measured by AMS (18) as afunction of c-ray dose measured by EPR (7) in the same enamel
samples. Data were fitted by a curvilinear non-weighted method (solidline); for multiple samples from the same survivors, weighted averages
were used.

regular regression model where the independent variables (the calculated 41Ca/Ca ratios of the x axis) wereassumed to be exact. However, the calculated 41Ca/Ca
ratios are subject to an error of about 30%, and anerrors-in-variables model should therefore be appliedinstead, which would result in an attenuation of theslope as obtained from the regular regression model. If
the error of the independent calculated variable corresponds roughly to 0.38 3 10214 (which is 30% of themean calculated value of 1.3 3 10214), then, given thatthe calculated values have a standard deviation of 0.72
3 10214, the expected attenuation in the regression slope
is about 1/(1 z (0.38/0.72)2) 5 0.78 [see e.g. ref. (28)]. A
simulation of the data taking into account the Poissoncounting statistics required due to the low number ofcounts measured confirmed this estimate and resulted ina value of 0.82 for the attenuated slope. The slope ofabout 0.68 obtained from the simple linear regressions iswell within the 95% confidence bounds of the slopes
obtained from the simulation, confirming that theresults of the simple linear regressions do not statisticallyreject the null hypothesis that the measured andcalculated values are estimating the same quantity. In
summary, the estimated error of about 30% in thecalculated values results in an attenuation of the slope
obtained in the simple regression model of about 0.8.
Correcting for this effect, the slope as obtained from
Fig. 6 translates to 0.68/0.8 5 0.85, which is still lower
than but quite close to the ideal number of 1.
Additionally, some portion of the lower response
could be due to the trend that, at high doses, those who
actually survived were more likely to have received
smaller true doses than their DS02 calculated dose,
because those whose doses were higher (lower) than their
DS02 doses were less likely (more likely) to have

151

FIG. 6. Comparison of the measured and calculated 41Ca/Ca
ratios, which used detailed shielding information. The line shows alinear non-weighted fit of the data (r2 5 0.61). Horizontal error bars
are based on an assumed 30% uncertainty of the calculated 41Ca/Ca
ratios (see text for details).

survived. However, this does not seem to be a likely
explanation in the present study since the EPRmeasured c-ray doses are generally in good agreementwith (or not smaller than) DS02-calculated c-ray
absorbed doses of the thyroid (Table 2). Note also that,
due to their small number, the individuals studied may
not be a representative sub-sample of the total LSS
cohort. Finally, calcium isotope exchange processes
between enamel and environment after the bombing
could also explain a lower measured than calculated
41
Ca/Ca ratio, because natural 41Ca/Ca ratios in the dietare low and of the order of 1 3 10215 as indicated by the
low ratios measured in the background enamel samples.
Note, however, that the age of all survivors studied issuch that enamel formation can be considered to havebeen completed at the time of bombing (see Table 1).
We thus feel that the present results indicate that 41Ca
measurement is a useful biodosimeter of neutrons.
Nevertheless, future investigations are needed to quantify, for example, any difference in 41Ca activation in the
thyroid compared to that in tooth enamel.
Figure 7 represents a comparison of the measured
41
Ca/Ca ratios with the ratios by standard DS02
calculations. Although the calculated ratios in somesurvivors may differ by about 40% between the standard
DS02 and customized calculations, the mean slope (i.e.,0.69) remains nearly the same between Figs. 6 and 7 (r25 0.56 for the DS02 approach and 0.61 for thecustomized calculations). Thus the results indicate that
DS02 provides sufficient precision to quantify survivor
exposure to neutrons. Although further calculations ofdetailed shielding and more accurate survivor locations
are expected to improve the calculated ratios, the present
results did not indicate the tendency clearly.
The last point relates to the detection limit of the
AMS technique used to detect neutron exposures. Total

152

RÜHM ET AL.

FIG. 7. Comparison of the measured and calculated 41Ca/Ca
ratios, which used standard DS02 calculations. The line shows alinear non-weighted fit of the data (r2 5 0.56). Horizontal error bars
are based on an assumed 30% uncertainty of the calculated 41Ca/Ca
ratios (see text for details).

neutron absorbed doses for the thyroids of the survivors
examined were calculated based on the DS02 neutron
spectra and were found to range from about 10 to
80 mGy (customized neutron spectra could not becalculated in the present study), which indicates thatAMS is highly sensitive. Figure 8 shows the contributionof low-energy neutrons to the total neutron absorbed
dose for the thyroid for the two survivors who donatedsamples D20 and E90. For the donor of the D20 sample,
who was exposed in the open, the dose contribution ofthermalized neutrons (,0.4 eV), which dominate 41Ca
production, was only about 10% to the total neutron
dose. By contrast, for the donor of the E90 sample, who
was exposed to the bomb very close to a cluster ofJapanese houses, the contribution of thermalized neutrons was larger, about 26%. The difference is attributable to differences in the energy spectrum of theneutrons; namely, if the exposure occurred outside faraway from a house, the fraction of thermal neutrons was
smaller (e.g., donor of sample D20), while it was muchlarger if the exposure occurred inside or close to a house
as a result of effective scattering and moderation ofneutrons by building structures (e.g., donor of E90
sample) (see Figs. 1 and 2). Since both survivors were
the same age, body size is probably not a major factor
for the differences we observed. Further, orientation
would not be a major factor either, because the donor of
the D20 sample was oriented with his left side to the
hypocenter while the donor of the E90 sample wasoriented with his right side to the hypocenter, whichshould not make much difference for neutron absorbed
dose of the thyroid. Thus, depending on the shape of theneutron spectrum at a survivor’s location, thermal
neutrons may contribute considerably to the total
neutron dose, which is mainly due to protons emitted

FIG. 8. Fraction of DS02 absorbed dose to the thyroid fromneutrons with energies below a specified energy relative to total
neutron absorbed dose to the thyroid for two selected samples (D20and E90).

at an energy of about 0.6 MeV from 14N(nthermal,p)14C
reactions that occur in tissue.
A contribution of thermal neutrons by 10–30% to thetotal neutron dose is similar to that of fast neutrons withan energy above 1 MeV (25–40%), which were considered
to be the major contributor to the total neutron dose. For
example, fast neutrons had been measured through thedetection of 63Ni in (inorganic) copper samples (14, 15, 29,30) and through the detection of 39Ar in (inorganic)
granite samples (16). In these studies, samples that were
exposed in the line of sight to the epicenter without muchshielding were selected. Since the surrounding materials
generally had a low moisture content, the neutron spectra
were similar to those for survivors who were exposed inopen conditions. Such survivors would have a smaller
fraction of thermal neutrons compared with those who
were more shielded or were surrounded by wooden
structures at the time of the bombing. These studies
showed that fast neutrons primarily contributed to thetotal neutron dose under circumstances of little shielding(e.g., survivors exposed in open conditions). By contrast,
the present study showed that the contribution of thermal
neutrons is also significant for those exposed in or close toa wooden house.
CONCLUSION

In summary, about 30 mg of the available 100 mg of
tooth enamel was sufficient to measure both c-ray doses
by EPR and neutron exposure by 41Ca AMS that werecaused by atomic bomb radiation in 1945. Although themeasured 41Ca activation in enamel appears to be some
15% lower than that calculated, we feel that the present
results indicate that 41Ca measurement is a usefulbiodosimeter of neutrons. Nevertheless, additional work
is required to quantify the origin of this remaining

41

Ca IN TOOTH ENAMEL. PART II

discrepancy. That work may include, for example,
detailed calculations to compare 41Ca activation by
neutrons in the thyroid (which was used as a proxyorgan) compared to that in tooth enamel.
The present results are the first that document a
biological fingerprint of neutron exposures in Hiroshima
and Nagasaki, and 41Ca AMS may detect neutron
exposures that correspond to about 10 mGy of total
neutron dose at a survivor’s location in Hiroshima. The
fact that the customized approach does not result in a
substantial improvement over the standard DS02
approach suggests that the standard DS02 approachproduces reliable individual dose estimates. This findingis important because it has not previously been verified
experimentally for neutrons. The proposed method willserve as a unique tool for evaluating the neutron dosethat accompanied c-ray exposures. It may also be used
to quantify accidental neutron exposures that occurredmany years earlier.
ACKNOWLEDGMENTS
The authors are deeply indebted to the atomic bomb survivors who
donated their extracted teeth; without their collaboration, the present
study would not have been possible. The authors greatly appreciate
Ms. S. Funamoto, Statistics Department of RERF, for her efforts inusing the DS02 system to provide spectral fluence data for the tooth
donors. This publication is partly based on research performed at theRadiation Effects Research Foundation (RERF), Hiroshima andNagasaki, Japan. RERF is a private foundation funded by theJapanese Ministry of Health, Labor and Welfare, and the U.S.
Department of Energy, the latter in part through the U.S. National
Academy of Sciences. This study was partly supported by the German
Research Society under contract number K01258/6-2 and by RERF
Research Protocol B-42.
Received: October 21, 2009; accepted: March 19, 2010; published online:
May 25, 2010

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