Strontium-90 concentration measurements in human bones and teeth in Greece.

Abstract

Strontium-90 concentration was measured in human bones and teeth collected in Greece during the period 1992-1996. One hundred and five bone samples, mainly cancellous bone, and 108 samples, taken from a total of 896 individual teeth were processed. Samples were classified according to the age and sex of the donors. Samples were chemically pre-treated according to a specially devised method to enable extraction of 90Y, at equilibrium with 90Sr in the original sample. Subsequently, 90Y beta activity was measured with a gas proportional counter. Radiostrontium concentration in bone samples showed small variations with respect to age or sex, with an average value of 30 mBq 90Sr/g Ca. However, 90Sr concentration measurements in teeth demonstrated a pronounced structure, which clearly reflects contamination from the 1960s atmospheric nuclear weapons tests and the more recent Chernobyl accident. This difference is attributed to the different histological structure of skeletal bones and teeth, the later consisting mainly of compact bone. An age-dependent model for radiostrontium concentration in human bones and teeth is developed which is able to successfully reproduce the experimental data. Through a fitting process, the model also yielded calcium turnover rates for compact bone, as a function of age, as well as an estimate of radiostrontium contamination of foodstuffs in Greece for the past four decades. The results obtained in this study indicate that radiostrontium environmental contamination which resulted from the atmospheric nuclear weapons tests in the 1960s, exceed by far that caused by the Chernobyl accident.

Full text

Page 1

Ž.
The Science of the Total Environment 229 1999 165?182
Strontium-90 concentration measurements in human
bones and teeth in Greece
K.C. Stamoulisa,?, P.A. Assimakopoulosa, K.G. Ioannidesa, E. Johnsonb,
P.N. Soucacosb
aNuclear Physics Laboratory, Department of Physics, The Uni?ersity of Ioannina, 45110 Ioannina, Greece
bSchool of Medicine, The Uni?ersity of Ioannina, 45110 Ioannina, Greece
Received 4 November 1998; accepted 10 February 1999
Abstract
Strontium-90 concentration was measured in human bones and teeth collected in Greece during the period
1992?1996. One hundred and five bone samples, mainly cancellous bone, and 108 samples, taken from a total of 896
individual teeth were processed. Samples were classified according to the age and sex of the donors. Samples were
chemically pre-treated according to a specially devised method to enable extraction of90Y, at equilibrium with90Sr
in the original sample. Subsequently,90Y ? activity was measured with a gas proportional counter. Radiostrontium
concentration in bone samples showed small variations with respect to age or sex, with an average value of 30 mBq
90Sr?g Ca. However,90Sr concentration measurements in teeth demonstrated a pronounced structure, which clearly
reflects contamination from the 1960s atmospheric nuclear weapons tests and the more recent Chernobyl accident.
This difference is attributed to the different histological structure of skeletal bones and teeth, the later consisting
mainly of compact bone. An age-dependent model for radiostrontium concentration in human bones and teeth is
developed which is able to successfully reproduce the experimental data. Through a fitting process, the model also
yielded calcium turnover rates for compact bone, as a function of age, as well as an estimate of radiostrontium
contamination of foodstuffs in Greece for the past four decades. The results obtained in this study indicate that
radiostrontium environmental contamination which resulted from the atmospheric nuclear weapons tests in the
1960s, exceed by far that caused by the Chernobyl accident.
? 1999 Elsevier Science B.V. All rights reserved.
Keywords: Radiostrontium;90Sr; Human bone; Human teeth
?Corresponding author.
0048-9697?99?$ - see front matter ? 1999 Elsevier Science B.V. All rights reserved.
Ž.
PII: S 0 0 4 8 - 9 6 9 7 9 9 0 0 0 5 2 - 2

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182166
1. Introduction
Strontium-90 is an artificial radioactive isotope,
produced by nuclear fission during the explosion
of a nuclear device and in nuclear energy plants.
A detailed table of nuclear explosions for the
period 1945?1994, including date, site and coun-
try responsible for the explosion is given by Law-
Ž.
son1994 . During this period, 881 nuclear
weapons tests were performed above ground and
in the atmosphere and 878 tests underground.
From tests during the first half of this period
Ž.
1945?1965 , it is estimated that about 10
90Sr and 1.3?1020Bq of
Ž
the atmosphere Christensen et al., 1975; Kritidis,
.
1989 . Serious nuclear accidents also added ra-
dioactive strontium isotopes into the atmosphere,
including the accident at Chernobyl which re-
leased about 1016Bq of
These releases of strontium isotopes, together
with fallout from other fission products, were
distributed world-wide.
Strontium is an element with chemical be-
haviour similar to that of calcium. As the human
skeleton consists of about 40% calcium,90Sr be-
18
Bq of
89Sr were released into
90Sr and 1018Bq of
89Sr.
haves as a bone-seeking nuclide. Radiostrontium
enters into the food chain and finally into the
human body, where through the biological path-
way of calcium it is deposited in bone and teeth.
The longest-lived of these radioactive isotopes,
90
Ž.
Sr T
?28.0 y , decays by ? emission to
1?2
also a radioactive nuclide, which further ?-decays
to the stable nuclide90Zr with a half-life T
64.1 h. The two successive ? emissions deposit
their energy within a small volume in the vicinity
of the decaying nuclei. This energy is absorbed by
bone or tooth tissue and the biological effect is
related to the total energy released and the rate
at which the energy is absorbed by the living cells.
The damage to the cells may be irreversible,
leadingto leukaemia
Knowledge of radiostrontium concentration in
bone tissue is necessary for estimating risk to
public health.
Many investigations concerning90Sr concentra-
tion levels in bone and teeth have been con-
ducted since the start of nuclear weapons tests in
the 1950s. Mean values of
bones throughout the world as a function of the
calendar year are presented in Fig. 1. These val-
90
Y,
?
1?2
andbone neoplasms.
90Sr concentration in
Fig. 1. World-wide mean annual values of90Sr concentration in bones grouped by age. A compilation of data from reports for the
Ž
period 1957?1986 Schulert et al., 1959; Bailey et al., 1960; Rosenthall et al., 1963, 1964; Jeanmaire and Patti, 1967, 1969, 1970,
1971, 1973, 1976, 1979; Christensen et al., 1975; Glowiak et al., 1977; Dehos and Kistner, 1980; Salonen, 1980; Klusek, 1984;
.
Aarkrog et al., 1988 .

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182 167
Fig. 2. World-wide mean annual values of90Sr concentration in teeth. A compilation of data from reports for the period 1950?1975
ŽButler, 1961; Reiss, 1961; Rosenthall et al., 1963; Santholzer and Knaifl, 1966; Aarkrog, 1968, 1971; Lerch et al., 1969; Rytomaa,
1971, 1972; Nagai and Ishii, 1972; Prokof’yev et al., 1973; Kolehmainen and Rytomaa, 1975; Glowiak et al., 1977; Turai et al., 1988;
.
Kulev et al., 1994 .
ues have been compiled from more than 20 stud-
ies reported in the scientific literature. Similarly,
mean annual values of90Sr concentration in teeth
throughout the world, also compiled from a num-
ber of independent investigations, are presented
in Fig. 2.
Only one report assesses levels of90Sr in bones
from the Greek population Mimikos and Du-
.
voyiannis, 1970 , covering the period 1962?1967.
Considering the geographical proximity of Greece
to the Ukraine, it was deemed important to assess
current radiostrontium levels in human bones in
Greece, especially after the Chernobyl accident.
A second reason for conducting the research
presented here pertains to our earlier study on
radiostrontium concentration in human teeth in
Ukraine, 5 years after the Chernobyl accident
Ž.
Kulev et al., 1994 . An unexpected feature in the
data from that investigation was observed; al-
though the overall trend of the data was a gradual
decrease of90Sr concentration with age, the 25?45
year age-groups showed abnormally high ra-
diostrontium concentrations see Fig. 3 . The ex-
planation offered for this anomaly at the time was
Ž
Ž.
Ž
that this age group 20?40 years of age at the
time of the Chernobyl accident contained a sig-
Ž
nificant number of men and women who, either
as part of the military or civilian staff of engineer-
ing firms, were mobilised immediately after the
accident for the extensive clean-up operations
within the 30-km zone around the damaged nu-
clear power plant. However, it was felt that this
explanation should be tested by repeating the
study for a population at a geographical position
far from the site of the accident.
.
.
2. Materials and methods
2.1. Sampling
One-hundred and five human bone samples
were collected during the period 1993?1995. Bone
samples were obtained from the Athens State
Morgue and the University of Ioannina General
Hospital. Although all donors of the samples were
residents of Greece, the geographical location of
residence of the donors within the country varied

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182168
Fig. 3. Age dependence of90Sr concentration in human teeth in the male population of South Ukraine, 5 years after the Chernobyl
Ž.
accident Adapted from Kulev et al., 1994 .
significantly. Eighty-one samples were from the
greater Athens area, 19 samples from the district
Ž
of Epirus about 300 km north-west of Athens ,
with the rest of the samples from various other
regions of Greece. However, since Greece is a
small country, the geographical area from which
all samples were obtained did not exceed a dis-
tance of 400 km. The texture of bone also varied
although samples generally consisted of cancel-
.
Ž.
lous
cluded 35 sterna, 34 ribs, 24 arthroses, 18 femoral
epiphyses, six knees, one clavicle and one verte-
brae sample. The distribution of samples accord-
ing to age and sex is shown in Fig. 4.
One-hundred and eight teeth samples were col-
lected by dentists in Athens, the city of Ioannina
and the town of Metsovo, as well as at the dental
clinics of the University of Athens Hospital and
spongybone. The samples collected in-
Fig. 4. Bone samples distribution according to age and sex. The last columns represent samples of unknown age.

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182 169
the ‘Hatzikosta’ General Hospital at Ioannina.
Teeth were grouped according to age and sex,
with each group containing typically 8?10 teeth.
A total of 896 teeth were processed and mea-
sured including, 225 molars, 203 premolars, 130
incisors, 45 canines and 246 roots of various teeth.
The distribution of tooth samples according to sex
and age is shown in Fig. 5.
2.2. Preparation of bone and teeth samples
Most of the bone samples were stored in a
formalin solution for more than 1 year. Sternum
and rib samples were stripped of remaining soft
tissue and dried at 80?100?C to constant weight
in order to remove formaldehyde from the sam-
ple. Femurs which were free of any soft tissue,
were stored at ?20?C. Typical dried mass of bone
samples was 30 g.
Tooth samples were stored in plastic bottles at
room temperature. A typical sample of dried tooth
was about 10 g. All bone and teeth samples, after
initial cleaning, were weighed and ashed in a
muffle at 500?600?C for about 1 day. The ash was
ground and blended to produce an homogenised
powder. Some samples were grouped in order to
obtain larger samples with enough ash quantity
for90Sr analysis.
2.3. Chemical treatment of the samples
For the purpose of the study reported here, a
new method of chemical treatment of samples
prior to
Nuclear Physics Laboratory NPL of the Univer-
sity of Ioannina. The chemical method is based
on the preferential chelation of90Y, the daughter
nucleus of90Sr disintegration. The chelating agent
is an organic solution of Bis 2-ethyl-hexyl hydro-
Ž
gen phosphate BEHHP
This is similar to a chemical separation method
used by the Los Alamos National Laboratory
Ž.
LANL, 1992 . The method also measures the
concentration of
the biological matrix.
The chemical method developed at the NPL is
presented in detail in Appendix A of this paper. It
involves the chemical extraction of all90Y which
at some recorded time T
90Sr in the original sample. The extracted
deposited on filter paper which is then subjected
to measurements of activity.
90Sr measurement was developed at the
Ž.
Ž.
.
diluted in dodecane.
89Sr which is often present in
is at equilibrium with
1
90Y is
2.4. Calculation of
90Sr concentration
Yttrium-90 concentration in the sample was
determined from the disintegration rate mea-
Fig. 5. Teeth samples distribution according to age and sex.

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182 170
sured in the filter, while
Ž
calculated in mBq?g Ca on the assumption that
90Y and90Sr are in equilibrium at time T of the
separation of the two isotopes and that the cal-
cium percentage of the bone or tooth ash is 40%
Ž
Bryant and Loutit, 1961; Glowiak et al., 1977 .
All samples used in this study were measured
using a Canberra 2404 ?-, ?-gas flow proportional
Ž
counter gas P10: Ar 90%-CH 10% for at least
3 times during a period of 7 days. These measure-
ments were necessary in order to follow
disintegration and assess whether
were present in the sample. The duration of each
measurement was typically 60 min. Background
was determined from periodic measurements of a
blank sample and averaged 0.69?0.10 cpm
Ž.
counts per minute .
Successive measurements
each sample were fitted to the function
90Sr concentration was
.
1
.
.
4
90Y
90Sr impurities
Ž.
three or more of
?Ž.4 Ž .
1Y?Y ?exp ?? T?T
01
in which:
Ž
Ž
Y ?
0
Yttrium disintegration rate at time T
.
h of Sr removal from the sample in
.
cpm ;
Ž
Net yttriumafter subtraction of the
.
background disintegration rate at time T
Ž.
in h , the mid-time for the time interval
of the measurement in cpm ; and
a constant equal to ln2?T
T
?64.1 h is the half-life of
1?2,Y
?1.
h.
in
1
90
Y ?
Ž.
? ?
where
90
Y in
1?2,Y
Ž
The90Y activity A , of the filter paper source
Y
was calculated using the expression
Y0
??
Ž .
2A ?
Y
Bq
60 C E
yY
in which:
E
?
90Y efficiency of the counter, which was
estimated as 0.26; and
Yttrium yield of the sample chemical
processing.
Y
C
?
Y
The
90Sr concentration of the sample is ex-
pressed in mBq?g Ca of the sample and is calcu-
lated using the expression
1000AY
0.4M
Ž .
3A ?
S
where
90
Ž
A
?
Sr activity of the sample, expressed in
.
mBq?g Ca ;
mass of the ashed sample in g ; and
constant for the calcium fraction in the
Ž.
ashed sample 40% .
S
Ž.
M ?
0.4 ?
3. Experimental results
3.1. Bone samples
Measurement of the mass of bone samples in
wet and ash form yielded an estimate of the
percentage of inorganic matter in each sample.
The percentage of inorganic matter did not show
statistically significant variations according to sex
Ž
and age confidence level?0.01 . However, sta-
tistically significant variations were evident with
regard to type of bone. Samples taken from the
sternumyielded 17 ? 6%
whereas ribs bones yielded 9?6%; femur epiph-
ysis and patellae showed much higher inorganic
matter content, measuring 28?7%.
Strontium-90 concentration in bone samples
did not show statistically significant variations with
regard to sex, age and residence of donor. The
mean concentration of
90Sr?g Ca. Fig. 6 shows90Sr bone concentrations
according to age. The number in each column
denotes the number of samples analysed per age
group, while error bars represent one standard
Ž
deviation see also Table 1 .
Statistically significant differences were found
in
bone sample measured. Patellae showed much
lower values of 16?7 mBq90Sr?g Ca in contrast
.
inorganicmatter,
90Sr was 30?13 mBq
.
90Sr concentration with regard to the type of

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182 171
Fig. 6.
for the samples in the group; error bars represent 1 S.D. Numbers in each column give the number of samples analysed per group.
90Sr concentration in bone samples according to age and sex. Each column represents the mean value of90Sr concentration
with rib, sternum and femur epiphysis samples,
where activity was almost double with a mean
90
value of about 31 mBq
. 2 .
Ž
Sr?g Ca see also Table
3.2. Tooth samples
Inorganic matter in tooth samples did not vary
statistically with sex and tooth category; the mean
value for all categories of teeth and for both sexes
was 71?4%. Inorganic matter in the roots of
teeth was found to be lower 64?3% for roots in
women and 62?2% for roots in men .
With regard to age, the inorganic matter of
Ž
.
teeth was found, in general, to decrease for both
sexes. Inorganic matter of deciduous teeth from
donors with ages up to 15 years was 79?3% for
male donors and 76?2% for female donors. In
contrast, inorganic matter in teeth from donors
with age 51?80 years was about 12% and 9%
lower, respectively for the two sexes.
In contrast to the results from bone samples,
90Sr concentration in teeth exhibited an interest-
ing variation with regard to age. Fig. 7 shows
radiostrontium concentration activities in teeth
from the various age groups up to 80 years. The
numbers in the columns denote the number of
samples analysed per group, while error bars rep-
Table 1
Radiostrontium concentration in male and female bone samples
a
Age
Ž
years
MaleFemale
.
90 90
Ž.Ž.
mBqSr?g Ca NmBqSr?g CaN
15?29
30?39
40?49
50?59
60?69
70?79
80?89
90?99
18?8
29?17
31?13
32?13
29?8
26?11
33?18
29?7
2
5
7
45?5
11?1
20?3
30?3
29?12
28?15
36?12
44?23
2
1
4
312
9
15
18
12
6
4
6
3
aMean values of each group with the respective 1 S.D. and the number N of samples analysed per group, are presented

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182172
Table 2
Radiostrontium concentration in bone samples according to
a
type of bone
90
Ž
mBq
Kind of boneSr concentration
90
Sr?g Ca
N
.
Patella
Rib
Sternum
Sternum and rib
Femoral heads
16?7
29?10
33?16
31?11
30?12
7
35
40
11
17
aMean values with the respective S.D. and the number N
of samples analysed per group are presented
Ž.
resent one standard deviation see also Table 3 .
The data in this figure show an increase of
concentration in teeth from 24?4 mBq
Ca at birth to 51?6 mBq90Sr?g Ca at the age of
20 years. For ages 21?40 years,
tions increased further from 19?8 mBq
Ca to 64?21 mBq
decreased steadily to 4?1 mBq
the 71?80 age group.
Similar, butnot as sharp variations, are
observed in female teeth. There is an increase
from 26?13 mBq
90Sr?g Ca for ages up to 20 years and a further
90Sr
90Sr?g
90Sr concentra-
90Sr?g
90Sr?g Ca; thereafter levels
90Sr?g Ca for
90Sr?g Ca to 32?27 mBq
increase from 24?9 mBq90Sr?g Ca to 48?24
mBq90Sr?g Ca up to 40 years. After the age of
40 years,
to 6?1 mBq90Sr?g Ca for the 71?80 age group.
Statistically significant differences were observed
between different age groups of the same sex, but
not between the sexes of the same age group see
.
also Table 3 . There were no statistically signifi-
cant differences between the different types of
teeth for the same age group for either male or
.
female .
90Sr concentrations decreased steadily
Ž
Ž
4. Modelling of
bones
90Sr concentration in human
The rate of uptake and removal of a radionu-
clide by the body can vary significantly with age.
This is well documented in the case of90Sr, which
has been measured in a large number of human
skeletons. The large quantity of data collected for
90Sr concentration in bones has been used in the
development of several age-dependent models.
Ž.
Leggett et al. 1982 proposed a metabolic model
that applies from birth through to adulthood.
This model utilises compartments which corre-
Fig. 7.
for the samples in the group; error bars represent 1 S.D. Numbers in each column give the number of samples analysed per group.
90Sr concentration in teeth samples according to age and sex. Each column represents the mean value of90Sr concentration

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182173
Table 3
Mean values of
90a
Sr concentration in tooth samples for each age and sex group
Age
Ž
years
MaleFemale
.
9090
Ž.Ž.
mBqSr?g CaN mBq Sr?g CaN
0?10
11?15
16?20
21?25
26?30
31?40
41?50
51?60
61?70
71?80
24?4
33?5
51?6
19?8
32?10
64?21
35?13
30?12
9?6
4?1
1
6
3
4
3
26?13
29?5
32?27
24?9
29?17
48?24
39?11
17?7
8?2
6?1
4
5
2
4
4
7
6
12
7
11
11
1
16
8
1
aOne standard deviation and the number N of samples analysed per group are also presented.
spond to physical processes or subsections of the
skeleton and examines the behaviour of
terms of the behaviour of calcium. Retaining cer-
tain features of this model, a new age-dependent
model was developed at the NPL.
90Sr in
4.1. Skeletal Compartments
Bone is often divided into two categories, struc-
tural bone which refers to the mechanical func-
tion of the skeleton and metabolic bone which
refers to the function of the skeleton in the
regulation of extracellular calcium levels. Based
on these two categories, the skeleton may be
viewed as consisting of three compartments, with
two compartments associated with structural bone
Ž
cancellous and compact bone and the third as-
sociated with metabolic bone
Cancellous and compact bones are differentiated
in terms of their surface to volume ratio. Surface
to volume ratios may vary significantly within
bone types and the distinction between the two
categories may not be readily evident at some
points in the skeleton and at some stages of
Ž
development Leggett et al., 1982 . Thus the clas-
sification of bone as cancellous or compact repre-
sents a simplification introduced for the purposes
of the model.
.
Ž.
bone surface .
.
4.2.90Sr kinetics in the skeletal compartments
Ž
For an individual born at time Tcalendar
.Ž .
90
year , the amount Q t
compartment at age t is described by the differ-
ential equation
of Sr in a skeletal
Ž .
dt
dQ t
Ž . Ž . Ž. Ž .Ž .
?A t B t F T?t ?L t X t
Ž .Ž .
4
??Q t
in which
Ž .
?
A t is the annual amount of calcium intake
Ž
as a function of age t g Ca y
Ž .
B t is the percentage of
food which is taken up by the skeletal com-
partment as a function of age t,
Ž.
F T?tis the mean
food during calendar year t?T Bq?g Ca ,
Ž .
L t is the annual rate of bone turnover which
is assumed to be equal to the annual removal
90
rate of Sr from the bones kg y
depends on the type of bone involved in the
exchange process described by Eq. 4
Ž .
Q t
Ž .
X t ?
is the concentration of
Ž .
M t
Ž.
Bq?kg in the skeletal; compartment of total
Ž .
mass M t ; and
? is the radiological decay constant of
Ž?1.
y.
?1.
Sr contained in
,
90
?
90
?
Sr concentration in
Ž.
?
Ž
?1. Ž .
; L t
Ž ..
90
?
Sr
?
90Sr
Ž .
The integration of Eq. 4 requires knowledge
Ž .Ž .
of the functions A t ,B t , F T , L t and M t .
With the exception of the level of
Ž .Ž .
90Sr contami-
Ž .

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182174
Ž .
nation in food F T which is a function of calen-
dar year T and depends on geographical location,
the rest of the functions are derived from physio-
logical considerations and data. Information on
these functions and analytic expressions in the
form of semi-empirical formulas are given in Ap-
pendix B.
There is scant data concerning radiostrontium
contamination of foodstuffs during the past 40
years in Greece. Some information is provided by
measurementsofmilk
1962?1971 and 1986?1994 and for total ? radia-
tionfalloutin Greece
1961?1983, performed by the Greek Atomic En-
ergy Commission. In reducing these data, the
value 0.24% proposed by Bakacs-Polgar Bakacs-
Polgar and Kurcs-Csiky, 1964 was adopted as the
percentage of
ratio of
Ž
taken as 1.5 Leggett et al., 1982 . The function
Ž .
F T obtained in this fashion, albeit with con-
siderable uncertainty, is plotted in Fig. 10 dashed
.
line . The two large excursions in this function
correspond to the period of intensive atmospheric
nuclear weapons testing
Ž
Chernobyl accident 1986 .
duringthe periods
duringthe period
Ž
.
90Sr in the total ? fallout. The
90Sr in all foodstuffs to that in milk was
.
Ž
Ž.
1963?1965and the
.
4.3. Model estimates of
compartments
90Sr le?els in skeletal
Predictions of the NPL model were compared
to the measurements obtained in the study pre-
sented here. For this purpose the data for both
sexes were averaged within the corresponding age
groups. Parameters for cancellous bone were used
in the case of bone samples and for compact bone
in the case of teeth. The predictions of the model,
by employing the response functions proposed
Ž.
see Appendix B by Leggett et al. 1982 are
contained in Figs. 8 and 9.
Although a straightforward application of the
model gave a satisfactory reproduction of the
overall trend observed in the data of Figs. 6 and
7, it was realised that considerable improvement
could be obtained by removing some of the un-
certainties associated with the response functions
Ž .
in Eq. 4 .
As already noted, the major uncertainties in
the model arise from:
Ž.
1.Incomplete knowledge of the levels of
foodstuffs in Greece during the past four
?
Ž .?
decades function F T .
90Sr in
Fig. 8. Mean age-group values of
experimental data, grey bars predictions of the model by using the response function suggested by Leggett et al. 1982 and dark
bars predictions obtained by using reassessed values of the parameters of response functions cancellous bone turnover rates and
90
.
Sr concentration in food in Greece .
90Sr concentration in bone samples and predictions of the NPL model. White bars represent
Ž.
Ž

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182175
Fig. 9. Mean age-group values of
experimental data, grey bars predictions of the model by using the response function suggested by Leggett et al. 1982 and dark
bars predictions obtained by using reassessed values of the parameters of response functions teeth turnover rates and
.
concentration in food in Greece .
90Sr concentration in teeth samples and predictions of the NPL model. White bars represent
Ž.
Ž
90
Sr
2. Incomplete
?
function L t , in particular for teeth for
which, in the absence of specific data, com-
pact bone parameters were used.
knowledge
Ž .?
ofturnover rates
It was thus decided to allow some of the
parameters of the corresponding response func-
tions to vary within their range of uncertainty, so
as to obtain the best values through a fitting
process against the data for
Some of the parameters of function L t
cancellous bone were also allowed to vary. The
fitting was performed with a modified version of
Ž
code MINUIT James and Ross, 1975 with the
results presented in Figs. 8 and 9. Details with
regard to modifications of the response functions
are given in Appendix B. Predictions of the model
with the adjusted response functions appear to
reproduce the data very well.
Adopting a different point of view, we may
consider the adjustment of the response functions
through the fitting of bone and teeth contamina-
tion data as constituting an indirect measurement
of these functions. Clearly, a response function
90Sr concentration.
Ž .
for
.
that yields a better fit to experimental data should
reflect more accurately the behaviour of the ef-
fect it represents.
Ž .
The functions F t and L t , as determined
from the fitting process, are contained in Figs.
10?12. The main modification arising from the
fitting process with regard to function F t seems
to be the adjustment of the relative impact of the
Chernobyl accident in comparison with that of
the atmospheric nuclear weapons tests period. As
seen in Fig. 10, the effect of the latter on the
contamination of foodstuffs was more intense and
lasted longer. Reassessed values of the turnover
response function for cancellous bone, although
they do not show any drastic change in structure,
are predicted to be much higher than the ones
used in the original calculations, especially for
adults over 45 years of age see Fig. 11 . There is
a dramatic difference between reassessed and
original values of function L t for compact teeth,
which are represented in a logarithmic scale in
Fig. 12. The very high excursion at around age 8
years, introduced by the fitting process, corre-
sponds to the formation of permanent teeth.
Ž .
Ž .
Ž.
Ž .

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()
K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182176
90
Ž.
Fig. 10. Mean annual values of
and assessed values derived by fitting model predictions to measurements of bone and teeth samples solid line . The heavier line
extending to 1970 represents values of90Sr concentration in foodstuffs in the UK.
Sr concentration in food in Greece for the period 1953?1994 dashed line; K. Stamoulis, 1998
Ž.
5. Discussion and conclusions
The human skeleton carries with it the history
of radiostrontium environmental contamination
during the period that the individual was alive. As
shown by the data in Fig. 1, any increase in90Sr
in the environment affects within a very short
period the younger age groups which in their
formative years accumulate calcium in their bones
at high rates. Once acquired, the concomitant
high concentration of radiostrontium, due to the
slow turnover rates of calcium later in life, re-
mains in the skeleton and as time passes is re-
flected in higher age groups. The effect is more
pronounced for compact bone, which after the
age of 10 years has a turnover rate of less than
0.2%, as compared to cancellous bone with a
turnover rate which, although it falls rapidly after
infancy, remains at a level of 10?20% throughout
adulthood. Thus, a more pronounced record of
past environmental radiostrontium contamination
is expected from measurements of
90Sr concen-
trations in teeth, which are primarily composed of
compact bone tissue.
Human bone samples from Greece measured
in this study yielded an average of about 30 mBq
90Sr?g Ca, with no pronounced structure as a
function of age. Since the samples considered
here were primarily composed of cancellous bone,
it is surmised in view of the above discussion that
any effects of the high90Sr contamination period
of the 1960s, which should affect the 35?50 age
groups, have been already washed out. Average
levels of
Greece for all ages have now been reduced to
pre-1960s levels.
Contrary to the results obtained from bones,
data from human teeth show a very interesting
structure. In the Ukrainian results presented in
Fig. 3, the data, obtained 5 years after the Cher-
nobyl accident, contain three prominent peaks
with centroids at the ages of 5.0?0.2, 14.2?0.4
and 35.4?0.5 years. The first two correspond to
children who were born or were shedding their
90Sr concentration in human bones in

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182 177
Ž.
Fig. 11. Cancellous bone turnover rates dashed line and response function derived by fitting model predictions to measurements
of bone samples.
deciduous teeth at the time of the Chernobyl
accident. The third broader peak corresponds to
individuals who were growing up during the pe-
riod of the atmospheric nuclear weapons tests
during the 1960s. In the Greek data which were
collected about 3 years later and are presented in
Fig. 9, the first peak observed in the Ukrainian
Ž
is missing. However, the later two peaks,
with centroids at the age of 17.5?0.4 and 38.5?
1.2 years are evident. This shift of about 3.5 years
coincides with the time elapsed between the col-
lection of the two sets of data.
As seen in Figs. 8 and 9, the model developed
data expected in the age group 0?10 years of
.
age
Ž.
Fig. 12. Compact bone turnover rates dashed line and response function derived by fitting model predictions to measurements of
teeth samples.

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182178
at the NPL was successful in reproducing
concentration measurements in bone and teeth.
In addition, through a fitting process, application
of the model yielded estimates of calcium turnover
rates in teeth and an estimate for radiostrontium
contamination of foodstuffs in Greece for the
past 40 years.
The results reported here clearly indicate that
the contaminating effects of the atmospheric nu-
clear weapons testing in the 1960s exceed by far
those of the Chernobyl accident. From both Figs.
3 and 9, it is apparent that the contamination
from Chernobyl, which at present affects the
teenage population, is considerably less than that
still remaining in the middle-aged individuals from
the 1960s. This is corroborated by the findings
presented in Fig. 10, which demonstrate that con-
tamination of foodstuffs in the 1960s far exceeded
that caused by the Chernobyl accident both in
intensity and duration.
90Sr
Appendix A: The NPL method for chemical
treatment of bone and teeth samples
Bone and tooth samples were treated chemi-
cally prior to radiostrontium concentration mea-
surement according to the following method.
A pre-weighed quantity of bone or tooth ash
Ž.
4.0?10.0 g was placed in a 150-ml glass beaker
and a 2 M hydrochloric acid solution was added
Ž.
40?100 ml . Using magnetic stirring the ash was
diluted completely and 1.0 ml of Y3?carrier was
added to the solution. By adding a small quantity
of hydrochloric acid solution 2 M or ammonia
Ž.
solution 25% w?v the pH was adjusted to about
pH?
1. The volume of the solution was recorded
and the solution was transferred into a separating
Ž.
funnel 125 ml or more . Solution of BEHHP in
Ž.
dodecane, 5% v?v , in the amount of one-quarter
of the previously recorded volume, was added to
the separation funnel and the mixture was shaken
vigorously for about 3 min. Time T
separationfrom the inorganic
recorded for subsequent calculation of the
disintegration. The organic and aqueous phases
were allowed to separate for about 30 min.
Ž.
of yttrium
solution
1
was
90Y
Ž.
The aqueous lower phase was discarded and
25 ml of 6 M nitric acid solution was added to the
Ž.
organic upper phase. The separating funnel was
shaken vigorously for about 3 min and the phases
were allowed to separate for 30 min. Subse-
quently, the aqueous phase was transferred to a
50-ml centrifuge tube. The procedure was re-
peated and the aqueous phase was transferred to
yet another centrifuge tube.
A quantity of 25 ml ammonia solution 25%
.
w?v was added to the centrifuge tubes in which,
after stirring, yttrium hydroxide gel formed. The
centrifuge tubes were allowed to cool at room
temperature and were
3500 rev.?min for about 5 min. The supernate
was discarded and 5 ml of 2 M hydrochloric
solution were added under stirring to the precipi-
tate of yttrium hydroxide. Distilled water in the
amount of 20 ml was added to the solution of
each centrifuge tube and the pH was adjusted to
about 1.7?1.8 with hydrochloric acid or ammonia
solution.
The centrifuge tubes were placed in a water
bath at 90?C for about 30 min and 5 ml of
saturated solution of oxalic acid was added to
each tube under stirring. White precipitate of
yttrium oxalate was thus formed. A filter paper
Ž.
Whatman No. 42 was weighed and placed in a
vacuum filtering apparatus. Solutions with the
precipitates were allowed to cool at room temper-
ature and were filtered trough the filter paper. A
few ml of distilled water was added to the cen-
trifuge tubes and was also filtered through the
same paper.
The filter paper was dried in an oven at 80?C
for about 20 min and allowed to cool at room
temperature. The filter was weighed and yttrium
yield was calculated from the yttrium oxalate in
?Ž. ?
the form of COOY ?9H O
2 3
The filter was then transferred to the ?-counter
apparatus and measured for activity.
Ž
centrifugedat
Ž
.
on the filter.
22
Appendix B: Physiological semi-empirical
formulas employed by the NPL model
The physiological response functions needed in

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K.C. Stamoulis et al.?The Science of the Total En?ironment 229 1999 165?182 179
the evaluation of the basic model equation Eq.
Ž . 4 were derived from data in the scientific litera-
ture.
Annual
was initially estimated using available data on
total ? fallout, and scatter data on90Sr concen-
tration in milk during the period 1961?1971 and
1986?1993. Estimates were calculated by fitting
data on total ? fallout and milk
tion with the UNSCEAR model Lassey, 1979 ,
which predicts milk
fallout data. The percentage of
fallout was taken as 0.24%, which was calculated
from data in total ? activity and90Sr concentra-
tion in soils given by Bakacs-Polgar
Polgar and Kurcs-Csiky, 1964 . The function F T
derived in this way is given by
90Sr concentration in food in Greece
90Sr concentra-
Ž.
90Sr concentration from90Sr
90Sr in total ?
Ž
Bakacs-
. Ž .
Ž .
F T ?
?
?f T?1952 ?f
5
?
f exp ?f T?1962
7
?f exp ?f
9
?
11
2
?
?
?
?
Ž.??
Ž. ?
f exp f T?1952 ?f exp ?f T?1959
12
Ž.
6
?
Ž.?
8
?
Ž
T?1962
10
?
Ž
f exp ?fT?1985 ?f
12
34
1953?T?1963
.?
1963?T?1986
1986?T?1995
.?
13
Table 4
Values of the parameters of the function of annual
concentration in food in Greece F T
90
Sr
a
( )
Parameters Initial values Reassessed
values
?5
?5
f
f
f
f
f
f
f
f
f
f
f
f
f
2.21?10
1.57
171
0.95
21.2
11.2
1370
0.92
418
0.06
2846
0.8
112
1.14?10
1.60
191
1.16
22.3
17.7
1316
1.93
814
0.12
1331
0.54
98.7
1
2
3
4
5
6
7
8
9
10
11
12
13
aThe second column contains values derived from the
Ž .
initial estimate of function F T , while in the third column
contains reassessed values of the parameters obtained by
fitting the model to experimental data.
where T is the calendar year. Values of the
parameters f , k?1,2,...,13 are given in the sec-
k
ond column of Table 4. In the third column of the
same table the reassessed values of the parame-
ters derived by fitting model to the experimental
data of
also shown.
Bone and teeth turnover rates were reassessed
also by fitting the model to respective
centrations. The fitting was performed indepen-
dently using the initial estimates for
presented in the second column of Table 5.
According to Leggett et al.
turnover rate as a function of age t is given by the
function
?
0?t?1.5
Ž .
C t
?
L t ?
l t?l 35?t?44
45
?l 44?t
6
90Sr concentration in bones and teeth are
90Sr con-
90Sr intake
Ž.
1982 , bone
l
1
Ž.
l exp ?l t
2
1.5?t?35
Ž .
3
Ž .
where C t is the total amount of calcium in the
skeleton at age t. Values of the parameters lk
k?1,2,...,6 are given in the second and third
column of Table 5. These values were used by our
model to predict
cancellous bone respectively. In the fourth column
of the same table the reassessed values for the
parameters used for cancellous bone are pre-
sented, derived by fitting the model to the
concentration measurements for cancellous bone.
In order to obtain better agreement for the
90Sr concentration in teeth a different function
was used in this case
90Sr concentration in teeth and
90Sr
Ž .
t ?l exp ?l t ?l exp
t1
??
L
teetht2t3
2
Ž.
?lt?l
?l
t4t5t6
in which t is the age of the donor. The use of the
gaussian factor in the proposed function is based
on the fact that deciduous teeth fall-out during
the period 6?10 years of age, with a maximum
occurring at the age of 8 years. During this pe-
riod, turnover rate increases rapidly and takes
values of the same order as during the calcifica-