Science of the Total Environment 367 (2006) 596 – 605
www.elsevier.com/locate/scitotenv

90

Sr in deciduous teeth from 1950 to 2002: The Swiss experience
P. Froidevaux ⁎, Jean-Jacques Geering, J.-F. Valley
Institute of Applied Radiophysics, University of Lausanne, Grand Pré 1, CH-1007 Lausanne, Switzerland
Received 1 February 2006; accepted 1 February 2006
Available online 20 March 2006

Abstract
Switzerland has recorded the level of activity of 90Sr in the milk teeth of children from different regions of the country since thefirst atomic explosions in the atmosphere. Activity peaked at 0.421 Bq g− 1 Ca at the beginning of the sixties, coinciding with thedetonation of many large nuclear devices. Following the Nuclear Test Ban Treaty that ended atmospheric nuclear weapon tests, asteady and significant decrease in 90Sr activity in milk teeth has been observed—down to a value of 0.03 Bq g− 1 Ca for children
born in 1994. The apparent half-life of 90Sr in milk teeth is 9.8 ± 3 years. With the exception of the period from 1962 to 1964, there
is no correlation between the activity in the teeth of children born in a given year and the year of extraction. Between 1953 and1992, the milk teeth of children born in Zürich county showed 16% less activity than teeth from children born in Vaud county.
Dairy consumption habits might be responsible for this trend. The effect of the 90Sr deposition from Chernobyl is barely
measurable in milk teeth, and no effect is seen from the five Swiss nuclear reactors. This paper emphasizes the necessity of a very
high purity chemical separation of 90Sr or 90Y to determine 90Sr activity in milk teeth or other samples.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Strontium-90; Deciduous teeth; Nuclear bomb tests; Chernobyl; Nuclear power plant

1. Introduction90

Sr is an artificial radionuclide produced by nuclear
fission during the explosion of a nuclear device and innuclear energy plants (Stamoulis et al., 1999). In Switzerland, environmental 90Sr comes from atmospheric nuclear
tests performed in the sixties, and more recently from the
Chernobyl accident. It has been estimated that about
1018 Bq of 90Sr was released in the atmosphere from 1945
to 1965 and subsequently deposited on the earth and in theoceans (Christensen et al., 1975). Hardy et al. (1973)
studied the deposition of plutonium from nuclear weapon⁎ Corresponding author. Tel.: +41 21 623 34 80; fax: +41 21 623 34
35.
E-mail address: pascal.froidevaux@inst.hospvd.ch(P. Froidevaux).
0048-9697/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2006.02.011

tests. They reported that the region from 40–50°N was themost heavily contaminated, and that the Arctic region (80–90°N) was the least contaminated, with activities of around
80 Bq m− 2 and 8.0 Bq m− 2 respectively. Apostoaei (2002)
studied the absorption of strontium from the gastrointestinal tract to the plasma in human adults and found that thefraction of strontium transferred to the plasma (f1) depends
on dietary calcium intake. There is a high variability in f1
between individuals, but no significant dependence on age
or sex. As an alkaline earth cation, 90Sr follows calcium inthe food chain–in particular in dairy products–before
being deposited in the skeleton and other calcified tissues(Leggett et al., 1982). Teeth are an extension of theskeleton and accumulate contaminant stable andradioactive bone-seeking metals that enter the body.
The 90Sr activity in deciduous teeth (milk teeth) reflects theactivity in food at around the time of the child's birth and inP. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605

the mother's diet during pregnancy (Webb et al., 2005).
Attention has been focused on 90Sr for several decades
because it is believed to be the most potentially hazardousof the long-lived fission products that had started toaccumulate as a result of nuclear weapon tests.
The level of 90Sr in bones and teeth has beenmonitored since the beginning of nuclear weapon tests.
There were two peaks in the concentration of 90Sr versus
year of birth (milk teeth) or death (bone) in 1958 and
1965, followed by an exponential decrease after theentry into force of the Nuclear Test Ban Treaty(Aarkrog, 1971; Hanson and Thomas, 1982; Stamoulis
et al., 1999). Recently Mangano et al. (2003) reported
on an unexpected rise during the 1990s in 90Sr in milk
teeth from children in the United States. They attributethe increase to nuclear power reactors.
In Switzerland, a monitoring program of 90Sr in milk
teeth and vertebrae was initiated by the Federal Office of
Public Health in the late fifties. Since this time, milk
teeth have been collected annually from three regions of
Switzerland. Of all the European countries, Switzerland
was one of the most contaminated by global fallout due
to the geomorphology of the country (Froidevaux et al.,2004). Plutonium deposition can reach 300 Bq m− 2, and90
Sr 3500 Bq m− 2. The Chernobyl accident added
numerous short and long-lived radionuclides, of which
only 137Cs is still measurable in the Swiss environment.
In the Italian-speaking part of Switzerland (south of theAlps), 137Cs deposition from Chernobyl is as high as
60 000Bq m− 2 in small areas. Since the beginning of theseventies there has also been a mere potential contribution from nuclear power plants. Switzerland has fivereactors producing a total of 3350 MWe.
In this paper we report the results of 90Sr measurements made on milk teeth extracted in Switzerland from1963 to 2002. We describe briefly the method used until
1971 and in more details the one used from 1972 until
now, which permit the determination of strontium
activity at very low levels by means of complex butvery robust protocols. Our results are compared with theresults of Mangano et al. (2003) and other authors(Kulev et al., 1994; O'Donnell et al., 1997; Stamoulis etal., 1999). Differences in between our method and themethod of Mangano et al., and the possible impact ofthese differences on our results are discussed.
2. Method
2.1. Reagents and equipment
All reagents used were analytical grade (Merck,
Darmstadt, Germany or Fluka, Buchs, Switzerland).

597

Chromatographic separations were carried out on a BioRad AG 50W-x8 (100–200 mesh) cationic exchanger.
Solutions were loaded on to the chromatographic
columns (50 ml, 8 ml respectively) by a peristaltic
pump (Ismatec IPS-12) with automatic control of thedelivered volume, elution rate and the end of elution(bubble detector). Yttrium oxalate sources were counted
on a Tennelec LB 4100 low background proportionalcounter. Background was 0.004 cps (counts per second).
The source was typically measured for 100 h withintermediate results recorded automatically every 4 h tocheck the purity of 90Y. Using this method, a detection
limit of 5·10− 3 Bq/g Ca can be achieved. Yttrium yield
was determined by atomic absorption on the dissolved
sources with a Perkin Elmer 4100 apparatus, using a
N2O/acethylene flame.
2.2. Sampling
From 1963 to 2002, milk teeth were collectedannually by dentists in three regions of Switzerland.
The first region (ZH) includes the county of Zürich anda large part of the Swiss German lowland. The Gösgen,
Beznau and Leibstadt nuclear power plants are in thisregion. The second region is the French-speaking part of
Switzerland, mainly the Vaud county (VD). There is apotential influence from the Mühleberg nuclear power
plant in this region. The third region is the Italianspeaking part of Switzerland (TI), which is separated
from the Swiss nuclear power plants by the Alps.
Each tooth was sent to our laboratory in a plastic baglabeled with the place and date of birth of the child, andthe place and date of extraction of the tooth. Only teeth
from children born in the specified area (ZH, VD, TI)
were used. It was assumed that the mother lived in thearea during the pregnancy.
2.2.1. 90Sr measurements
Method used until 1971: After dissolution of the ash
in hydrochloric acid, Sr carrier was added, then thealkaline earth were separated as oxalate, heated at 600°
to destroy oxalate. After dissolution of the alkaline
earth in nitric acid, strontium was specifically separated
as nitrate by two precipitations with fuming nitric acid.
Strontium was further purified by washing with ethanol
followed by iron scavenging. After a partial ingrowthof 90Y, this radionuclide was separated by two successive precipitations as hydroxide, then as oxalate(Lerch et al., 1965). After filtration, the yttrium oxalate
precipitate was measured using in-house built low
background Geiger counter described by Lerch andBercier (1964).

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P. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605

Method used from 1972 to 2004: A minimum of 5teeth from the same region and year of birth were used
for each measurement. If necessary, fillings were
removed mechanically by crushing the tooth in a mortar.
The samples were ashed by heating at 600 °C for 24 h tooxidize the organic matter. Then 5 ml of 0.2 M Sr carrier
solution was added and the ashes were dissolved in 8 M
nitric acid. After dilution to 250 ml and filtration (ifnecessary), an aliquot (3 ml) was taken for calcium
determination by atomic absorption. Then 4 M ammonium carbamate was added until the pH of the solution
reached 8–9. After centrifuging, the carbonate precipitate was dissolved in 8 M nitric acid. The solution was
diluted to 500 ml and 125 ml of 0.5 M EDTA was added.
The pH of the solution was carefully adjusted to 4.6 andthe solution was pumped onto the cationic exchanger(AG 50W-x8, 50 ml). Ca and Mg were eluted from thecolumn with 0.09 M CyDTA (trans-1,2-cyclohexylenedinitrilo tetraacetic acid) (pH 5.5). Strontium was eluted
with 300 ml of 0.075 M CyDTA (pH 6.5). The solution
was adjusted to pH 4.2 and pumped onto the cationicexchanger (AG 50W-x8, 8 ml). The column was thenwashed with 80 ml of water. Sr was eluted into a flask
containing 5 ml of a 0.0225 M Y carrier with 100 ml of
0.2 M sodium citrate (pH 7.5). This solution was left in
the refrigerator for at least 12 days until the equilibrium
between 90Sr and its daughter product, 90Y, was partiallyreached. The solution was adjusted to pH 2 and thenpumped onto the 8 ml column of the cationic exchanger(AG 50W-x8). The column was washed with 0.75 M
NaCl until the pH of the effluent reached 4. Yttrium waseluted with 100 ml of a 0.25 M sodium malonate
solution. When half of the solution had passed throughthe column, the time was recorded to permit a correction
for the decrease in 90Y. Strontium was eluted with 125 mlof a 4 M NaCl solution for determination of the strontium
chemical yield by atomic absorption. Yttrium oxalate
was precipitated from the malonate solution by adding
oxalic acid, filtered on a Millipore GSWOP 02400 filter,
and then counted in a low background proportional gas
counter (Tennelec LB 4100). Counting efficiency,
enhanced by backscattering, was 50.0 ± 0.5%. Aftercounting, the yttrium source was dissolved in hydrochloric acid and the chemical yield of yttrium determinedby atomic absorption (Perkin Elmer 4100). Using thismethod, the detection limit is 5 mBq g− 1 Ca.
The method is described in detail by Geering et al.
(1990). Unfortunately, no interlaboratories comparison
samples were available to assess the quality of theanalytical method for the determination of 90Sr in milk
teeth. However, many interlaboratory comparisons and
IAEA proficiency tests have been done for quality

assurance of the same method for 90Sr measurements onother materials: 90 Sr in urine (average bias 3%,
PROCORAD 2000, France), 90 Sr in soil samples(average bias 7.5%, IAEA ALMERA proficiency test,
2001, Austria), 90Sr in a mineral matrix (average bias
8%, IAEA proficiency test, 1999), 90 Sr in water(average bias 5%, Bundesamt für Strahlenschutz, Ringversuch 1/1998, Germany), 90Sr in water (average bias
3%, Bundesamt für Strahlenschutz, Ringversuch 1/
2000, Germany), 90Sr in milk powder (average bias 3%,
IAEA-152, 1988, Austria), 90 Sr in whey powder(average bias 3%, IAEA-154, 1988, Austria). Results
show that the method is perfectly designed for the 90Sr
determination in various kinds of samples, even withcomplex matrices.
3. Results
In this study, activities are calculated at, and results
are presented as a function of the year of birth. However,milk teeth from children born during the same year canbe extracted at different ages. Therefore it is possible
that, in the case of an abrupt increase in the level of 90Srin the food chain, the milk teeth of children born at thetime of the event but extracted at different ages will havedifferent 90Sr activities due to the continuous exchangeof calcium between the blood plasma and the tooth rootzone (Shishkina et al., 2001). Thus milk teeth extracted
from older children might have a lower 90Sr content
when contamination in the food chain is decreasing, anda higher content when it is increasing. This was checkedusing the data collected in Vaud county since 1963. For
each year of birth, milk teeth extracted in at least fivedifferent years were collected. Table 1 shows the resultsof a statistical analysis of at least 10 (but usually 20 to30) activity determinations for each extraction period. A
t-test on the data gives the parameter P, which represents
the probability that the correlation between the measured activity in a given birth year and the year of
extraction is due to random chance. Fig. 1 shows that theprobability P is less than 5% only for the years 1962–
1964, when activities peaked at their highest values andthere were strong variations in activity over shortperiods of time. For the other periods, P is too high toconclude that the extraction year has an effect on the90
Sr activity of a given birth year. When the contamination level of the food chain does not change
significantly, there is no significant difference between
teeth from the same year of birth that have been
extracted in different years. For example, the reduced
centered variables (x − xm / σ) for the year of birth 1983
and the period of extraction [1992–2000] are within the

P. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605
Table 1
Probability that the correlation observed between the 90Sr activity ofteeth for a given year of birth and the year of extraction is due torandom chance, calculated as a Student's law (t)Year of birthYears ofextraction

N

t

P

Slope

1955–1956
1956–1957
1958–1959
1960
1961
1962
1963
1964
1965
1966–1967
1967–1968
1978–1979
1980–1981
1982–1983
1984–1985
1986–1987
1988–1990

1964–1968
1964–19691966–1971
1966–1973
1968–1975
1969–1975
1971–1976
1969–1976
1970–1976
1972–1976
1972–1976
1988–1991
1988–1991
1988–1999
1993–2000
1996–2000
1997–2001

29
40
24
29
29
30
33
21
18
17
10
7
11
12
10
11
10

0.473
0.042
0.409
− 0.529
2.867
3.933
4.989
2.938
3.121
1.893
0.419
0.050
0.447
1.424
1.665
0.873
1.703

0.650
0.967
0.69
0.61
0.017
0.00340.00110.01480.0168
0.088
0.685
0.962
0.66
0.1778
0.130
0.401
0.120

− 0.001
0.0002− 0.0010− 0.0016
0.01670.03370.06430.01400.01200.015220.0027− 0.0003− 0.00092− 0.00092− 0.00128− 0.00146
0.00203

N is the number of measurements.

1

0.08

0.8

0.06

0.6

0.04

0.4

0.02

0.2

0

0

1955-1956
1956-1957
1958-1959
1960
1961
1962
1963
1964
1965
1966-1967
1967-1968
1978-1979
1980-1981
1982-1983
1984-1985
1986-1987
1988-1990

slope

Probability

intervals [− 1.3; 1.3] for Zürich county, [− 1.2; 0.13] for
the French-speaking part of Switzerland and [− 1.5; 1.3]
for Tessin county. No outlier was detected, which meansthat within ± 2σ, the distribution is not changing
significantly. Table 1 and Fig. 1 show that the slope of90
Sr activity for a given year of birth as a function ofdifferent years of extraction is only significantly
different from zero for the corresponding low probabilities P. Also, the slopes are shallow, indicating that the-0.02

year of birthFig. 1. Probability (striped bars) that the correlation between the 90Sr
activity of milk teeth for a given year of birth and different years of
extraction is due to random chance, calculated as a Student's law andcorresponding slopes (white bars).

599

accumulation of 90Sr in milk teeth during childhood islow. This means that milk teeth from different collection
years can be pooled to give a larger sample size withmore statistically significant measurement results foreach birth year. Table 2 and Fig. 2 show the results forthe three regions. There is a peak in 90Sr activity in milk
teeth in 1964 and a sharp decline from then until now. A
shoulder associated with the main peak corresponds tothe years 1958–1959, when the United States and theSoviet Union suspended atmospheric nuclear weapon
tests. The sharp increase in 90Sr activity in milk teeth at
the beginning of the sixties is the consequence of theTable 2
Sr activity (Bq g− 1 Ca) in milk teeth collected in three different
regions of Switzerland as a function of the year of birth90Year of
birth
1951
1952
1953
1954
1955
1956
1957
1958
1959
1960
1961
1962
1963
1964
1965
1966
1967
1968
1969
1977
1978
1979
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1996

Vaud county
N

−1

Bq g

Tessin county
Ca

5
13
11
18
22
24
23
32
27
30
33
21
18
9
6
3
1

0.059 ± 0.003
0.089 ± 0.010
0.109 ± 0.010
0.116 ± 0.007
0.146 ± 0.010
0.161 ± 0.012
0.158 ± 0.012
0.155 ± 0.010
0.177 ± 0.009
0.279 ± 0.009
0.421 ± 0.015
0.388 ± 0.014
0.294 ± 0.011
0.238 ± 0.024
0.181 ± 0.013
0.166 ± 0.017
0.138 ± 0.005

2
3
5
6
8
5
5
4
7
5
5
3
3
2

0.077 ± 0.010
0.064 ± 0.008
0.069 ± 0.008
0.054 ± 0.003
0.044 ± 0.003
0.039 ± 0.004
0.043 ± 0.002
0.037 ± 0.002
0.043 ± 0.006
0.031 ± 0.003
0.037 ± 0.003
0.035 ± 0.003
0.029 ± 0.003
0.028 ± 0.003

10.017 ± 0.003

20.025 ± 0.003

N

−1

Bq g

Ca

2
1
4
6
5
5
3
2

0.138 ± 0.02
0.184 ± 0.012
0.208 ± 0.005
0.357 ± 0.007
0.324 ± 0.002
0.270 ± 0.005
0.227 ± 0.004
0.202 ± 0.007

2
4
4
6
5
4
8
5
6
6
4
3
1
1
2
2

0.066 ± 0.019
0.058 ± 0.012
0.062 ± 0.009
0.070 ± 0.009
0.064 ± 0.010
0.052 ± 0.006
0.045 ± 0.004
0.043 ± 0.004
0.049 ± 0.004
0.050 ± 0.003
0.052 ± 0.004
0.044 ± 0.004
0.040±0.005
0.032 ± 0.003
0.027 ± 0.003
0.028 ± 0.003

20.020 ± 0.004

Zürich countyN

Bq g− 1 Ca

3
4
3
3
2
2
1
7
7
18
28
34
44
42
44
31
20
9
3

0.020 ± 0.003
0.026 ± 0.005
0.034 ± 0.001
0.051 ± 0.005
0.086 ± 0.006
0.093 ± 0.020
0.114 ± 0.008
0.142 ± 0.007
0.141 ± 0.004
0.141 ± 0.005
0.161 ± 0.010
0.253 ± 0.010
0.353 ± 0.015
0.309 ± 0.013
0.257 ± 0.014
0.185 ± 0.008
0.161 ± 0.009
0.146 ± 0.015
0.154 ± 0.013

2
4
4
10
6
8
9
7
7
5
3
4
3
1
2

0.050 ± 0.013
0.059 ± 0.020
0.043 ± 0.005
0.045 ± 0.003
0.040 ± 0.003
0.042 ± 0.003
0.043 ± 0.007
0.038 ± 0.002
0.038 ± 0.001
0.034 ± 0.002
0.031 ± 0.003
0.024 ± 0.003
0.023 ± 0.003
0.020 ± 0.003
0.025 ± 0.003

22

0.020 ± 0.003
0.028 ± 0.003

N is the number of measurements with at least 5 teeth used for eachmeasurement.

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P. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605
0.50

0.30

-1

Sr (Bq g Ca)

0.40

90

0.20

0.10

0.00
1950

1960

1970
1980
year of birth

1990

2000

Fig. 2. 90Sr activities (Bq g− 1 Ca) in milk teeth extracted from Swiss children from 1963 to 2001, for three different regions: Zürich county (lozange),
Vaud county (circle) and Tessin county (triangle).

where a higher deposition of 137Cs from the Chernobyl
cloud also occurred (Fig. 3).
Froidevaux et al. (2004) showed that 90Sr activity incheeses produced in Western Europe are strongly
correlated with grazing altitude. When cows graze
between 100 and 400 m in altitude, cheeses have 90Sr
activities between 0.028 and 0.036 Bq g Ca− 1. Whencheeses are produced at higher altitudes (> 700 m)
activities of up to 0.12 Bq g Ca− 1 are observed. This ismainly due to the higher deposition of radionuclides inmountainous areas, often correlated with precipitation
rates (Wright et al., 1999; Hölgye and Filgas, 1995).
This leads to different 90Sr body burdens for people
living in different regions.
Chernobyl

0.080

Sr (Bq/ g Ca)

0.060

0.040

90

detonation of many very powerful devices. After theentry into force of the Partial Nuclear Test Ban Treaty
that ended American, British and Soviet atmosphericnuclear weapon tests, a large and regular decrease in90
Sr activitiy in milk teeth is observed. Unfortunately,budget restrictions prohibited the collection of milk
teeth for children born between 1970 and 1977. The
program was restarted after the Chernobyl nuclear
power plant accident and teeth have been collected forchildren born from 1978 up until now. A fit of the datafrom 1964 to 1996 with an exponential curve, gives anapparent half-life for 90Sr in milk teeth of 9.8 ± 3 years.
This is close to the half-life of 9 ± 2 years in grass andsoil and 13 ± 3 years in milk as determined by Friedli etal. (1991) in Switzerland.
An examination of the period from 1975–1994 reveals
several interesting features (Fig. 3). The Chernobyl
nuclear power plant accident occurred in 1986. At close
examination, the Chernobyl contribution is visible.
Following the Chernobyl accident, special attention wasgiven to milk and milk products in Switzerland. Typically,values for milk increased temporarily by a factor of 2,
passing from 0.1 Bq kg− 1 to 0.2 Bq kg− 1 in some regionsof Switzerland (Geering et al., 1990). Interestingly, thisChernobyl 90Sr has vanished rapidly from the upper layerof the soil, indicating that its chemical form was different
from the one deposited during the sixties. Thus, milk
activity returned to the pre-Chernobyl value within a few
months (Friedli et al., 1991). In spite of the increase inmilk activity for the few months following the accident,
only a very slight increase in 90Sr in milk teeth wasobserved for children born in 1986 and 1987. In
Switzerland, the increase was largest in Tessin county

0.020

0.000
1978

1983

1988

1993

1998

year of birthFig. 3. Activities in milk teeth of Tessin county children born between
1980 and 1994. The arrow highlights the effect of the Chernobyl
accident.

P. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605

4. Discussion
4.1. Analytical method
The chemical separation method used in this workfor the determination of 90Sr in milk teeth gives resultswith a very low detection limit (5 mBq g− 1 Ca), lowmeasurement uncertainties (± 15% at 95% of confidence level) and an efficient means of checking thesource purity by measuring the half-life, which should
be close to 64 h for a pure 90Y source (Fig. 4). Thismethod has been used in our laboratory to measure 90Srin milk teeth and human vertebrae, as well as in milk,
grass, wheat, vegetables and soil since 1972 (Geering
et al., 1990). Prior to 1972, a strontium specificprecipitation by fuming nitric acid followed by ironscavenging was used. After a partial ingrowth of 90Y,
this radionuclide was separated by two successive
precipitations as hydroxide, then as oxalate (Lerch etal., 1965). This method was replaced in 1972 by thechromatographic separation of strontium and yttrium
described above. No difference was observed between
the results obtained from the two methods. This is as
expected since the results depend only on the primary90
Y source used to calibrate the proportional countersused to measure source activity. Nevertheless thechromatographic method is preferred because it canbe partly automated and is less hazardous for theoperator than the fuming nitric acid method. Using a
combination of extractions by TBP and precipitation
steps, Neuzil and Dysart (1984) demonstrated that 90Srand 228Ra can be determined in teeth samples, due tothe fact that 228Ac follows yttrium in the chemical
separation scheme. They concluded that the radium
400

300
250
200
150
100

90

Y (counts per 4 hours)

350

50
0
0

10

20
30
number of measures40

Fig. 4. Activity (counts per 4 h) determined for a yttrium oxalate
source obtained from 3 g of ashed milk teeth from Tessin county
children born in 1992 (teeth extracted in 2002). Black line represents
the background. Dotted lines are the upper and lower limits of theconfidence interval for the background (2σ).

601

isotope accumulates from the decay of its parent 232 Th
which appears to be deposited in teeth as a phosphatein calcium-bearing tissue. Meanwhile the 228 Ra activity
is equal to the 90Sr activity in the teeth of children from
0–10 years of age, at a level of 0.030 Bq g− 1 Ca. Thus
if the chemical separation does not allow a complete
purification of the dosed radionuclide (90Sr or 90Y), a
large overestimation of the 90Sr activity is possible.
Altzitzoglou et al. (1998) made similar observations forthe measurement of 90Sr in bone ash. Stamoulis et al.
(1999) and O'Donnell et al. (1997) used a complete
separation of either 90Y or 90Sr to assess the level of90
Sr in milk and permanent teeth.
In the method used by Mangano et al. (2003), it islikely that radium and actinium are not completely
separated from thorium. Because these two radionuclides are in secular equilibrium with their parent,
232
Th, this will add about 100 mBq g− 1 Ca to the 90Sr
activity. At current levels of activity (e.g. 30 mBq g− 1Ca), this may be sufficient to account for the increasein milk teeth activity reported by the authors. In themethod of Mangano et al. it is also possible thateventually other natural radionuclides (e.g. leadisotopes) will follow strontium. Also, the liquid
scintillation counting method used for activity determination is not specific enough to the 90Sr/90Y pair. Anyother beta emitters present in the flask will also be
counted. If Mangano's method might be satisfactory toevaluate 90Sr in case of a large increase in milk teeth
activity, it is compulsory to use a method that allows atotal decontamination of the 90Sr or 90Y sources whenmeasuring them in milk teeth at present time 90Sr
activity. Altzitzoglou et al. (1998) emphasized thenecessity of a complete chemical separation schemeand the importance of using a sufficient quantity ofmaterial when undergoing a rigorous certification
process to separate 232 Th, natural U, 239/240Pu, 241Am,
226
Ra, 228 Ra, 210Pb, 210Po and 90Sr in bone ash samples.
Problems can arise from the use of a very small
sample. Mangano et al. used 100 mg of tooth ash. In ourstudy, a usual amount of 3–5 g of teeth ash is used (poolof at least 5 teeth from children from the same region,born during the same year), leading to a 90Y signal about
4 times higher than the background at the year 2002
level of activity, the background signal being 0.004 cps(Fig. 4). Using 100 mg of tooth ash would not allow us
to quantify the tooth activity. Stamoulis et al. (1999) alsoemphasized the necessity of pooling teeth to obtainlarger samples with enough ash (4–10 g) for 90Sr
analysis, while O'Donnell et al. (1997) used batches ofat least 50 permanent teeth. Aarkrog (1971) used asmaller quantity of tooth ash during the sixties due toP. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605

Switzerland is characterized by large variations ingeomorphology, with three distinct regions: the Swiss
lowland, the Jura mountains, and the Alps. The highest
137
Cs, 90Sr and plutonium depositions were in the Alpsand the Jura Mountains (Froidevaux et al., 2003). Part ofTessin county was also more contaminated than the
Swiss lowland due to topography and high rainfall.
Higher 137Cs deposition from the Chernobyl accident
was also detected there. On the other hand, Tessincounty is separated from the Swiss nuclear power plants
by the Alps, excluding any potential effects of thenuclear power plants on the level of 90Sr in milk teeth.
Meanwhile there is no difference in the level of 90Sr in
the milk teeth of children born in Tessin county
compared with children born in lowland Switzerland;
the maximum value is 0.360 Bq g− 1 Ca in Tessincounty, 0.421 Bq g− 1 Ca in Vaud county and 0.353 Bq
g− 1 Ca in Zürich county. Variation in 90Sr content fromplace to place and sample to sample is the rule rather
than the exception. High inhomogeneity has been
observed for the Chernobyl and fallout depositions(Schimmack et al., 2003; Pourcelot et al., 2003).
Transfer of radioactivity from the environment to thefood chain varies between regions and depends on thealtitude of production of dairy products (Froidevaux et

0.50
0.40

:

0.30

-1

4.2. Radioecological considerationsal., 2004). Natural radioactivity is also highly inhomogeneous in the environment. The radium content of well,mineral and tap water can vary greatly, giving different
activity levels in the skeleton and teeth, depending on
consumption habits. Consumption habits for milk anddiary products are of particular importance when
attributing the variation in 90Sr activity in milk teeth
to different factors, including the presence of a nuclear
reactor in the vicinity. An assessment of the 90Sr content
of milk is essential. In our opinion it is not possible toexplain an increase in milk teeth activity, withoutobserving the same increase in milk samples. An
evaluation of the average 90Sr deposition and content
in milk is necessary for assessing the body contamination in a given region. In Switzerland, higher activities
are present in milk produced in upland Switzerland(Alps) than in lowland Switzerland. No effect of thenuclear power plants on milk activity has been observed(e.g. Geering et al., 1997).
Fig. 5 shows a comparison of the 90Sr activity in milk
teeth from children from Vaud and Zürich counties
between 1953 and 1992. The 90Sr activities are strongly
correlated (r = 0.99), indicating the same evolution ofcontamination of the food chain in both regions. Yet, thevalue of the slope of the linear regression is 0.84. Thismeans that milk teeth from Zürich county contained on
average 16% less 90Sr than milk teeth from the Frenchspeaking part of Switzerland between 1953 and 1992.
One explanation for this difference is the different
average deposition of 90Sr fallout from nuclear tests,
leading to a different level of contamination of diary
products. An alternative explanation is a difference in
consumption habits. In fact, the Zürich county is anurban region where the consumption of dairy products
may be less than in Vaud county, which includes large
farming areas. Note that Zürich county is within 50 km

Sr (Bq g Ca) Zurich

higher levels of activity, but not less than 2–5 g. As aquality control assessment, Mangano et al. measured
milk teeth of children from the Philippines born in 1991
and 1992. They obtained a value of 75 mBq g− 1 Ca. In
Switzerland, this is the value obtained for children born
during the 1970s. The Philippine Archipelago is situatedbetween 8°N and 20°N while Switzerland is situated ataround 46°N. UNSCEAR (1977) indicated an average
integrated 90Sr deposition density of 3 × 109 Bq km− 2
for the latitude 40–50°N. Deposition between 10 and
20°N is three times lower. Thus it is doubtful that
Philippine children born in the early 1990s would have
had such a high level of 90Sr activity in their milk teeth.
Using a method that allowed a total decontamination of
the measured 90Y source, Stamoulis et al. (1999)
measured the 90Sr activity in milk teeth from Greek
children of 0–10 years of age born during the nineties
and obtained a value close to 0.030 Bq g− 1 Ca. This issimilar to the value obtained in Switzerland, eventhough Greece was more heavily contaminated by the
Chernobyl accident. Activities as high as those reportedby Mangano et al. have not been measured elsewhere,
even in places where the 90Sr deposition from the
Chernobyl accident was measurable.

90

602

0.20
0.10
0.00
0.00

0.10

0.20
90

0.30

0.40

0.50

-1

Sr (Bq g Ca) Vaud

Fig. 5. Activity of 90Sr in milk teeth (Bq g− 1 Ca) from Zürich county as
a function of 90Sr activity in milk teeth from Vaud county, for the same
year of birth (from 1953 to 1990).

P. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605

of four nuclear reactors (3000 MWe), while Vaud county
is 150 km from a reactor, and Tessin county is separated
from the nuclear power plants by the Alps. Still, the 90Sr
activity in milk teeth of children born in Zürich county iscurrently the lowest of the three regions. The activity inmilk teeth from Tessin county is slightly higher than theother regions due to a higher deposition of 90Sr from theglobal fallout and the Chernobyl accident in that part of
Switzerland (Fig. 3). 90Sr activities in food samples (e.g.
milk and wheat) and bones or teeth in Switzerland since
the start of the year 2000 show evidence of an
equilibrium situation where activities expressed as Bq
g Ca− 1 are almost identical. The activity in milk
produced in the Swiss lowland is between 0.04 and0.06 Bq g Ca− 1. For wheat it is between 0.1 and 0.15 Bq
g Ca− 1 (Völkle et al., 2003). The average activity ofvertebrae sampled from people deceased during 2003
was 0.035 ± 0.010 Bq g Ca− 1, a value very close to thevalue reported for milk. Milk teeth measured during
2003 for children born between 1987 and 1992 averaged
0.030 ± 0.010 (Froidevaux et al., 2003). Thus the 90Sr
activity in milk, milk teeth and vertebrae has reached anequilibrium value of about 0.030 Bq g Ca− 1 throughout
lowland Switzerland. The trend in activities from the
Zürich, Tessin and Vaud areas towards the same value ofabout 0.030 mBq g Ca− 1 indicates a downward trend in
the transfer factor from soil-to-milk due to the migrationof 90Sr to depth in the soil and to irreversible adsorption
mechanisms in soil. As well, modern dairy farming
practices involve the mixing of milk from numerous
farms before redistribution around the country. As aconsequence, the activity in milk and in milk teeth isaveraged out. Stamoulis et al. (1999) observed that the90
Sr profile for milk teeth is similar to that for humanvertebrae. This is also true for Switzerland. Since thebeginning of the 1980s milk teeth and human vertebrae
have had almost the same 90Sr activity, decreasing
steadily down to 0.030 Bq g− 1 Ca in 2001 (Geering etal., 2001). Any suspected important increase in 90Sr
activity in milk teeth should be verifiable by measurements of 90Sr in milk and in human vertebrae of adults
from the same area, using a radiochemical method thatallows for a total decontamination of the strontium (oryttrium) source from natural radionuclides. O'Donnell
et al. (1997) did not observe any increase in 90Sr in themilk teeth of children living in the proximity of the
Sellafield reprocessing plant. They reported an average
activity of 8 Bq kg− 1 ash wt. Using a calcium content of
0.370 kg Ca per kg of ash (average of 130 milk teeth
from Swiss children born between 1988 and 1997) we
calculate an activity of 0.021 Bq g Ca− 1 for O'Donnell's
study. In a study carried out in South Ukraine between

603

1990 and 1991, Kulev et al. (1994) observed thatmeasured 90Sr concentrations of human teeth (N = 1000)
were lower by a factor of 10 compared with measurements made in the mid-1960s and mid-1970s. The effectof the Chernobyl accident was measurable as a 3-foldincrease in activity in the teeth of the male population
aged 25–45 years, possibly due to the mobilization ofthis age group for clean-up operations within the 30-km
zone around the damaged reactor. The maximum value
reported by Kulev et al. was less than 50 mBq g Ca− 1.
This is much lower than the 100–180 mBq g Ca− 1reported by Mangano et al. (2003). The maximum
activities reported for milk teeth during the peak period
from 1962–1964 were 0.350 Bq g Ca− 1 in the UnitedStates (Mangano et al., 2003), 0.250 Bq g Ca− 1 as aworld-wide average (Stamoulis et al., 1999), 0.240 Bq g
Ca− 1 in Denmark (Aarkrog, 1971) and 0.421 Bq g Ca− 1
in Switzerland (this work). Thus neither our study, nor
Stamoulis's, nor Kulev's nor O'Donnell's studies
confirm Mangano's observations for 90Sr.
4.3. Limitations of the scope and method
This report represents a long-term study of in vivo
Sr levels in Switzerland that has been carried out
under the direction of the Federal Office of Public
Health. Another aspect of this study, the yearly samplingof vertebrae from deceased people by different pathology institutes in Switzerland, is not discussed here. This
program of the survey of the radiation exposure of the
Swiss population is complemented by an analysis of90
Sr in milk sampled all over the country. One limitationof this work concerns the extrapolation of the results tothe entire Swiss population. Milk teeth were collected
mainly from the Swiss lowland, while it was observedthat dairy products from mountainous regions were morecontaminated by 90Sr than lowland dairy products(Froidevaux et al., 2004). This could introduce variationsin 90Sr exposure that are not taken into account in thiswork. It is also worth noting that farming habits changed
from the sixties to the nineties from small independent
production units to larger farms with centralized milkcollection and processing. This makes it difficult tocompare different regions in Switzerland when, forexample, the pooling of milk between the Zürich and
Vaud regions may be responsible for the convergence ofactivities in milk and milk teeth in these two regions in
the eighties and nineties.
The Federal Office of Public Health restarted themilk teeth program following the Chernobyl nuclear
power plant accident, recognizing the importance of
the information obtained from 90Sr determination in
90

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P. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605

these samples. Today the milk teeth program, and also
the determination of 90Sr in vertebrae, is part of an
ongoing national program of environmental radioactivity monitoring.
5. Conclusions
The Swiss experience monitoring 90Sr activity inmilk teeth shows a sharp increase in activity that is
attributable to atmospheric nuclear weapon tests thatwere carried out by the Soviet Union, the United Statesand, to a lesser extent, England and France during the1950s and the 1960s. Since the entry into force of thePartial Nuclear Test Ban Treaty that ended atmospherictests in 1963, the 90Sr activity in the milk teeth of Swiss
children has decreased rapidly, with an apparent half-lifeof about 10 years. The Chernobyl nuclear power plant
accident doubled the 90Sr activity in milk for a period ofa few months, but the resultant increase in activity in themilk teeth of children born in 1986 was barely
measurable. In contrast with the work of Mangano etal. (2003), no increase in 90Sr has been observed in themilk teeth of Swiss children living close to nuclear
power plants during the 1990s. Milk teeth activities
determined in Switzerland during the nineties are similar(within the limits of uncertainty) to the activities
reported by Kulev et al. (1994), O'Donnell et al.
(1997) and Stamoulis et al. (1999), but not to the milk
teeth activities reported by Mangano et al. (2003).
The method used for 90Sr determination in milk teeth
in Switzerland permits a complete separation of 90Sr/
90
Y from other natural and artificially occurring radionuclides, and allows the purity of the measured source tobe checked. A very low detection limit is obtained byusing a large quantity of tooth ash. Statistical analysis of
the data shows no correlation between the activity of theteeth and the year of extraction, with the exception ofteeth from children born during the period 1962–1964,
when large changes in the 90 Sr activity in theenvironment and food chain were observed. Measurements of milk teeth collected in Vaud county show 16%
more activity than those collected in Zürich county. This
work demonstrates the importance of applying a very
careful chemical separation scheme with high decontamination factors for 90Sr or 90Y from natural uranium
and thorium series when measuring 90Sr in milk teeth orother samples. It is likely that the absence of a highpurity chemical separation of strontium or yttrium fromnatural uranium and thorium series, and the use of only avery small amount of tooth ash, gave rise to the elevatedactivities reported for milk teeth in the United States by
Mangano et al. compared with previous measurements.

Acknowledgement
The authors gratefully acknowledge F. Barraud fortechnical help, J.-P. Laedermann for assistance withthe statistical treatment of the data, S. Bulling for
proof reading, and the dentists of Vaud, Tessin and
Zürich counties for the long term collection of milk
teeth. This work was supported by the Federal Officeof Public Health under contract no. 3189.001.4.
References
Aarkrog A. Prediction models for 90Sr in shed deciduous teeth andinfant bone. Health Phys 1971;21:803–9.
Altzitzoglou T, Larosa JJ, Nicholl C. Measurement of 90Sr in bone ash.
Appl Radiat Isotopes 1998;49:1313–7.
Apostoaei AI. Absorption of strontium from the gastrointestinal
tract into plasma in healthy human adults. Health Phys 2002;
83:56–65.
Christensen GC, Alstad J, Evale E, Pappas AC. 90Sr in human bone in
Norway 1956–1972. Health Phys 1975;28:677–84.
Friedli C, Geering JJ, Lerch P. Some aspects of the behaviour of 90Sr in
the environment. Radiochim Acta 1991;52:237–40.
Froidevaux P, Friedrich-Bénet K, Barraud F, Schmittler T, Valley JF.
Mesures de 90Sr dans les vertèbres et les dents de lait.
Environmental radioactivity and radiation exposure in Switzerland; 2003. chap. 6.2, SFOPH, 1700 Fribourg 2003, ISBN3905235-44-7.
Froidevaux P, Geering JJ, Pillonel L, Bosset JO, Valley JF. 90Sr, 238U,
234
U, 137Cs, 40K and 239/240Pu in Emmental type cheese produced indifferent regions of Western Europe. J Environ Radioact 2004;
72:287–98.
Geering JJ, Friedli C, Lerch P. Method of determination of 90Sr in theenvironment. J Trace Microprobe Tech 1990;8:211–30.
Geering JJ, Froidevaux P, Valley JF, Burger M, Holzer R, Figueiredo
V, et al. Mesures de strontium-90 dans le sol, l'herbe, le lait et lefroment. Environmental radioactivity and radiation exposure in
Switzerland; 1997. chap. 7.2, SFOPH, 1700 Fribourg 1997,
ISBN3-905235-28-5.
Geering JJ, Barraud F, Froidevaux P, Valley JF. Mesure de 90Sr dans lesvertèbres et les dents. Environmental radioactivity and radiation
exposure in Switzerland; 2002. chap. 6.2, SFOPH, 1700 Fribourg
2001, ISBN3-905235-40-4.
Hanson WC, Thomas JM. Prediction of 90Sr body burdens andradiation dose in Anaktuvuk Pass Alaska Esquimos due to fallout.
Health Phys 1982;43:323–33.
Hardy EP, Krey PW, Volchok HL. Global inventory and distribution of
fallout plutonium. Nature 1973;241:444–5.
Hölgye Z, Filgas R. Inventory of 238Pu and 239/240Pu in the soil ofCzechoslovakia in 1990. J Environ Radioact 1995;27:181–9.
Kulev YD, Polikarpova GG, Prigodeyb EV, Assimakopoulos PA.
Strontium-90 concentration in human teeth in South Ukraine, 5
years after the Chernobyl accident. Sci Total Environ 1994;
155:215–9.
Leggett RW, Eckerman KF, Williams LR. Strontium-90 in bone: a casestudy in age-dependent dosimetric modeling. Health Phys
1982;43:307–22.
Lerch P, Bercier P. Nouvelle installation de comptage à bas-niveau
pour la mesure du strontium-90 dans les os humains. Chimia
1964;18:16–20.

P. Froidevaux et al. / Science of the Total Environment 367 (2006) 596–605
Lerch P, Geering J-J, Delay A. Méthode radiochimique d'analyse dustrontium-90 dans les os en présence de contaminants radioactifs.
Chimia 1965;19:43–4.
Mangano JJ, Gould JM, Sternglass EJ, Sherman JD, McDonnell W. An
unexpected rise in strontium-90 in deciduous teeth in the 1990. Sci
Total Environ 2003;317:37–51.
Neuzil EF, Dysart ME. The determination of 90Sr and 228Ra in humanteeth by age groups and in other substances. Int J Appl Radiat Isot
1984;35:1113–5.
O'Donnell RG, Mitchell PI, Priest ND, Strange L, Fox A, Henshaw
DL, et al. Variation in the concentration of plutonium, strontium-90
and total alpha-emitters in human teeth collected within the British
Isles. Sci Total Environ 1997;201:235–43.
Pourcelot L, Louvat D, Gauthier-Lafaye F, Stille P. Formation ofradioactivity enriched soils in mountain areas. J Environ Radioact
2003;8:215–33.
Schimmack W, Kracke W, Sommer M. Spatial variability of fallout90
Sr in soil and vegetation of an alpine pasture. J Environ Radioact
2003;65:281–96.
Shishkina EA, Lyubashevskii NM, Tolstykh EI, Ignatiev EA,
Betenekova TA, Nikiforov SV. A mathematical model for
calculation of 90Sr absorbed dose in dental tissues: elaborationand comparison to EPR measurements. Appl Radiat Isotopes
2001;55:363–74.

605

Stamoulis KC, Assimakopoulos PA, Ioannides KG, Johnson E,
Soucacos PN. Strontium-90 concentration measurements inhuman bones and teeth in Greece. Sci Total Environ 1999;
229:165–82.
UNSCEAR. Sources and Effects of Ionizing Radiation. United Nation
Scientific Committee on the Effects of Atomic Radiation 1977
report to the General assembly, vol. 40 (A/32/40). New York;
1977.
Völkle H, Andrey JL, Estier S, Ferreri G, Gurtner A, Jungck M, et al.
Environmental Radioactivity and Radiation Exposure in Switzerland; 2003. chap. 5, SFOPH, 1700 Fribourg 2003, ISBN3-90523544-7.
Webb E, Amarasiriwardena D, Tauch S, Green EF, Jones J, Goodman
AH. Inductively coupled plasma-mass (ICP-MS) and atomic
emission spectrometry (ICP-AES): versatile analytical techniques
to identify the archived elemental information in human teeth.
Microchemical Journal 2005;81:201–8.
Wright SM, Howard BJ, Strand P, Nylén T, Sickel MAK. Prediction of137
Cs deposition from atmospheric nuclear weapons tests within
the Arctic. Environ Pollut 1999;104:131–43.