Sunteți pe pagina 1din 10

Environmental Geochemistry and Health (2006) 28:421–430  Springer 2006

DOI 10.1007/s10653-006-9041-5

Human teeth as historical biomonitors of environmental and dietary lead: some


lessons from isotopic studies of 19th and 20th century archival material

J.G. Farmer1,4, A.B. MacKenzie2 & G.H. Moody3


1
School of GeoSciences, University of Edinburgh, Edinburgh, EH9 3JJ, Scotland, UK
2
Scottish Universities Environmental Research Centre, East Kilbride, G75 0QF, Scotland, UK
3
Edinburgh Dental Institute, University of Edinburgh, Edinburgh, EH3 9HA, Scotland, UK;
4
Author for correspondence (tel.: +44-131-650-4757; fax: +44-131-650-4757;
e-mail: J.G.Farmer@ed.ac.uk)

Received 25 October 2005; Accepted 6 February 2006

Key words: biomonitor, human, lead, lead isotopes, teeth

Abstract
The lead isotopic composition of various sections (crown, crown base, root) of teeth was determined in
specimens collected from 19th century skulls preserved in museum collections and, upon extraction or
exfoliation, from humans of known ages residing in Scotland in the 1990s. For most 20th century samples,
calculation of accurate crown-complete or root-complete dates of tooth formation ranging from the 1920s
to the 1990s enabled comparison of 206Pb/207Pb ratios for teeth sections (crown base root) with corre-
sponding decadally averaged data for archival herbarium Sphagnum moss samples. This showed that the
teeth sections had been significantly influenced by incorporation of non-contemporaneous (more recent)
lead subsequent to the time of tooth formation, most probably via continuous uptake by dentine. This
finding confirmed that separation of enamel from dentine is necessary for the potential of teeth sections as
historical biomonitors of environmental (and dietary) lead exposure at the time of tooth formation to be
realised. Nevertheless, the mean 19th century value of 1.172±0.007 for the 206Pb/207Pb ratio in teeth was
very similar to the corresponding mean value of 1.173±0.004 for 19th century archival moss, although
relative contributions from environmental sources – whether direct, by inhalation/ingestion of dust con-
taminated by local lead smelting (206Pb/207Pb1.17) and coal combustion (206Pb/207Pb1.18) emissions, or
indirect, through ingestion of similarly contaminated food – and drinking/cooking water contaminated by
lead pipes of local origin, cannot readily be determined. In the 20th century, however, the much lower
values of the 206Pb/207Pb ratio (range 1.100–1.166, mean 1.126±0.013, median 1.124) for the teeth collected
from various age groups in the 1990s reflect the significant influence of imported Australian lead of lower
206
Pb/207Pb ratio (1.04) and released to the environment most notably through car-exhaust emissions
arising from the use of alkyl lead additives (206Pb/207Pb1.06–1.09) in petrol in the U.K. from ca. 1930 until
the end of the 20th century.

Introduction Needleman et al. 1979; Paterson et al. 1988;


Fergusson et al. 1989; Tsuji et al. 2001) to the
Human teeth have often been used to monitor opportunistic use of permanent teeth found at
human exposure to the harmful heavy element ancient burial sites to investigate the degree of
lead. Studies have ranged from the deliberate use human exposure up to several thousand years ago
of shed deciduous teeth to monitor the extent (e.g. Patterson et al. 1991; Budd et al. 1998, 2000,
of childhood exposure in recent decades (e.g. 2004). In addition to concentration, the isotopic
422 j.g. farmer et al.

composition of the lead present in teeth has the part (e.g. whole, crown, root) and chemical
sometimes been used to estimate the contributions component (e.g. enamel, dentine) of the tooth
of different sources and pathways of exposure to analysed and, for teeth not specifically collected
lead (e.g. Alexander et al. 1993; Delves & Camp- for analysis at the time of exfoliation, extraction or
bell 1993; Farmer et al. 1994; Gulson & Wilson death, the effects of possible contamination or
1994; Gulson 1996; Åberg et al. 1998, 2001; Budd alteration during storage or burial (Delves et al.
et al. 1998, 2004; Yoshinaga et al. 1998). In Brit- 1982; Purchase & Fergusson 1986; Fergusson &
ain, variations in stable lead isotope ratios, in Purchase 1987; Paterson et al. 1988; Bercovitz &
particular the 206Pb/207Pb atom ratio, have been Laufer 1991; Budd et al. 1998, 2000, 2004; Lee
exploited because of the considerable interest, et al. 1999; Arora et al. 2004). Although lead in
especially during the 1980s and 1990s, in evaluat- tooth enamel is thought to reflect the presence of
ing the relative magnitude of contributions lead at the time of tooth formation (Hillson 1996)
from petrol lead (206Pb/207Pb = 1.06–1.09) and concerns have been raised at various times about
drinking water in contact with lead pipes the possibility of subsequent uptake of lead ions
(206Pb/207Pb = 1.16–1.18) (e.g. Alexander et al. (e.g. from food and water) into surface enamel
1993). This difference in the 206Pb/207Pb ratio (e.g. Purchase & Fergusson 1986; Fergusson &
arose from the distinctiveness of the isotopic Purchase 1987; Budd et al. 1998, 2004; Brown
signature of the original sources of the lead used, et al. 2004). Tooth dentine, which is in direct
e.g. the influence of the comparatively low 206Pb- contact with blood, is thought to reflect exposure
content Australian ores (206Pb/207Pb = 1.04) to lead during the lifetime of the tooth (Needleman
used, along with British Columbian ores et al. 1979; Purchase & Fergusson 1986; Fergusson
(206Pb/207Pb = 1.16), in the manufacture of petrol & Purchase 1987; Paterson et al. 1988; Fergusson
lead additives from the 1920s until their complete et al. 1989; Tsuji et al. 2001). The purposes of the
withdrawal in 2000 and, at the other extreme, the particular study and the origins and nature of the
typical 1.16–1.18 range for the 206Pb/207Pb ratio of material available must be taken into account.
British and other ores used in the manufacture of In seeking to investigate the use of human tooth
many products, including lead pipes for domestic lead as a historical biomonitor of environmental
plumbing systems, in Victorian times (Campbell & and dietary lead exposure, via isotopic analysis of
Delves 1989; Sugden et al. 1993; Farmer et al. 19th and 20th century archival material, we here
2000). Such differences in the lead isotopic com- report previously unpublished tooth lead data and
position of various sources of lead release to the compare them with our extensive database of the
atmosphere (e.g. car exhausts, smelting, combus- lead isotopic composition of the Scottish envi-
tion of coal (206Pb/207Pb1.18)) have also con- ronment during the 19th and 20th centuries.
tributed to temporal variations in the 206Pb/207Pb
ratio of atmospherically deposited lead, e.g. as
preserved in the accumulating layers of lake sedi- Materials and methods
ments (e.g. Farmer et al. 1996; Eades et al. 2002),
peat bogs (e.g. Farmer et al. 1997) and peaty soils 19th century teeth
(Farmer et al. 2005) and in collected specimens of
vegetation, such as moss, now stored in herbaria Specific parts of teeth were provided from 25
(e.g. Farmer et al. 2002). adults in total. Five samples, consisting of crown
Notwithstanding the successful use of lead iso- slices/chips, came from molar teeth in five Scottish
topic composition in both source apportionment skulls held in the Turner Collection, a human
studies of lead in modern teeth (e.g. Alexander cranial collection in the Department of Anatomy,
et al. 1993; Delves & Campbell 1993; Farmer et al. Medical School, University of Edinburgh, which
1994; Gulson 1996) and investigations of the spe- also provided crown slices/chips of five Inuit molar
cific source of lead in ancient teeth (e.g. Budd et al. teeth collected in 1896. The Royal College of
1998, 2004), however, it has long been recognised Surgeons of Edinburgh permitted samples (discs
that there can be difficulties in interpretation of taken 2 mm up from the apex of the tooth root) to
tooth lead data. These may be related to the po- be cut from teeth (67% of which were bicuspid) in
sition in the mouth of the particular tooth selected, 15 Scottish skulls held in its Greig Collection. It
human teeth as historical biomonitors of environmental and dietary lead 423

was a condition of sampling that there be minimal 2% v/v Decon 90 solution in a water bath at
disturbance to the appearance of the museum 80 C for 30 min, and then rinsed six times with
specimens and collection from the root also re- MilliQ deionised water, before drying in a drying
duced the risk of surface contamination arising cabinet at 30 C for 3–4 days. Each section was
from display under museum conditions. If the age weighed into a 5 mL beaker to which 1 mL 8 M
of the person at death was known, then the posi- nitric acid was added before heating at 80 C on
tion of the tooth in the mouth enabled dating of a hotplate to enable dissolution and evaporation
the (root complete) formation of that part of the to dryness. The residues were ashed at 460 C for
tooth to within ±10 years for 19th century teeth. 16 h in a muffle furnace before redissolution in
0.5 mL 8 M nitric acid and repetition of the
20th century teeth process. The resultant residues were dissolved in
0.2 mL 16 M nitric acid and transferred by
Samples from adult teeth, extracted at dental Pasteur pipette to 10 mL volumetric flasks. After
surgery from people currently living in Scotland, addition of 2 mL of lead-free acidified 10% m/v
were provided in three batches. The first, collected ammonium citrate solution and adjustment of
in 1993, consisted of slices through the crowns of pH to 4.5 using concentrated ammonia and nitric
17 teeth from 17 adults aged 19–64 years. The acid as required, 1 mL 10% ammonium pyrrol-
second, collected in 1994, consisted of discs taken idine dithiocarbamate was added to each to
2 mm up from the apex of the tooth root in 40 complex the lead as Pb(II) (Delves et al. 1982).
teeth (70% of which were molar) from 39 adults This was extracted by adding 1 mL methyl
aged 18–69 years. This enabled dating of the (root isobutyl ketone to each and shaking for 1 min.
complete) formation of that part of the tooth to Once the phases had separated, the organic layer
±1 year. The third, collected in 1995, consisted of was transferred by Pasteur pipette into a clean
2-mm-thick discs taken from the area adjacent to 5 mL beaker and evaporated slowly at 40–50 C
the tooth neck, near the base of the crown, in 52 on a hotplate, after which the residue was re-
teeth (75% of which were molar) from 50 adults dissolved in 2% nitric acid and the volume made
aged 20–75 years. This was thought to minimise up to 5 mL in a volumetric flask.
the possibility of surface contamination of the
crown enamel and enabled dating of the (crown Analysis
complete) formation of that particular part of the
tooth to ±1 year. Lead concentrations were determined by atomic
Children’s extracted deciduous teeth were pro- absorption spectrometry with a Pye Unicam SP9-
vided in two batches. The first of these, collected in 800 spectrometer at 217.0 nm, using a lead hollow
1993, consisted of slices through the crowns of cathode lamp (5 mA), an air-acetylene flame plus
seven teeth from seven children aged 5–12 years. slotted tube atom trap for enhancement of sensi-
The second, collected in 1994, consisted of discs tivity, a deuterium arc background correction sys-
taken 2 mm up from the apex of the tooth root in tem, and a spectral bandpass setting of 0.5 nm. Lead
10 teeth from 8 children aged 3–7 years. This en- calibration standards were prepared by dilution of a
abled calculation of the date of (root complete) 1000 mg L)1 standard solution and sample solution
formation of that part of the tooth to ±0.5 year. concentrations calculated from the linear portion of
the absorbance–concentration calibration curve,
Preparation of teeth for analysis prior to conversion to tooth lead concentrations
expressed in mg kg)1 dry tooth. A mean lead con-
The sections of modern 20th century teeth were centration of 2.8±0.9 mg kg)1 was obtained for the
soaked in 10% v/v hydrogen peroxide in 5 mL IAEA Certified Reference Material Animal Bone
beakers overnight to remove blood and fat. The H-5, for which the certified lead concentration is
19th century samples were not so treated as any 3.1 mg kg)1 (confidence interval 2.6–3.7 mg kg)1).
blood and fat had long since turned to dust and After dilution of sample solutions to
they were too brittle and fragile for this treat- <50 lg L)1, determination of lead isotope ratios
ment. All sections, 19th and 20th century, were (206Pb/207Pb, 208Pb/207Pb, 208Pb/206Pb) was carried
then rinsed well with deionised water, heated in out using a PlasmaQuad 2 Turbo Plus ICP-MS
424 j.g. farmer et al.

(Fisons Instruments, Winsford, UK). The forward Scottish teeth from the Greig Collection) are
plasma power was 1350 W, with reflected power summarised in Table 1. The mean value of the
206
<5 W. Argon flow rates for cool gas, auxiliary gas Pb/207Pb ratio for the Turner and Greig col-
and nebuliser flow were 14 L min)1, 1 L min)1 and lection teeth was 1.172±0.007 (±1SD).
0.9 mL min)1, respectively. The electron multiplier The lead concentration and 206Pb/207Pb data for
detector voltage was 2800 V and scanning over the 20th century teeth (crown slices) collected from
mass range 201.6–211.4 a.m.u. consisted of 2000 people in 1993 are summarised for four different
sweeps with a dwell time per channel of 80 ls over age groups (64, 30–39, 19–24 and 5–12 years) in
the 20 channels allocated per a.m.u. Correction for Table 2. Lead concentrations were markedly
mass bias was carried out using a solution of the greater for the two oldest individuals born ca.
National Institute of Standards and Technology 1930, but the mean values of the 206Pb/207Pb ratio
(NIST) common Pb isotopic reference standard for the different age groups differed only slightly,
SRM 981 (206Pb/207Pb = 1.093, 208Pb/206Pb = from 1.133±0.021 for the oldest group to
2.168, 208Pb/207Pb = 2.370). Each sample solution 1.119±0.009 for the youngest category (deciduous
was analysed five times, with the mean isotope ratios teeth of children).
and associated standard deviations being calculated The lead concentration and 206Pb/207Pb data for
automatically by the IBM PC-AT data handling sections of 20th century teeth (root disc in the case
system. The average precision on measurements of of those collected from people in 1994 and crown
the above lead isotopic ratios by ICP-MS was base disc in the case of those collected from people
±0.5%. For the IAEA Animal Bone H-5, which is in 1995) are summarised for eight different decades
not certified for lead isotopic composition, mean (1920s to 1990s), with respect to the time of for-
values of 1.127±0.004, 2.411±0.009 and mation of the different teeth, in Table 2. Lead
2.138±0.006 were obtained for the 206Pb/207Pb, concentrations were markedly greater for the
208
Pb/207Pb and 208Pb/206Pb ratios, respectively. 1920s and 1930s, averaging 20 mg kg)1, and
decreased steadily to £1.1 mg kg)1 in the 1990s.
The mean values of the 206Pb/207Pb ratio for the
Results different decades decreased from 1.139±0.012 for
the 1920s and 1.136±0.002 for the 1930s to a
The lead concentration and 206Pb/207Pb data for minimum value of 1.119±0.010 in the 1970s, be-
19th century teeth (crown slices in the case of the fore increasing to 1.139±0.009 in the 1990s.
Inuit teeth and the Scottish teeth from the Turner The 206Pb/207Pb data for all Scottish teeth
collection; root disc samples in the case of the samples are plotted against the corresponding
206
Table 1. Summary of lead concentrations and Pb/207Pb ratios for 19th century teeth.

Collection n Pb concn. range mg kg)1 Pb concn. mean mg kg)1 (±1SD) 206


Pb/207Pb range 206
Pb/207Pb mean (±1SD)

Inuita 5 1.6–12.8 6.7±4.6 1.157–1.169 1.164±0.005


Turnera 5 1.3–8.6 4.6±3.0 1.159–1.175 1.167±0.006
Greigb 15 0.9–27 8.8±7.7 1.156–1.181 1.173±0.007
Turnera+Greigb 20 0.9–27 7.7±7.0 1.156–1.181 1.172±0.007
a
Crown slices from teeth in Turner Colletion.
b
Root discs from teeth in Greig Collection.

206
Table 2. Summary of lead concentrations and Pb/207Pb ratios for 20th century teeth collected in 1993a.

Age group (years) n Pb concn. range mg kg)1 Pb concn. mean mg kg)1 (±1SD) 206
Pb/207Pb range 206
Pb/207Pb mean (±1SD)

64 2 14.1–17.3 15.7±2.3 1.118–1.148 1.133±0.021


30–39 6 0.8–6.2 2.4±2.1 1.111–1.153 1.132±0.015
19–24 9 0.3–3.7 1.4±1.3 1.104–1.130 1.120±0.007
5–12 7 2.2–4.9 3.7±1.2 1.106–1.131 1.119±0.009
a
Crown slices from extracted or exfoliated teeth.
human teeth as historical biomonitors of environmental and dietary lead 425
208
Pb/206Pb data (n = 141) in the three-isotope teeth (Turner+Greig collection, n = 20, Table 1)
plot of Figure 1. The best straight line through the is in agreement with the corresponding mean value
points is defined by 208Pb/206Pb = 2.983– of 1.173±0.004 for 19th century archival Scottish
0.735(206Pb/207Pb), with r = )0.560. Also plot- Sphagnum moss samples (n = 34) (Farmer et al.
ted are mean values of the corresponding ratios 2002). The latter, which is itself in agreement with
for: Australian lead ore (Chow et al. 1975); Aus- other proxy values for atmospheric lead in 19th
tralian-lead-influenced leaded additives in petrol century Scotland, for example from dated om-
on sale in Scotland from 1989 to 1998 resulting in brotrophic peat bogs (Farmer et al. 1997), repre-
car-exhaust emissions of lead to the atmosphere sents the average 206Pb/207Pb ratio of lead emitted
(Farmer et al. 2000); indigenous lead ore from to the atmosphere primarily via the smelting of
Leadhills/Wanlockhead in Scotland (Moorbath, indigenous lead ores and the combustion of coal
1962; Sugden et al. 1993); drinking water with (Farmer et al. 1999). In the case of the lead in
domestic lead water pipes (Sugden et al. 1993; human teeth, however, it cannot be stated with
Farmer et al. 1994); and Scottish coal (Farmer certainty that the source (and route of uptake) of
et al. 1999) the combustion of which resulted in the lead was environmental, either directly via
emissions of lead to the atmosphere. inhalation of atmospheric lead emitted by smelt-
ing/coal combustion or indirectly via ingestion of
atmospheric lead deposited upon, or taken up by
Discussion the roots of, food plants. There could also have
been a contribution from the direct ingestion of
The value of 1.172±0.007 for the mean drinking (or cooking) water contaminated with
206
Pb/207Pb ratio for 19th century Scottish adult lead as a result of the contact of soft, acidic water

2.30
Australian
lead ore

2.25

2.20
Pb/206Pb

2.15 Scottish
leaded petrol
208

2.10
Drinking water in
contact with lead pipes
Scottish lead ore (L/W) Scottish
coal
2.05

2.00
1.04 1.06 1.08 1.10 1.12 1.14 1.16 1.18 1.20
206 207
Pb/ Pb

Fig. 1. A three-isotope plot of 208Pb/206Pb versus 206Pb/207Pb for individual 19th century crown slices (adult, n = 5, d), 20th cen-
tury crown slices (adult and children, n = 24, s), 19th century root discs (adult, n = 15, .), 20th century root discs (adult and
children, n = 48, ,) and 20th century crown base discs (adult, n = 52, h), along with mean values for Australian lead ore, leaded
additives in petrol on sale in Scotland from 1989 to 1998 (Farmer et al. 2000), indigenous lead ores from Leadhills/Wanlockhead
(L/W) in Scotland (Moorbath 1962; Sugden et al. 1993), water in contact with domestic lead water pipes (Sugden et al. 1993;
Farmer et al. 1994), and Scottish coal (Farmer et al. 1999).
426 j.g. farmer et al.
206
Table 3. Summary of lead concentrations and Pb/207Pb ratios for sections of 20th century teeth collected in 1994a,b and 1995c.

206
Date of formation n Pb concn. range Pb concn. mean Pb/207Pb range 206
Pb/207Pb mean
of tooth mg kg)1 mg kg)1 (±1SD) (±1SD)

1920s
Roota – – – – –
Crownc 2 21.5–22.1 21.8±0.4 1.130–1.147 1.139±0.012
All 2 21.5–22.1 21.8±0.4 1.130–1.147 1.139±0.012
1930s
Roota 1 6.1 6.1 1.138 1.138±0.003
Crownc 3 14.7–35.9 24.4±10.7 1.133–1.138 1.135±0.003
All 4 6.1–35.9 19.9±12.7 1.133–1.138 1.136±0.002
1940s
Roota 1 19 19 1.127 1.127±0.004
Crownc 1 3.2 3.2 1.118 1.118±0.002
All 2 3.2–19 11.1±11.2 1.118–1.127 1.123±0.006
1950s
Roota 4 4.2–6.3 5.3±0.9 1.123–1.140 1.132±0.007
Crownc 15 0.1–13.8 4.7±3.9 1.108–1.143 1.124±0.010
All 19 0.1–13.8 4.8±3.4 1.108–1.143 1.125±0.010
1960s
Roota 7 1.3–7.4 3.8±2.4 1.110–1.134 1.124±0.010
Crownc 13 0.8–7.9 3.1±2.0 1.100–1.166 1.127±0.018
All 20 0.8–7.9 3.3±2.1 1.100–1.166 1.126±0.015
1970s
Roota 11 0.3–5.8 2.2±1.7 1.111–1.143 1.123±0.011
Crownc 12 0.2–6.7 2.2±1.9 1.102–1.125 1.116±0.007
All 23 0.2–6.7 2.2±1.8 1.102–1.143 1.119±0.010
1980s
Roota 14 0.5–6.6 1.7±1.8 1.106–1.157 1.125±0.015
Crownc 6 0.4–4.7 2.4±1.8 1.111–1.137 1.125±0.009
All 20 0.4–6.6 1.9±1.8 1.106–1.157 1.125±0.013
1990s
Roota 2 0.5–0.8 0.7±0.2 1.134–1.146 1.140±0.008
Rootb 8 0.3–1.1 0.4±0.3 1.124–1.150 1.139±0.009
Crownc – – – – –
All 10 0.3–1.1 0.5±0.3 1.124–1.150 1.139±0.009
a
Root discs.
b
Root discs (deciduous); all from extracted or exfoliated teeth.
c
Crown base discs from extracted teeth.

with the lead pipes of Victorian plumbing systems 1.124±0.014 was found for teeth from four young
manufactured from indigenous lead ores adults in Edinburgh (Farmer et al. 1994). For the
(206Pb/207Pb = 1.16–1.18). children’s teeth (n = 7) collected in 1993, mean
On the basis of the decline in 206Pb/207Pb ratios values of 3.7±1.2 mg kg)1 and 1.119±0.009 for
from the mean value for the 19th century Scottish lead concentration and 206Pb/207Pb ratio (Table 2),
adult teeth (1.172±0.007 for the Turner+Greig respectively, were in excellent agreement with the
collections, Table 1) to the mean values for the corresponding mean values of 3.2±1.2 mg kg)1
20th century Scottish adult teeth (1.126±0.013 for and 1.131±0.015 reported by Farmer et al. (1994)
crown slices from all adults, n = 17, in Table 2) for whole teeth (n = 7) collected from ‘low-lead
collected in 1993, the influence of lead of much exposure’ children in Edinburgh earlier in the
lower 206Pb/207Pb ratio (e.g. the 1.04 of Australian 1990s. At that time, the mean 206Pb/207Pb ratio
lead, as used in combination with other sources in was considered to be intermediate between the
the leaded petrol additives introduced from the then observed values for leaded petrol
1930s) is apparent. Previously, a mean value of (1.075±0.013) and tap water in contact with
human teeth as historical biomonitors of environmental and dietary lead 427

1.20

1.18

1.16
Pb/207Pb
206

1.14

1.12

1.10
1800 1850 1900 1950 2000

date

Fig. 2. A comparison of temporal trends in the decadal average 206Pb/207Pb ratios (±1SD) for teeth (root and crown base discs,
Table 3, d; time of root complete or crown complete formation) and Scottish Sphagnum moss samples (s) (Farmer et al. 2000)
during the 19th and 20th centuries.

leaded pipes (1.160±0.012) and comparable with previously successful physical separation method
that reported for lead in food (1.12–1.13). (Farmer et al. 1994) failed, it is the suitability and
In using teeth, the question arises of the applicabilty of whole root discs and crown base
appropriateness of different parts for use as bio- discs that comes under scrutiny below.
monitors of value over varying lengths of time in Table 3 demonstrates general agreement
studies aimed at source identification or appor- between the 206Pb/207Pb data for root discs and
tionment. Both from our previous work (Farmer crown base discs over the decades of the 20th
et al. 1994) and the comparison of crown slice data century for which data were available. Figure 2,
in this study, it seemed clear to us that separation therefore, compares the decadally averaged tem-
into enamel and dentine components would be poral trend in the combined 206Pb/207Pb data for
beneficial. We were concerned, however, that the root and crown base disc samples (Table 3) for
crown enamel, although potentially easier to relate the 20th (and 19th – root disc only) centuries with
to a specific period of tooth formation and com- that subsequently established for archival herbar-
pletion, might have been subject to post-eruption ium Sphagnum moss samples from Scotland
oral exchange and uptake of lead from lead-con- (Farmer et al. 2002). There is good agreement for
taminated food and water (e.g. Fergusson & Pur- the 19th century data, where the decadal values
chase 1987). This is why we decided, at least for ranged from 1.167 to 1.176 for teeth and 1.169 to
the teeth collected in 1994, to try to sample from a 1.176 for moss (Figure 2). However, as is clear
section of tooth (root) equally easy to relate to a from the corresponding comparison of 20th cen-
specific period of tooth formation and completion tury 206Pb/207Pb data, most notably from the
but much less subject to surficial exchange and 1920s to 1970s (Figure 2), there was a strong
uptake. In the subsequent attempt, in 1995, we subsequent contributory influence from lead that
hoped that the collection of discs from near the was non-contemporaneous (more recent) to the
base of the crown, near the neck of the tooth, time of tooth formation and completion, possibly
would also minimise lead contamination of surface also reflected in the increased lead concentration
enamel. As, in both cases, our attempts to separate with age of tooth (Table 3). Bearing in mind the
enamel and dentine components by a simple and practical difficulty experienced in separating
428 j.g. farmer et al.

enamel from dentine, this most probably occurred lead from the consumption of drinking water
via dentine incorporation of lead circulating in the contaminated by lead pipes during the formation
blood. While the bulk of the root section analysed of the tooth, the lead isotopic composition of the
would have been primary dentine, the pulpal cav- treated crown enamel will not necessarily reflect
ity at the centre of the tooth where lead can enter that of the environment (e.g. the atmosphere) at
from the bloodstream is lined with circumpulpal or that time. Furthermore, the dietary intake of lead
secondary dentine, which has a higher organic at that time also need not necessarily reflect the
content and tends to have a much higher lead prevailing isotopic composition of atmospheric
concentration (w/w) than in primary dentine or lead as dietary sources such as food plants may
enamel (e.g. Fergusson & Purchase 1987). The lead have accumulated previously deposited lead from
isotopic data for the root disc samples (Table 3), soil.
therefore, probably reflect some more recent Nevertheless, in these teeth samples, it is clear
accumulation of lead in the secondary dentine that direct (inhalation/ingestion) or indirect (die-
surrounding the pulp cavity with age through the tary) exposure to environmental lead, in addition
years. Similarly, the crown base discs were no to the (unknown) possibility of exposure to lead
more successful in terms of generating specific present in drinking water from contact with lead
date-related lead isotopic data that were uninflu- pipes, has been significant. This is demonstrated
enced by subsequent exposure to and incorpora- by the mean value of 1.126±0.013 (median 1.124)
tion of lead, suggesting that they too have been for the 206Pb/207Pb ratio of teeth (n = 141) col-
affected to a similar extent by accumulation of lead lected from various age groups during the 1990s
deposited in coronal dentine in the years after (Tables 2, 3), reflecting the influence of releases of
crown completion. It is noticeable, however, that imported Australian lead of lower 206Pb/207Pb ra-
the difference between teeth and moss 206Pb/207Pb tio (1.04) to the environment primarily through
data for samples from younger people with more car-exhaust emissions arising from the use of alkyl
recent dates of tooth formation (1980s to 1990s) lead additives (206Pb/207Pb1.06–1.09) in petrol.
was much lower (Figure 2), there being less time The mean value of 1.126 is intermediate between
for subsequent accumulation of lead of potentially that of 1.076 for leaded petrol (Farmer et al. 2000)
different 206Pb/207Pb ratio. and the 1.170 for local indigenous lead ore and
The lessons to be learned from this tooth study 1.181 for Scottish coal (Farmer et al. 1999). Al-
have emerged as a consequence of the establish- though source apportionment calculation was not
ment of the trends in the 206Pb/207Pb ratio of the purpose of this study, the demonstration of
atmospheric lead in the Scottish environment over significant contributions to human exposure from
the past two centuries. To some extent, these the petrol-derived source and pathways of lead has
reinforce the recommendations or findings of other been borne out by the remarkable observed decline
subsequent studies of lead in teeth. In particular, in blood lead not only in the U.K. but elsewhere in
if, as in this historical biomonitoring study, the the world where unleaded petrol has been intro-
isotopic composition of lead that prevailed in the duced and leaded petrol banned (Thomas et al.
environment (and to which humans were exposed) 1999). Measures to reduce exposure to lead from
over a short interval of time (i.e. corresponding to other sources, for example from water and
tooth formation) is sought, then, for adult teeth, adventitious sources such as leaded paint), have
the crown enamel (after removal of the surface also been important. On the basis of our previous
enamel) should be preferred for analysis (Budd tooth study (Farmer et al. 1994), the presence of a
et al. 1998, 2000, 2004), as dentine integrates few outliers in the 208Pb/206Pb versus 206Pb/207Pb
exposure to lead over the lifetime of the tooth. plot of Figure 1 could possibly reflect the influence
Removal of the surface enamel removes contri- of exposure to leaded paint.
butions resulting from the subsequent ion-ex-
change uptake of lead from contaminated drinking
water in contact with lead pipes and, in longer- Conclusions
term archaeological studies, from post-burial ion-
exchange with lead in soil (Budd et al. 1998, 2000, The influence of changes in environmental sources
2004). Of course, where there has been exposure to of lead of varying isotopic composition during the
human teeth as historical biomonitors of environmental and dietary lead 429

20th century could readily be discerned in the lead human teeth: implications for long-term and historical
isotopic composition of sections (crown, crown exposure monitoring. Sci Total Environ 220, 121–136.
Budd P, Montgomery J, Evans J, Barreiro B. 2000 Human
base, root disc) of teeth of known date of forma- tooth enamel as a record of the comparative lead exposure of
tion. The demonstrable non-contemporaneous prehistoric and modern people. Sci Total Environ 263, 1–10.
uptake of lead, however, probably via incorpora- Budd P, Montgomery J, Evans J, Trickett M. 2004 Human lead
tion in dentine, serves to preclude the use of such exposure in England from approximately 5500 BP to the 16th
teeth sections as accurate biomonitors (for periods century AD. Sci Total Environ 318, 45–58.
Campbell MJ, Delves HT. 1989 Accurate and precise determi-
corresponding to the time of tooth formation) of nation of lead isotopic ratios in clinical and environmental
(i) the prevailing isotopic composition of atmo- samples using inductively coupled plasma mass spectrometry.
spheric lead and (ii) environmental and dietary J Anal Atomic Spectrometry 4, 235–256.
exposure to lead. Accordingly, the findings indi- Chow TJ, Snyder CB, Earl JL. 1975. Isotope ratios of lead as
rectly support the use of the enamel component of pollutant source indicators. In Isotope Ratios as Pollutant
Source Indicators. Vienna: IAEA, pp. 95–107.
teeth in historical biomonitoring studies, and the Delves HT, Campbell MJ. 1993 Identification and apportion-
use of the dentine component of short-lived ment of sources of lead in human tissue. Environ Geochem
deciduous teeth in surveys of recent childhood Health 15, 75–83.
exposure to lead. Delves HT, Clayton BE, Carmichael A, Bubear M, Smith M.
1982 An appraisal of the analytical significance of tooth-lead
measurements as possible indices of environmental exposure
of children to lead. Ann Clin Biochem 16, 329–337.
Acknowledgements Eades LJ, Farmer JG, MacKenzie AB, Kirika A, Bailey-Watts
AE. 2002 Stable lead isotopic characterisation of the histor-
We thank the Department of Anatomy and the ical record of environmental lead contamination in dated
Edinburgh Dental Institute, University of Edin- freshwater lake sediment cores from northern and central
Scotland. Sci Total Environ 292, 55–67.
burgh, and the Royal College of Surgeons of
Farmer JG, Sugden CL, MacKenzie AB, Moody GH, Fulton
Edinburgh for provision of teeth samples, M. 1994 Isotopic ratios of lead in human teeth and sources of
K. Cotton, J. Hitchen and E. Kane for chemical lead exposure in Edinburgh. Environ Technol 15, 593–599.
preparation of samples in the laboratory and Farmer JG, Eades LJ, MacKenzie AB, Kirika A, Bailey-Watts
K. Sampson for ICP-MS analysis. AE. 1996 Stable lead isotope record of lead pollution in Loch
Lomond sediments since 1630 A.D. Environ Sci Technol 30,
3080–3083.
Farmer JG, MacKenzie AB, Sugden CL, Edgar PJ, Eades LJ.
References 1997 A comparison of the historical lead pollution records in
freshwater lake sediments and peat cores from central
Åberg G, Fosse G, Stray H. 1998 Man, nutrition and mobility: Scotland. Water Air Soil Poll 100, 253–270.
a comparison of teeth and bone from the Medieval era and Farmer JG, Eades LJ, Graham MC. 1999 The lead content and
the present from Pb and Sr isotopes. Sci Total Environ 224, isotopic composition of British coals and their implications
109–119. for past and present releases of lead to the U.K. environment.
Åberg G, Charalampides G, Fosse G, Hjelmseth H. 2001 The Environ Geochem Health 21, 257–272.
use of Pb isotopes to differentiate between contemporary and Farmer JG, Eades LJ, Graham MC, Bacon JR. 2000 The
ancient sources of pollution in Greece. Atmos Environ 35, changing nature of the 206Pb/207Pb isotopic ratio of lead in
4609–4615. rainwater, atmospheric particulates, pine needles and leaded
Alexander LM, Heaven A, Delves HT, Moreton J, Trenouth petrol in Scotland 1982–1998. J Environ Monitor 2, 49–57.
MJ. 1993 Relative exposure of children to lead from dust and Farmer JG, Eades LJ, Atkins H, Chamberlain DF. 2002
soil. Arch Environ Health 48, 392–400. Historical trends in the lead isotopic composition of archival
Arora M, Chan SWY, Kennedy BJ, Sharma A, Crisante D, Sphagnum mosses from Scotland (1838–2000). Environ Sci
Walker DM. 2004 Spatial distribution of lead in the roots of Technol 36, 152–157.
human primary teeth. J Trace Elem Med Biol 18, 135–139. Farmer JG, Graham MC, Vinogradoff SI, Bacon JR, Dunn
Bercovitz K, Laufer D. 1991 Age and gender influence on lead SM, MacKenzie AB. 2005 Isotopic characterisation of the
accumulation in root dentine of human permanent teeth. historical lead deposition record at Glensaugh, an organic-
Arch Oral Biol 36, 671–673. rich, upland catchment in rural N.E. Scotland. Sci Total
Brown CJ, Chenery SRN, Smith B, Mason C, Tomkins A, Environ 346, 121–137.
Roberts GJ, Sserunjogi L, Tiberindwa JV. 2004 Environ- Fergusson JE, Purchase NG. 1987 The analysis and levels of
mental influences on the trace element content of teeth – lead in human teeth: a review. Environ Poll 46, 11–44.
implications for disease and nutritional status. Arch Oral Biol Fergusson JE, Kinzett N, Ferguson DM, Horwood LT. 1989 A
49, 705–717. longitudinal study of dentine lead levels, intelligence, school
Budd P, Montgomery J, Cox A, Krause P, Barreiro B, Thomas performance and behaviour: the measurement of dentine
RG. 1998 The distribution of lead within ancient and modern lead. Sci Total Environ 80, 229–241.
430 j.g. farmer et al.

Gulson BL. 1996 Tooth analyses of sources and intensity of Patterson C, Ericson J, Manea-Krichten M, Shirahata H. 1991
lead exposure in children. Environ Health Persp 104, 306–312. Natural skeletal levels of lead in Homo sapiens sapiens
Gulson BL, Wilson D. 1994 History of lead exposure in uncontaminated by technological lead. Sci Total Environ 107,
children revealed from isotopic analyses of teeth. Arch 205–236.
Environ Health 49, 279–283. Purchase NG, Fergusson JE. 1986 Lead in teeth: the influence
Hillson S. 1996 Dental Anthropology, Cambridge: Cambridge of the tooth type and the sample within a tooth on lead levels.
University Press. Sci Total Environ 52, 239–250.
Lee KM, Appleton J, Cooke M, Keenan F, Sawicka-Kapusta Sugden CL, Farmer JG, MacKenzie AB. 1993 Isotopic ratios of
K. 1999 Use of laser ablation inductively coupled plasma lead in contemporary environmental material from Scotland.
mass spectrometry to provide element versus time profiles in Environ Geochem Health 15, 59–65.
teeth. Anal Chim Acta 395, 179–185. Thomas VM, Socolow RH, Fanelli JJ, Spiro TG. 1999 Effects
Moorbath S. 1962 Lead isotope abundance studies on mineral of reducing lead in gasoline: an analysis of the international
occurrences in the British Isles and their geological signifi- experience. Environ Sci Technol 33, 3942–3948.
cance. Philos Trans Royal Soc London A 254, 295–360. Tsuji LJS, Karagatzides JD, Katapatuk B, Young J, Kozlovic
Needleman HL, Gunnoe C, Leviton A, Reed R, Peresie H, DR, Hanning RM, Nieboer E. 2001 Elevated dentine-lead
Maher C, Barrett P. 1979 Deficits in psychologic and levels in deciduous teeth collected from remote First Nation
classroom performance of children with elevated dentine communities located in the western James Bay region of
lead levels. N Eng J Med 300, 689–695. northern Ontario, Canada. J Environ Monitor 3, 702–705.
Paterson LJ, Raab GM, Hunter R, Laxen DPH, Fulton M, Fell Yoshinaga J, Yoneda M, Morita M, Suzuki T. 1998 Lead in
GS, Halls DJ, Sutcliffe P. 1988 Factors influencing lead prehistoric, historic and contemporary Japanese: stable
concentrations in shed deciduous teeth. Sci Total Environ 74, isotopic study by ICP mass spectrometry. Appl Geochem
219–233. 13, 403–413.