Journal of Archaeological Science xxx (2012) 1e5

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Journal of Archaeological Science

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Element localization in archaeological bone using synchrotron radiation X-ray

uorescence: identication of biogenic uptake
Treena Swanston a, *, Tamara Varney b, Ian Coulthard c, Renfei Feng c, Brian Bewer c, Reg Murphy d,
Cheryl Hennig a, David Cooper a
a

Department of Anatomy and Cell Biology, A302-107 Wiggins Rd., University of Saskatchewan, Saskatoon, SK S7N 5E5, Canada
Department of Anthropology, Lakehead University, Thunder Bay, ON P7B 5E1, Canada
Canadian Light Source, 101 Perimeter Road, Saskatoon, SK S7N 0X4, Canada
d
National Parks Antigua, West Indies
b
c

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 30 November 2011
Received in revised form
17 January 2012
Accepted 26 January 2012

Trace element analysis related to archaeological bone is viewed as one way to determine levels of
element exposure in past populations. This area of research is complex because there is the potential for
the incorporation of trace elements from the burial environment into archaeological bone. We tested the
hypothesis that matching the spatial distribution of trace elements within cortical bone with the biological structures would provide evidence of biogenic uptake. We examined samples from a nonsegregated Royal British Naval cemetery (1793e1822) in Antigua, West Indies. A key historical question related to this population was the extent of exposure to lead and the resulting health effects. Images
from conventional light microscopy (histological) analysis of the bone samples were matched with
elemental maps of calcium, strontium, and lead that were created through the use of synchrotron
radiation X-ray uorescence (SR-XRF). Biogenic uptake of both strontium and lead was indicated based
on the localization of these trace elements within discreet microstructural elements. The successful
integration of histological information with XRF data is a powerful technique for the interpretation of
past biological events through trace elements.
2012 Elsevier Ltd. All rights reserved.

Keywords:
Bone
SR-XRF
Microarchitecture
Strontium
Lead

1. Introduction
Bone is a dynamic tissue that is continually replaced throughout
life. This turnover, known as remodeling, replaces existing bone
through focal resorption events and new bone formation. In the
cortex of bones, these remodeling events create cylindrical microstructures known as osteons (Haversian systems), which have
a mean diameter of approximately 250 mm in humans (Britz et al.,
2009). Bone microstructure survives death and can be preserved in
the archaeological (Mulhern and Van Gerven, 1997) and fossil
record (Abbott et al., 1996). The continual nature of the remodeling
process in humans ensures that new bone is always being formed
even after growth is completed. This provides the primary mechanism for the accumulation of trace elements in the adult skeleton.

* Corresponding author. Tel.: 1 306 966 7854.

E-mail addresses: treena.swanston@gmail.com (T. Swanston), tvarney@
lakeheadu.ca (T. Varney), ian.coulthard@lightsource.ca (I. Coulthard), renfei.feng@
lightsource.ca (R. Feng), cheryl.hennig11@gmail.com (C. Hennig), dml.cooper@
usask.ca (D. Cooper).

Osteons which are actively forming at the time of exposure are

enriched or labelled with the trace element if a suitable chemical
substitute is present in the apatite.
Trace element analysis of archaeological bone was initially
considered a promising area of research because of the connection
between certain trace elements (e.g. strontium, barium) and an
individuals diet (Brown, 1974). It was realized though that bone
chemistry is complex. The application of trace elements has largely
shifted from paleodietary reconstruction to their utility as diagenetic indicators, the two exceptions being strontium and barium
(Burton and Price, 2001). Many studies related to understanding
the impact of diagenesis have been recently summarized (King
et al., 2011, Maurer et al., 2011).
Efforts have been made to take advantage of the brilliant light
created at synchrotron facilities in the attempt to visualize trace
element patterns. With synchrotron radiation, faster scans are
obtained, and the brilliance of the light results in a greater sensitivity to elements present only in small concentrations. Varying
levels of success have been achieved with archaeological tissues
such as teeth (Martin et al., 2010, Martin et al., 2004, Martin et al.,
2007a), hair (Bertrand et al., 2003, Kempson et al., 2009) and bone

0305-4403/$ e see front matter 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jas.2012.01.041

Please cite this article in press as: Swanston, T., et al., Element localization in archaeological bone using synchrotron radiation X-ray uorescence: identication of biogenic uptake, Journal of Archaeological Science (2012), doi:10.1016/j.jas.2012.01.041

T. Swanston et al. / Journal of Archaeological Science xxx (2012) 1e5

(Dumont et al., 2009, Kuczumow et al., 2010, Martin et al., 2007b,

Wittmers et al., 2008). With the knowledge that previous studies
were not able to identify the biogenic uptake of lead due to the
limitations of the bone samples that were clearly affected by the
burial environment (Wittmers et al., 2008), our primary objective
was to expand on these previous methods through the fusion of
conventional light microscopy (histological) analysis of the bone
samples with elemental mapping obtained through the use of
synchrotron radiation X-ray uorescence (SR-XRF) technology. In
this preliminary study we focused on bone samples from an
historical Antiguan cemetery (1793e1822) with a population of
individuals who lived during the colonial era. A key historical
question related to this population was the extent of exposure to
lead and the resulting health effects. Lead is an element that is toxic
at low levels, and is easily and rapidly incorporated into bone
(Aufderheide and Wittmers, 1992). We hypothesized that these
individuals would exhibit lead exposure during life and thus this
toxic element would be localized to histological structures formed
during life.
2. Material and methods
2.1. Samples
One bular fragment (burial number 19a1) from an individual
originally interred at the Royal Naval Hospital Cemetery (c. A.D.
1793e1822) near English Harbour, Antigua was chosen from the
osteological material that is currently being curated at Lakehead
University, Thunder Bay, Ontario, Canada. A pre-contact (c. A.D.
1200 post Saladoid) bone sample from Antigua was also processed
to provide contextual information related to background
elemental levels for the region. Before the samples were processed,
ethics approval was obtained from the University of Saskatchewan
Biomedical Research Ethics Board. Initial testing of the samples
included a bulk analysis of the element concentrations by inductively coupled plasma mass spectroscopy (ICP-MS) using standard
methodologies at the ICP-MS Laboratory in the Department of
Geological Sciences, University of Saskatchewan (Jenner et al., 1990,
Stefanova et al., 2003).
Thin sections of bone were prepared with a Buehler IsoMet
Low Speed Saw with a diamond wheel (Norton Company). After an
approximately 300 micron bone section was removed, the fragment was ground to a thickness of approximately 100 microns with
2000 Grit 3M sandpaper. Residual material was removed from the
thin sections by soaking for 10 min in an ultrasonicator. The
approximate dimensions of the bone samples were 2 mm by 3 mm.
2.2. Histological analysis
The ground sections were placed on Thermanox metal-free
plastic coverslips (Cedarlane, Burlington, ON) and examined by
light microscopy. The digital images of the histological structure
were created using a PAXcam high-resolution digital microscope
camera (PAXcam, Villa, IL) at 10 magnication.
2.3. Element mapping
Two dimensional spatial maps of calcium, strontium, and lead
associated with the bone thin sections were generated using X-ray
uorescence (XRF) with the Very Sensitive Elemental and Structural Probe Employing Radiation from a Synchrotron (VESPERS)
hard X-ray microprobe bending magnet beamline located at the
third generation Canadian Light Source in Saskatoon, Saskatchewan, Canada (Feng et al., 2007). The bone thin sections were
placed between two Thermanox metal-free plastic coverslips that

were joined together with double-sided scotch tape providing

a shelf for the sample. An area of 2.61 mm by 1.88 mm of the bone
sample associated with the Royal Naval Hospital cemetery was
imaged.
The XRF technique for elemental mapping is based on the fact
that individual elements uoresce or emit characteristic radiation
from the drop of outer-shell electrons into inner-shell core-holes
generated by removal of inner-shell electrons by a primary radiation source of a specic energy. A synchrotron is a cyclic particle
accelerator that is capable of generating this primary radiation of
a specic energy in great quantities. The experiment was performed using a polychromatic beam (pink beam) with an incident
X-ray energy of 5e30 keV, a beam spot-size of approximately 5 mm,
and a resolution of 10 mm. A Vortex Silicon Drift Detector was used
for measuring the resulting XRF radiation. It was positioned at an
angle of 45 to the sample and set to capture the uorescence
spectra containing calcium (Ca) Ka lines (mainly Ka1 line at
3692 eV), strontium (Sr) Ka lines (mainly Ka1 line at 14,166 eV), and
lead (Pb) La lines (mainly La1 line at 10,551 eV). The Pb Lb and Pb Lg
lines were also followed in addition to Pb La.
Open source (ImageJ; http://rsbweb.nih.gov/ij/) and custom
software were utilized to convert the raw data into images,
normalize the data relative to the ionization chamber values,
register the images and produce multi-channel visualizations.
3. Results
Bulk concentrations of the two elements of interest indicated
that the level of Pb was high in the historical sample 19a1
(253.94 ppm) but relatively low in the pre-European contact
sample (26.91 ppm). The Sr bulk concentration in the historical
sample (324.31 ppm) was less than the bulk level in the preEuropean contact sample (548.74 ppm). Quality control standard
BCR-2 shows that long term analytical errors for Pb and Sr are 7%
and 5% respectively.
The XRF map of the historical sample corresponded closely with
the histological image with Ca appearing relatively homogeneous
while Pb and Sr varied considerably (Fig. 1). Due to the geometry of
the detector (45 to the sample from the right) and the highly
absorbing nature of the sample, edge artifacts were observed. These
took the form of elevated levels on surfaces with emitted edges
facing right - particularly the periosteal surface on the right edge of
the scan eld. These artifacts were most pronounced for Ca and
decreased due to increasing uorescent photon energy and lower
concentration for Pb and Sr, respectively.
Close inspection of the images (Fig. 2) revealed that the Pb and
Sr-XRF patterns, although different, both corresponded to the bone
microarchitecture of the historical sample. While Pb was observed
on most canal surfaces, only two osteons were completely enriched
with Pb (Fig. 2.2 and 2.4). Many of the osteons also had evidence of
lead localized in cement lines or individual lamellae (Fig. 2.1 and
2.3). The most striking variation was observed in the Sr distribution. Many entire osteons were enriched in Sr relative the
surrounding bone. In comparison, the XRF Pb map for the preEuropean contact sample was diffuse and uniform, and while it is
notable that the Sr map showed variable levels, the level of correspondence between the XRF patterns and the bone microarchitecture was not ideal due to poor sample preservation.
4. Discussion
The technique of matching histology with SR-XRF data provided
unique insight into the uptake of Pb and Sr in our sample. The close
correlation of the distribution of these elements with microstructural elements is compelling evidence of antemortem biogenic

Please cite this article in press as: Swanston, T., et al., Element localization in archaeological bone using synchrotron radiation X-ray uorescence: identication of biogenic uptake, Journal of Archaeological Science (2012), doi:10.1016/j.jas.2012.01.041

T. Swanston et al. / Journal of Archaeological Science xxx (2012) 1e5

Fig. 1. SR-XRF Spatial Maps. Histological image (A.) Highlighting regions of interest depicted in Fig. 2. The periosteal surface faces right. Corresponding XRF spatial maps of Ca in
yellow (B.), Pb in red (C.) and Sr in blue (D.). Since the detector was placed 45 to the right, surfaces facing right exhibit increased intensity due to less self-absorption while surfaces
facing left have a reduced intensity. This artefact is most noticeable for Ca on all larger canals and the periosteal surface. It is reduced in Pb and Sr but still evident on the periosteal
surface. The colour scale indicates the normalized XRF intensity but the values do not reect the true concentration.

deposition within the bone. As such, the results from this preliminary analysis strongly support the conclusion that this individual
from 18th century Antigua was exposed to Pb during life. Evidence
of biogenic Pb is not surprising considering the time frame (A.D.
1793e1822) of the cemetery and the knowledge that many items
that contained Pb were utilized during that time, including tableware, distillation equipment, and water catchment systems
(McCord, 1953; Wittmers et al., 2002).
Just as this approach can provide evidence for antemortem
uptake, we believe it may help to identify diagenetic changes in
subsequent applications. The burial environment of archaeological
bone is a source of trace elements, and it is known that these
elements can be incorporated during post-mortem alteration
(Koenig et al., 2009, Lebon et al., 2010, Reiche et al., 2010, Trueman
et al., 2008). Research on the fossilization of bone has demonstrated
recrystallization of apatite (Koenig et al., 2009). Indeed, trace
elements in pore water have been found to adsorb to bone mineral
during the fossilization process (Trueman et al., 2011). Previous LAICP-MS studies on fossilized bone have also shown the uptake of
rare earth elements with patterns that indicate the extent of
diagenesis (Koenig et al., 2009, Trueman et al., 2008).
Post-mortem modication of bone chemistry is initially
concentrated on the bone surfaces (Trueman et al., 2008). For
example, ubiquitous Pb penetrating all surfaces would be

suggestive of post-mortem contamination. The labelling of nearly

all canal surfaces with Pb in our sample could be interpreted as
evidence of diagenesis. That said, the localized labelling of surface
lamellae combined with the fact that some canals exhibit no
labelling is, again, suggestive of biogenic uptake. Notably,
a previous publication has indicated the presence of element rings
(Sr, Fe, Zn, and Cu) that were concentrated in the Haversian canals
of the bone samples that were being analyzed (Kuczumow et al.,
2010). Elevated levels of trace elements near canal surfaces could
represent the slowing rate of formation as the canal narrows (Yen
and Shaw, 1977). Alternatively, it could represent subsequent
deposition of trace elements into bone that is in closest proximity
to the osteons blood supply. Indeed, bone hydroxyapatite is known
to passively take up lead (Meirer et al., 2011). It is unclear if a similar
process occurs during life but this could explain, in part, the Pb
distribution we observed. Further work, possibly involving animal
models, is needed to fully elucidate the nature of trace element
uptake into bone on this scale.
Variation in Sr within this individuals bones is suggestive of
seasonal or geographic changes in diet. Sr shares similar chemical
properties with Ca as they are both alkaline earth elements but Sr is
absorbed from the digestive system less efciently (Papworth and
Patrick, 1970). Any Sr that is absorbed is deposited in the bone
where it can substitute for Ca (Burton and Wright, 1995). Sr has

Please cite this article in press as: Swanston, T., et al., Element localization in archaeological bone using synchrotron radiation X-ray uorescence: identication of biogenic uptake, Journal of Archaeological Science (2012), doi:10.1016/j.jas.2012.01.041

T. Swanston et al. / Journal of Archaeological Science xxx (2012) 1e5

Fig. 2. Details of regions highlighted in Fig. 1. Each set includes a Sr map (blue), a Pb map (red), a composite Sr and Pb map and a histological image (grey). Region 1 depicts an
osteon with a heterogeneous Sr distribution and Pb labelling of the cement line. Region 2 depicts an osteon which is enriched in Sr and Pb. This osteon was higher in Pb than any
other in the specimen and had two bright rings indicative of lamellae formed during peak exposure. Region 3 contains a pair of osteons. The superior exhibits strong Pb labelling of
the canal surface while the inferior shows labelling of the cement line with no enrichment at the canal surface. Region 4 contains an irregularly shaped osteon which is enriched in
both Sr and Pb. Notably, the canals of this structure also show little Pb enrichment, particularly the upper portion. Scale bar (centre) is 250 microns long.

been used as a paleodietary indicator because Sr/Ca ratios have

been found to vary between trophic levels (Sillen, 1986), although
the variability is not a strict trophic level effect but a reection the
actual dietary Sr/Ca ratios (Burton and Price, 2001). It was previously published that Sr was homogeneous throughout an archaeological long bone based on studies using XRF and a scanning
electron microscope (Lambert et al., 1983). With our new Sr data, it
is now clear that with the high sensitivity of synchrotron radiation,
the Sr can be visualized as having been differentially incorporated
into the bone during the remodeling process. It is intriguing to
consider that pre-contact individuals from Antigua exhibited

higher bulk levels of Sr when compared to subsequent European

colonists. It is possible that the Sr enriched osteons observed in the
individual associated with the Royal Naval Hospital cemetery were
formed during his time in the Caribbean and the lower strontium
levels in other osteons reect formation elsewhere. Similarly, dietary variation during extended periods on military ships could also
account for this variation. Testing such hypotheses is beyond XRF
alone but the technique employed here could be combined with
isotopic analysis by laser ablation in the future.
While SR-XRF has great potential, it is not without limitations.
Access to synchrotron beamtime is always limited. From a technical

Please cite this article in press as: Swanston, T., et al., Element localization in archaeological bone using synchrotron radiation X-ray uorescence: identication of biogenic uptake, Journal of Archaeological Science (2012), doi:10.1016/j.jas.2012.01.041

T. Swanston et al. / Journal of Archaeological Science xxx (2012) 1e5

perspective, scanning a highly absorbing sample, such as bone,

results in artifacts related to self-attenuation of uorescent
photons. While these artifacts were an issue for our analysis, they
only completely obscured spatial distributions at the periosteal
surface. Admittedly this surface is of primary interest with respect
to diagenesis. The issue of self-attenuation also complicates quantitative analysis as different elements with different photon energies will reect sampling of differing depths. We intend to pursue
methods to correct for this artefact in the future.
5. Conclusions
We employed the XRF capability of the VESPERS beamline at the
Canadian Light Source to obtain SR-XRF data and this was matched
with bone histology. The correlation of these two methods
provided compelling evidence of the antemortem deposition of Pb
and Sr in our historical sample. This approach, alone and combined
with additional techniques such as laser ablation, hold great
potential to overcome some conventional limitations faced by trace
element analysis.
Acknowledgements
This research was supported in part by the University of Saskatchewan Presidents SSHRC Research Fund and the Lakehead
University SSHRC 4A Fund. We would like to thank the Canadian
Light Source and the CLS funding agencies.
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Please cite this article in press as: Swanston, T., et al., Element localization in archaeological bone using synchrotron radiation X-ray uorescence: identication of biogenic uptake, Journal of Archaeological Science (2012), doi:10.1016/j.jas.2012.01.041