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Bone strontium: calcium ratios and duration of breastfeeding in a
Mediaeval skeletal population
Simon Mays *
Ancient Monuments Laboratory, English Heritage Centre for Archaeology, Fort Cumberland, Eastney, Portsmouth PO4 9LD, UK
Received 11 January 2002; received in revised form 23 May 2002; accepted 20 August 2002
Abstract
This work is an investigation of the value of bone strontium:calcium ratios in the study of duration of breastfeeding in earlier
human populations. The study material comprised human skeletal remains of Mediaeval date from England. Investigation of
diagenesis suggested that bone Sr:Ca ratios preserved a biogenic signal. Statistical analysis indicated significant age-related
patterning in bone Sr:Ca ratios in the juvenile cohort. Duration of breastfeeding estimated from infant bone Sr:Ca ratios was
concordant with that inferred from an earlier study of nitrogen stable isotope ratios from the same population. The value of bone
Sr:Ca data for studying weaning practices in earlier human populations is discussed.
2003 Elsevier Science Ltd. All rights reserved.
Keywords: Sr:Ca ratio; Bone; Weaning; Human; Wharram Percy
1. Introduction
In most cultures, babies are breastfed from birth, but
at some point other foods are introduced into the diet,
supplementing and eventually replacing breast milk, a
process known as weaning. Duration of breastfeeding
may have important implications for population dynam-
ics. Because lactation suppresses ovulation, duration of
breastfeeding is a major determinant of fecundity in
societies lacking effective artificial methods of contra-
ception. In addition, the immunity provided by breast
milk and the avoidance of early contact with potentially
contaminated food and drink has meant that histori-
cally, societies, which practiced regular breastfeeding
have shown lower infant mortality and morbidity than
those in which breastfeeding was rare or its duration
curtailed [68].
Recently, there has been considerable interest in
studying infant feeding practices in earlier populations
[29]. A number of studies have utilised bone chemistry to
investigate duration of breastfeeding in ancient times.
Most (e.g. Refs. [12,24,28,50,59,60]) have used bone-
stable isotopes, particularly those of nitrogen. Breast
milk is enriched in nitrogen-15 compared with mostpost-weaning foods and this is reflected in the infants
bones. However, another chemical technique, measure-
ment of infant bone strontium (Sr):calcium (Ca) ratios,
has also been used to shed light on weaning practices in
ancient times.
Strontium and calcium share similar chemical prop-
erties, and the behaviour of Sr and Ca in biological
systems has been extensively studied, principally in the
1950s and 1960s as a result of concern over the biologi-
cal effects of radioactive Sr-90 produced by atmospheric
nuclear tests. A number of aspects of the behaviour of Sr
and Ca render bone Sr:Ca ratios useful for investigatingancient weaning practices. Strontium is absorbed less
efficiently from food stuffs than is Ca, and a greater
proportion of Sr is excreted, so that Sr:Ca ratios in living
tissues are less than in the diet [8]. Most of the bodys
strontium is located in the skeleton [58], and there is a
firm relationship between the Sr:Ca ratio in diet and
in the bones of the consumer [9,14,48]. In human adults,
the relationship between dietary and bone Sr:Ca levels,
the bonediet Observed Ratio (ORbonediet), appears to
be about 0.18 [51]. In lactating women, the OR milkdietis
somewhat less than this at about 0.1 [38]. Sr:Ca ratios
in foetal tissues are lower than in maternal tissues, the* Tel.: +44-2392-856-779; fax: +44-2392-856-701.
Journal of Archaeological Science 30 (2003) 731741
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ORfoetusmother is about 0.5 [8]. These latter two obser-
vations imply preferential transport of Ca with respect
to Sr across the mammary gland during lactation, and
during pregnancy across the placenta to the developing
foetus, and laboratory studies support this [23,32]. More
recent work [33,53] has elucidated this further, suggest-
ing that whilst there is active placental and mammarygland transfer of Ca, the transfer of Sr simply follows
concentration gradients. The studies of Krachler et al.
[33] and Rossipal et al. [53] appear consistent with
previous work in that they suggest somewhat higher
Sr:Ca ratios in maternal sera than in umbilical cord sera
or colostrum, although these authors did not statistically
analyse the patterning in Sr:Ca ratios. In any event, it is
clear that milk has a low Sr:Ca ratio compared to most
other foods [52].
The interpretation of infant bone Sr:Ca values is
complicated somewhat by the fact that the ability of
the gastro-intestinal system to discriminate against
strontium develops with age, only reaching adult levels
at about 810 years old [51]. Age-related changes in
bone Sr:Ca ratios may therefore be expected in infants
and children due both to the increasing discrimination
against strontium absorption and to the dietary changes
of weaning. The precise form of the plot of Sr:Ca ratio
against age is affected by a number of variables, particu-
larly timing and duration of weaning, however, in
general, one might expect fairly low Sr:Ca ratios in
neonatal infants and the breastfed, then a rise reflecting
the introduction of solid foods of higher Sr:Ca ratio,
followed by a steady reduction as the guts ability to
discriminate against strontium develops so that eventu-ally the bone Sr:Ca ratio resembles to that seen in adults
[63]. The ORbonedietis known for immature humans at
different ages [51] so that dietary Sr:Ca ratios can be
estimated from bone values.
Although the potential of bone Sr:Ca ratios for the
investigation of weaning in palaeopopulations was rec-
ognised nearly 20 years ago, long before the nitrogen
isotope technique was applied, to date, few Sr:Ca studies
of weaning have been published [19,26,63]. In part, this
reflects the general move away from bone trace-element
studies for investigating ancient diets, which has oc-
curred since about the mid-1980s in the face of thegrowing realisation both of the pervasiveness of dia-
genetic chemical change in bone mineral, and of the
complexity of the physiological determinants of trace-
element concentrations in biological tissues [56,64].
The present study is an investigation of the value of
the Sr:Ca method for estimating the duration of breast-
feeding in an archaeological population.
2. Materials and methods
The human skeletal material for this study came from
the deserted Mediaeval village of Wharram Percy,
England [3,4]. The burials date mainly from AD 10th
to 16th century, and represent interments of ordinary
peasants who lived at the village of Wharram Percy or
elsewhere in this rural parish. This material was selected
for a number of reasons. The assemblage contains large
numbers of juvenile skeletons, permitting study of a
larger sample of immature individuals than has beenpossible in previous bone Sr:Ca investigations of wean-
ing, facilitating statistical validation of results. A nitro-
gen isotope study of duration of breastfeeding in this
population [44,50] has previously been conducted, al-
lowing comparison of results using the two different
techniques. The soil conditions at the site make the
skeletal material a promising substrate for bone trace-
element studies. The burials were inserted into calcare-
ous soil overlying cretaceous chalk. Unfortunately, no
soil samples are available from the graves themselves,
but analyses of samples from various parts of the site
indicate that local soils are alkaline, pH ranging from
7.3 to 8.3 [1,30]. Acidic conditions favour dissolution of
hydroxy-apatite [37], so skeletal material buried in an
alkaline soil environment is likely to be preferable for
trace-element work.
The strategy for the present work is as follows.
Firstly, attempts will be made to demonstrate that the
level of diagenesis in the study material is likely to be
sufficiently slight so that a biogenic bone Sr:Ca signal
can be discerned. Secondly, any age-related patterns in
Sr:Ca ratios will be described and attempts will be made
to validate them using statistical techniques. Thirdly,
ORbonedietdata, derived from Sr-90 studies on modern
subjects [51], will be used to estimate dietary Sr:Ca ratiosand, hence, to make inferences about weaning practices.
Bone samples were taken for analysis from 50 imma-
ture skeletons, ranging in age at death from neonatal to
17 years. Samples from 50 adult (18+ years) skeletons
were also taken; these provide a base line with which to
compare the juvenile cohort. Compact bone rather than
trabecular bone was chosen for analysis; the latter
was avoided as its large surface area renders it more
vulnerable to diagenesis [18,34].
Samples consisted of diaphysial bone from the femur
or humerus. Approximately 12 g of bone was removed
using a hack-saw. In each sample, periosteal and endo-steal surfaces were removed by scraping to a depth of
12 mm to remove soil contaminants, which may accu-
mulate on the surfaces of buried bone [35]. Samples were
then cleaned in an ultrasonic cleaner and dried to
constant weight at 110 (C. They were then pulverised in
an agate ball-mortar.
All elemental determinations were carried out in
the Mineralogy Department at the Natural History
Museum, London. Samples were analysed for a spec-
trum of trace and bulk elements using inductively
coupled plasma atomic emission spectroscopy (ICP
AES). In this article, only Sr, Ca and phosphorus (P)
S. Mays / Journal of Archaeological Science 30 (2003) 731741732
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results are reported. Approximately 500 mg aliquots of
powdered bone (accurately weighed) were digested in a
mixture of concentrated nitric and perchloric acids and
the resulting solutions made up to 50 ml for analysis.
Analytical grade reagents, or better, and de-ionised
water were used throughout. The ICP instrument (an
ARL 3410 Minitorch system) was calibrated using solu-
tions prepared from commercial single element stand-
ards. Under the instrumental operating parameters used,
the detection limits for Sr, Ca and P in the bones were
0.5, 150 and 100 ppm (parts per million), respectively.
Replicate analyses of test solutions showed the precision
of the analytical procedure to be better than 1.5%. The
accuracy of the method was tested by analysing a
standard reference material, H-5. The results obtained
were in good agreement with the published data and are
presented in Table 1.
In whole bone from archaeological contexts, concen-
tration of trace and bulk elements mainly or entirely
residing in the mineral fraction will vary according to
the amount of organic material surviving in the speci-
mens. This dilution of element concentrations by the
variable amount of organics preserved is generally anunwanted source of variability in the data. Destruction
of the organic component by ashing at elevated tempera-
ture has frequently been used to circumvent this problem
in studies of archaeological bone. However, exposure of
bone to high temperatures may lead to losses in some
elements [13,20]. The preliminary step of ashing the
samples was therefore avoided in the current study.
Instead, the weight of the organic component was
estimated from the bone nitrogen content and sub-
tracted from the whole to give an estimated weight for
the mineral part. Elemental concentrations were then
expressed relative to this value. The purpose here was toenable comparison of levels of individual elements in the
buried bone from Wharram Percy with values in modern
bone reported with respect to the mineral component.
This procedure will, of course, leave Sr:Ca ratios un-
affected. Whole-bone nitrogen was determined using a
CHN elemental analyser. A separate sub-sample of bone
(815 mg, accurately weighed) was used. The detection
limit for nitrogen was 3000 ppm. Nitrogen content of
whole bone reflects accurately the organic content, pro-
vided, the nitrogen level is greater than about 0.4% by
weight [46], as was invariably the case in the current
material. Collagen makes up approximately 8590% of
the organic component of bone [27], and for the pur-
poses of providing an approximate estimate of the
weight of organics, it was assumed that the composition
of the entire organic component resembled that of
collagen. The proportion of nitrogen by weight in bone
collagen was taken as 0.1591 [15].
For the juveniles, age at death was determined usingdental development [57]. Adult age at death was esti-
mated using dental wear, calibrated using the juvenile
part of the assemblage [45]. Sex in adults was determined
using dimorphic aspects of the pelvis and skull [5].
No attempt was made, for the present purposes, to
determine sex in juveniles.
3. Results
Summary statistics for the results in juveniles and
adults are given in Table 2. Lilliefors tests [11] provided
no evidence for deviations from normality for any of theparameters listed in Table 2.
3.1. Diagenesis
There are a number of techniques for evaluating
diagenesis in elemental composition of ancient bones
[40, p. 192]. Rather than relying on a single technique,
most researchers use a combination to build up a picture
of diagenetic change in the material under study (e.g.
articles in Ref. [55]). This is the approach used in this
study.
The Ca:P ratio has frequently been used as a generalindicator of the preservational integrity of the mineral
fraction of buried bone, following Ref. [62]. Discrepan-
cies from values characteristic of living bone are taken as
indicative of diagenesis (although it should be born in
mind that Ca:P ratios are, at best, only proxy measures
of the integrity of bone Sr:Ca ratios [7]). Mean Ca:P
ratios in modern bone lie approximately in the range
2.212.27 (calculated from Ref. [22]: Table 1). The
Wharram Percy mean Ca:P ratios (Table 2) resemble
modern values.
If element levels in buried bones are outside physio-
logical levels seen in modern bone, then this suggests
Table 1
Measurements on standard reference material animal bone H-5
Sr
(ppm)
Ca
(%)
P
(%)
Reference
100 21.4 10.3 This work (mean of four replicate analyses)
96 21.2 10.2 IAEA, Vienna, Austriaproposed values
Table 2
Summary statistics for elemental analyses
Adults (N50) Juveniles (N50)
Mean SD Mean SD
Sr (ppm) 249.6 54.7 306.8 42.6
Ca (%) 36.2 1.3 35.9 1.1Ca:P 2.27 0.10 2.28 0.11
Sr:Ca (104) 6.92 1.57 8.55 1.20
Bone Sr and Ca concentrations expressed with respect to the
mineral component (see text)
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diagenesis in the ancient specimens [49]. Mean bone Sr
levels reported in studies of modern adults generally lie
in the range 100300 ppm [22,25,58,65,66], mean Ca
levels in the range 3640% [22,47,51]. Table 2 indicates
that the Wharram Percy data are consistent with these
values. Concentrations of essential elements (those
which fulfil vital physiological functions) would be ex-pected to be normally distributed, reflecting the fact that
their concentrations are homeostatically regulated [36].
There is evidence that some non-essential trace elements
show a lognormal distribution in human populations
[36]. However, although it is a non-essential trace ele-
ment, this does not appear to be the case for Sr in bone,
for which a normal distribution has been reported [65].
The distributions of Sr and Ca in the Wharram Percy
group resemble those in modern samples in that they do
not deviate from normality.
For bone buried in calcareous soils, such as at
Wharram Percy, contamination with calcite is a concern
[2]. However, evidence suggests that in the present
material, this problem may not be great. There is no
sign of increased calcium concentrations. Work on the
Wharram Percy bone using X-ray diffraction [42] and
carbonate:phosphate ratios (Ref. [46]: Table 4) provides
no evidence for elevated calcite levels.
Evaluation of histological sections of Wharram Percy
bone by scanning electron microscopy [43,46,67] indi-
cates that preservation of histological detail is poor.
Grupe and Piepenbrink [21] suggest, from laboratory
experiments, that this type of alteration in the histologi-
cal structure of buried bone, which is generally accepted
to be caused by the activities of soil-dwelling micro-organisms, may potentially cause changes in elemental
composition. However, the degree to which the existence
of such changes in archaeological material can be used
as an indicator of diagenetic changes in particular
elements is unclear. Schutkowski et al. [61] found that
there was no correlation between the state of histological
preservation of early Mediaeval bones and their mineral
integrity (as measured by the Ca:P ratio), and they felt
that the histological preservation of specimens was not a
good guide to the validity of element data derived from
them. The fact that bone Sr and Ca levels at Wharram
Percy remain within modern ranges, despite the poorhistological state of the material, is consistent with
this. In addition, preliminary results on Wharram Percy
bone [67] suggest that although biodeterioration due to
invasion by micro-organisms may result in localised
dissolution and re-precipitation of bone mineral, for
calcium at least there is little net loss or gain. The poor
preservation of Wharram Percy bone at the histological
level does not necessarily mean poor preservation of
biogenic trace or bulk element signals.
Although the evidence is not fully conclusive, it seems
reasonable from the above discussion to suggest that
diagenetic changes in Sr and Ca levels may be suf-
ficiently slight to permit a biogenic signal to be dis-
cerned. On this basis, we proceed to the next phase of
the analysis, the investigation of age-related trends in the
Sr:Ca data.
3.2. Age-related variation in Sr:Ca ratios
Analysis of variance and t-tests revealed no evidence
for any significant variation in Sr:Ca ratios with age or
sex in the adult cohort. Variation in Sr:Ca ratios with
respect to age in juveniles is depicted in Fig. 1.
Fig. 1 suggests that infants and young children show
higher Sr:Ca ratios than older individuals, and that there
is a steady decline in Sr:Ca ratios from about 2 years so
that by the age of about 8 years, values resemble those of
adults. Statistical analyses confirm the validity of these
patterns (Tables 3 and 4).
A high Sr:Ca ratio in young children, with a subse-
quent decline to adult values, is expected on physiologi-
cal grounds, given the increasing discrimination against
Sr absorption with respect to calcium with age in the
immature gut [51]. The presence of such a trend rein-
forces the idea that biogenic signals are preserved in the
present Sr:Ca data. However, there is no evidence of a
particularly low Sr:Ca ratio in very young infants, a
pattern which might have been expected in those exclu-
sively breastfed, given the low Sr:Ca ratio of human
breast milk.
3.3. Inferring age at weaning
The ORbonediet values from Ref. [51] were used toestimate dietary Sr:Ca ratios. The results are plotted
against age in Fig. 2. A dietary Sr:Ca ratio of about
1103 is indicated for those under about 1 year. This
appears to rise steeply between about 1 and 2 years so
that by the latter age it reaches a value of about
4103, which resembles the adult mean value of
3.8103.
The question arises as to how realistic these inferred
dietary Sr:Ca ratios are likely to be, given what is known
of Mediaeval diet. Wharram Percy was a poor agrarian
community primarily based on arable farming, but with
some livestock. Peasant diet in Mediaeval times waschiefly made up of foods derived from cereals; animal fat
and protein were at a premium [17]. At Wharram Percy,
it is known that the sea-food component of diets was
minor [39]. Runia [54] measured Sr and Ca in experi-
mentally grown cereal crops, and found ratios ranging
between 3103 and 6103. There is variation in
Sr:Ca ratios in crops according to the soils upon which
they are grown, but if Runias figures can at least be
taken as a very general guide (and the obser-
vation that they resemble figures given for Sr:Ca ratios
in cereal-based diets in different parts of the world [8,52]
suggests that they can), the dietary Sr:Ca ratios inferred
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Fig. 1. Strontium:calcium ratios (104) in immature individuals from Wharram Percy. Mean values according to age groups are superim
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for adults and older juveniles at Wharram Percy appear
reasonable. Given an ORmilkdiet of approximately 0.1
[38], our estimated dietary Sr:Ca ratio of 3.8103 in
adults gives an approximate Sr:Ca ratio of 3.8104
in breast milk. This is in approximate agreement with
values found for human milk in modern studies (ap-
proximately 1.43.4104 [33,52]). However, the in-
ferred dietary Sr:Ca ratios of young infants are greater
than this value, by a factor of at least three for those
under 1 year (Fig. 2).
Fig. 2 indicates a fairly rapid rise in dietary Sr:Ca ratiobetween 1 and 2 years, suggesting that weaning likely
occurred at around that time, so that by the latter age
breast milk had ceased to make a significant contribution
to diet. It is difficult to be more precise about timings
because of uncertainties over the rapidity with which
dietary change in infants is reflected in bone Sr:Ca ratios.
A further caveat is that because these results were gener-
ated on those who died in childhood, they may not be
fully representative of those who survived to older ages.
At this juncture, it is useful to make comparison
between the inferences made from the present results
and those made from previous work on nitrogen stable
isotope ratios at Wharram Percy [44,50]. The nitrogen
isotope results plotted against age are reproduced in Fig.
3. The stable isotope ratios are elevated in young infants,
with a peak at about 1 year. There is a rapid decline
between about 1 and 2 years, indicating weaning, so that
by the latter age, values resemble those in older children
and adults, showing that breast milk was no longer
making a significant contribution. The concordance of
the isotopic and Sr:Ca data indicating weaning between
1 and 2 years of age is striking.
It is worth returning to the observation, made earlier,
of the rather high Sr:Ca ratios in infants under about
1 year of age. The nitrogen data (Fig. 3) indicate thatindividuals in this age range were not yet weaned, but
nevertheless the Sr:Ca ratios are higher than might be
expected with a wholly breast-milk diet. A possible
explanation may be that at Wharram Percy, maternal
milk was being supplemented with small amounts of
foods of higher Sr:Ca ratio even in very young infants.
Mediaeval documentary evidence suggests the use of
cereal-based foods or animal milk to supplement and
eventually replace breast milk in the weaning process
[16]. The inclusion of animal milk would be difficult to
detect using the nitrogen isotope technique, as wouldsupplementation with modest amounts of cereal-based
foods because of their low-protein content. Herbivore
milk appears to have a somewhat higher Sr:Ca ratio
(about 2.41041.5103 [8,52]) than human milk,
and the Sr:Ca ratio of cereal-based foods is up to an
order of magnitude greater [54]. Bone Sr:Ca ratios are
disproportionately influenced by foods with a high cal-
cium content, so that high calcium foods will tend to
mask, in bone Sr:Ca signals, the contribution to diets of
foods lower in calcium [6]. Calcium levels in human milk
are about 200300 ppm [33,38], in cows milk about
10001200 ppm [52] and in cereal grains about 300600 ppm [54]. Given that the calcium levels in the latter
two foods are somewhat greater than that in human
milk, their signals ought not to be masked by the
breast-milk signal. Supplementation of infant diets with
animal milk or cereal foods should therefore be poten-
tially detectable in the bone Sr:Ca technique by elevation
in Sr:Ca ratios in infants.
Studies on other Mediaeval European skeletal
material [19,26] resemble the present one in that they
have also found somewhat greater Sr:Ca ratios in young
infants than might have been expected given breastfeed-
ing alone. These authors ascribed this phenomenon to
early supplementation of breast milk with other foods,
specifically animal milk. It may be that a similar expla-
nation applies at Wharram Percy. A close clustering of
data-points for infants under 1 year is observed (Fig. 2),
so if this explanation is correct, supplementation must
have been undertaken almost from birth and it must
have been a general practice, at least as far as the infants
sampled were concerned, rather than representing an
unusual feeding regime. If it occurred, such an early
supplementation would have had potentially damaging
consequences in that it would expose the infant to poten-
tial sources of infection associated with foods other than
breast milk at an unnecessarily early age. This practicedoes not accord with most Mediaeval documentary
sources on infant feeding, which do not recommend
supplementation of breast milk with other foods imme-
diately from birth, but at some later time, generally when
Table 3
Infant or young child (age:birth3 years) Sr:Ca ratios (104)
N Mean SD tadult vs infant/young child p
32 8.85 1.07 6.58
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Fig. 2. Dietary strontium:calcium ratios (104) in immature individuals from Wharram Percy estimated from bone Sr:Ca ratios using the OR bonediet daSr:Ca value for adults is superimposed.
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Fig. 3. Rib 15N for immature individuals from Wharram Percy aged from birth to 17 years (N65). Mean values for foetal material (aged 2839 weeksuperimposed. Data from Ref. [44].
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providing background data on technical aspects of ICP
AES. Two anonymous reviewers are thanked for perti-
nent comments, which have improved this article.
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