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KEY WORDS femur; paleopathology; bone mineral density; fractures; dual X-ray absorptiometry
ABSTRACT Modern populations from Norway and in the Norwegian and the English group were similar.
England differ in their experience of osteoporosis, the Among females, the prevalence of osteoporotic fractures
former showing lower bone mineral density (BMD) and a was greater in the Norwegian than in the English popu-
higher fragility fracture rate. The aim of the present lation. The BMD results suggest that differences in
work was to investigate whether this was also the case BMD between English and Norwegians are of recent ori-
during the Middle Ages. Age-dependent loss of BMD in gin, although given the fairly modest sample sizes, fur-
the proximal femur was assessed using dual X-ray ther work is needed to confirm this. Reasons for the
absorptiometry (DXA) in male and female adult skele- greater prevalence of osteoporotic fractures in women in
tons from a cemetery in the medieval town of Trond- the Norwegian skeletal series are unclear, but the colder
heim, Norway. Fracture prevalence was also investi- climate and greater frequency of hard surfaces may have
gated. Results were compared with those previously meant that falls were more frequent, and when they
reported for a skeletal series from Wharram Percy, a occurred, were more likely to result in fractures than in
deserted medieval village in England. Results indicate the rural English group. Am J Phys Anthropol 131:343–
that peak BMD and patterns of age-related loss of BMD 351, 2006. V 2006 Wiley-Liss, Inc.
C
Osteoporosis in a condition in which there is a reduc- eral density is about 91% of that in the UK (Lunt et al.,
tion in bone mass and microstructural deterioration of 1997). The reasons for these patterns are incompletely
bone tissue. This results in increased skeletal fragility understood, but both genetic and environmental factors
and increased risk of fracture (Christodoulou and Cooper, are likely to play a part (Meyer and Johnell, 1997; Nel-
2003). Osteoporosis is associated with advancing age in son and Villa, 2003).
both sexes, but skeletal fragility is greater in elderly The importance of osteoporosis today has stimulated
women than in elderly men. In women, a principal cause interest in its occurrence in earlier populations, and
of bone loss is the hormonal changes which accompany studies have been conducted on excavated skeletal re-
menopause. Although the causes of osteoporosis in men mains from around the world (Agarwal and Grynpas,
are less well-understood, it appears that, as in women, 1996; Mays, 1999). No paleopathological work on the dis-
an age-related decline in sex hormones plays a major ease in earlier Norwegian populations has yet been car-
role (Anderson et al., 1998). In both sexes, various ex- ried out, despite the observation that the severity of
traneous factors, such as cigarette smoking, calcium de- osteoporosis in modern Norwegians makes this of com-
ficiency, and sedentary lifestyle, have been held to exac- pelling interest. The current study is a first investigation
erbate the disease (Ross, 1996; Nguyen and Eisman, of osteoporosis in ancient skeletal remains from Norway.
1999). It is of interest, from the point of view of understand-
In most modern populations, osteoporosis (or more ing present-day differences in osteoporosis in European
exactly, its attendant fractures) is a major cause of mor- populations, to investigate whether such differences
bidity and mortality (Randell et al., 1995), but there is have arisen recently, or whether they have their roots in
marked interpopulation variation in the severity of the more ancient times. In the current context, this means
condition. Populations of European origin are among comparing the Norwegian results to another, coeval skel-
those most at risk for osteoporosis (Villa, 1994). How- etal series, from a region where today the severity of
ever, there is also considerable variation between differ-
ent European groups. Populations from Scandinavia
appear to be more at risk than those from other regions
*Correspondence to: S. Mays, Ancient Monuments Laboratory,
(Meyer and Johnell, 1997). Norwegian populations in English Heritage Centre for Archaeology, Fort Cumberland, East-
particular show high frequencies of osteoporotic fracture ney, Portsmouth PO4 9LD, UK.
(Falch et al., 1985; O’Neill et al., 1996; Lofthus et al., E-mail: simon.mays@english-heritage.org.uk
2001; Kanis et al., 2002) and low levels of bone mass
(Lunt et al., 1997; Falch and Meyer, 1998; Gjesdal et al., Received 25 September 2005; accepted 14 February 2006.
2004). For example, osteoporotic fractures are between
approximately one-and-a-half and twice as frequent DOI 10.1002/ajpa.20445
among Norwegians than in the UK (O’Neill et al., 1996; Published online 21 April 2006 in Wiley InterScience
Lofthus et al., 2001; Kanis et al., 2002), and bone min- (www.interscience.wiley.com).
C 2006
V WILEY-LISS, INC.
344 S. MAYS ET AL.
osteoporosis is lower than in Norway. A number of pub- analyses of fracture patterns and bone mineral density
lished studies investigated osteoporosis in earlier Euro- at Wharram Percy were carried out by teams headed by
pean populations (reviewed in Mays, 1999). However, one of us (S.M.), the same methods and protocols can
differences between studies in methodologies, both for readily be applied to the current material.
measuring bone mineral status and for estimating age at
death (Mays, 1999; Brickley and Agarwal, 2003), gener-
ally make direct comparisons problematic. The current METHODS
study aims to circumvent this problem by adopting me- In the paleopathological study of age-progressive con-
thods which resemble, as closely as practicable, those ditions such as osteoporosis, the choice of skeletal aging
used in earlier work on another European paleopopula- technique is critical. In the current work, the Trondheim
tion, from medieval England. adults were aged using dental wear. For populations
The overall aims of the current work are to character- showing significant wear on the dentition, assessment of
ize age-related bone loss and fracture patterns in a medi- degree of wear on the molar teeth has been shown to be
eval population from Norway, and to compare the find- a reliable technique for adult age estimation (Tomenchuk
ings with a population from medieval England. The aim and Mayhall, 1979; Richards and Brown, 1981; Kieser
of the comparison is to address the question of whether, et al., 1983; Zhang and Ji, 1988; Song and Jia, 1989;
as is the case today, the medieval Norwegian people Richards and Miller, 1991; Song et al., 1991; Li and Ji,
show a lower bone mass and higher frequency of osteo- 1995; Kim et al., 2000; Mays, 2002), and has been shown
porotic fracture than do their coeval English counter- to outperform other skeletal age indicators (Johnson,
parts. This may shed light upon whether current differ- 1976; Lovejoy, 1985; Constandse-Westermann, 1997).
ences have arisen recently, perhaps due to modern life- Rate of molar wear varies between different populations,
style factors, or whether they also existed for ancient chiefly as a result of differences in diet and food-prepara-
groups whose lifeways were very different from those of tion techniques. However, examination of the permanent
today, which might imply some inherent difference be- molars of juvenile individuals whose ages can be accu-
tween British and Norwegian populations. Reference will rately estimated using dental development enables esti-
be made to biocultural context, to help interpret any pat- mation of the rate of wear in the specific population
terns which may emerge. under study, using the methodology of Miles (1963).
Briefly, this method involves using the age at eruption of
MATERIALS the various molars to relate the degree of wear to the
functional age of the tooth in the juvenile cohort. By a
The skeletal material for the present study comes from process of extrapolation from this baseline, the age at
a series of excavations carried out in central Trondheim death is estimated for the entire adult cohort, starting
during the 1970s and 1980s, principally on the church- with the youngest and working through to those individ-
yard of St. Olav’s church (Anderson and Göthberg, uals showing the heaviest wear (discussion in Hillson,
1986). The collection comprises 928 skeletons dating to 1996, p. 239–242; Mays, 1998, p. 60–62). Juveniles in
the period 1100–1600 AD. Trondheim is situated on the the Trondheim assemblage were used to calibrate the
Norwegian coast. The mean annual temperature is ap- wear rate in that population, using the methodology of
proximately 58C, and there are an average of 122 days per Miles (1963). Dental-wear aging using the technique of
year with a minimum temperature below 08C (Norwegian Miles (1963) has been specifically tested on known-age
Meteorological Institute, 2005). During the medieval pe- individuals, and its reliability confirmed (Kieser et al.,
riod, the population of Trondheim was in the low thou- 1983). The Wharram Percy adults were aged using
sands. It was an important town in medieval Norway, dental wear (Mays, 1996), calibrated using juveniles from
and had many characteristics of an urban settlement: it that population according to the technique of Miles
had major ecclesiastical and secular administrative func- (1963). Many workers using molar wear to age adult skel-
tions within the Kingdom of Norway, and was a center etal remains from archaeological sites use 10-year age
for trade and for the manufacture of goods (Danielsen categories. However, for the present purposes, a conserva-
et al., 1995). tive strategy was adopted, whereby individuals were sim-
The comparative group, from the medieval village of ply classified as young adults (ca. 18–29 years), middle
Wharram Percy, England, dates primarily from the adults (ca. 30–49 years), or older adults (ca. 50þ years).
10th–16th centuries AD. Wharram Percy is situated in This matches the strategy used for Wharram Percy
northeast England, about 20 miles northeast of York. It (Mays, 1996).
is located, at about 150 m above sea level, in the York- Sex was determined in the Trondheim material using
shire Wolds, an area of chalk upland. The climate is dimorphic aspects of the pelvis and skull (Brothwell,
milder than in Trondheim, with an annual mean temper- 1981). The same techniques were used at Wharram Percy
ature of approximately 88C, and an average of 59 days (Mays, 1996).
per year with a minimum temperature below 08C (UK The technique used to evaluate bone mineral status
Meteorological Office, 2005). In the medieval period, the was dual X-ray absorptiometry (DXA) of the proximal fe-
great majority of inhabitants of the village, and of the mur. The criteria for acceptance of a bone for study were
sparsely populated rural parish in which it lay, were or- as follows: femurs should be complete and undamaged,
dinary peasants engaged primarily in agricultural pro- and show no external signs of soil erosion in the area to
duction. Osteoporosis is particularly well-characterized be scanned; there should be no sign of soil infiltration
in that group; various aspects were investigated, includ- into the bone interior on X-ray; all femoral epiphyses
ing bone mineral density (Mays et al., 1998; McEwan should be fused; and skeletal survival should permit age
et al., 2004), cortical thickness (Mays, 1996; Mays et al., at death to be estimated in the categories described
1998), bone microarchitectural features (Agarwal et al., above, and permit unambiguous sex determination. Us-
2004; Rossi, 2004), fracture patterns (Mays, 1996, in ing these criteria, femurs from 128 adults (63 males and
press), and hip geometry (Chumley et al., 2004). Because 65 females) were suitable for inclusion in the study.
ences between the two populations in peak bone density dence of intrusive calcite. Turning to the Trondheim ma-
(taken to be that in the 18–29-year age groups). They terial, as with Wharram Percy, few mineral inclusions
also provide no great evidence for differences in patterns are visible in the microstructure under scanning electron
of age-related decline in BMD. The only suggestion of a microscopy. Unlike Wharram Percy, no bulk chemical
difference is the slightly earlier loss of BMD at Ward’s analyses or X-ray diffraction spectra are available for
triangle in the Trondheim males: BMDW in the 30–49- the skeletal remains. This makes it difficult to exclude
year group is lower in the Trondheim than in the Whar- the possibility of minor soil infiltration. However, the fol-
ram Percy males (t ¼ 2.5, v ¼ 57, P < 0.05). lowing observations suggest that, even if present, this is
When interpreting BMD results from buried bone, the unlikely to affect BMD significantly. The Wharram Percy
possibility that diagenetic change (particularly, physical specimens showing gross soil infiltration were measured
contamination of bone by soil infiltration and microstruc- for BMD, even though they were subsequently excluded
tural alteration of bone) might influence results should from analysis. BMD values were found to be little differ-
be considered. In the current context, one might reason- ent from radiographically uncontaminated specimens
ably suggest that, since the broad age- and sex-related (Mays et al., 1998). This indicates that even a degree of
patterning in BMD both at Wharram Percy (Mays et al., physical contamination sufficient to be visible in plain
1998) and at Trondheim resembles in general terms that film radiographs had no great effect on BMD. Slight,
in modern reference data, this implies that postdeposi- radiographically invisible soil infiltration is therefore
tional changes in BMD values are slight. It seems highly unlikely to greatly affect BMD values.
improbable that some complex pattern of differential dia- Microscopic study (Mays et al., 2001; Turner-Walker
genesis between different sex and age groups could have and Syversen, 2002; Turner-Walker et al., 2002) indicated
fortuitously reproduced these patterns. Nevertheless, it that the Wharram Percy bones show advanced microstruc-
was thought prudent to consider further the possibility tural diagenesis (of the type described by Hackett, 1981;
of diagenetic change, as any differential alterations Hedges et al., 1995), whereas those from Trondheim are
between the two sets of material could potentially preju- minimally altered. The question is therefore whether the
dice the comparisons which are a major focus of this diagenetic alterations in the Wharram Percy material
paper. Physical contamination of bone with soil, and have affected BMD. Several observations are pertinent
microstructural diagenesis, are each considered, both for here. Both the absolute BMD values and age-related
Wharram Percy (Mays et al., 1998) and for Trondheim. trends are similar to those at Trondheim (Table 3), despite
At both Wharram Percy and Trondheim, all femurs the fact that the latter are well-preserved microstructur-
were radiographed, and specimens showing evidence of ally; were diagenetic effects a great influence on BMD, we
soil infiltration were excluded from analysis. Nonethe- would have expected differences in BMD between two col-
less, one might still suggest that minor contamination lections with such different microstructural preservation.
with soil particles, too subtle to be visible on plain film Examination of histological sections of the Wharram
radiographs, may be present and may potentially affect Percy bones (Turner-Walker and Syversen, 2002) showed
BMD values. Investigation of bone microstructure was that microstructural diagenesis resulted in discrete areas
carried out using scanning electron microscopy on bone of hyper- and hypomineralization, visible as areas of dif-
from both sites (Mays et al., 2001; Turner-Walker and ferent tonal values under scanning electron microscopy.
Syversen, 2002; Turner-Walker et al., 2002). At Whar- Elemental analysis by energy-dispersive X-ray spectrome-
ram Percy, there was little evidence of physical contami- try on areas of the bone section exhibiting different tonal
nation in microstructural features such as Haversian values suggests that, although diagenesis has caused dis-
canals. The soils at this burial site are calcareous (Abra- solution and reprecipitation of bone mineral, movement of
hams, 1977). If significant physical contamination from bone mineral in this process appears to have been a highly
the soil was a problem at Wharram Percy, then we localized phenomenon, and bulk calcium content is little
would expect to find elevated bulk calcium levels in the changed (Turner-Walker and Syversen, 2002). That bulk
bones. This is not the case: calcium levels, measured calcium levels in the Wharram Percy bones resemble mod-
using inductively coupled plasma atomic emission spec- ern values was confirmed by ICP-AES (Mays, 2003). This
trometry (ICP-AES), resemble those in modern bone implies that bulk bone density should be little affected by
(Mays, 2003). Consistent with this, X-ray diffraction the microstructural diagenesis seen in that material.
(Mays, in press) and analysis of carbonate:phosphate The above considerations suggest that the BMD values
ratios (Nielsen-Marsh and Hedges, 2000) provide no evi- in both sets of archaeological material considered in this