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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 131:343–351 (2006)

Osteoporosis in a Population From Medieval Norway


S. Mays,1* G. Turner-Walker,2 and U. Syversen3
1
Ancient Monuments Laboratory, English Heritage Centre for Archaeology, Eastney, Portsmouth PO4 9LD, UK
2
School of Cultural Heritage Conservation, National Yunlin University of Science and Technology, Touliou,
640 Yunlin, Taiwan (Republic of China)
3
Department of Intra-abdominal Diseases, Faculty of Medicine, Norwegian University of Science and Technology,
N7489 Trondheim, Norway

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.

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OSTEOPOROSIS IN MEDIEVAL NORWEGIAN POPULATION 345
TABLE 1. Summary statistics for BMDN and BMDW TABLE 2. Results of analysis of variance for BMDN and
at Trondheim1 BMDW vs. age at Trondheim1
BMDN BMDW Analysis of variance
Age-group N Mean SD Mean SD Significance Multiple
F-value of F comparison tests
Females
18–29 10 0.953 0.105 0.883 0.118 Females
30–49 44 0.783 0.097 0.636 0.115 BMDN 18.3 <0.001 All
50þ 11 0.702 0.097 0.532 0.114 BMDW 26.4 <0.001 All
Males Males
18–29 25 0.981 0.148 0.923 0.166 BMDN 6.1 0.004 18–29 vs. 30–49
30–49 29 0.886 0.117 0.713 0.143 18–29 vs. 50þ
50þ 9 0.828 0.101 0.603 0.146 BMDW 19.7 <0.001 18–29 vs. 30–49
1
18–29 vs. 50þ
BMDN, bone mineral density at femur neck; BMDW, bone
1
mineral density at Ward’s triangle; N, number of individuals. Multiple comparison tests, indication of between which age
Age in years. BMDN and BMDW in g cm2. groups significant differences (P < 0.05) in bone mineral density
lie by least significant difference statistic.
One femur from each individual was scanned using a
Hologic QDR-4500A bone densitometer (Hologic, Inc.,
Bedford, MA). Each femur was placed in a plastic box P < 0.001). In both sexes, age-related loss of BMD, mea-
containing dry rice as a soft-tissue substitute. The bone sured by comparison of levels in those aged 50þ years
was placed anterior-surface uppermost, so that the femo- with those aged 18–29 years, is greater at Ward’s triangle
ral neck lay flat, and the diaphysis was oriented parallel than at the femur neck (females: t ¼ 2.7, P < 0.02; males:
to the axis of the scanner. Measurements were made of t ¼ 2.86, P < 0.02). Loss of BMD at the femur neck is
bone mineral density (BMD) at the femur neck (BMDN) greater in females than in males (t ¼ 2.34, P ¼ 0.032).
and Ward’s triangle (BMDW). This protocol matches that The same pattern would be expected at Ward’s triangle,
used for the Wharram Percy femurs (Mays et al., 1998), but in the current data, the difference fails to reach sta-
but those were scanned using a Lunar DPX densitome- tistical significance (t ¼ 0.77, P ¼ 0.45).
ter (Lunar Corp., Madison, WI). Technical differences in There are, however, some differences between patterns
hardware and software mean that absolute values ob- seen in the Trondheim group and those in the modern
tained on equipment from different manufacturers can- reference data. In the modern reference data (Looker
not be directly compared (Genant et al., 1994; Hui et al., et al., 1995), adult males show sequentially lower BMD
1997; Boonen et al., 2003). For this reason, it is usual, in successive age groups. In the current male data, sig-
when conducting multicenter studies, to undertake nificant differences could only be demonstrated between
cross-calibration of equipment. To this end, nine femurs the 18–29-year group and the other two age groups.
were scanned in both machines. Scatterplots suggested a That no significant difference was found between the
linear relationship between results from the two ma- 50þ and 30–49-year age groups may reflect the small
chines. Relationships were expressed as linear regres- sample size (N ¼ 9) for the male 50þ group and the ob-
sion equations, which were used to convert the Lunar servation that, because less age-related loss of BMD is
values into their Hologic equivalents. Hui et al. (1997) expected in males than in females, larger sample sizes
described a similar standardization procedure for bone would be needed in males in order for patterns to reach
mineral density measurements using patients. statistical significance. Interestingly, a significant differ-
A skeletal inventory was compiled for 91 (44 males ence was found in female BMD between the 18–29 and
and 47 females) of 128 individuals whose femurs were 30–49 age groups. However, in the modern reference
scanned, and the presence of fractured elements was data (Looker et al., 1995), femur BMD differences be-
noted using careful gross inspection. Factors beyond our tween females in these two categories were minor. This
control precluded recording these aspects on the remain- phenomenon, which implies pre- or perimenopausal bone
ing 37 skeletons. For the females, those not examined loss in the medieval women, was noted previously for
for fractures resembled those that were, in terms of both Wharram Percy females (Mays et al., 1998). Turner-
age at death and BMD, so this was unlikely to bias the Walker et al. (2000, 2001) suggested that this may reflect
results. However, by chance, few of the males examined the effects of high parity and relatively late weaning of
for fractures were aged over 50 at death; this inhibited offspring, which may have been customary in medieval
the investigation of fractures in elderly men. times (Shahar, 1990; Benedictow, 1992; Richards et al.,
2002). In modern populations, minor reductions in BMD
may occur during pregnancy and lactation, but are
RESULTS quickly recovered (Kohlmeier and Marcus, 1995; Kalk-
Bone mineral density warf and Specker, 1995; Laskey and Prentice, 1999).
Turner-Walker et al. (2001) suggested that, in medieval
The results for BMDN and BMDW are shown in Table 1. times, recovery of bone mass following pregnancy and
Many aspects of the results are broadly consistent with lactation may have been slowed by poor maternal nutri-
patterns that might be expected on physiological grounds tion. This may explain the apparent greater loss of bone
on the basis of comparison with modern European refer- during the reproductive years in the medieval women,
ence data (Looker et al., 1995, 1998). Analysis of variance although other as yet unidentified factors may also be
(Table 2) indicates that both sexes show a significant age- involved.
related decline in both BMDN and BMDW. In the study Comparison of the Trondheim BMD results with those
group as a whole, BMD is greater in males than in from Wharram Percy is shown in Table 3. Intergroup
females (BMDN: t ¼ 5.21, P < 0.001; BMDW: t ¼ 4.01, comparisons using t-tests reveal no evidence for differ-

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346 S. MAYS ET AL.
TABLE 3. Mean values for BMDN and BMDW for three age classes at Trondheim and Wharram Percy1
BMDN BMDW
Trondheim Wharram Percy Trondheim Wharram Percy
Females
18–29 0.953 (100%) 0.951 (100%) 0.883 (100%) 0.877 (100%)
30–49 0.783 (82.2%) 0.808 (85.0%) 0.636 (72.0%) 0.642 (73.2%)
50þ 0.702 (73.7%) 0.724 (76.1%) 0.532 (60.2%) 0.535 (61.0%)
Males
18–29 0.981 (100%) 0.988 (100%) 0.923 (100%) 0.910 (100%)
30–49 0.886 (90.3%) 0.934 (94.5%) 0.713 (77.2%) 0.811 (89.1%)
50þ 0.828 (84.4%) 0.826 (83.6%) 0.603 (65.3%) 0.625 (68.7%)
1
Figures in parentheses are values expressed as percentage of those in young adult (18–29-year) age groups. Wharram Percy data
(N ¼ 54 females, 75 males) are values from Mays et al. (1998) transformed to Hologic values, using following equations: Hologic
BMDN ¼ 0.789126 3 Lunar BMDN þ 0.081403; Hologic BMDW ¼ 0.934769 3 Lunar BMDW  0.140822. For methods used to gen-
erate these conversion algorithms, see text. Age in years. BMDN and BMDW in g cm2.

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

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OSTEOPOROSIS IN MEDIEVAL NORWEGIAN POPULATION 347
TABLE 4. Frequency of fracture types at Trondheim
by age and sex1
Age group
18–29 30–49 50þ
Females
‘‘Osteoporotic fracture’’ 0 2 3
Other fracture 0 5 0
No fracture 8 24 5
Males
‘‘Osteoporotic fracture’’ 0 1 1
Other fracture 3 3 0
No fracture 21 13 2
1
Age in years. ‘‘Osteoporotic fracture’’, Colles’ fracture or verte-
bral compression fracture. Other fracture, individuals lacking
‘‘osteoporotic’’ fractures but showing fractures in other skeletal
elements.

TABLE 5. BMD values at Trondheim for those showing


osteoporotic fractures and those without osteoporotic fractures,
but showing other types of fractures
BMDN BMDW
N Mean SD Mean SD
Females
With osteoporotic 5 0.620 0.146 0.458 0.130
fracture
With other 5 0.804 0.085 0.628 0.083
fracture
t-test t ¼ 2.43, P ¼ 0.04 t ¼ 2.47, P ¼ 0.04
Males
With osteoporotic 2 0.789 0.028 0.537 0.113
fracture
With other 6 0.968 0.147 0.833 0.090
fracture
t-test t ¼ 1.63, P ¼ 0.15 t ¼ 3.84, P ¼ 0.01
Fig. 1. First through fourth lumbar vertebrae, Sk115
(female, aged 50þ years). There is a healed compression frac-
ture of L1. Femur BMDN and BMDW are 0.671 g cm2 and
0.559 g cm2, respectively. Each is approximately 2.7 standard the age of individuals when fractures occurred, save that
deviations below young adult female mean. they were not confined to the oldest age groups in either
males or females. In order to determine whether osteo-
work are likely representative of in vivo values, rather porotic-type fractures are collectively associated with low
than being artifacts of diagenesis. We therefore infer bone mass, and hence are distinct from other fractures,
that the Trondheim population resembled the Wharram it needs to be demonstrated that individuals with osteo-
Percy people, in terms of both age-dependent loss of porotic-type fractures show lower BMD than those with
BMD and peak BMD values. other fracture types. Results of this comparison (Table 5)
show that, for females, individuals with osteoporotic-type
fractures do indeed show lower BMD than those with
Fracture patterns other fracture types. This supports the idea that the for-
mer are distinct from other fracture types and are as-
The classic fractures of osteoporosis occur at the hip sociated with osteoporosis, as they are in modern popula-
(neck of the femur), wrist (Colles’ fracture of the distal tions. For males, too few show osteoporotic-type frac-
radial metaphysis), and spine (compression fracture of tures to permit firm conclusions in these respects.
thoracic or lumbar vertebral bodies) (Resnick and A comparison of the frequency of osteoporotic fractures
Niwayama, 1988). In the Trondheim population, 18 of 91 in females over age 50 years at Trondheim and at Whar-
individuals examined showed a combined total of 30 ram Percy is given in Table 6. Sample sizes for males
fractured bones (out of a total of 10,245 bones exam- over age 50 years were too small to permit a worthwhile
ined). Of these, seven individuals showed eight fractures comparison for males. All three cases of osteoporotic
in skeletal locations consistent with osteoporotic frac- fracture in the Wharram Percy women were vertebral
ture. Three females and two males showed a combined compression fractures; there were no hip or wrist frac-
total of six vertebral compression fractures (Fig. 1), and tures. Table 6 indicates a higher prevalence of osteopor-
two females each showed a Colles’ fracture. There were otic fractures among Trondheim females over age 50,
no hip fractures. The distribution of these ‘‘osteoporotic and Fischer’s exact test indicates that the difference is
fractures’’ and fractures of other types with respect to statistically significant (P ¼ 0.04). This is not an artifact
age and sex is shown in Table 4. of differential representation of skeletal elements. Rates
All osteoporotic-type fractures were firmly healed. of recovery of distal parts of the radii, and of thoracic/
Other than that they did not occur immediately prior to lumbar vertebral bodies, are similar in females aged over
death, there is little further that can be said concerning 50 at the two sites (the frequencies of these elements,

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348 S. MAYS ET AL.
TABLE 6. Prevalence of osteoporotic fractures among females is of recent origin. However, given the rather modest
over age 50 years at death at Trondheim and Wharram Percy1 sample size and the limitations of skeletal aging tech-
Trondheim Wharram Percy niques, this interpretation must be made with caution.
Despite the evidence for age-related bone loss in the
With osteoporotic fracture 3 3 femur neck area, there were no hip fractures in the
Without osteoporotic fracture 5 41
Trondheim material. In this respect, the study popula-
Total 8 44
tion appears to resemble other paleopopulations: frac-
1
Wharram Percy data from Mays (in press). tures of the femur neck generally seem to have been
rare in the past (Agarwal and Grynpas, 1996; Brickley,
2000). Precise reasons for the dearth of hip fractures at
expressed as percentages of those expected if all skele- Trondheim are unclear, but some possibilities can be
tons were complete, are 63% and 87%, respectively, for
suggested. In modern populations, the frequency of hip
Trondheim; for Wharram Percy, the figures are 75% and fracture only begins to rise in women after about age
79%, respectively). Nor does the greater prevalence of 75–80 years, and is associated with so-called type II or
osteoporotic fractures in the Trondheim women appear senile osteoporosis. By contrast, the frequency of wrist
to reflect a generally higher frequency of trauma in the and vertebral compression fractures begins to rise imme-
Trondheim females, as prevalences of nonosteoporotic diately after menopause; they are a feature of postmeno-
fractures (i.e., fractures of elements other than the verte- pausal or type I osteoporosis. Wrist and vertebral com-
bral bodies and distal radial metaphyses) are similar at
pression fractures outnumber hip fractures in modern
the two sites (frequency for Trondheim females ¼ 5/47 populations until about age 75 years (Buhr and Cooke,
individuals ¼ 10.6%; for Wharram Percy females, 18/140 1959; Black and Cooper, 2000). It has been suggested
¼ 12.9%). that, in paleopopulations, too few people generally sur-
vived into advanced old age for hip-fracture prevalence
DISCUSSION to be appreciable (Brickley, 2000), and medieval docu-
A problem in comparing age-related bone loss in osteo- mentary evidence (discussed in Mays, 1996) supports this
porosis between skeletal populations is that even if simi- suggestion. Hip geometry influences resistance of the fe-
lar aging techniques are used, their imprecision means mur neck to fracture, i.e., a longer femoral neck is associ-
that we cannot precisely age-match samples. The prob- ated with increased risk of fracture (Faulkner et al.,
lem is most acute in the 50þ-year age category: if the 1993; Cummings et al., 1994). Recent work (Chumley
mean age of the 50þ cohort was greater at one site than et al., 2004) suggests that femur necks are shorter at
at the other, this would seriously prejudice comparisons. Wharram Percy than in a modern reference sample, so
Because the question of the age composition of the 50þ- perhaps this is a factor in the dearth of hip fractures in
year cohort is not one which can be resolved osteologi- that population. This aspect has yet to be investigated in
cally, previous approaches with other paleopopulations the Trondheim group. Other as yet unidentified factors
(Mays, 1996, 2006) involved modeling the likely age may also be involved in the lack of hip fractures at Trond-
structure of the 50þ group using documentary evidence. heim.
However, there appear to be no documentary demo- Although hip fractures were absent, Colles’ fracture
graphic data which would allow this for medieval Trond- and compression fractures of the vertebral bodies were
heim. Although there is no a priori reason to suppose identified in the study material. For females, an associa-
that the age distribution of the over-50 cohort is very dif- tion was demonstrated between low BMD and fractures
ferent at Trondheim and Wharram Percy, there is no at the wrist and spine, but too few men showed these
direct evidence to confirm this. fracture types to permit firm conclusions for males. Loss
One could suggest that the similarity in BMD between of BMD in osteoporosis is clinically silent. It only has
the medieval Wharram Percy and Norwegian popula- health implications when it leads to fractures. Hip
tions examined in this work might, given the substantial fractures are the principal contributor to the morbidity
evidence for a genetic influence on BMD (Prentice, 2001; and excess mortality associated with osteoporosis (Chri-
Rapuri et al., 2004), simply reflect a Norse contribution schilles et al., 1994). However, wrist and vertebral frac-
to the Wharram Percy gene pool, making the two groups tures may also give rise to chronic pain, and are to some
rather similar genetically. Viking raids on England extent associated with long-term residual disability
started in the late 8th century, and by the 9th century (Ettinger et al., 1992; O’Neill et al., 2001). The presence
Norse settlement began, most particularly in northeast of these fractures, and their association with low BMD,
England (Richards, 1991). Craniometric analyses (Mays, show that osteoporosis would have had a significant
in press) indicate that although crania from medieval health impact for women in medieval Trondheim.
York resemble those from medieval Norway, the crania Despite the lack of any indication of differences in hip
from Wharram Percy do not. This suggests that the BMD between Trondheim and Wharram Percy, there
Norse contribution to the Wharram Percy population was evidence for a difference in fracture patterns, with
was probably minor, at least compared with that to me- Colles’ fractures and vertebral compression fractures
dieval York (where there is other archaeological and his- being collectively more frequent in older females from
torical evidence for a strong Norse presence; Hall, 1994). Trondheim. It might be suggested that in the Trondheim
In this light, it seems unlikely that a Norse contribution population, hip BMD has been not a good indicator of
to the Wharram Percy population could explain why spine or wrist BMD, and hence the present results do
BMD at Wharram Percy is similar to that in medieval not exclude the possibility of differences in BMD at the
Trondheim. skeletal sites showing fractures. Although further study
The observation that no difference in BMD was of the Trondheim material would be required to settle
detected between the two medieval study samples in the this conclusively, clinical studies suggest that it is
current work might suggest that the difference in BMD unlikely. Hip BMD has been shown to be correlated with
observed today between Norwegian and UK populations spine and wrist BMD (Deng et al., 1998; Augat et al.,

American Journal of Physical Anthropology—DOI 10.1002/ajpa


OSTEOPOROSIS IN MEDIEVAL NORWEGIAN POPULATION 349
1998), and low hip BMD is a predictor of fracture risk at almost invariably be smaller than those typical in epide-
the wrist and spine (Dey et al., 2000; Kanterewicz et al., miological studies on living subjects, with a consequent
2002). lack of statistical power in the paleopathological work.
Although BMD is probably the most important indica- Although differences between archaeological groups which
tor for risk of osteoporotic fracture (Miller and McClung, are confirmed by adequate inferential statistical tests
1996; Ammann and Rizzoli, 2003; Moyad, 2003), other can be considered robust, the status of negative findings
factors also play a part. The role of gross bone geometry will tend to be somewhat equivocal. The extent to which
has already been referred to, but various microstructural this is a problem for comparative work on paleopopula-
features of living bone, sometimes collectively known as tions will clearly depend on the subtlety of the pattern-
‘‘bone quality,’’ may deteriorate in osteoporosis and influ- ing we are trying to detect. Interpopulation BMD differ-
ence bone fragility (Grynpas, 2003). These features com- ences today can be quite marked: variation in femur-
prise bone microarchitecture, mineralization, and me- neck BMD between different European populations is
chanical properties, and these in turn may be influenced such that the mean value in the population with the low-
by bone turnover, which is a factor in the efficiency with est BMD is only about 86% of that in the group with the
which fatigue-damaged bone is renewed (Schnitzler and highest (Lunt et al., 1997). Although the UK is not at
Mesquita, 1998). Bone quality has yet to be investigated the extreme end of the spectrum, the mean femur-neck
in the Trondheim remains. A further factor affecting BMD for females over age 50 from Oslo is only 91% of
fracture prevalence is exposure of older individuals to that for women over age 50 from northern England
risk of skeletal trauma, particularly through falls. (Lunt et al., 1997). Differences of this degree are poten-
Colles’ fracture occurs a result of a fall onto an out- tially detectable not only with the very large sample
stretched hand (Vogt et al., 2001). In those with very se- sizes of modern epidemiological studies, but also with
vere osteoporotic bone loss, most often those in advanced the more modest samples customarily available to paleo-
old age, vertebral compression fractures may occur with pathologists. This indicates the value of paleopathologi-
negligible trauma, such as lifting a trivial object or sneez- cal work in determining whether some of the interpopu-
ing. However, in most cases, significant trauma is re- lation differences which exist in BMD today also existed
quired to induce a fracture. Causes are generally a fall or in past European populations.
stumble, or heavy lifting (Old and Calvert, 2004). There The greater frequency of osteoporotic fractures at medi-
is no reason to suspect a greater frequency of heavy lift- eval Trondheim than at Wharram Percy echoes the higher
ing among Trondheim women than among those from frequency found in Norwegian populations today. The
Wharram Percy; indeed, given the generally higher activ- degree to which this represents some inherent difference
ity levels that were inferred for the Wharram Percy between populations and/or living environments is
women compared with coeval urban females (Mays, in unclear. It is suggested here that the pattern may, to some
press), one might, if anything, expect that the reverse extent, reflect the fact that the Norwegian medieval group
should be the case. It may be that frequency and type of came from an urban environment where there was a
falls differed between the two groups. In the rural envi- greater likelihood of fracture when falls occurred because
ronment of Wharram Percy, Mays (1996) suggested that of the greater frequency of hard surfaces, and from a re-
falls, when they occurred, were generally onto grass, gion with a colder climate so that falls due to slippery con-
earth, or mud, and that these yielding surfaces tended to ditions underfoot were probably more frequent. Although
absorb energy on impact, helping to minimize fracture the lower BMD seen in modern Scandinavian populations
risk. In a more urban environment, such as at medieval compared with other European groups must be implicated
Trondheim, cobbled or stone surfaces were likely more in the higher rates of osteoporotic fractures in Scandina-
frequent, and falls onto such surfaces might more often via, it was suggested that cold climate might also be a
be expected to result in fractures for those (most often, el- contributory factor (e.g., Rogmark et al., 1999). Although
derly females) whose skeletal integrity was compromised this is controversial (Lofthus et al., 2001), there is evi-
by loss of BMD. Climatic differences between Trondheim dence that osteoporotic fractures of a type which generally
and Wharram Percy mean that in Trondheim, slippery occur in an outdoor setting do show winter peaks in occur-
conditions caused by ice or snow would be more frequent, rence in Norway today (Hove et al., 1995).
making falls more likely, and compact ice would form a Despite the above, reasons for the elevated prevalence
surface of similar hardness to stone or cobbles for many of fractures in modern Norwegian populations remain
weeks of the year. incompletely understood. Given the constraints on paleo-
pathological work imposed by the nature of skeletal sam-
ples, understanding differences in earlier populations is
CONCLUSIONS likely to prove even more challenging. However, in the
The results of the current study suggest that both current case, further work on trabecular bone quality,
sexes at medieval Trondheim showed age-related loss of cortical bone status, and femur-neck morphology in the
BMD. For females, this appears to have rendered the Trondheim material, to match the studies done on the
skeleton sufficiently fragile to predispose to fractures at Wharram Percy population (Mays, 1996; Agarwal et al.,
the wrist and spine. 2004; Chumley et al., 2004; Rossi, 2004), would help shed
The Trondheim population appeared to resemble the further light on any differences in osteoporosis between
Wharram Percy people, both in terms of age-dependent the two groups.
loss of BMD and peak BMD values. This may suggest
that the difference in BMD observed today between Nor-
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