HOMO - Journal of Comparative Human Biology 61 (2010) 178190

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HOMO - Journal of Comparative
Human Biology
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Demographic, temporal and environmental effects on the
frequency of cribra orbitalia in three Early Medieval
populations from western Slovakia
Radoslav Be nu s
a,
, Zuzana Obertov
a,b
, So na Masnicov
c
a
Department of Anthropology, Comenius University, Mlynsk dolina B2, 84215 Bratislava 4, Slovak Republic
b
Institute of Pre- and Protohistory, Eberhard-Karls University, Palaeoanthropology, Rmelinstr. 23, 72070 Tbingen, Germany
c
Department of Criminalistics and Forensic Sciences, Academy of Police Forces, Sklabinsk 1, 83517 Bratislava 3, Slovak Republic
a r t i c l e i n f o
Article history:
Received 9 July 2008
Accepted 25 October 2009
a b s t r a c t
The frequency of cribra orbitalia was examined in Early Medieval
skeletal samples from Devn and Borovce (Slovakia). The effects of
environmental and socio-economic factors on the distribution of
orbital lesions are explored and discussed. The frequency of cribra
orbitalia was lowest in Devn-Hrad (11th12th c. A.D.), followed
by Devn-Za kostolom (9th c. A.D.) and Borovce (8thbeginning of
12th c. A.D.). The increased frequency of cribra orbitalia at Borovce
can be attributed to inadequate sanitation and increased pathogen
load at this rural site compared to urban Devn. Borovce (BO) sub-
adults displayed orbital lesions signicantly more frequently than
BOadults and sub-adults in the Devn-Za kostolom(FR) and Devn-
Hrad (DH) samples. Although the total mortality of sub-adults did
not differ between the sites, BO sub-adults with cribra orbitalia
showed a considerably higher mortality. Their counterparts from
FR and DH showed similar mortality patterns irrespective of the
presence of orbital lesions. As in most reference samples, no sig-
nicant sex differences in the frequency of cribra orbitalia were
observedinBO, DHandFR. However, a considerably increasedmor-
tality was observedinyoung males fromDevn-Hradirrespective of
thepresenceof orbital lesions. This ndingcanbeattributedtotheir
involvement in violent conicts. Reference data from Medieval
Central European skeletal samples suggest that an increased occur-
rence of cribra orbitalia was associated withcrop failures, migration
and interpersonal conicts. These factors favour the spread of and

Corresponding author. Tel.: +421 2 602 96 472; fax: +421 2 654 29 064.
E-mail address: benus@nic.fns.uniba.sk (R. Be nu s).
0018-442X/$ see front matter 2010 Elsevier GmbH. All rights reserved.
doi:10.1016/j.jchb.2010.04.001
R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190 179
vulnerability to infectious diseases, which are considered to be the
major cause of iron deciency anaemia.
2010 Elsevier GmbH. All rights reserved.
Introduction
First described by Welcker (1888), cribra orbitalia refer to a sieve-like porosity of the orbital roof.
The skeletal changes develop as a result of hypertrophy and hyperplasia of the red bone marrow that
occur in response to an underlying anemic stimulus (Moseley, 1965).
A majority of researchers suggest that cribra orbitalia found in archaeological samples result from
iron deciency anaemia (e.g., Hengen, 1971; Mensforth et al., 1978; Stuart-Macadam, 1992, 1998).
As the name implies, iron deciency anaemia can be dened as a reduction below normal in levels
of haemoglobin and hematocrit in blood. This can occur for a variety of reasons including blood loss,
increaseddemands of growthor pregnancy, inadequate absorptionof iron, andnutritional deciencies
(e.g., El-Najjar et al., 1975; Steinbock, 1976).
The present study agrees with the statement by Mensforth et al. (1978:2), that the pathogenesis of
cribra orbitalia can best be understood in terms of the synergistic interactions between constitutional
factors, diet, and infectious disease. Several researchers mention the combination of factors such as
parasitic infestation, infectious diseases, and to a lesser degree inadequate nutrition as the most plau-
sible explanation for the development of iron deciency anaemia (e.g., Kent, 1986; Stuart-Macadam,
1992, 1998; Sullivan, 2005; Walker, 1986; Wapler et al., 2004).
The aim of the present research was to examine the frequency of cribra orbitalia in Early Medieval
skeletal remains from three Slovak sites Devn-Za kostolom, Devn-Hrad, and Borovce. The com-
parison focused on the age- and sex-specic distribution of orbital lesions, and the association
between the presence of these lesions and mortality patterns. In addition, comparisons with ref-
erence data on the frequency of cribra orbitalia in skeletal series of similar dates from Central
Europe were included. Moreover, historical records were consulted, and environmental and socio-
economic variables are explored that might explain the distribution of cribra orbitalia in these
samples.
Historical and archaeological background
Devn, with the ruins of an extensive fortication overlooking the conuence of the Danube and
Morava River, is situated just northwest of the Slovak capital city of Bratislava (Fig. 1). Archaeological
excavations at this site revealed settlement remains dated to the Later Stone Age (ca. 5000 B.C.), Latene
(400100 B.C.), and Roman Era (100500 AD) as well as to the Early Medieval (8th12th c. A.D.), and
particularly the Great Moravian (9th c. A.D.) period (Plach et al., 1990).
The sturdy Devn Castle obviously served as a shelter for Medieval peasants during military attacks.
Moreover, due to the convenient locationat the crossroads of two important trade routes the Danube
Fig. 1. Location of the examined burial sites on the map of Slovakia.
180 R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190
Route, which ran along the Danube River connecting Eastern and Western Europe, and the Amber
Route, which connected the Baltic and the Adriatic Sea the Devn site was predestined to become a
trading centre, and at times the residence of reigning families.
The Early Medieval Slavic cemetery at Borovce (8thbeginning of 12th c. A.D.) is situated 80kmNE
from Bratislava at the Vh River bank (Fig. 1). From an archaeological point of view, this burial site
is characterised by the greatest concentration of niche graves of the podmola type, and the north-
ernmost occurrence of niche graves of the tunnel type in Central Europe. Niche graves sporadically
occurred in Central Europe during the Roman Era and the Migration Period (Sta s skov-

Stukovsk,
2001). They were often found at nomadic cemeteries, and therefore linked to the Avar settle-
ment in present-day Slovak territory (

Stefanovi cov, 2002). The grave goods, particularly jewellery,

indicate the presence of a Slavic social upper class at the site (Sta s skov-

Stukovsk, 1997). In con-

trast to the Devn site, which was an urban trading centre, the Borovce site represents a rural
settlement.
The Early Middle Ages in Slovak territory are linked to the existence of the Great Moravian
Empire. This Slavic feudal state established in 833 A.D. extended over a territory on both sides of
the Morava River, including present-day Slovakia and the Czech Republic. During its existence the
Empire expanded into what are today parts of Hungary, Romania, Poland, Austria, Germany, Serbia,
Slovenia, Croatia and Ukraine (Havlk, 1992). The rulers of this Slavic state left behind a lasting legacy
in Central and Eastern Europe, especially due to inviting Constantinus the Philosopher and his brother
Methodius to share their religion, knowledge and experience with Slavic people, and who developed
the rst written form of the Old Slavonic language the Cyrillic alphabet, and translated the Gospel
into this language. This cultural progress stood in contrast with the turbulent times reected by the
construction of numerous fortied castles throughout the country. By the early 10th c. A.D., Great
Moravia was weakened by internal conicts and frequent wars with the Carolingian Empire, and was
ultimately overrun by Magyar invaders (

Stefanovi cov, 1989; Havlk, 1992).

Nevertheless, theexcavations of Great Moraviancastles showcontinuityof settlement andarchitec-
tural styleafter thedisintegrationof theEmpire, thus asignicant part of thelocal aristocracyremained
more or less undisturbed and their descendants became nobles in the newly formed Kingdom of
Hungary (Ku cera, 1974).
Skeletal samples and methods
The Devn-Za kostolom (FR) cemetery (9th c. A.D.) is located on the periphery of the Devn Castle
fortication (Fig. 2) and consists of 111 individuals: 38 males, 27 females, 10 adults of undetermined
sex and 36 sub-adults (015 years old). The Devn-Hrad (DH) burial site (11th12th c. A.D.) from
inside the fortication (Fig. 2) is represented by 215 individuals: 61 males, 68 females, 21 adults of
undetermined sex and 65 sub-adults.
The Borovce skeletal series (8th to the beginning of 12th c. A.D.) includes 451 individuals: 118
adult males, 142 adult females, 16 adults of undetermined sex, and 174 sub-adults (015 years old).
Since the internal chronology of the Borovce cemetery has not been established yet, it is currently
not possible to link individual interments with more precise burial spans. Nevertheless, the large
sample size of juveniles and the generally well-preserved skeletons, make the Early Medieval Slavic
population from Borovce unique in its ability to demonstrate the age- and sex-specic distribution of
pathological skeletal alterations, such as cribra orbitalia.
The skeletal samples from both Devn sites are housed at the Department of Anthropology
of the Comenius University in Bratislava. Both samples were subject to several previous analy-
ses (Be nu s, 1999; Be nu s et al., 1999a,b; Be nu s and Thurzo, 2001; Be nu s and Masnicov, 2002a,b;
Masnicov and Be nu s, 2002; Masnicov and Hanulk, 1999; Tibensk, 2006). The skeletal remains
from Borovce are deposited at the Department of Anthropology of the Slovak National Museum in
Bratislava. Ongoing research focuses on various aspects of skeletal and dental health in the Borovce
skeletal series (Domonko sov-Tibensk et al., 2006; Obertov, 2005; Obertov and Thurzo, 2004;
Obertov and Thurzo, 2008; Sta s skov-

Stukovsk et al., 2005;

Sef ckov, 2003;

Sef ckov et al.,
2001).
R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190 181
Fig. 2. Location of the Early Medieval cemeteries Za kostolom (FR) and Hrad (DH) at the Devn site.
Age and sex estimation of the Devn skeletal remains was undertaken by the senior author. Age and
sex of the Borovce individuals were determined by M. Thurzo and A.

Sef ckov. Standard morpholog-
ical criteria for the age and sex estimation were used following Ferembach et al. (1979), and Buikstra
and Ubelaker (1994). In this study, individuals aged 15 years and older are viewed as adults. Although
this age does not match the biological or modern-day sociological age limit for maturity, accord-
ing to the studies on Medieval social organization (e.g., Power, 1986; Shahar, 1990) 1519-year-old
individuals were sociologically treated as adults during this time period.
The skeletal remains of individuals with at least one intact eye socket were scored for the presence
of cribra orbitalia following the scale by Nathan and Haas (1966). Only osseous changes associated
with marrow hyperplasia were classied as cribra orbitalia; lesions of a periostotic nature that might
occur in the orbits due to scurvy or rickets (Ortner and Ericksen, 1997; Ortner and Mays, 1998; Ortner
et al., 2001) were not included in the analysis.
Frequencies of orbital lesions were calculated as the number of affected individuals (A) divided by
the number of observed individuals with preserved orbits (O). Statistical differences were analysed
by the
2
test (Yates corrected if appropriate) or Fishers exact test suitable for small sample sizes.
Palaeodemographic analysis was based on composite life tables, as described by Acsdi and
Nemeskri (1970). The mortality values (d
x
) were extracted from these tables and used in further
analysis. Mortality (d
x
) is calculated as the proportion of deaths in each age category from the total
number of deaths. Separate tables were constructed for individuals with and without orbital lesions.
182 R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190
Table 1
Frequencies of sub-adults with cribra orbitalia (with Fishers-test results).
Age (years) FR
a
DH
a
BO
a
Fishers exact test P
A/O
b
% A/O
b
% A/O
b
% FR/DH FR/BO DH/BO
01 0/2 0.0 1/10 10.0 10/20 50.0 1.0000 0.4805 0.0485
14 3/9 33.3 6/15 40.0 33/40 82.5 1.0000 0.0065 0.0057
59 4/11 36.4 6/17 35.3 25/30 83.3 0.9999 0.0066 0.0014
1014 0/2 0.0 0/4 0.0 12/14 85.7 0.0500 0.0049
a
FR: Devn-Za kostolom, DH: Devn-Hrad, BO: Borovce.
b
A: affected, O: observed.
Results
Palaeopathological analysis
The total frequency of cribra orbitalia was 26.6% in Devn-Za kostolom (FR), 25.8% in Devn-Hrad
(DH) and48.8%inthe Borovce (BO) series. The populationat Borovce was signicantly more frequently
affected than those from both Devn sites (
2
P
FR/BO
=0.0010 and
2
P
DH/BO
=0.0000, respectively).
Sub-adults (014 years old) and adults in both Devn samples displayed similar frequencies of orbital
lesions: 29.2% in FR sub-adults vs. 25.0% in adults, and 28.3% in DH sub-adults vs. 24.4% in adults.
In the BO sample, sub-adults with cribra orbitalia (76.9%) signicantly outnumbered the adults with
orbital lesions (34.7%; Yates
2
P=0.0000). Cribra orbitalia occurred signicantly more frequently
in BO 014-year-olds compared to their counterparts from both Devn sites (
2
P
FR/BO
=0.0000 and
P
DH/BO
=0.0000, respectively). Adults from DH showed orbital lesions less frequently than those from
BO (
2
P
DH/BO
=0.0441). No statistically signicant difference was observed between FR and BO, and
FR and DH adults.
FR and BO females showed a slightly higher frequency of cribra orbitalia than FR and BO males
(28.6% vs. 21.1% (FR) and 37.4% vs. 28.9% (BO), respectively), but the differences were non-signicant.
Aninverse patternwas observedinDHmales (24.3%) andfemales (14.7%), but again, the difference was
not statistically signicant. The comparison between males and females from these samples revealed
only one statistically signicant difference BO females showed cribra orbitalia more frequently than
DH females (37.4% vs. 14.7%; Yates
2
P=0.0218).
Among FR sub-adults the highest frequency of affected individuals was found at the age of 59
(36.4%) and 14 years (33.3%). In DH sub-adults, orbital lesions occurred most frequently at the age
of 14 years (40%) and 59 years (35.3%). At Borovce, the frequency of cribra orbitalia consistently
increased throughout the subadult age categories with a peak at 1014 years (85.7%). BO sub-adults
aged between 1 and 14 years were signicantly more frequently affected than their peers from both
Devn sites (Table 1).
For adults, the comparisons focus onsex differences inthe 2029-year-olds because of the common
suggestion that young females particularly those with cribra orbitalia experience a higher risk of dying
during the reproductive period (Stuart-Macadam, 1985; Sullivan, 2005). Twice as many FR and BO
2029-year-old females showed cribra orbitalia compared to their male counterparts (42.9% vs. 20.0%
(FR), and 36.8% vs. 16.7% (BO), respectively), but the differences were not statistically signicant. On
the other hand, young adult males from DH (42.1%) showed orbital lesions more frequently than
females from this site (9.1%; Fishers-test P=0.0265).
Palaeodemographic analysis
The mortality patterns in the total samples from Devn-Za kostolom (FR), Devn-Hrad (DH) and
Borovce (BO) were relatively similar, except for 01-year-old infants and 2029-years old adults. The
01-year-olds occurred more frequently in the BO sample compared to both Devn sites, while most
2029-year-olds died at Devn-Hrad (Fig. 3). At all three sites, the mortality of sub-adults (014 years
old) equaled approximately one-third of the total samples.
R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190 183
Fig. 3. Age-specic mortality (d
x
) in total samples by site.
The age-specic mortality of individuals with and without orbital lesions is depicted in Table 2.
The sub-adults with cribra orbitalia showed the highest mortality at the ages of 14 and 59 years.
At the FR site, 59-year-old (23.5%) died slightly more frequently than the 14-year-olds (17.6%);
this relation was reversed in the BO sample (19.8% vs. 15.8%). At DH, the affected sub-adults in these
two age groups died equally often (18.2%). In general, 14- and 59-year-old individuals with cribra
orbitalia showed a higher mortality than their unaffected counterparts in all three samples. However,
signicant differences were observed only in the BO sample, where 14- and 59-year-olds with-
out cribra orbitalia died less frequently than their affected peers (Yates
2
P=0.0000 and Yates
2
P=0.0002, respectively). At the age of 1014 years, affected BO individuals died still in relatively high
numbers, while inthe FRandDHsamples, no individuals withcribra orbitalia were observedinthis age
category.
The overall mortality of 2029-year-old individuals with orbital lesions (Table 2) was signicantly
higher at both Devn sites than at the BO site (Yates
2
P
FR/BO
=0.0006 and Yates
2
P
DH/BO
=0.0000,
respectively). In the DH sample, the mortality of 2029-year-olds without cribra orbitalia was also
signicantly higher compared to the unaffected BO individuals of the same age.
The sex-specic comparisons revealed that 2029-year-old males and females from Devn-Hrad
(DH) died signicantly more frequently than their peers from FR and BO (Table 3). In particular, the
mortality of DH males with cribra orbitalia was considerably increased, whereas the mortality of DH
Table 2
Mortality (d
x
) by age, site and presence of cribra orbitalia.
Age group (years) Cribra orbitalia present (%) Cribra orbitalia absent (%)
FR
a
DH
a
BO
a
FR DH BO
01 0.0 3.0 6.0 4.3 9.5 5.7
14 17.6 18.2 19.8 12.8 9.5 4.0
59 23.5 18.2 15.0 14.9 11.6 2.9
1014 0.0 0.0 7.2 4.3 4.2 1.1
1519 0.0 6.1 5.4 6.4 4.2 2.3
2029 35.3 36.4 6.6 19.1 32.6 13.1
3039 23.5 6.1 9.0 23.4 12.6 16.6
4049 0.0 9.1 13.8 10.6 9.5 21.1
5059 0.0 0.0 13.8 2.1 4.2 22.9
60+ 0.0 3.0 3.6 2.1 2.1 10.3
a
FR: Devn-Za kostolom, DH: Devn-Hrad, BO: Borovce.
184 R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190
Table 3
Mortality (d
x
) of the 2029 years old individuals by site, sex and presence of cribra orbitalia (with F-test results).
Sex/site FR
a
DH
a
BO
a
Fishers exact test P
n/N
b
% n/N % n/N % FR/DH FR/BO DH/BO
Males (total) 8/33 24.2 28/52 53.8 15/111 13.5 0.0079 0.1397
c
0.0000
c
Females (total) 8/19 42.1 41/60 68.3 21/135 15.6 0.0575 0.0056
c
0.0000
c
Males with cribra orbitalia 1/4 25.0 8/9 88.9 2/26 7.7 0.0517 0.3586 0.0000
Females with cribra orbitalia 3/4 75.0 2/5 40.0 7/46 15.2 0.5238 0.0218 0.2090
a
FR: Devn-Za kostolom, DH: Devn-Hrad, BO: Borovce.
b
n: number of deaths in the age class, N: total number of deaths.
c

2
test probability results, since the sample size was sufcient.
females with orbital lesions showed no signicant difference from that of FR and BO females. How-
ever, females from FR died signicantly more frequently at the age of 2029 years than BO females
(Table 3).
Comparative data
Data fromthe present study were compared with the literature on the frequency of cribra orbitalia
in Medieval skeletal samples from Central Europe. The reference data listing the frequency of cribra
orbitalia in the total sample, in both sexes, and in sub-adults and adults are summarised in Table 4.
Skeletal samples from Germany, Poland, Ukraine, Hungary, Croatia, Czech Republic and Slovakia are
included. The samples date from the 5th to the 14th century A.D.
In several studies, only the frequencies of orbital lesions in the total sample, in the sub-adult
or the adult sample are presented. Marcsik and Baglyas (1989) found 13.5% individuals with cribra
orbitalia in the total sample from Szeged-Makkoserd (8th c. A.D., Hungary). The frequency of orbital
lesions in adults from Medieval Poland was reported to be as follows: Cedynia (10th12th c. A.D.)
26.6% (Piontek et al., 2001), Milicz (12th14th c. A.D.) 37.0% (Bergman, 1988), and Ostrw Lednicki
(12th14th c. A.D.) 30.2% (Lubocka, 1999). Orbital porosity occurred in 88% of sub-adults (019 years
old) fromSchleswig (11th/12th c. A.D., Germany) (Hhne-Osterloh, 1989), in 85.9% of 015-year-olds
from Gruczno (12th14th c. A.D., Poland) (Piontek and Kozowski, 2002), and in 50.8% of sub-adults
(014 years old) from Stara Torina (Late Medieval, Serbia) (Djuri c et al., 2008).
The comparison revealed that the highest frequency of cribra orbitalia was found in samples from
the 5th8th century A.D. No signicant differences between males and females were observed. How-
ever, in most populations females showed somewhat higher frequencies of orbital lesions compared
to males. In general, orbital lesions occurred more frequently in sub-adults than in adults from the
same sample.
Discussion
In agreement with previous studies (e.g., Hengen, 1971; Mensforth et al., 1978; Stuart-Macadam,
1992), iron deciency anaemia is accepted as the most frequent cause of cribra orbitalia in the Early
Medieval skeletal samples from western Slovakia. Although some studies have emphasized iron de-
cient diets as the primary cause of the anaemia underlying cribra orbitalia (e.g., El-Najjar et al., 1975),
it has been recently shown that the aetiology of this condition can rather be retraced to an interaction
of several factors, including individual constitution, disease patterns, and diet (e.g., Hallberg et al.,
1970; Kent et al., 1994; Lallo et al., 1977; Mensforth et al., 1978; Ryan, 1997; Stuart-Macadam, 1992;
Woodruff, 1958). The latest technical advances enable the visualization of cribra orbitalia in living
subjects by computer tomography (Exner et al., 2004). These developments will hopefully soon lead
to a better understanding of the causative factors for the orbital lesions.
In several studies (e.g., Hengen, 1971; Kent, 1986; Stuart-Macadam, 1992; Walker, 1986), high
infection rates in a population were suggested to contribute signicantly to an increased occurrence
of iron deciency anaemia. Recent research into anaemia in chronic disease revealed a link between
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Table 4
Comparative data on the frequency of cribra orbitalia in Medieval skeletal samples from Central Europe with respective references.
Burial site Country Dating (century A.D.) Reference Frequency of cribra orbitalia (%)
Total Sub-adults Adults Adult
males
Adult
females
Devn-Za kostolom (FR) Slovakia 9th This study 25 26.9
a
23.8 20.0 25.0
Devn-Hrad (DH) Slovakia 11th12th This study 33.8 27.7
a
25.3 27.0 14.3
Borovce (BO) Slovakia 8thbegin 12th This study; Obertov and Thurzo
(2004); Obertov and Thurzo (2008)
48.8 76.9
a
36.6 30.5 39.2

Sebastovce Slovakia 7th9th Krlov et al. (1997) 50.0 74.1

b

Mal Kosihy Slovakia 10th11th Vondrkov (1994) 12.1 31.2
b
6.7 5.7 6.4
Mikul cice-Kostelisko Czech Republic 9th Velemnsk y (2000) 32.8 43.4
b
13.8 21.7 17.2
Doln V estonice-Na pskch (NP) Czech Republic 9thbegin 11th Jaro sov (2007) 14.5 24.8
b
5.8 11.2 11.7
Libice nad Cidlinou Czech Republic 9th11th Vyhnnek (1969) 11.0 9.2 2.3
Blina Czech Republic 10th13th Vyhnnek (1971) 9.6 2.6 9.0
Doln V estonice-Vysok zahrada
(VZ)
Czech Republic 12th Jaro sov (2007) 19.1 35.0
b
7.3 6.5 19.2
Lipove, Kazarovi ci, Luca,
Grigorovka, Bu cak (pooled)
Ukraine 10th12th Piontek et al. (2001) 55.2 51.5 59.3
Continental: Stari Jankovci,
Privlaka, Vinkovci (pooled)
Croatia 6th9th

Slaus (2008) 19.7 53.7
a
11.9 10.3 22.5
Adriatic: Velim, Rada sinovci,

Sibenik (pooled)
Croatia 7th9th

Slaus (2008) 32.5 61.4
a
20.7 13.3 18.8
Horb-Altheim Germany Mid 5thbegin 6th Obertov and Wahl (2007), Obertov
(2008)
31.1 50.0
a
29.8 26.9 34.3
Hemmingen Germany Mid 5thbegin 6th Obertov and Wahl (2007), Obertov
(2008)
60.0 80.0
a
56.7 68.8 52.6
Pleidelsheim Germany Mid 5thbegin 6th Obertov and Wahl (2007), Obertov
(2008)
52.3 100
a
40.0 38.1 65.2
Nusplingen Germany 5th8th Hengen (1971) 60.2 77.8
b
60.4 37.0 65.1
Neresheim Germany 5th8th Hahn (1993) 57.6 49.0
b

1519 years old individuals included in adults
a
or in sub-adults
b
.
186 R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190
decreased plasma iron levels and inammatory reactions (Weiss and Goodnough, 2005). Moreover,
parasites, such as hookworms, may cause chronic blood loss and thus, iron deciency anaemia due to
their attachment patterns in their host (Awasthi and Bundy, 2007; Cox, 1993; El-Shazly et al., 2005;
Gilles et al., 1964; Jrovec et al., 1977; Johnson, 2003; Layrisse and Roche, 1964; Lotfollahzadeh et al.,
2008; Pasricha et al., 2008). Anaemia can also develop as a side effect of liver disease, renal failure,
lead poisoning, or alcohol abuse (Ryan, 1997).
As mentioned previously, Devn and Borovce are both located in an immediate vicinity of rivers.
Thus the exploitation of aquatic resources, such as shing or mussel collecting might have played a
role in the subsistence strategy at both sites. Indeed, the analysis of faunal remains from the Devn
site conrmed the presence of a considerable number of mussel shells, such as Helix pomatia, Cepea
sp., and Unio sp. (Be nu s et al., 1999b). A frequent contact with water- or sh-borne parasites (e.g.,
Fasciola hepatica, Diphyllobothrium latum) could be a likely source of infection for the inhabitants
of Devn and Borovce. Several studies found a link between infestation with these parasites and
anaemia (Awasthi and Bundy, 2007; Cox, 1993; El-Shazly et al., 2005; Gilles et al., 1964; Jrovec
et al., 1977; Johnson, 2003; Layrisse and Roche, 1964; Lotfollahzadeh et al., 2008; Pasricha et al.,
2008).
Today it is known that iron deciency anaemia can affect any sex and age group, although young
children and women of childbearing age are the most vulnerable (e.g., Ryan, 1997). However, since
bone changes in the orbits indicative of anaemia are thought to develop exclusively during early
childhood(Stuart-Macadam, 1985), cribra orbitalia seeninadults indicate impairedremodeling caused
by repetitive episodes of stress at a later age (May et al., 1993).
Borovce (BO) sub-adults showed orbital lesions signicantly more frequently than their counter-
parts from DH and FR. In these Slavic samples, the most commonly affected sub-adults were found
in the age categories of 14 and 59 years. In general, sub-adults are particularly vulnerable to the
development of iron deciency anaemia due to high iron requirements, especially during the wean-
ing period and during the periods of growth spurts (Kent, 1986). Weaning also signicantly increases
exposure of sub-adults to gastrointestinal pathogens that often cause diarrhea. This disease increases
metabolic loss of essential nutrients including iron with the result that a child can become anemic
despite a diet containing sufcient amounts of iron (Kent, 1986; Ryan, 1997). Moreover, the increased
vulnerability of 59-year-old children in Medieval Europe can be attributed to the fact that approxi-
mately fromthe age of 7 years they were often involved in daily work tasks of the community (Power,
1986; Shahar, 1990) that might not match their actual physical abilities.
In contrast to FR and DH individuals, the frequency of cribra orbitalia in BO sub-adults was con-
sistently high until the age of 1014 years. An initial study on cribra orbitalia of the Borovce skeletal
remains suggested that such age distribution could be attributed to a prolonged period of disease
and/or nutritional stress starting at the vulnerable infant years, at weaning in particular, and culmi-
nating during the period of pubertal growth, which is accompanied by increased nutritional demands,
greater susceptibility to pathogens and social claims for better physical performance in terms of more
strenuous work tasks (Obertov and Thurzo, 2004, 2008).
The basic difference betweenthe BOandbothDevnsamples is the highfrequency of cribra orbitalia
in BO sub-adults, while the frequencies of orbital lesions for sub-adults and adults in both Devn sam-
ples wererelativelybalanced. Althoughthetotal mortalityof sub-adults didnot actuallydiffer between
the sites, BOsub-adults showed a considerably higher mortality when displaying cribra orbitalia. Their
counterparts fromFR and DHshowed relatively similar mortality patterns irrespective of the presence
of orbital lesions. Thus, the life style of BOsub-adults triggeredthe development of cribra orbitalia more
frequently, and its presence was also a factor in the increased mortality of these individuals. Under-
lying factors may have included repetitive bouts of disease and/or periods of food shortages. In the
Devn samples, more sub-adults died of acute diseases, which did not result in skeletal lesions, at least
not in cribra orbitalia.
The mortality of young adults (2029 years old), particularly males from Devn-Hrad was distinc-
tively increased compared to BOand FRsamples. This nding might be explained by their involvement
in armed conicts since an increased frequency of cranial trauma, which is indicative of interpersonal
violence, was reported for these young DH males (Be nu s, 2002; Be nu s and Masnicov, 2002a). More-
over, historical records (

Spiesz, 2001) indicate that there were at least four raids at Devn during this
R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190 187
time period (11th12th c. A.D.). The comparably lower mortality of young adult males from the FR
site suggests that during the Great Moravian Era life was less violent for the inhabitants of the Devn
fortication.
The inter-site and temporal comparisons focused on the frequency of cribra orbitalia in Medieval
samples from Central Europe. Since it would be beyond the scope of this study to go into the detail of
the archaeological, historical, and environmental background of every single one of the comparative
populations, general historical events and environmental patterns are discussed instead.
The frequency of cribra orbitalia was relatively high in the 5th8th century A.D., which would
be in agreement with the political turmoil of the Migration Period, with numerous armed conicts
and migration of different peoples that would facilitate the spread of various diseases either through
weakened immunity or the unfamiliarity of the individuals with new environments.
The 8th10th-century sites showed a decrease in the frequency of cribra orbitalia, which could be
explained by favourable environmental conditions, since little climatic optimum has been reported
for the years 8751194 A.D. in Central Europe (Svoboda et al., 2003). However, several years in the
beginning 11th century A.D. were marked by oods or droughts, which in consequence led to crop
failures followedby periods of starvationandevenspreadof acute diseases, suchas plague (Svoboda et
al., 2003). Althoughthe frequency of cribra orbitalia was relatively lower thaninthe previous centuries,
it should be noted that acute diseases with high mortality would not necessarily result in skeletal
changes.
The frequency of cribra orbitalia was lowest at the burial site of Devn-Hrad (11th12th c. A.D.),
followed by Devn-Za kostolom(9th c. A.D.) and Borovce (8thbeginning of 12th c. A.D.). The distribu-
tion of cribra orbitalia in the BOsample was very similar to that found at

Sebastovce, an Early Medieval
cemetery (7th9th c. A.D.) from Eastern Slovakia (Krlov et al., 1997), and to the samples from the
Migration Period.
Ingeneral, increasedfrequency of orbital lesions has beenfoundinsedentary populations withhigh
population density, inadequate sanitation, and high pathogen load resulting in frequent occurrence
of infectious diseases (e.g., Blom et al., 2005; Buzon, 2006; Hengen, 1971; Kent, 1986; Palkovich,
1987; Stuart-Macadam, 1992; Walker, 1986). The sanitation at Medieval rural sites, such as Borovce
was most probably less developed than in trading centres such as Devn. Moreover, the presence of
various burial types at Borovce indicates that an immigration of peoples with differing burial rites
occurred during this time period. Migration of people is often associated with the spread of unfamiliar
pathogens, and the necessity to adjust to the new environment, which can result in increased disease
load in the respective population (Dunn, 2009).
In all reference samples the proportion of sub-adults with cribra orbitalia was higher than that of
adults. The sex differences in the occurrence of orbital lesions were mostly not signicant, although in
most cases females were more frequently affected than their male counterparts. A higher frequency
of cribra orbitalia in adult females, particularly of reproductive age, has been interpreted as evidence
of increased female susceptibility to iron deciency anaemia resulting from increased demands for
iron in menstruation, pregnancies, and lactation (Larsen, 1997; Ryan, 1997; Sullivan, 2005).
In conclusion, the data fromMedieval Central European skeletal samples suggest that an increased
occurrence of cribra orbitalia was associated with environmental conditions, such as crop failures,
and socio-economic factors, such as migration and interpersonal conicts. These factors favour the
spread of and vulnerability to infectious diseases, which are considered to be the major cause of iron
deciency anaemia.
Acknowledgements
This study was supported by VEGA Grant No. 1/3279/06 (Environmental aspects of pathological
lesions in the non-adult individuals from historical populations on the Slovak territory).
We wish to thank Assoc. Prof. Milan Thurzo and Dr. Alena

Sef ckov, the Head of the Department of
Anthropology of the Slovak National Museum in Bratislava for allowing access to the skeletal sample
from Borovce. We also thank Laura Niven for improving the language. We are very grateful to the
reviewers for providing helpful comments on an earlier version of the manuscript.
188 R. Be nu s et al. / HOMO - Journal of Comparative Human Biology 61 (2010) 178190
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