Bennike Et Al., 2005

Comparison of Child Morbidity in Two ContrastingMedieval Cemeteries From Denmark

P. Bennike,1* M.E. Lewis,2 H. Schutkowski,3 and F. Valentin4

1Laboratory of Biological Anthropology, Institute of Forensic Medicine, University of Copenhagen, DK 2200Copenhagen N, Denmark2Department of Archaeology, Whiteknights, Reading RG6 6AB, UK3Department of Archaeological Sciences, University of Bradford, Bradford BD7 1DP, UK4CNRS UMR 7041, MAE, 92023 Nanterre, France

KEY WORDS preadults; stress indicators; growth; BMC; leprosy; Later Medieval Denmark

ABSTRACT This study compares associations betweendemographic profiles, long bone lengths, bone mineral con-tent, and frequencies of stress indicators in the preadultpopulations of two medieval skeletal assemblages fromDenmark. One is from a leprosarium, and thus probablyrepresents a disadvantaged group (Næstved). The othercomes from a normal, and in comparison rather privileged,medieval community (Æbelholt). Previous studies of theadult population indicated differences between the twoskeletal collections with regard to mortality, dental size,and metabolic and specific infectious disease. The twosamples were analyzed against the view known as the‘‘osteological paradox’’ (Wood et al. [1992] Curr. Anthropol.33:343–370), according to which skeletons display-ing pathological modification are likely to represent the

healthier individuals of a population, whereas those with-out lesions would have died without acquiring modifica-tions as a result of a depressed immune response. Resultsreveal that older age groups among the preadults fromNæstved are shorter and have less bone mineral contentthan their peers from Æbelholt. On average, the Næstvedchildren have a higher prevalence of stress indicators, andin some cases display skeletal signs of leprosy. This islikely a result of the combination of compromised healthand social disadvantage, thus supporting a more tradi-tional interpretation. The study provides insights into thehealth of children from two different biocultural settingsof medieval Danish society and illustrates the importanceof comparing samples of single age groups. Am J PhysAnthropol 128:734–746, 2005. VVC 2005 Wiley-Liss, Inc.

It was demonstrated that any attempt to reconstructhealth patterns of past populations from skeletal remainsis paradoxical, as these data can only provide informationabout the morbidity and mortality rates of nonsurvivors(Wood et al., 1992). The frequencies of disease in a skeletalassemblage would be higher than for the surviving popu-lation from which they were derived. Individuals display-ing pathological lesions, including stress indicators, in askeletal population were traditionally thought to repre-sent the less advantaged members of that society. Theseindividuals may have had a depressed immune system,may have been malnourished, and probably lived in anovercrowded, unhygienic environment that increasedtheir risk of exposure to a greater number of pathogenicorganisms. In contrast, those without lesions werethought to represent that part of the population who, per-haps due to nutritional and cultural advantages, encoun-tered fewer episodes of stress until time of death. How-ever, Ortner (1991, p. 10) stated that the presence of skele-tal lesions diagnostic of infectious diseases ‘‘implies a goodimmune response and a relatively healthy individual.’’Thus, in order to display pathological lesions on the skele-ton, the individual must either recover from or adapt tothe stress. Ortner (1991, p. 10) went on to state that ‘‘suchan immune response is not as effective as the one that suc-cessfully rids the body of the infectious organism duringthe early stages of the disease.’’ This led Wood et al. (1992)to question basic and widely accepted assumptions aboutpast health patterns by pointing out the ‘‘osteological par-adox’’ and to provoke researchers to revisit the methodsand interpretative techniques employed in the discipline.

The critical response by Goodman (1993) highlighted,among other things, the need to organize samples into agecategories and use multiple indicators of disease andnutritional stress in order to identify any hidden sub-groups within a given sample. In addition, Saunders andHoppa (1993) examined the question of linear growth insurvivors and nonsurvivors in order to ascertain whetherskeletal samples accurately represented the populationfrom which they were derived. Their study revealed thatshort stature seems to be disease-dependent.The use of stress models, such as those developed by Lit-

tle (1995) and Goodman et al. (1984), illustrates the com-plex nature of factors contributing to, and resulting from,physiological stress. Morbidity, mortality, and fertility areinfluenced by the synergistic interaction of environmentalparameters, economics, and cultural restraints, expressed

Grant sponsor: EU Program Human Capital and Mobility; Grantnumbers: ERBCHRXCT 930193.

*Correspondence to: Dr. Pia Bennike, Laboratory of BiologicalAnthropology, University of Copenhagen, Blegdamsvej 3, DK-2200Copenhagen N, Denmark.E-mail: [email protected]

Received 7 January 2004; accepted 22 September 2004.

DOI 10.1002/ajpa.20233Published online 25 July 2005 in Wiley InterScience

(www.interscience.wiley.com).

VVC 2005 WILEY-LISS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 128:734–746 (2005)

for example in birth rates, weaning practices, and foodtaboos that may buffer or induce stress in a specific popu-lation. The impact of stress relies on host resistance deter-mined by genetic factors, age, and sex (Goodman et al.,1988; Wall, 1991). An emphasis on the study of multipleindicators of stress in skeletal material thus represents amove away from the identification of specific diseases, toan assessment of nutritional and disease status within apopulation (Goodman et al., 1988).In the light of this discussion and the fact that biocul-

tural studies of children’s skeletons in medieval Europeare limited (but see Lewis, 2002a,b), two skeletal samplescomprising infants and juveniles (henceforth referred toas preadults) from medieval Denmark were examined.The Danish Middle Ages (AD 1050 until the dissolution ofthe Roman Catholic Church in 1536) saw a rise in contactwith the rest of Europe due to the introduction of Christi-anity, increased trading, and warfare. The vast majorityof the medieval population (about 90%) lived in the coun-tryside and worked on the land. During the second half ofthe Middle Ages, almshouses provided shelter for the sickand poor in the cities. However, those who were afflictedwith leprosy were ostracized and sequestered into specialhospitals known as leprosaria (Bennike and Brade, 1999;Arentoft, 1999). Both assemblages are from rural sites;the first consists of individuals interred within a leprosa-rium at Næstved, (Southern) Zealand, during the LateMedieval period (Møller-Christensen, 1978). The secondsample was contemporary to the first and derived from amonastic community at Æbelholt (Northern Zealand) andthe surrounding parish (Møller-Christensen, 1982). Manyof these individuals were expected to have been relativelyhealthy in comparison to those at Næstved, and the major-ity probably entered the mortuary sample as the result ofacute disease or social standing allowing them to afford aburial. Even though documentation is rather scarce, theskeletons are supposed to represent not only the prior,monks, and novices. The monastery provided lodging forrich people and shelter for the poor; food was free. Some ofthe visitors were travellers, while others came to receivetreatment and get cured, as the monastery housed a smallhospital. The number of monks was probably no higherthan 12, including the prior. The monastery employed lay-men to carry out various practical tasks, and their num-bers may have been considerable in relation to the monks.Thus, in addition to the brethren and some of the sick whomay have died during their stay, all other skeletons, asthe large numbers of female and childrens’ skeletonsshow, are most likely to represent members of the lay-men’s families, together with members of richer familieswho could afford high-status burials inside the church(Møller-Christensen, 1982).Previous studies of adult skeletons illustrated differen-

ces in the disease patterns of the two populations. Morethan 70% of the Næstved skeletons were reported to showclear evidence of changes due to leprosy (Møller-Christen-sen, 1978). Fifty-five percent of them had cribra orbitalia,as opposed to only 20% at Æbelholt (Møller-Christensen,1978; Møller-Christensen and Sandison, 1963). Moreover,the adult mortality profile revealed that many more fromthe leprosarium died between 20–35 years of age (40% inNæstved vs. 14% in Æbelholt) and only a few at age 55and above (2% in Næstved vs. 12% in Æbelholt) (Møller-Christensen, 1978). Lunt (1969) demonstrated that thepermanent teeth from Næstved in general were slightly,yet not significantly, smaller than those from the Æbelholtmonastery. It therefore can be reasonably assumed that

the preadults from Næstved also belonged to a less privi-leged community.If traditional interpretations were correct, one would

expect that, as the more advantaged group, those fromÆbelholt would have fewer early deaths and a lower fre-quency of stress indicators. In contrast, those at Næstvedshould die earlier on average and display more stress indi-cators, and their growth should be stunted compared withtheir peers from Æbelholt, thus illustrating lifetimesstricken with illness and all its social ramifications. How-ever, if skeletal assemblages do indeed reflect a paradox,then one would expect preadults at Æbelholt to displaymore stress indicators as a result of their biological andcultural advantage and ability to be strong enough torecover from disease insults.Age-at-death of individuals with and without stress

indicators was already used to help identify those most atrisk from morbidity and mortality. Goodman and Rose(1990) associated hypoplasia in Guatemalan children witha lower mean age-at-death. This finding was confirmed ina study of prehistoric Native Americans from the Libbensite by Duray (1996). Both Van Gerven et al. (1981) andMittler et al. (1992) found a high correspondence of cribraorbitalia and the probability of dying in infancy and earlyadolescence in a Nubian sample, and Cook and Buikstra(1979) found an association of those with linear enamelhypoplasia on deciduous teeth with increased mortality.In her study of a British population from York, Grauer(1993) reported increased ages-at-death for those display-ing remodeled periostitis once adulthood had beenreached, while Mensforth (1985) and Mensforth et al.(1978) found a decreased mean age-at-death for those withunremodeled porotic hyperostosis and periostitis in theLibben sample.With the exception of Goodman and Rose (1990) and

Cook and Buikstra (1979), all these studies involved usingmean age-at-death for the whole skeletal sample. As willbe demonstrated, this is likely to obscure the more subtlevariability in death rates within the preadult sample,where these lesions first appear. It was shown that stressindicators are associated with decreased age-at-death inadulthood, but is this also true of the preadult sample?Are those without any stress indicators outliving the chil-dren displaying them or did they succumb to death beforethe lesions could appear? By restricting the study to prea-dults (those under 20 years of age), it is hoped to provide amore precise picture of the nature of stress indicators inrelation to age patterns. In particular, the study aims toaddress whether preadults from the leprosarium ofNæstved were shorter, had lower bone mineral content,and developed more skeletal modifications following epi-sodes of stress than their contemporaneous peers from theparish community at Æbelholt.

MATERIALS

The morbidity and mortality profiles of 259 preadultskeletons from later medieval Sjælland (Zealand) in Den-mark were compared. The first sample comprised 76 prea-dult skeletons interred in the cemetery connected to St.George’s Hospital at Aaderup, Næstved (total number ¼650), one of 31 leprosaria established in Denmark in thelater medieval period (AD 1250–1550). The second com-prised 183 preadults from the cemetery connected to theAugustinian monastery at Æbelholt between AD 1175–1550 (total number ¼ 756). Both sites are contemporane-

735CHILD MORBIDITY IN DENMARK

ous and, being only 150 km apart, from the same geo-graphical area.Møller Christensen excavated the skeletons at Æbelholt

from 1935–1965 and uncovered burials within the cloisterambulatory and garth (Bennike, 2002). The adult skele-tons, 60% males and 40% females, together with the 183children, suggested that some individuals were the mar-ried servants of the monastic community and their off-spring. Further burials in the nave of the church and thechurchyard to the northwest of the monastery representedmonks and privileged lay persons (Møller Christensen,1982). Thus, those buried in the cemetery probably repre-sent children of farmers connected to and employed by themonastery, pupils, and the children of parents who couldafford to have them buried within the foundations. This issupported by the fact that the age distribution atÆbelholt is very similar to that of other medieval ceme-teries in Denmark.The discoveries at Æbelholt prompted the excavation of

the cemetery at Næstved (1948–1968). The hospital atNæstved was first mentioned in AD 1261 and is known tohave functioned solely as a leprosarium until AD 1542,when the Ribe Recess ordered all leprosy hospitals in Den-mark to be disestablished and patients to be admitted tolarger general hospitals. The socioeconomic status of thoseinterred at Næstved would have varied, as inmates wereadmitted to the hospital from the town of Næstved andthe surrounding area (Møller Christensen, 1961; Ander-sen, 1969).Documentary evidence suggests that the Danish medie-

val community could recognize the classic signs of leprosyas most of the documents describe the classic facialchanges (Andersen, 1991). In fact, no clear evidence of lep-rosy was found in over 300 skeletons excavated from analmshouse (or Helligandshus) in the center of Næstved(AD 1400–1800) (Macey, 1996) or in 60 skeletons of a massgrave nearby dated to the 14th century (Bennike, 2000).However, in a study of Danish and Swedish medieval skel-etons based on a number of specific and nonspecific crite-ria used for calculation of specificity and sensitivity of thediagnosis of leprosy, Boldsen (2001) claimed that a highproportion of the rural Danish population was infectedwith leprosy in the 13th century. This conclusion still hasto be proven.The preadults at Næstved may have entered the sample

in a number of ways. Firstly, children may have beenadmitted to the hospital when they presented soft-tissuelesions associated with leprosy. Today, some children bornto parents with lepromatous leprosy normally developclinical signs of the disease by age 5 years (Melsom et al.,1982; Lewis, 2002c). Richards (1977) cited many cases ofchildren being examined and admitted to leprosaria in hisstudy of the disease in Scandinavia, and it was notunusual to separate the child from its parents. However,today, infants displaying single leprous lesions are oftenoverlooked if they are concealed by clothing or ignored bythe mother, and the lesions may heal spontaneously (Laraand Nolasco, 1956), only to recur at a stressful time dur-ing the child’s development, e.g., during puberty. There-fore, it is unlikely that the youngest preadults in this sam-ple (0–2.5 years) were admitted to the hospital diagnosedwith leprosy; yet congenital contraction of the disease can-not be ruled out.There were equal numbers of male and female skele-

tons, and some children may have accompanied theirinfected parent or parents into the hospital if they weresuspected of being contaminated or, more likely, to pre-

vent them becoming ‘‘orphaned.’’ Richards (1977, p. 60)cited the case of a young woman from Sweden who hadentered the hospital with her parents and, although shenever developed the disease, remained there for 16 years.Some preadults may represent babies born to women withlepromatous leprosy or to the healthy wives of inmates.Early accounts from Næstved referred to ‘‘womenfolk ofsick brothers and sisters’’ entering the leprosarium to carefor their family (Richards, 1977, p. 36). Husbands andwives were often segregated or advised to divorce whenthey entered a leprosarium (Brody, 1974), and male infer-tility sometimes caused by the disease would havedecreased the number of children born in the hospital.Thus, the sample at Næstved provides an unusual oppor-tunity to study the skeletons of preadults exposed toMycobacterium leprae.From historical records, it is known that leprosaria in

Scandinavia were almost completely dependent on theparishes to which they belonged for food supply, financialsupport, maintenance, and administration (Andersen,1969; Richards, 1977; Arentoft, 1999). It is also possiblethat, in times of hardship in the parish, these duties wereneglected and would have led to poorer hygienic and diet-ary conditions, which would have taken their toll onalready disease-burdened inmates.

METHODS

Age at death

Data from preadult skeletal material are widelybelieved to represent the most demographically variableand sensitive barometer of biocultural change (VanGerven and Armelagos, 1983; Roth, 1992). Patterns of in-fant and child mortality were shown to have a profoundeffect on the crude death rates of a population and, whencoupled with evidence of childhood morbidity, have becomeaccepted as a measure of population fitness and an indicatorof fertility (Mensforth et al., 1978). Although the differentialpreservation of fragile preadult skeletons, and selective bur-ial due to cultural factors, may present a serious problemwith underrepresentation, preadult data are relatively freefrom the problems of age assignment that plague paleode-mographic studies based on adult skeletons. Age estimatesof preadult skeletons are derived using age-specific markersof growth and maturation. The timing and outcome of theseevents are thought to be tentatively linked to a genetic blue-print, as opposed to the degenerative age determinants ofadulthood (Rallison, 1986). For this reason, preadult skele-tons allow for more precise skeletal age estimation than ispossible for adults.Growth studies on modern populations showed that

dental development, characterized by tooth formationand eruption, is less sensitive to environmental influen-ces such as malnutrition and infection, and is moregenetically controlled than skeletal maturation and size(Schour and Massler, 1940; Acheson, 1959; Stini, 1985;Eveleth, 1986). Dental development is believed to be themost accurate indicator of age-at-death on the preadultskeleton (Lewis and Garn, 1960; Smith, 1991, Hillson,2000).The age distribution of any given skeletal sample is

determined by the mortality and fertility distribution, andtherefore, growth patterns determined from nonsurvivorsmay not provide a true reflection of the growth pattern ofsurviving individuals in an age group (Johnston, 1962; VanGerven and Armelagos, 1983; Jantz and Owsley, 1984;Saunders and Hoppa, 1993; Wood et al., 1992). On the other

736 P. BENNIKE ET AL.

hand, when attempting to compare the health status of twocemetery samples, age-at-death and growth data coupledwith evidence of disease and nutritional stress can provideuseful information on selective mortality in certain culturalor ecological circumstances.Skeletons were omitted from the preadult (ca. <20

years) sample when the epiphyseal head had completelyfused to the femoral diaphysis. The femoral head waschosen to exclude individuals above age 20 years (Buik-stra and Ubelaker, 1994). Age-at-death for preadults wasassessed by the crown and root formation of the deciduousand permanent dentition, as described by Moorrees et al.(1963a,b) and tabulated by Smith (1991). When no teethwere preserved, epiphyseal fusion was employed (Buik-stra and Ubelaker, 1994). This was necessary in only sixcases. The age of perinates was estimated using diaphy-seal long bone lengths (Olivier and Pineau, 1960; Scheuerand Black, 2000).Skeletons were divided into five age categories: newborn

(0)–2.5 years, 2.6–6.5 years, 6.6–10.5 years, 10.6–14.5years, and over 14.6 years. The average age in each cate-gory was calculated for both cemeteries (Table 1). By usingbroad age categories, it was hoped to reduce the errorsintroduced by inter- and intrapopulation variability ofage-related skeletal traits (Lampl and Johnston, 1996).

Bone length, bone mineral content, nonspecificstress, and disease

Skeletons were examined for bone length, bone mineralcontent (BMC), and indicators of stress including cribraorbitalia and dental enamel hypoplasia. Evidence of non-specific infections (maxillary sinusitis, endocranial le-sions, and periostitis) was also recorded, as was evidenceof leprosy in the Næstved preadult sample.Today, child health studies rely on anthropometric

measurements such as height for age, weight for height,and arm circumference; a deficit in these measurementsmay increase the individual’s risk of death (WHO Work-ing Group, 1986; Saunders and Hoppa, 1993). A lowerheight for age and slowed maturation in a given popula-tion are associated with malnutrition, disease, and phys-iological stress (Scrimshaw et al., 1959; Eveleth and Tan-ner, 1990; Mensforth, 1985). During a stressful period,the ‘‘undernourished child slows down and waits for bet-ter times’’ (Tanner 1990, p. 130). The level of slowedgrowth relates to the severity of the episode, with thefetal stage and the first 3 years of life shown to be a par-ticularly susceptible period for growth retardation (Eve-leth and Tanner, 1990; Saunders and Hoppa, 1993). Stini(1985) referred to growth retardation as ‘‘developmentaladaptation,’’ as this response should increase an individu-al’s chance of survival due to fewer nutritional require-ments. Seckler (1982) took this interpretation one stepfurther and suggested that ‘‘small is healthy,’’ but sincegrowth retardation is correlated with negative health fac-

tors, it is attributed to an adjustment to environmentalstress factors, rather than adaptation per se (Scrimshawand Young, 1989, cited in Saunders and Hoppa, 1993;Beaton, 1989).Once equilibrium has been restored after an episode of

stress, children have the ability to ‘‘catch up’’ with theirhealthy peers and resume growth at a rate that will ena-ble them to reach the ‘‘target’’ growth curve. This abilityto increase the velocity of growth until the optimum levelis reached is impaired with age and cannot occur duringor after puberty (Rallison, 1986; Eveleth and Tanner,1990). Mensforth (1985) correlated growth retardationwith iron-deficiency anemia in the Libben Late Woodlandsample, and attributed it to nutritional stress in the wean-ing period. Due to its association with malnutrition anddisease, growth retardation is expected to be associatedwith an increase in the frequency of stress indicators inour samples. Infection and malnutrition were also shownto affect growth and maturation in modern populations(Acheson and Macintyre, 1958; Stini, 1985; Duncan, 1980;Cole, 1989; Wall, 1991). Therefore, it is expected that prea-dult individuals at Næstved are smaller and have lowerBMC values than their counterparts from Æbelholt.Only a handful of studies examined bone cortical thick-

ness as an indicator of childhood stress in skeletal popula-tions (e.g., Huss Ashmore, 1978; Martin and Armelagos,1979; Cook, 1984), and to the knowledge of the authors,even fewer examined bone mineral content in preadultskeletal samples. Such data are widely accepted to serveas standards for bone mineralization (Thompson, 1980;Malina and Bouchard, 1991). They are generally consid-ered to reflect the prevailing status of physical activityand nutritional supply as well as (for adults) hormonalinfluences connected with mineralization, growth, andremodeling of bone (Carlson et al., 1976; Thompson, 1980;Ruff and Hayes, 1984; Bennike et al., 1993). As malnutri-tion, or more specifically protein calorie deficiency, wasshown to affect linear growth and maturation, a change inthe appositional growth of bone laid down in this periodshould also be expected.Mean diaphyseal length was plotted against dental age

to produce skeletal growth profiles for the humerus,femur, and tibia, and BMC measurements were performedon femora and humeri. Specimens were rejected for BMCmeasurements if there were visible signs of erosion atmidshaft. In addition, radiographs were taken in order toexclude bones with evidence of soil in the medullary cav-ity. BMC measurements were performed on a GammatecGC 50 Dual Photon scanner (for a detailed description ofthe method, see Bennike et al., 1993). The region of inter-est was defined as being 61 cm around the diaphysealmidshaft, corresponding to 10 scans, each with a breadthof 2 mm. This scanning breadth was applied to all speci-mens, irrespective of age. Quality control included a checkof the scanner parameters against a marble standard atthe beginning and end of a measurement set. Precisionwas checked by 21 replicate measurements of onearchaeological bone specimen, a 331-mm femur from an11.4-year-old child. The measurement results of the mar-ble standard (n ¼ 36) were obtained with an error of0.31%, and the mean mineral content (6.50 6 0.047 units/cm) lay within the known 95% confidence interval of thestandard (6.49–6.50 units/cm). Precision measurementsfrom the control femur revealed a small measurementerror (coefficient of variation) of 0.89%.Cribra orbitalia is thought to be indicative of childhood

malnutrition and/or pathogen load resulting in iron-defi-

TABLE 1. Mean ages at death

Age

Æbelholt Næstved

N Mean SD N Mean SD

<2.5 43 1.17 0.71 14 1.32 0.592.6–6.5 57 4.73 1.13 11 4.98 0.796.6–10.5 35 8.86 1.12 17 8.95 1.2010.6–14.5 17 12.20 0.99 11 12.04 0.9914.6–20.0 9 16.61 1.87 20 17.62 2.94

Total mean 161 6.19 73 9.49


ciency anemia (Mensforth et al., 1978, Weinburg, 1992;Stuart-Macadam and Kent, 1992 ). It was also suggestedthat acute and chronic infections may stimulate theimmune system to withhold iron from invading microor-ganisms as a defense mechanism. In some studies, cribraorbitalia was thought to be a useful indicator of dietarydeficiency of iron in past populations (El-Najjar et al.,1979; Cohen and Armelagos, 1984; Gilbert, 1985). How-ever, clinical studies and bone chemical analyses ques-tioned the validity of this association or suggested a linkbetween metabolic deficiencies and severity of lesions(Reinhard, 1992; Schutkowski and Grupe, 1997; Subiraet al., 1992). Ortner and Ericksen (1997) and Ortner et al.(2001) suggested that vitamin C deficiency (scurvy)caused cribra orbitalia, while in a recent study of adultskeletons, Wapler et al. (2004) showed that the micro-scopic appearance of ‘‘cribra orbitalia’’ may be due to sev-eral pathological causes (including anemia in 30–40%) aswell as ‘‘postmortem’’ erosions (2 %).In this study, lesions were graded according to the

scheme by Stuart-Macadam (1991, p. 109), but lesionsdescribed as type 1, which show very weak ‘‘capillary-likeimpressions,’’ were not recorded, as these lesions are con-sidered too mild to represent serious health problems. Wealso found that the very mild cases could easily be mis-taken for postmortem changes and could lead to consider-able inter- and intraobserver bias. This exclusion obvi-ously means that only ‘‘the tip of the iceberg’’ was regis-tered, which is common in most skeletal studies.Furthermore, active and healed cases of cribra orbitaliawere not registered separately, as they proved to be hardto distinguish from one another macroscopically.Dental enamel hypoplasia was identified as grooves or

pits on the dental enamel surface of the deciduous andpermanent dentition. They represent a prenatal or child-hood growth disturbance due to disease or malnutrition,and are associated with decreased longevity (Larsen,1997). Measurements were taken from the proximal mar-gin of the defect to the cemento-enamel junction at theanterior aspect of the deciduous and permanent teeth.Enamel hypoplasia was considered present when morethan two teeth on opposite sides of the jaws were affected,and absent when four or more anterior teeth were avail-able for examination but did not show any lesions. Premo-lars were included in this number as, in some individualsof the leprosy sample, the central incisors may have beenlost due to atrophy of the maxillary alveolar bone, andmay have caused the defects to be under-recorded. Theage of defect formation in 1-year age categories was deter-mined using a conversion chart (Goodman and Rose,1991, p. 288). The mean age of formation and the numberof lines in each sample were calculated.New bone formation on the endocranial surfaces was

recorded morphologically as either layers of new bone onthe original cortical surface, ‘‘hair-on-end’’ extensions ofthe diploe, or as vascular impressions extending into theinner lamina of the cranium (Schultz, 2001). New boneformation on the postcranial skeleton was recorded ashealed (lamellar bone formation) or active (immature newbone) (Ortner, 2003). Lewis (2004) discussed the etiologyof endocranial lesions and suggested that they should bereferred to as infection or nonspecific indicators of hemor-rhage, which may be caused by vitamin C deficiency orchild abuse.Periostitis on the tibiae and fibulae is common in individu-

als with leprosy, and in these cases was considered ‘‘nonspe-cific’’ in its etiology. Maxillary sinusitis was recorded accord-

ing to the criteria of Boocock et al. (1995), with the exceptionof large ‘‘pits’’ that are believed to represent growth changesin the antra (Lewis et al., 1995). For this reason, it was onlyrecorded in individuals from age 2.6 years onward, whensinus development is advanced enough to allowmore effectivevisualization of the cavities (Maresh, 1940). Maxillary sinusi-tis has many etiologies, including environmental air pollu-tion, upper respiratory tract infections, and dental disease(Wald et al., 1981; Lewis et al., 1995; Merrett and Pfeiffer,2000). More specifically, maxillary sinusitis is associated withinflammation of the rhinomaxilla in leprosy (Wright, 1979).Chi-square tests for 2 � 2 and 2 � c tables, with Yate’s

continuity correction (Kirkwood, 1988), were carried out totest the differences in prevalence of stress indicatorsbetween sites. Wilcoxon’s rank correlations were performedto test for differences in long bone lengths. Mean age-at-death of those individuals with and without stress indica-tors was tested using the Kolmogorov-Smirnov statistic.Leprosy was diagnosed when the characteristic lesions,

distributed on the maxilla (frontal alveolar absorption,porotic areas on the palate, resorption of the nasal spine,and remodeling of the nasal area), hands and feet (mainlyresorption and remodeling), or lower limbs (periostealreaction), were recognized (Lewis, 2002c). Lepromatousleprosy causes bilateral neuropathy, and in older individ-uals can cause osteopenia in males due to reduced testos-terone levels (Jopling and McDougall, 1988). Therefore,BMC measurements were compared between the twosamples.

RESULTS

Age distribution

In order to assess whether the preadult age distribu-tion at Æbelholt was attritional, and thus comparable toother contemporary Danish populations, a comparisonwas made with a sample of preadult skeletons (n ¼ 252)from a completely excavated medieval rural cemetery atTirup (Kieffer Olsen, 1993). Despite a slight difference inthe ranges of age groups, the demographic pattern atÆbelholt was similar to that of Tirup. There were 60%and 61% of preadults between 0–6.5 years at Tirup andÆbelholt, respectively, with 33% of the sample making upchildren between 6.6–14.5 years, and 6% in the 14.6–20.0-year age categories, with a similar distribution atboth sites. This similarity in age distribution with a ‘‘nor-mal’’ medieval cemetery seems to indicate that the prea-dult skeletons at Æbelholt were not a special, selectedgroup, e.g., one derived from the hospital section of themonastery. Contrary to this pattern, we found that whenthe mortality profiles of Næstved and Æbelholt were com-pared, the two populations had significantly different dis-tributions in all age groups (�2 ¼ 28.3, df ¼ 4, P < 0.01)(Fig. 1). For example, at Næstved, a significantly lowernumber of individuals was in the 2.6–6.5-year age group(�2 ¼ 9.5, P < 0.01), representing only 15% of the totalsample (Æbelholt, 35 %), and a significantly higher num-ber of 14.6–20.0-year-olds (�2 ¼ 21.7, P < 0.01), account-ing for 27% of the Næstved population (Table 1). Calcula-tions of average age in each age group were rather similar.

Indicators of bone length, BMC, andnonspecific stress

Growth profiles for both sites followed a similar patternuntil the 10.6–14.5-year age category, where the Næstved


children were significantly shorter than their peers fromÆbelholt by up to 3.8 cm for femoral diaphyseal lengths(P < 0.05) (Table 2, Fig. 2). The BMC-for-age data are pre-sented in Table 3 and Figure 3 and reveal congruent pat-terns, which seem to support the linear growth data.The average prevalence of stress indicators at Æbelholt

was lower than in preadults from Næstved, who had signifi-cantly higher rates of enamel hypoplasia and maxillarysinusitis (Table 4, Fig. 4). In both samples, the prevalence ofendocranial lesions peaked in the 0–2.5-year age categoryand was significantly higher at Næstved than Æbelholt inthe 2.6–6.5-year age category. When the prevalence of stressindicators was compared within samples, cribra orbitaliapeaked in the 2.6–6.5-year age group at Æbelholt, whereasat Næstved, cribra orbitalia was most prevalent in the 14.5–20.0-year age category (Table 4). The age of hypoplasia for-mation, divided into 1-year periods, showed that the majorityof defects were formed between 2.6–3.5 years of age in bothgroups, with 55% (84 of 153 defects in 23 individuals) affectedat Æbelholt and 41% (68 of 167 defects in 21 individuals) atNæstved (Fig. 5).Mean ages at death were calculated for individuals with

and without stress indicators. The results suggested thatchildren with stress indicators in general were living lon-ger than those without (Table 5). At Æbelholt, childrenwith enamel hypoplasia were 10.8 years old on average,i.e., 4.5 years older than those not displaying the lesion(K ¼ 2.0, P ¼ 0.01, where K ¼ Kolmogorov-Smimov). Thosewith cribra orbitalia also lived longer than those without(on average, 2.8 years), but the difference was not signifi-cant. Those with maxillary sinusitis were associated withsignificantly increased longevity (K ¼ 1.43, P ¼ 0.05), asthey were living 2.4 years longer than those without. AtNæstved there was a similar trend, although not signifi-cant: those with hypoplasia, periostitis, or rhinomaxillarysyndrome (pathognomonic of leprosy) survived longerthan those who did not display the lesions.However, in the case of endocranial lesions, the pattern

was reversed. At Æbelholt, the presence of endocraniallesions was associated with decreased longevity. Thosedisplaying lesions died around age 1.6 years, and thosewithout lived significantly (K ¼ 1.78, P ¼ 0.05) longer andattained a mean age-at-death of 6.8 years. At Næstved,children without endocranial lesions also lived signifi-cantly (K ¼ 1.84, P ¼ 0.05) longer (7.5 years) than thosewith the lesions (3.4 years).

Childhood leprosy at Næstved

At Næstved, 16 of 60 children that could be examined(27%) had evidence of leprosy. Fifteen of those (25%) werediagnosed with lepromatous leprosy (LL) on the basis ofcharacteristic changes to the rhinomaxilla. Thirteen of 16had postcranial bones preserved as well, and of those,seven (54%) displayed additional postcranial lesions. Onefurther individual, whose maxilla was missing, was diag-nosed on the basis of bilateral periostitis on the tibiae andfibulae and destructive changes to the feet. The changesassociated with lepromatous leprosy were found toincrease in older individuals. The three youngest childrenbelonged to the 6.6–10.5-year age category, representing18% of that group. When the prevalence of stress indica-tors was compared between those with and without visiblesigns of leprosy, there was a higher prevalence of periosti-tis and maxillary sinusitis (�2 ¼ 9.13 and 7.81, respec-tively; P ¼ 0.005) in children diagnosed with leprosy. How-ever, with the exception of shorter humeri in the Næstvedadolescents (14.6–20.0 years) with leprosy compared tothose at Æbelholt, the growth profiles of leprous and non-leprous individuals at Næstved did not differ. Due to thepossibility of regional anesthesia or disuse, the leprouschildren were expected to display lower bone length andBMC in comparison to the rest of the sample. However,although all the leprosy children were generally found tohave shorter long bones and lower BMC values than theother children at both sites, none of these differences wassignificant.

DISCUSSION

Is it logical to assume that a group of skeletons display-ing pathological lesions and other stress indicators repre-sent the disadvantaged of the society from which theywere derived? Wood et al. (1992) argued that this basicassumption, commonly used to measure past populationmorbidity, is paradoxical. In order to display a stress indi-cator such as enamel hypoplasia or cribra orbitalia, it isnecessary to recover from the stress that resulted in a ces-sation of growth (as these lesions only become visiblewhen normal growth is resumed), or some kind of long-standing condition has to be present. Thus it follows thatonly those with a strong immune system and perhaps cul-tural advantages are likely to survive episodes of stress.In fact, should not weaker or culturally disadvantagedindividuals enter the mortality sample with no or fewerskeletal markers of stress and disease because of theirinability to recover from an episode of stress? When allpreadults were combined in each of the two samples, thisassumption could not be confirmed because the lessadvantaged group from the leprosy cemetery displayedmore stress-related skeletal modifications throughout(Fig. 3). However, when the various age groups of the twosamples were compared separately, a much more complexpattern emerged (Table 5) that demonstrates the impor-tance of subdividing a sample into age groups in compara-tive studies. Contrasting the groups with and withoutskeletal stress indicators revealed higher average ages ofthose with lesions than those without, except for endocra-nial lesions. Thus, at least in terms of longevity, yet contraother parameters, overcoming episodes of stress doesmean surviving them by a measurable margin, whichlends some support to Wood et al. (1992).In order to assess those most at risk from stress, it is

important to be aware of the environmental and cultural

Fig. 1. Age distribution.


factors that may buffer or expose the population to physio-logical disruption. Goodman (1993, p. 284) argued thatevidence from developing countries refutes the idea of thehealthiest individuals having more stress indicators and

states: ‘‘I know of no situation in which a clearly advan-taged group, living or past, has more hypoplasia than adisadvantaged group.’’ He suggested that by taking themean age-at-death, the weakest individuals would beidentified as those who died at an earlier age. Althoughstress indicators are generally unrelated to the final causeof death, the process causing the lesion may have left theindividual more susceptible. Therefore, individuals withstress indicators may have been prone to die at an earlierage, something that Saunders and Hoppa (1993) termed‘‘selective mortality.’’ Individuals with certain stress indi-cators on their skeletons should be entering the mortalityrecord earlier than those who do not display the lesions.At Æbelholt, the mortality curve followed a pattern sim-

ilar to that of rural Tirup, with a high number of infantdeaths and mortality decreasing as children reach adoles-cence. Here, preadults represent 24% of the total sample,whereas at Næstved, preadults represent only 12% of thetotal sample, and mortality rates increase with age. Incontrast, the group of preadults represented most atNæstved is between 14.6–20.0 years of age (27%). Thisage distribution cannot be considered an accurate repre-sentation of the living population from which the samplewas derived, because normally only sick individuals wereselected for admission, and due to the incubation period of

TABLE 2. Diaphyseal lengths for long bones (mm)

Diaphyseal lengths (mm)

Humerus Femur Tibia

Age (years) N Mean Range N Mean Range N Mean Range

Æbelholt0–2.5 26 95.8 6 19.9 75.9–115.7 24 113.6 6 31.1 82.5–144.7 16 96.5 6 24.3 72.2–120.82.6–6.5 42 159.0 6 21.6 137.4–180.6 39 212.3 6 32.8 179.5–245.1 31 169.9 6 22.6 147.3–192.56.6–10.5 23 208.3 621.2 187.1–229.5 23 293.9 6 29.6 264.3–322.6 20 225.4 6 22.9 202.5–248.310.6–14.5 9 255.1 6 27.9 227.2–283.0 8 359.3 6 39.9 319.4–399.2 9 292.4 6 33.3 259.1–325.714.6–20.0 6 302.5 6 24.4 278.1–326.9 5 418.6 6 31.3 387.3–449.9 3 375.0 6 22.6 352.4–397.6

Total 106 99 79

Næstved0–2.5 6 99.6 6 13.6 86.0–113.2 5 114.8 6 28.7 86.1–143.5 3 97.5 6 16.0 81.5–113.52.6–6.5 6 140.8 6 36.9 103.9–177.7 4 224.5 6 39.8 184.7–264.3 4 174.0 6 33.2 140.8–207.26.6–10.5 12 209.4 6 15.4 194.0–224.8 7 299.7 6 20.7 279.0–320.4 6 235.0 6 16.4 218.6–251.410.6–14.5 8 228.5 6 24.2 204.3–252.7 7 330.4 6 26.5 303.9–356.9 6 261.0 6 20.4 240.6–281.414.6–20.0 13 275.6 6 29.6 246.0–305.2 10 380.9 6 29.3* 351.6–410.2 7 315.0 6 24.3* 290.7–339.3

Total 45 33 26

* Samples differ significantly at P < 0.05 (Wilcoxon rank sum test).

Fig. 2. a: Femur diaphyseal length (cm). b: Humerus dia-physeal length (cm).

TABLE 3. Bone mineral content (g/cm)

Age (years)

Humerus Femur

N Mean and SD N Mean and SD

Æbelholt0–2.5 25 0.26 6 0.28 24 0.40 6 0.172.6–6.5 38 0.64 6 0.23 37 1.04 6 0.296.6–10.5 22 0.94 6 0.16 23 1.74 6 0.3510.6–14.5 9 1.37 6 0.36 8 2.65 6 0.6714.6–20.0 6 1.85 6 0.79 4 3.56 6 1.64

Total 100 96

Næstved0–2.5 6 0.25 6 0.05 6 0.37 6 0.112.6–6.5 5 0.55 6 0.28 4 0.91 6 0.476.6–10.5 12 1.09 6 0.18 7 1.91 6 0.2810.6–14.5 7 1.12 6 0.20 7 1.91 6 0.2714.6–20.0 13 1.39 6 0.46 10 2.68 6 0.84

Total 43 34


leprosy (ca. 7 years), only older individuals would showthe most obvious signs of the disease. The skewed demo-graphic profile continues into adulthood, with the groupsof youngest and oldest adults from Næstved comprising46% and 2%, respectively, whereas Æbelholt shows amuch more balanced pattern, with 12% and 13%, respec-tively. These differences were plausibly attributed to theoverall poor health of adult leprosarium inmates (MøllerChristensen, 1978).Due to the association between chronic infections and

growth retardation in modern populations (Eveleth andTanner, 1990), it was expected that preadults from theleprosarium at Næstved would be consistently shorter forage than their peers from Æbelholt. The growth profilesdemonstrate this to be the case, with deviations most pro-nounced in the 10.6–14.5-year and 14.6–20.0-year age cat-egories. The BMC results followed a similar pattern,although to some extent, sexual dimorphism may beresponsible for the differences between samples. In a liv-ing population, boys and girls generally follow a similarcourse of skeletal growth during infancy and childhood(Falkner and Tanner, 1986; Eveleth and Tanner, 1990).After the adolescent growth spurt, which girls generallyexperience 2 years ahead of boys, boys surpass girls inbody size (Malina and Bouchard, 1991). Females wouldprobably have started their growth spurt earlier thanmales, around age 12–14 years. However, by age 14–16years, the boys, with a greater growth velocity, should

have surpassed the mean lengths of bones of females. AtNæstved, a greater number of females might be expected,as modern studies indicate that women develop leprosy atan earlier age than men. In India, 50% of women with lep-rosy developed the disease before age 20 years, comparedto 30% of men (Duncan et al., 1981). This pattern is per-haps linked to endocrine activity and a depressed cell-mediated immunity due to pregnancy (Jopling andMcDougall, 1988). Conversely, the fact that the Æbelholtsample was derived from a monastery may have resultedin a surplus number of males in the sample of adolescents.However, in the total skeletal sample, adult malesaccounted for only 60% of all adults. The more pronounceddifference in the BMC-for-age curve seen in the oldest agecategory of preadults may be the result of sexual dimor-phism, with males making up the majority at Æbelholtand shorter females dominating the sample at Næstved.However, there were no sex-related differences in toothsize between the two populations (Lunt, 1969). Rather, thelower values for bone mineral content in the Næstved pre-adults resulted from reduced physical activity of theinmates, damage to the peripheral nerves, and an imbal-ance in osteoclastic/osteoblastic equilibrium that couldhave resulted in paralysis of the limbs and subsequentosteopenia.Age-related differences in long bone lengths between the

two samples may also be due to the impact of leprosy ongrowth in the Næstved adolescents. That the differencesbetween Æbelholt and Næstved appear to be more pro-nounced after 10.5 years can be explained by the fact that bythis age, the prevalence of the disease in children increases,and that ‘‘catch up’’ growth can no longer disguise the differ-ences between the two groups (Rallison, 1986).Periostitis is an almost constant feature of lepromatous

leprosy (LL) caused by neuropathy and secondary infec-tion. Therefore, an association with higher frequencies ofleprosy is not surprising. Maxillary sinusitis is known inmodern leprosy patients to be associated with facialchanges due to the concentration of bacilli in the anteriorparts of the maxilla, palate, and nasal region (Soni, 1989;Hauhnar et al., 1992; Boocock et al., 1995). Therefore, thehigher prevalence of these infections in the LL group isconsidered to be the result of secondary infections associ-ated with leprosy, rather than indicating general exposureto nonspecific stress factors. The only lesions significantlyassociated with decreased longevity were those on theendocranial surfaces. One of the major causes for theselesions is believed to be chronic meningitis caused by vari-ous pathogens and resulting from numerous childhoodinfections. In this study, 10% (9) of children between ages0–10.5 years at Æbelholt and 38% (11) of these children atNæstved displayed new bone formation on the endocranialsurfaces. The prevalence rate at Næstved is high, evencompared with an Illinois Woodland population, whereCook and Buikstra (1979) found 27% of endocraniallesions in children between ages 0–10 years. It is possiblethat the young children from Næstved were susceptible tomeningitis due to frequent childhood illnesses, over-crowded conditions, or perhaps as a result of leprosy.Although nothing has been published about meningealinfections and leprosy, another mycobacterium, M. tuber-culosis, is known to result in inflammation of themeninges in children (Schultz, 2001).Møller-Christensen and Sandison (1963) and Møller-

Christensen (1978) found an association between leprosyand cribra orbitalia in the adult Næstved sample, where63% had evidence of lesions, compared to 20% of the

Fig. 3. a: Bone mineral content of midshaft femur (g/cm).b: Bone mineral content of midshaft humerus (g/cm).


adults at Æbelholt. It may be that in order to develop cri-bra orbitalia, a threshold level of health-associated factors(such as infectious diseases or nutrirional deficiencies)needs to be reached. Despite the lack of a significant peakin cribra orbitalia in the preadult sample at Næstved, thefrequency of this lesion is still higher than at Æbelholt. AtNæstved, 61% of preadults have cribra orbitalia, com-pared to 54% at Æbelholt. The similar pattern of cribraorbitalia of the preadult and adult population of Næstvedmay reflect the same pathogen load and hygienic andnutritional factors, while the much lower prevalence inadults at Æbelholt is thought to represent the expecteddistribution, with the presence of most cribra orbitalia inthe preadult group compared to adults (Stuart-Macadam,1991).The absence of rhinomaxillary changes in the majority

of Næstved preadults does not necessarily confirm thatthey were free from leprosy. While they may have sufferedfrom leprosy at the lower end of the immunity scale, theyoungest individuals may never have developed leprosy.Although there is evidence of lepromatous leprosy in 3 of23 individuals from the 6.6–10.5-year age group, theirnumbers are probably too small for any differences toaffect the BMC and long bone length curves (Fig. 3). It isunlikely that the youngest members of the sample (0–6.5year) entered the site by virtue of having leprosy, which

TABLE

4.Percentageof

stress

indicators,divided

into

ageca

tegories(prevalence)1

Cribra

orbitalia

Enamel

hypop

lasias

Periostitis

Endocraniallesion

sMaxillary

sinusitis

Age(yea

rs)

Nwith

orbits

%A

(N)

%b

Nwith

teeth

%A

(N)

%b

Nwith

tibiae

%A

(N)

%b

Nwith

skulls

%A

(N)

%b

Nwith

sinuses

%A

(N)

%b

Æbelh

olt

0–2.5

29

10(6)

21

19

0(0)

019

0(0)

025

77(7)

28

110(0)

02.6–6.5

37

37(21)

58

48

0(0)

037

3(3)

845

22(2)

436

0(0)

06.6–10.5

25

28(16)

64

31

52(11)

35

21

2(2)

19

23

0(0)

020

57(4)

20

10.6–14.5

12

19(11)

92

18

38(8)

44

550(2)

50

12

0(0)

011

43(3)

27

14.6–20.0

55(3)

60

79(2)

28

30(0)

07

0(0)

04

0(0)

0

Total

108

53(57)

123

17(21)

88

8(7)

112

8(9)

82

8.5

(7)

Næstved

0–2.5

13

19(7)

54*

10

9(2)

20

714(2)

28

13

54(6)

46

88(1)

12

2.6–6.5

10

19(7)

70

70(0)

05

7(1)

20

10

36(4)

40*

80(0)

06.6–10.5

15

17(6)

40

12

39(9)

75

914(2)

22

69(1)

612

15(2)

17

10.6–14.5

717(6)

86

922(5)

75

714(2)

28

80(0)

08

23(3)

37

14.6–20.0

15

28(10)

67

17

30(7)

56

1150(7)

64

17

0(0)

018

54(7)

39

Total

60

60(36)

55

42(23)*

39

35(14)

64

17(11)

54

24(13)*

1%A,percentageaffectedof

totalindividuals

observed

;%b,percentageaffectedin

each

agegroup.

*Significantlyhigher

atNæstved

comparedto

Æbelholt(�

2,P¼

0.005).

Fig. 4. Prevalence of stress indicators.

Fig. 5. Developmental age of dental hypoplasia.


would suggest that they contracted the disease in utero,or shortly after birth. Such infections are rarely recog-nized today, and even less so in the medieval period(Alford et al., 1975). The small number of fetal and infantremains (n ¼ 14) at Næstved suggests that few babieswere born in the hospital sample. Those born to motherswith lepromatous leprosy today are very weak, growslowly, and die early if untreated. Therefore, if babieswere regularly born in the leprosarium, a higher numberof infant deaths would be expected than at Æbelholt, eventhough the fertility rate was lower.It is more probable that children who entered the lepro-

sarium with their parents eventually developed the dis-ease. In South India, a study of children living in a lepro-sarium showed that, after long exposure to the diseasethrough parents and patients, children did contract thedisease, but that 75% of them had complete remissionwithin 6 years (Berreman, 1984). It is possible that someof these children relapsed with the onset of puberty.Children may also have contracted the disease in the vil-

lage and surrounding area and been brought into the lepro-sarium during later childhood, around age 6–10 years.Modern studies show an increase in the prevalence of lep-rosy in children by the age 7 years, and indeed in theNæstved sample, the youngest skeleton displaying rhino-maxillary changes is 8 years old. The increase in number ofpreadults older than 6.6 years may indicate that after thisage, children were being identified as leprous and enteredthe sample from outside. The greater number of childrenbetween ages 6–17 in the leprosarium would of course haveincreased the number of children who died and entered themortuary sample. This further increase in number of indi-viduals is consistent with the observation that the diseaseis most prominent in the late teens (Duncan, 1985).

CONCLUSIONS

Compared with children interred at the monastery siteof Æbelholt, those from the leprosarium at Næstved canbe considered socially disadvantaged and suffering fromcompromised health. They displayed higher frequencies ofstress indicators, which is likely an illustration of thehigher exposure to risk and greater susceptibility of theseindividuals to infection and malnutrition.

While the demographic profile at Æbelholt was similarto an ordinary medieval parish cemetery, Næstved hadrather few young children but high numbers in their lateteens. This pattern is clearly a product of the artificialnature of the Næstved population, reflecting the late ageof admission to the leprosarium and an altered reproduc-tive pattern of the inmates. Also, the adult populationfrom Næstved displays a skewed profile, with high figuresfor young adults and a sparse representation of old adults.Thus the nonattritional demographic profile at Næstved ischaracteristic of the entire population. It indicates thesocially imposed selection of the living population and theinevitably resulting unusual mortality profile in the skele-tal assemblage. Leprosy and its concomitant pathologicalchanges only exacerbated a situation in which social seg-regation was already a high price to pay.The distribution of stress indicators of preadults at

Æbelholt and Næstved related to age bears a vague indi-cation that, in general, stress indicators were more preva-lent in older age groups. However, this may in part beinfluenced by both the age distribution of the samples andthe skeletal modifications themselves. Yet there is a cleartrend toward gradual age-related accumulation of stressindicators in the leprosarium sample. The only lesionsthat were significantly associated with decreased longev-ity in both groups were those on the endocranial surfaces.By age 10 years, long bone growth of the Næstved chil-

dren fell behind that of Æbelholt, which is most likelyattributable to growth retardation resulting from effectsof leprosy. This is corroborated by a drop in bone mineralcontent values during adolescence, demonstrating theusefulness of this noninvasive method in providing dataon appositional growth and mineralization.Studies of preadult samples are beneficial to skeletal

studies because they are not stricken with the inherentmethodical flaws of adult aging, and are thus able to pro-vide a sensitive indicator of health for past societies byexamining those particularly susceptible to disease andmost at risk. However, these studies are limited to thoseindividuals who failed to adapt to the environmental andcultural factors influencing their community. At Næstved,preadults were ‘‘selected’’ to enter the leprosarium, andlater the mortuary sample, because they were sufferingfrom a disease, and therefore their members are not repre-sentative of the society from which they were drawn. The

TABLE 5. Mean ages at death for individuals with and without stress indicators1

Stress indicator

With WithoutDifference(years)

Statics(Kolmogorov-

Smimov)Mean SD Mean SD

ÆbelholtCribra orbitalia 7.62 3.69 4.79 4.4 2.8Enamel hypoplasia 10.8 2.53 6.27 4.06 4.5** K ¼ 2.0Periostitis 8.1 3.03 5.6 4.22 2.5Endocranial lesions 1.62 0.77 6.8 4.34 5.1* K ¼ 1.78Sinusitis 8.0 3.49 5.57 4.24 2.4* K ¼ 1.43

NæstvedCribra orbitalia 9.91 6.28 9.3 6.57 0.6Enamel hypoplasia 12.7 5.03 9.16 6.21 6.5Periostitis 13.8 5.48 9.83 5.86 3.9Endocranial lesions 3.4 3.02 10.9 5.89 7.5* K ¼ 1.84Sinusitis 12.45 6.52 9.27 5.16 3.1Rhinomaxillary syndrome 14.4 4.29 8.89 5.49 5.5

* K, Kolmogorov-Smimov.** Significant at P < 0.05.


study shows that it is imperative to be aware of the cul-tural, historical, and economic context from which a popu-lation is derived before the morbidity and mortality pat-terns of a past society can be reconstructed.This becomes evident, in particular, when single age

groups rather than bulk categories are examined. Whilethe combined preadult samples create patterns that favortraditional views on the meaning of skeletal modifications,only a differential analysis of single age groups reveals theparadoxical relationship of health, morbidity, and osseousmanifestations that is advocated as typical of skeletalassemblages. Thus the characteristic distribution of stress-related skeletal modifications across various preadult agegroups lends itself to a biocultural analysis that is able toidentify the more subtle effects of social disadvantage andcompromised health.

ACKNOWLEDGMENTS

The research was funded by grant ERBCHRXCT930193 to P.B. under EU Program Human Capital andMobility and carried out at the Museum of Medical His-tory and Laboratory of Biological Anthropology, Univer-sity of Copenhagen, Denmark. We are most grateful toInger Kjær,Verner Alexandersen and Birgitte Sejersen forhelpful discussions.

LITERATURE CITED

Acheson RM. 1959. Effects of starvation, septicaemia and chronicillness on the growth cartilage plate and metaphysis of theimmature rat. J Anat 9:123–134.

Acheson RM,MacIntyre MN. 1958. The effects of acute infection andstarvation on skeletal development. Br J Exp Pathol 39:37–45.

Alford CA, Stagno S, Reynolds W. 1975. Diagnosis of chronicperinatal infections. Am J Dis Child 129:455–463.

Andersen JG. 1969. Studies in the medieval diagnosis of leprosyin Denmark: an osteological, historical and clinical study.Copenhagen: Costers Bogtrykkeri.

Andersen JG. 1991. The medieval diagnosis of leprosy. In: OrtnerDJ, Aufderheide AC, editors. Human paleopathology: currentsynthesis and future options. Washington, DC: SmithsonianInstitution Press. p 205–208.

Arentoft E. 1999. De spedalskes hospital. Fynske studier 18.Odense: Odense Bys Museer.

Beaton GH. 1989. Small but healthy? Are we asking the rightquestion? Hum Organisation 48:30–39.

Bennike P. 2000. A Medieval mass grave from Denmark (1300–1350 AD). Am J Phys Anthropol [Suppl]30:106 [abstract].

Bennike P. 2002. Vilhelm Møller-Christensen: his work and leg-acy. In: Roberts CA, Lewis ME, Manchester K, editors. Thepast and present of leprosy. BAR international series 1954.Oxford: Archaeopress. p 135–144.

Bennike P, Brade AE. 1999. Middelalderens sygdomme ogbehandlingsformer i Danmark [Disease and treatment in medi-eval Denmark]. Copenhagen: Museum of Medical History.

Bennike P, Bohr H, Toft T. 1993. Determination of mineral con-tent and organic matrix in bone using dual photon absorpti-ometry. Int J Anthropol 8:111–116.

Berreman JM. 1984. Childhood leprosy and social response inSouth India. Soc Sci Med 19:853–865.

Boldsen J. 2001. Epidemiological approach to the paleopatholog-ical diagnosis of leprosy. Am J Phys Anthropol 115:380–387.

Boocock PA, Roberts CA, Manchester K. 1995. Prevalence ofmaxillary sinusitis in leprous individuals from a medieval lep-rosy hospital. Int J Lepr 63:265–268.

Brody SN. 1974. The disease of the soul: leprosy in medieval lit-erature. Ithaca: Cornell University Press.

Buikstra JE, Ubelaker DH. 1994. Standards for data collectionfrom human skeletal remains.Arkansas Archaeological Surveyresearch series44. Fayetteville: Arkansas Archaeological Survey.

Carlson DS, Armelagos GJ, Van Gerven DP. 1976. Patterns ofage-related cortical bone loss (osteoporosis) within the femoraldiaphysis. Hum Biol 48:295–314.

Cohen MN, Armelagos GJ. 1984. Paleopathology at the originsof agriculture. New York: Academic Press, Inc.

Cole TJ. 1989. Relating growth rate to environmental factors—methodological problems in the study of growth-infection in-teraction. Acta Paediatr Scand Suppl 350:14–20.

Cook DC. 1984. Subsistence and health in the Lower IllinoisValley: osteological evidence. In: Cohen MN, Armelagos GJ,editors. Paleopathology at the origins of agriculture. Orlando,FL: Academic Press, Inc. p 235–269

Cook DC, Buikstra JE. 1979. Health and differential survival inprehistoric populations: prenatal dental defects. Am J PhysAnthropol 51:649–664.

Duncan ME. 1980. Babies of mothers with leprosy have smallplacentae, low birth weights and grow slowly. Br J ObstetGynaecol 87:471–479.

Duncan ME. 1985. Leprosy in young children-past, present andfuture. Int J Lepr 53:468–473.

Duncan ME, Melsom R, Pearson JMH, Ridley DS. 1981. Theassociation of pregnancy and leprosy. Lepr Rev 52:245–262.

Duray SM. 1996. Dental indicators of stress and reduced age ofprehistoric Native Americans. Am J Phys Anthropol 99:275–286.

El-Najjar M, Ryan DJ, Turner C, Lozoff B. 1979. The aetiologyof porotic hyperostosis among the historic and prehistoricAnasazi Indians of southwestern United States. Am J PhysAnthropol 44:477–488.

Eveleth PB. 1986. Population differences in growth: environ-mental and genetic factors. In: Falkner F, Tanner JM, editors.Human growth: a comprehensive treatise. New York: PlenumPress. p 221–239.

Eveleth PB, Tanner JM. 1990. Worldwide variation in humangrowth. Cambridge: Cambridge University Press.

Falkner F, Tanner JM. 1986. Human growth: a comprehensivetreatise. New York: Plenum Press.

Gilbert RI. 1985. Stress, paleonutrition, and trace elements. In:Gilbert RI, Mielke JM, editors. The analysis of prehistoricdiets. Orlando, FL: Academic Press, Inc. p 339–356.

Goodman AH. 1993. On the interpretation of health from skele-tal remains. Curr Anthropol 34:281–288.

Goodman AH, Rose JC. 1990. Assessment of systemic physiolog-ical perturbations from dental enamel hypoplasia and associ-ated histological structures. Yrbk Phys Anthropol 33:59–110.

Goodman AH, Rose JC. 1991. Dental enamel hypoplasia as indi-cators of nutritional status. In: Kelley MA, Larsen CS, edi-tors. Advances in dental anthropology. New York: Wiley andLiss Inc. p 279–293.

Goodman AH, Martin DL, Armelagos GJ, Clark G. 1984. Indica-tors of stress from bone and teeth. In: Cohen MN, ArmelagosGJ, editors. Paleopathology at the origins of agriculture.Orlando, FL: Academic Press, Inc. p 13–49.

Goodman AH, Thomas RB, Swedlund AC, Armelagos GJ. 1988. Bio-cultural perspectives on stress in prehistoric, historical, and con-temporary population research. Yrbk Phys Anthropol 31:169–202.

Grauer AL. 1993. Patterns of anaemia and infection from Medi-eval York, England. Am J Phys Anthropol 91:203–215.

Hauhnar CZ, Mann SBS, Sharma VK, Mehta S, Radota BD.1992. Maxillary antrum involvement in multibacillary lep-rosy: a radiological, sinuscopic and histological assessment.Int J Lepr 60:390–395.

Hillson S. 2000. Dental anthropology. Cambridge: CambridgeUniversity Press.

Huss-Ashmore R. 1978. Nutritional determination in skeletalpopulations. Am J Phys Anthropol 48:407.

Jantz RL, Owsley WD. 1984. Long bone growth variation amongArikara skeletal populations. Am J Phys Anthropol 63:13–20.

Johnston FE. 1962. Growth of the long bones of infant and youngchildren at Indian Knoll. Am J Phys Anthropol 20: 249–254.

Jopling WH, McDougall AC. 1988. Handbook of leprosy. Oxford:William Heinemann Medical Books.

Kieffer-Olsen J. 1993.Grav og gravskik i det middelalderligeDanmark. 8 kirkegardsudgravninger. Unpublished Ph.D. the-sis. Aarhus: Aarhus University.


Kirkwood BR. 1988. Essentials of medical statistics. London:Blackwell Scientific Publications.

Lampl M, Johnston FE. 1996. Problems in the aging of skeletaljuveniles: perspectives from maturation assessments of livingchildren. Am J Phys Anthropol 101:345–355.

Lara CB, Nolesco JO. 1956. Self-healing or abortive, and resid-ual forms of childhood leprosy and their probable significance.Int J Lepr 24:245–263.

Larsen CS. 1997. Bioarchaeology. Interpreting behavior fromthe human skeleton. Cambridge: Cambridge University Press.

Lewis AB, Garn SM. 1960. The relationship between tooth forma-tion and other maturational factors. Angle Orthod 30:70–77.

Lewis M. 2002a. Urbanisation and child health in medievaland post-medieval England. BAR British series 339. Oxford:Archaeopress.

Lewis M. 2002b. The impact of industrialization: comparativestudy of child health in four sites from medieval and post-medieval England (850–1859 AD). Am J Phys Anthropol119:211–223.

Lewis M. 2002c. Infant and childhood leprosy: clinical andpalaeopathological implications. In: Roberts C, Lewis M,Manchester K, editors. The past and present of leprosy.BARinternational series1954. Oxford: Archaeopress. p 163–170.

Lewis M. 2004. Endocranial lesions in non-adult skeletons:understanding the aetiology. Int J Osteoarchaeol 14:82–97.

Lewis ME, Roberts CA, Manchester K. 1995. Comparative studyof the prevalence of maxillary sinusitis in later medievalurban and rural populations in Northern England. Am J PhysAnthropol 98:497–506.

Little MA. 1995. Adaptation, adaptability and multidisciplinaryresearch. In: Boaz NT, LD Wolfe, editors. Biological anthropol-ogy: the state of the science. Corvallis: Oregon State Univer-sity Press. p 121–147.

Lunt DA. 1969. An odontometric study of Medieval Danes. ActaOdontol Scand [Suppl]55:27.

Macey JF. 1996. Demography and disease of the Næstved Helli-gandshus collection. MA thesis. Memorial University ofNewfoundland, St. Johns.

Malina RM, Bouchard C. 1991. Growth, maturation and physi-cal activity. Champaign: Human Kinetics Publishers Inc.

Maresh MM. 1940. Paranasal sinuses from birth to adolescence.Am J Dis Child 60:55–78.

Martin D, Armelagos GJ. 1979. Morphometrics of compact bone:an example from Sudanese Nubia. Am J Phys Anthropol51:571–578.

Melsom R, Harboe M, Duncan ME. 1982. IgA, IgM and IgAanti-M-leprae antibodies in babies of leprosy mothers duringthe first 2 years of life. Clini Exp Immunol 49:532–542.

Mensforth RP. 1985. Relative tibia long bone growth in the Lib-ben and Bt-5 prehistoric skeletal populations. Am J PhysAnthropol 68:247–262

Mensforth RP, Lovejoy CO, Lallo JW, Armelagos GJ. 1978. Therole of constitutional factors, diet and infectious disease inthe aetiology of porotic hyperostosis and periosteal reactionsin prehistoric infants and children. Med Anthropol 2:1–59.

Merrett DC, Pfeiffer S. 2000. Maxillary sinusitis as an indicatorof respiratory health in past populations. Am J Phys Anthro-pol 111:301–318.

Mittler DM, Van Gerven DP, Sheridan SG, Beck R. 1992. Theepidemiology of enamel hypoplasia, cribra orbitalia, and sub-adult mortality in an ancient Nubian population. J Palaeopa-thol 2:143–150.

Møller-Christensen V. 1961. Bone changes in leprosy. Copenha-gen: Munksgaard.

Møller-Christensen V. 1978. Leprosy changes of the skull.Odense: Odense University Press.

Møller-Christensen V. 1982. Æbelholt kloster. 2nd ed. Copenha-gen: Nationalmuseet.

Møller-Christensen V, Sandison AT. 1963. Usura orbitae (cribraorbitalia) in the collection of crania in the Anatomy Departmentof the University of Glasgow. Pathol Microbiol 26:175–183.

Moorrees CFA, Fanning EA, Hunt EE. 1963a. Formation andresorption of three deciduous teeth in children. Am J PhysAnthropol 21:205–213.

Moorrees CFA, Fanning EA, Hunt EE. 1963b. Age variation offormation stages for ten permanent teeth. J Dent Res 42:1491–1502.

Olivier G, Pineau H. 1960. Nouvelle determination de la taillefœtale d’apres les longueurs diaphysaires des os longs. AnnMed Legale 40:141–144.

Ortner DJ. 1991. Theoretical and methodological issues in pale-opathology. In: Ortner DJ, Aufderheide AC, editors. Humanpaleopathology: current synthesis and future options. Washington,DC: Smithsonian Institute Press. p 5–11.

Ortner DJ. 2003. Identification of pathological conditions inhuman skeletal remains. London: Academic Press.

Ortner DJ, Ericksen MF. 1997 Bone changes in the human skullprobably resulting from scurvy in infancy and childhood. IntJ Osteoarchaeol 7:212–220.

Ortner DJ, Butler W, Cafarella J, Milligan L. 2001 Evidence ofprobable scurvy in subadults from archaeological sites inNorth America. Am J Phys Anthropol 114;343–351.

Rallison ML. 1986. Growth disorders in infants, children andadolescents. New York: John Wiley and Sons, Inc.

Reinhard KJ. 1992. Patterns of diet, parasitism and anaemia inprehistoric west North America. In: Stuart-Macadam P, Kent S,editors. Diet, demography and disease: changing perspectives ofanaemia. NewYork: Aldine de Gruyter. p 219–260.

Richards P. 1977. The medieval leper and his northern heirs.Cambridge: D.S. Brewer.

Roth EA. 1992. Applications of demographic models to paleode-mograpy. In: Saunders SR, Katzenberg MA, editors. Skeletalbiology of past peoples: research methods. New York: Wiley-Liss, Inc. p 175–188.

Ruff CB, Haynes C. 1984. Bone mineral content in the lowerlimb. J Bone Joint Surg [Am] 66:1024–1031.

Saunders SR, Hoppa RD. 1993. Growth deficit in survivors andnon-survivors: biological mortality bias in subadult skeletalsamples. Yrbk Phys Anthropol 36:127–151.

Scheuer L, Black S. 2000. Development: juvenile osteology. Lon-don: Academic Press.

Schour I, Massler M. 1940. Studies in tooth development: thegrowth pattern of human teeth. J Am Dent Assoc 27:1778–1793, 1918–1931.

Schultz M. 2001. Palaeohistopathology of bone: a new approach tothe study of ancient diseases. Yrbk Phys Anthropol 44:106–147.

Schutkowski H, Grupe G. 1997. Correlations between cribraorbitalia, archaeometric analyses and habitat conditions.Anthropol Anz 55:155–166.

Scrimshaw NS, Young WR. 1989. Adaptation to low protein andenergy intakes. Hum Organisation 48:20–30.

Scrimshaw NS, Taylor CE, Gordon JE. 1959. Interactions ofnutrition and infection. Am J Med Sci 237:367–403.

Seckler D. 1982. Small but healthy? Some basic problems in theconcept of malnutrition. In: Sukhatme PV, editor. Newerconcepts in nutrition and their implications for policy. Pune,India: Maharashtra Association for the Cultivation of Science.p 139–148.

Smith HB. 1991. Standards of human tooth formation and den-tal age assessment. Adv Dent Anthropol 8:143–168.

Soni NK. 1989. Antroscopic study of the maxillary antrum inlepromatous leprosy. J Laryngol Otol 103:502–503.

Stini WA. 1985. Growth rates and sexual dimorphism in evolu-tionary perspective. In: Gilbert RI, Mielke JH, editors. Theanalysis of prehistoric diets. Orlando: Academic Press. p 191–222.

Stuart-Macadam P. 1991. Anaemia in Roman Britain.BAR inter-national series199. Oxford Archaeopress. p 101–113.

Stuart-Macadam P, Kent S. 1992. Diet, demography and dis-ease: changing perspectives of anaemia. New York: Aldine deGruyter.

Subira M, Alesan A, Malgosa A. 1992. Cribra orbitalia andnutritional deficiency. Studies of trace elements. Munibe[Suppl]8:153–158.

Tanner JM. 1990. Foetus into man: physical growth from concep-tion to maturity. Cambridge, MA: Harvard University Press.

Thompson DD. 1980. Age changes in bone mineralization, corticalthickness, and Haversian canal area. Calcif Tissue Int 31:5–11.


Van Gerven DP, Armelagos GJ. 1983. ‘‘Farewell to paleodemog-raphy?’’ Rumours of its death have been greatly exaggerated.J Hum Evol 12:353–360.

Van Gerven DP, Sandford MK, Hummert JR. 1981. Mortalityand culture change in Nubia’s Batn el Hajar. J Hum Evol 10:395–408.

Wald ER, Milmoe GJ, Bowen AD, Ledesma-Medina J, SalamonN, Bluestone CD. 1981. Acute maxillary sinusitis in children.N Engl J Med 304:749–755.

Wall CE. 1991. Evidence of weaning stress and catch-up growthin the long bones of a central California Amerindian sample.Ann Hum Biol 18:9–22.

Wapler U, Crubezy E, Schultz M. 2004. Is cribra orbitalia syn-onymous with anemia? Analysis and interpretation of cranialpathology in Sudan. Am J Phys Anthropol 123:333–339.

Weinberg ED. 1992. Iron withholding in prevention of disease.In: Stuart-Macadam P, Kent S, editors. Diet, demography anddisease: changing perspectives of anaemia. New York: Aldinede Gruyter. p 105–150.

WHO Working Group. 1986. Use and interpretation of anthro-pometric indicators of nutritional status. Bulletin WHO 64:929–941.

Wood JW, Milner GR, Harpending HC, Weiss KM. 1992.The osteological paradox. Problems of inferring prehis-toric health from skeletal samples. Curr Anthropol 33:343–370.

Wright D. 1979. Acute sinusitis. In: Ballantyne J, Groves J,editors. Scott-Browne’s diseases of the ear, nose and throat.London: Butterworths. p 243–271.


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