Developmental diachronic and demographic analysis of cribra orbitalia in the medieval christian populations of Kulubnarti.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 93287-297 (1994) Developmental, Diachronic, and Demographic Analysis of Cribra Orbitalia in the Medieval Christian Populations of Kulubnarti DIANE M. MITTLER AND DENNIS P. VANGERVEN Department of Anthropology, University of Colorado, Boulder, Colorado 80309 KEY WORDS Stress, Nubia Porotic hyperostosis, Iron deficiency anemia, ABSTRACT Previous analysis of cribra orbitalia in the medieval populations of Kulubnarti focused only on the presence or absence of the lesion relative to age, sex, and cultural period. Demographic consideration of the lesion was limited to a gross comparison of lesion frequencies and probabilities of dying by age group. The scope of the earlier work has been expanded in the present research to include the consideration of cribra orbitalia from a developmental, demographic, and diachronic perspective. The sample consisted of the same 334 crania analyzed by Van Gerven et al. ( J. Hum. Evol. 10:395408). All skulls showing the lesion were dichotomized as active or healing, and separate life tables were constructed for those with lesions and those without. The results demonstrate that active lesions are confined entirely to infancy and childhood with formation beginning as early as six months and ending by the twelfth year. This childhood pattern is consistent with the iron deficiency anemia hypothesis proposed by Carlson et al. ( J. Hum. Evol. 3:405410). Among young adults (16-40), healing lesions occur more frequently in males than females. In the older age categories, however, females exhibit a higher frequency of partially healed lesions than males. A life table comparison of those with and those without cribra orbitalia reveals a dramatic reduction in mean life expectancy for those with the lesion across the formative childhood years (birth-16). This reduction peaks at age 5 where 78% of the children exhibit lesions and where they, as a group, have a mean life expectancy 15.5 years below those without the lesion. 0 1994 Wiley-Liss, Inc The purpose of this research was to pro- tirely on the presence or absence of the levide a developmental, demographic, and sion relative to age, sex, and cultural period. diachronic analysis of cribra orbitalia in two The present research provides a more deChristian populations from the medieval tailed developmental, demographic, and diasite of Kulubnarti in Sudanese Nubia. Cri- chronic consideration of the lesion. Clinical and archaeological studies have bra orbitalia and other types of porotic hyperostosis are valuable markers of nutri- provided evidence supporting iron defitional stress, which have been applied ciency anemia as the principle factor conwidely to archaeological remains (Goodman tributing to cribra orbitalia. In 1936, Shelet al., 1984; Huss-Ashmore et al., 1982) in- don clinically described bony changes in the cluding Nubian skeletal populations from several cultural horizons (Carlson et al., 1974; Sandford et al., 1983; Van Gerven et Received August 23,1991; accepted October 5,1993. al., 1981). Previous studies of cribra orbitaAddress reprint requests to Diane Mittler, 203 Road 2800, lia in the Kulubnarti remains focused en- Aztec, NM 87410. 0 1994 WILEY-LISS, INC. 288 D.M. MI’ITLER AND D.P. VANGERVEN skull occurring with iron deficiency anemia. Roentgenograhic analyses have since provided additional evidence of cranial changes (including diploic thickening and a hair-onend pattern in the trabeculae) occurring with iron deficiency anemia (Aksoy et al., 1966; Britton et al., 1960; Burko et al., 1961; Eng, 1958; Moseley, 1961; Powell e t al., 1965; Shahidi and Diamond, 1960). Eng (1958) argued that these changes were suggestive of bone marrow hyperplasia. This results from a n increase in the production of erythrocytes and of the precursors of red blood cells accompanying iron deficiency anemia (El-Najjar et al., 1976). Hyperplasia of the marrow leads to the physical expansion of the diploic space and to the thinning and destruction of the outer table of the cranium (El-Najjar et al., 1976). Similar bony changes have been documented in archaeological populations. Having examined the skeletal remains of over 400 European, tropical, and sub-tropical individuals, Hengen (1971) concluded that iron deficiency anemia, resulting primarily from parasitism, was strongly associated with the occurrence of cribra orbitalia. In 1974, Carlson et al. examined Nubian skeletal remains from Meroitic, X-Group, and Christian cultural horizons excavated near Wadi Halfa and concluded that chronic iron deficiency anemia contributed to the observed pattern of orbital lesions. These investigations were followed by a wave of research applying the iron deficiency hypothesis to additional populations. El-Najjar e t al. (1976) recognized a probable relationship between iron deficiency anemia and porotic hyperostosis (including cribra orbitalia) among prehistoric and historic Anasazi Indians of the United States. Lallo et al. (1977) examined the roles of diet, disease, and physiology in the etiology of porotic hyperostosis in remains from the Dickson Mounds site and concluded that dietary iron deficiency was a contributing factor. In a comparative discussion summarizing the possible etiologies of porotic hyperostosis in the Americas, Mensforth et al. (1978) presented several lines of evidence supporting iron deficiency. They noted that iron deficiency anemia is the most prevalent nutritional deficiency worldwide today; porotic hyperostosis is a similarly widespread phenomenon, observable in prehistoric populations of both the Old and New World. In addition, a high correspondence between lesion frequency and the distribution of low iron diets was noted. Finally, Mensforth et al. observed t h a t “at present, there is no reliable evidence to suggest that any of the hemolytic anemias associated with the skeletal changes observed in porotic hyperostosis in the Old World were operative as a selective factor in the pre-Columbian New W o r l d (Mensforth et al., 1978:7). Amino acid and trace element analyses of bone and hair from skeletal populations have provided evidence of lower iron levels among those exhibiting porotic hyperostosis. Von Endt and Ortner (1982) analyzed the amino acid content of bone from a prehistoric native American Indian child with porotic hyperostosis and compared it to unaffected prehistoric and modern individuals. These authors observed trends in the amino acid profile of the affected child which were consistent with iron deficiency anemia. Sandford et al. (1983) performed trace element analysis on the hair of the present Christian sample. A comparison of iron levels demonstrated that those with porotic hyperostosis had significantly lower levels of iron than those without the lesion. Given the strong association between porotic hyperostosis and iron deficiency anemia, a more detailed consideration of the orbital lesions a t Kulubnarti may provide insight into the effects of this nutritional anemia in ancient Nubia. The benefits of considering the physical state of the lesion, active or healing, have been discussed by Huss-Ashmore et al. (1982). They asserted that “analysis of healed and nonhealed lesions can provide the basis €or evaluating the age of onset for nutritional anemias and for determining the impact on the survival of those with the condition” (Huss-Ashmore et al., 1982:418). Analysis of activity and healing can also provide the opportunity for evaluation of Stuart-Macadam’s (1985) suggestion that cribra orbitalia is typically a childhood condition. Stuart-Macadam proposed that adult iron deficiency anemia may not result in diploic expansion because “compensation for CRIBRA ORBITALIA IN MEDIEVAL KULUBNARTI the anemia can occur without the utilization of all the available marrow space; therefore, there is no necessity for outward expansion, even if the bone were malleable enough to respond” (Stuart-Macadam, 1985:397). If iron deficiency in adults does not result in orbital bony changes, the absence of active lesions would be predicted. Cribra orbitalia in adults, then, would reflect anemia occurring during childhood. MATERIALS AND METHODS The present sample included 334 crania representing both sexes and all ages from 5 months in utero to 51+ years. The remains were exhumed from two diachronic cemeteries at the medieval site of Kulubnarti located in the Batn el Hajar (“belly of rock) region of Upper Nubia (Fig. 1). The earliest cemetery (2143-46) dates t o early Christian times (circa 550-750 A.D.) and provided 170 individuals for the present investigation. The remainder of the sample (164 individuals) was exhumed from a late to terminal Christian cemetery (21-R-2) dated from circa 750-1500-t A.D. Criteria used t o estimate age at death and sex have been described by Van Gerven and associates (1981). All crania were examined macroscopically for the presence of cribra orbitalia; lesions were then classified as either active or healing (Figs. 2, 3). Active lesions were defined as those exhibiting porosity interspersed with increasingly thin bridges of bone, creating a sieve-like appearance. Healing lesions were identified based on the presence of a “smooth lamellar texture with bone filling of the peripheral pores” (Mensforth et al., 1978:23). Following the classification, individuals with and without the orbital lesions were compared using composite life table techniques. Age categories used for the tables were adapted from Van Gerven et al. (1981). RESULTS The initial demographic analysis by age and sex were conducted on the combined cemetery sample. Cribra orbitalia was observed in 149 (45%)of the 334 crania examined (Table 1). The lesion first appears at 6 months of age and increases in frequency to 289 a maximum of 78% between ages 4 and 6 (Fig. 4). This age-related increase is statistically significant (P< 0.0005) and corresponds closely to the results of previous examinations of the Kulubnarti population (Van Gerven et al., 1981; Sanford et al., 1983). The percentage of affected individuals remains above 70% until age 13. Throughout adulthood (16-51 +), lesion frequencies fluctuate between 17 and 38%with an overall post-childhood average of 30%. The significantly ( P < 0.05) higher lesion frequency associated with infancy and childhood is consistent with the pattern observed in other skeletal populations (Carlson et al., 1974; Cybulski, 1977; El-Najjar et al., 1976; Hengen, 1971; Nathan and Haas, 1966; Stuart-Macadam, 1985; Walker, 1985,1986). The implication of the age association is clarified further when a distinction is made between active and healing lesions (Fig. 4; Table 1). Through the first year of life, 100% of the individuals affected exhibit active lesions. However, between ages 1 and 3 the percentage with active lesions drops to 59%. This decline continues through age 12, beyond which all individuals show evidence of healing. Whether the underlying anemia ameliorates in later childhood or the skeleton changes in its ability to respond, the active formation of cribra orbitalia is clearly an early childhood event. The analysis of sex differences requires the examination of older adolescents and adults, all of whom show healing. Although not statistically significant, the results are nevertheless informative (Fig. 5; Table 2). Between ages 16 and 40, male lesion frequencies exceed female frequencies by an average of 48% (males = 43%; females = 29%). While this does not constitute proof of a greater male susceptability in childhood, it is highly suggestive of such a difference. Among older adults, however, the pattern is reversed. After age 40, male lesion frequencies drop to 15%while female frequencies remain near 27%. In short, while lesion frequencies in younger adult males exceed females by 48%,male frequencies fall behind females by 44%in old age. While differences in morbidity by age and sex appear evident from these data, an assessment of mortality patterns relative to D.M. MITTLER AND D.P. VANG E R W N 290 v EGYPT ’ AD1----HALFA --y 2nd CATARACT BATN EL HAJAR 5/ KULUBNARTl DAL CATARACT SUDAN 3rd CATARACT 5 t h CATARACT 4 t h CATARACF / / I I / 6th CATARACT Fig. 1. . Map of Nubia indicating Kulubnarti and the Batn el Hujur region. lesion frequencies requires a more direct demographic approach. Mean life expectancies calculated for those with and without the lesion reveal a dramatic difference, particularly during the subadult years (birth-16) (Fig. 6). Between ages 4 and 6, the life ex- CRIBRA ORBITALIA IN MEDIEVAL KULUBNARTI 291 Fig. 2. Active cribra orbitalia in the left orbit of an 8-year-old child. Fig. 3. Lesions exhibiting partial healing in the left orbit of an 11-year-old. pectancies of children with the lesion fall 15.5 years below their unaffected counterparts. In order to assess diachronic shifts in lesion frequency and pattern, the total sample was broken down into its early and late Christian components. As illustrated in Figure 7 and Table 3, lesion frequencies are higher in the sample from the early Chris- tian cemetery (21-S-46). Cribra orbitalia also appears a full year earlier and is maintained at high frequency longer. Indeed, from birth through age 12, significantly more early Christian children express active lesions (P < 0.05). The lesion may also have had a more pronounced impact on childhood mortality during early Christian times. From birth through age 15, early Christian D.M. MITTLER AND D.P. VANGERVEN 292 TABLE I. Summary data for those exhibiting cribra orbitalia and those with active lesions, by age, in the combined samnle Cribra orbitalia Active lesions A g e Total N nl % n2 0-1 2-3 41 34 54 19 24 16 16 25 46 42 17 334 7 17 42 14 18 8 6 7 17 10 3 149 17.07 50.00 77.78 73.68 75.00 50.00 37.50 28.00 36.96 23.81 17.65 44.61 7 10 16 4 3 0 0 0 0 0 0 40 4 4 7-9 10-12 13-15 16-20 21-30 3140 41-50 51+ Total ACTlVE 80 - so - MALFS P 3 s9 * 4 Y 4)- Y 30 - 5F 20 - f! T 50 u e ' * 30 c. 5 2 'L: 20 10 O 100.00 58.82 38.10 28.57 16.67 0.00 0.00 0.00 0.00 0.00 0.00 26.85 I: 70 --+ t %ofnl .~ l0- - c l , , , , o o o , , , , , 7 "o "m p, ;- - - r o - i + - m I O &N - 0 e AGE Fig. 4. Percentages of those with cribra orbitalia exhibiting active and healing lesions by age. 0 c1 N T 0 P - c. 0 r .+ rn 0 AGE Fig. 5. Percentages of adult males and adult females in the combined cemeteries cribra orbitalia by age. ford, 1984; Van Gerven et al., 1981, 1990) have demonstrated that the Kulubnarti populations were experiencing high levels of stress, including poor nutrition and disease. In this context, the high incidence of iron deficiency, as reflected by cribra orbitalia, is not surprising. Like their modern counterparts, the people of Kulubnarti subsisted as sedentary agDISCUSSION riculturalists practicing small scale farming The high frequency of cribra orbitalia is (Carlson et al., 1974; Adams, 1968, 1977). consistent with previous research on the Their diet consisted primarily of cereal Kulubnarti populations. Studies of growth grains supplemented by small amounts of and development (Hummert, 1983; Hum- animal protein (Adams, 1977). Clinical mert and Van Gerven, 1983),mortality (Van research has demonstrated a strong relaGerven, et al., 1981), and pathology (Sand- tionship between this type of diet and iron children with the lesion have substantially lower mean life expectancies than those in the later Christian (21-R-2)population (Fig. 8). While this difference in survival is no doubt due t o a multiplicity of factors, it appears that one major contributor was a more frequent and longer lasting childhood anemia during earlier Christian times. CRIBRA ORBITALIA IN MEDIEVAL KULUBNARTI 293 TABLE 2. Summary data, by age and sex, for adults exhibiting cribra orbitalia in the combined sample Age Total N 16-20 21-30 3140 41-50 51+ Total Males __ Cribra orbitalia n % of males 6 3 50.00 11 3 20 25 1 63 10 27.27 50.00 16.00 0.00 31.75 4 0 20 25 - 20 - 15 - 10 - Total N 9 14 26 17 16 82 Females Cribra orbitalia n 9%of females 3 4 7 6 3 23 33.33 28.57 26.92 35.29 18.75 28.05 5 - Fig. 6. Comparison of mean life expectancies of those with and those without lesions from the combined cemeteries. deficiency. Specifically, iron deficiency frequently results from the low bioavailability of iron in many cultigens, particularly cereal grains high in phytates (Morris, 1987). The impact of low levels of dietary iron is often intensified by parasitic infections typically accompanied by gastrointestinal bleeding. The age distribution of the lesion at Kulubnarti is also consistent with the clinical pattern of iron deficiency. Just as lesion frequencies are rare among the youngest infants at Kulubnarti, iron deficiency in the first 6 months of life is extremely rare in the living. This is because iron stores accumulated in utero provide for the neonate. However, by the end of the fifth or sixth month, these stores are exhausted (Bernat, 1983) and iron deficiency becomes increasingly prevalent among infants and children. Clinically, the frequency of iron deficiency shows a further increase with weaning as children are introduced to adult foods and are increasingly exposed to gastrointestinal pathogens (Gordon et al., 1963). The resultant weanling diarrhea leads to further deterioration of nutritional status due to decreased appetite and increased metabolic loss of essential nutrients, including iron and magnesium (Gordon et al., 1963). Absence of the lesion in young infants at Kulubnarti is followed by a dramatic increase beginning in the second year of life. This trend peaks with 78% of those between 4 and 6 exhibiting the lesion. This pattern appears to reflect the increasing impact of iron deficiency accompanying weaning and weanling diarrhea. This association is further clarified by the D.M. MITTLER AND D.P. VANGERVEN 294 'In 7 xo 90 70 - 6050 - 40 - 30 20 10 0 - ' -,6 - , - c . N , \tr 1 I -'I I I q P - O " c - I , \ r P ' t 4 I 2 * 1 - I 0 2 P, N ' o , 1 N - I + 2 ' . _ ' r - - , - r e AGE Fig. 7. Comparison of percentages ofthose with cribra orbitalia in t h e early (21-S-46) and late (21-R-2) Christian cemeteries. TABLE 3. Summary data, by age and temporal period, for those exhibiting cribra orbitali and those with active lesions ~~ Ace 0-1 2-3 4 6 7-9 10-12 13-15 16-20 21-30 3140 41-50 51+ Total Total N 31 20 35 10 16 8 4 8 13 16 9 170 Early Christian (21-5-46) Cribra orbitalia Active lesions n1 o/u n2 3'% o f n 1 7 13 26 8 14 5 1 3 5 4 2 88 22.58 65.00 74.29 80.00 87.50 62.50 25.00 37.50 38.46 25.00 22.22 51.76 7 8 13 1 3 0 0 0 0 0 0 32 100.00 61.54 50.00 12.50 21.43 0.00 0.00 0.00 0.00 0.00 0.00 36.36 distinction between those with and without active lesions. All of the Kulubnarti infants and children with cribra orbitalia show active lesion development. With age, however, an increasing number of individuals show signs of healing, with all affected children showing some signs of healing by age 12. Such a pattern lends strong support to Stuart-Macadam's (1985) hypothesis that cribra orbitalia (and porotic hyperostosis in general) is a childhood condition. Patterns of healing among adults may nevertheless be informative. Most notably, the analysis of lesion frequencies and healing patterns by sex may shed light on differences in nutritional stress as well as bone maintenance. Late Christian (21-R-2) Cribra orbitalia Active lesions n3 96 n4 %ofn3 ~~ ~~ Total N 10 14 19 9 8 8 12 17 33 26 8 164 0 7 16 6 4 3 5 4 12 6 1 64 0.00 50.00 84.21 66.67 50.00 37.50 41.67 23.53 36.36 23.08 12.50 39.02 0 2 3 3 0 0 0 0 0 0 0 8 0.00 28.57 18.75 50.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 12.50 Although male-female differences in lesion frequency at Kulubnarti are not statistically signifcant, certain trends are notable. Males between 16 and 40 show higher lesion frequencies than do females. This may indicate higher lesion frequencies among subadult males. Previous analyses of childhood stress at Kulubnarti lend support to this hypothesis. For example, Moore et al. (1986) observed that subadult males experienced a significant retardation in skeletal development (relative to dental development) while females expressed no such pattern. Similarly, Van Gerven et al. (1990) observed an earlier onset and longer duration of enamel hypoplasias among males. CRIBRA ORBITALIA IN MEDIEVAL KULUBNARTI 25 - - 20 - 15 - 10 - Y 295 ?I-S-ih ? I -11-1 5 - AGE Fig. 8. Mean life expectancies of those with cribra orbitalia from the early (21-S-46)and late (21-R-2) Christian cemeteries. After age 40, the relationship of lesion frequencies between males and females changes, with the male frequency falling behind the female's by 44%.Sex differences in bone maintenance and repair provide one explanation for this shift in older adults. Moore (1987) noted a sharp decline in bone maintenance among Kulubnarti women over 40, which corresponds to a similar trend in modern post-menopausal women. Impairment of bone maintenance, resulting in osteoporosis, is accompanied by a decreased ability to lay down new bone, necessary for healing. This would explain the higher frequency of partially healed lesions among the older Kulubnarti females. Such an explanation is indirectly corroborated by the assertion of Weintroub et al. (1982) that severely osteoporotic individuals form relatively less new bone than others of the same age. While iron deficiency rarely causes death among moderns (Assembly of Life Sciences National Research Council, 1979), the pattern of reduced life expectancies among those with cribra orbitalia at Kulubnarti remains interpretable. Such anemia inhibits growth and increases susceptibility to infection (Assembly of Life Sciences National Research Council, 1979). In fact, it is often difficult to distinguish between the effects of iron deficiency on growth and the effects of other dietary insufficiencies which frequently accompany anemia. Iron deficiency may also contribute to decreased immunocompetence and a corresponding increased susceptibility to infectious disease (Bhaskaram, 1988; Sherman, 1984). In support of this relationship Basta et al. (1979) reported a higher incidence of infectious diseases among anemic individuals. Given this body of evidence, the strong association between iron deficiency and mortality at Kulubnarti is not surprising. These results also help clarify temporal changes in health and mortality from early to late Christian times. A diachronic comparison of cribra orbitalia reveals that the early Christian population experienced higher levels of stress than the later. Mean life expectancies for children with cribra orbitalia are substantially lower in the earlier population. The results of this investigation support the findings of previous research which has demonstrated that individuals living in Kulubnarti during the early Christian times were experiencing more biological stress than those living during the later period (Hummert and Van Gerven, 1983; Moore et al., 1986; Van Gerven et al., 1981, 1990). Culturally, the earlier part of the Christian era was characterized by a centralized political authority, whereas the later part was a period of political fragmentation and 296 D.M. MITTLER AND D.P. VANGERVEN regional autonomy (Van Gerven et al., 1990). Van Gerven et al. (1990) have concluded that from a biological perspective of mortality, growth and development, nutrition, and disease, the people of Kulubnarti were better off during the later period of village autonomy. This research lends strong support to that interpretation. CONCLUSIONS The analysis of cribra orbitalia at Kulubnarti demonstrates the value of this generalized stress indicator to our understanding of nutrition, health, and mortality in this ancient Medieval community. The large percentage of subadults expressing the lesion suggests a high level of childhood nutritional stress. Lesion frequency peaks between ages 4 and 6, where 78% of the children are affected. Examination of lesion status, either active or healing, also provides support for Stuart-Macadam’s (1985) assertion that cribra orbitalia represents a childhood condition. As for the consequence of the underlying anemia on childhood health and mortality, life table analysis indicates a severe reduction in life expectancy among affected individuals. Among the age groups with the highest lesion frequency (ages 4-6) there is a 15.5 year reduction in mean life expectancy. While there are no active cases of cribra orbitalia after age 12, sex differences in healing lesions among adults appear to reflect differences in childhood susceptability. Prior to age 40, male frequencies are consistently higher than female frequencies, suggesting, we believe, higher rates of anemia among subadult males. Following age 40, however, lesion frequencies among females outnumber those of males. We interpret this to reflect a general inability of older, osteoporotic, females to build the bone necessary for continued lesion healing. The present results also support earlier diachronic analyses of stress and mortality. We observe a reduction in both the frequency and severity of cribra orbitalia from early to late Christian times as well as a reduction in mortality associated with the condition. Once again, it seems clear that the Christians of Kulubnarti were better off during the later period of regional autonomy when small hamlets such as this were left to their own economic and political devices. ACKNOWLEDGMENTS This research was supported by NSF grant 9077-5-535Band by a Summer Undergraduate Research Followship from the Undergraduate Research Opportunities Program at the University of Colorado, Boulder. We are grateful to Dr. George Armelagos for his many helpful comments and suggestions during the preparation of this manuscript. We would also like t o thank Paul and Madeline Meyer for their assistance with the translation of Welcker’s original description of cribra orbitalia. 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