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Developmental diachronic and demographic analysis of cribra orbitalia in the medieval christian populations of Kulubnarti.

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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.
([1981] 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. ([1974] 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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Aksoy M, Camli N, and Erdem S (1966) Roentgenographic bone changes in chronic iron deficiency anemia: A study in twelve patients. Blood 27r677-686.
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deficiency anemia and the productivity of adult males
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