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Cortical bone maintenance and geometry of the tibia in prehistoric children from Nubia's Batn el Hajar.

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Cortical Bone Maintenance and Geometry of the Tibia in
Prehistoric Children From Nubia’s Batn el Hajar
University of Colorado, Boulder 0 . P . V,J . RH.),
West Virginia University,
Morgantown D.B.B.)
KEY WORDS Nubia, Kulubnarti, Cortical bone maintenance, Bone
geometry, Growth.
ABSTRACT The relationship between advancing age in adults and patterns of cortical bone maintenance has been extensively documented for archaeological populations (Dewey, et al., 1969; Van Gerven et al., 1969;
Perzigian, 1973). Most recently, this research has been expanded to include a
more thorough consideration of the geometric properties of bone in relationship
to adult age changes (Martin and Atkinsin, 1977; Ruff and Hayes, 1983). To
date, however, few studies have documented subadult patterns of cortical bone
maintenance in archaeological populations and none have incorporated the
relationship between patterns of cortical bone loss and gain and the changing
geometric properties of growing bone. Using a sample of 172 tibias from
children excavated from the Medieval Christian site of Kulubnarti, located in
Nubia’s Batn el Hajar, the present research examines the relationship between
percent cortical area, bone mineral content, and cross-sectional moments of
inertia. Among these children, bone mineral content increases steadily from
birth in spite of a reduction in percent cortical area during early and late
childhood. It appears, therefore, that tissue quality of the bone is not adversely
affected by the reduction. Furthermore, the reduction in percent cortical area
in later childhood corresponds to a dramatic increase in bending strength
measured by cross-sectional moments of inertia. Thus, whether this cortical
reduction is due entirely or in part to either normal modeling or nutritional
stress, the tissue and organ quality of the bone is not adversely affected.
Few statements in the annals of physical
anthropology have proven to be as incorrect
and yet as useful as Jarcho’s (1964) suggestion that ancient human populations did not
experience osteoporosis. Beginning with
Dewey’s initial study of cortical thickness in
adult males and females from three ancient
Nubian populations, a host of research has
demonstrated a broadly universal pattern of
bone loss with aging in ancient times generally consistent with patterns observed for
modern adults (Dewey, et al., 1969; Van Gerven et al, 1969 Perzigian, 1973). While ancient females tended to lose bone sooner and
few survived to experience the consequences
of clinical osteoporosis, then as now females
lost significant amounts of bone with advancing age while men showed less advanced-age
0 1985 ALAN R. LISS, INC.
Beyond extending our knowledge of agerelated bone loss in time and space, the analysis of ancient skeletal remains has contributed important methodological and theoretical insights into skeletal biology as a
whole. Unlike data derived from extant populations where direct measurement is frequently limited to biopsy or dissecting room
materials, archaeological remains have provided large samples of whole bones suitable
for a variety of direct and indirect methods
of measurements. Van Gerven and co-workers (1969) used archaeological remains to
conduct a controlled comparison of direct and
x-ray measurement techniques as applied to
the measurement of cortical thickness and
Received June 25,19&1, accepted September 17,1984.
cortical area in the human femur. By comparing estimates of cortical area calculated
from antero-posterior x-rays with direct measurements made from cut cross-sections of
the same bones, the research demonstrated a
serious bias in the x-ray technique. By failing to account adequately for differential
bone loss around the circumference of the
bone as well as differences in cross-sectional
geometry resulting from sex differences and
age changes in femur morphology, the x-ray
technique seriously overestimated cortical
area in older females and underestimated it
in males. Carlson et al. (1976)later sectioned
the same femurs at five sites along the diaphysis in order to further assess differential
rates of remodeling and bone loss within the
Most recently Ruff and Hayes (1983) sectioned a sample of adult femurs and tibias
from Pecos Pueblo at ten diaphyseal sites
(five femur and five tibia). In order to assess
age changes in the geometric and mechanical properties of the bones in addition to patterns of tissue loss and gain with aging, they
measured first and second moments of area
in addition to cortical, total subperiosteal,
and medullary areas. Their results revealed
an interesting interaction between age, cortical area, and geometry of the diaphysis.
While females eventually lose cortical area
as endosteal resorption exceeds subperiosteal
gain, bending strength of the diaphysis in
both the femur and tibia is not adversely
affected. In fact, the age-related redistribution of cortex from the endosteum to the subperiosteal surface results in an increase in
both maximum and minimum bending
strength (maximum and minimum moments
of area). Beyond demonstrating through direct measurement an interaction between
bending strength and geometry initially
measured indirectly through x-ray (Smith
and Walker, 1964), Ruff and Hayes have
added an important geometric and mechanical perspective to the question of osteoporotic
bone loss.
While the role of archaeological materials
in the study of adult cortical bone maintenance has been clearly extensive, the analysis of subadult remains has been less so. This
is unfortunate in view of a substantial body
of data derived largely through radiographic
techniques suggesting that cortical bone loss
is not restricted to adults. For example, a
number of researchers (Garn et al., 1964,
1969; Garn,1970; Frisancho et al., 1970 a,b;
Himes et al., 1975, 1976; Himes, 1978) have
found that among living populations relative
reductions in bone mass occur among subadults. Such reductions are frequently associated with nutritional stress.
For example, Garn et al. (1964) radiographed Guatemalan children suffering from
protein+alorie malnutrition. Relative to
healthy children, Garn observed a significant reduction in compact bone. Of particular
interest in light of Ruff and Hayes’ recent
mechanical and geometric assessment of
adult long bones, Garn found that among
malnourished children there was a trend toward greater subperiosteal diameters and reduced cortical bone (Garn, 1969).
Among the few studies of prehistoric children that have been done, a similar pattern
emerges. Cook (19791, for example, observed
a pronounced loss of cortical thickness in the
femur of Late Woodland infants during what
she estimated to be the weaning period.
Hummert (1983) examined the relationship
between longitudinal growth of the tibia1
diaphysis and percent cortical area (cortical
bone aredtotal subperiosteal area) in a large
series of ancient Nubian children from the
site of Kulubnarti in Nubia’s Batn el Hajar.
He found that among these children growth
in bone length as well as cortical area measured at the midshaft was well maintained
from birth through age 16 but that percent
cortical area reflected excessive endosteal resorption during early and later childhood. In
other words, while absolute cortical area increased steadily with bone growth, it lost
ground to the medullary canal as a percentage of total area within the periosteum.
Hummert concluded that this relative reduction in bone was generally consistent with
cortical bone loss observed among malnourished living children and interpreted his results as additional evidence of the dietary
stress previously reported for the population
(Van Gerven et al., 1981).
Taken together, analyses of cortical bone
maintenance in living as well as archaeologically derived subadults suggest a complex
interaction between growth, periosteal apposition, endosteal resorption, and cortical bone
maintenance similar to that observed for
adults. Research on subadults has not, however, taken the next logical step suggested
by Ruff and Hayes’ analysis of the adult femur and tibia, that is, to ask how changes in
the geometric properties of growing bone affect bone strength during periods of bone loss
and gain.
The purpose of the present research is to
examine the relationship between percent
cortical area, bone mineral content, and
bending strength (proportional to antero-posterior and medio-lateral cross sectional moments of inertia) in the subadult tibia. By
examining the relationship between these
variables, it should be possible to further assess the impact of cortical bone changes on
the organ and tissue properties of this long
bone in children.
The materials selected for study were excavated by the senior author from the Medieval Christian site of Kulubnarti located
some 80 miles south of Wadi Halfa in Nubia's Batn el Hajar (now part of the Republic
of Sudan). They represent the same subadult
sample examined by Hummert (1983) for
changes in percent cortical area. The total
sample of 172 individuals ranged in age from
birth (0 years) to age 16. Age categories and
sample sizes within categories is presented
in Table 1.
Age at death was determined by patterns
of dental formation and eruption as discussed
by Van Gerven et al. (1981). While sex could
be determined in a few cases as a result of
preserved genitalia, the sample was predominantly unsexable. In all cases the quality of
preservation was excellent and in most cases
some soft tissues such as skin and hair were
also preserved. Upon sectioning at midshaft,
many tibias contained some dried blood and
other soft tissues in vascular spaces within
the bone.
After sectioning, each individual was examined under a x 10 magnifying lens while
positioned beneath a transparent millimeter
grid. Calculations were made for total subperiosteal area, cortical area, and medullary
area by counting grid intersections as discussed by Martin and Armelagos (1979) and
Hummert (1983). In order to reduce error,
each count was repeated three times and averaged. Percent cortical area was then calculated by dividing cortical area by total
subperiosteal area.
Measurements of bone mineral content and
cross-sectionalmoments of inertia were made
using a Norland Cameron Bone Mineral
Analyzer with a standard 118-inch detector
Sample size
collimator, interfaced to a MITS microcomputer with an A/D input. Each tibia was
wrapped in tissue equivalence bag and
scanned at midshaft in the AP and ML
planes. Two scans were made in each plane
and the values averaged. The photon absorption curve was recorded for each scan, and
the bone mineral content (BMC) and crosssectional moments of inertia about the ML
and AP axes were calculated for this curve.
The antero-posterior cross-sectional moment
of inertia (AP CSMI) is therefore proportional to the antero-posterior bending
strength, and the medio-lateral cross-sectional moment of inertia (ML CSMn is proportional to medio-lateral bending strength.
Details of these techniques and the method
of calculating the variables are described
elsewhere (Martin and Burr, 1984).
Figure 1presents tibia length and percent
cortical areas by age group for the Nubian
sample. While growth in tibia1 length appears well maintained from birth onward,
agechanges in percent cortical area reveal a
more complex pattern. For example, there is
a considerable decline in percent cortical area
after birth followed by a steady increase to
the 12-year age group. While such a decline
followed by steady increase is normal for
modern children, Hummert (1983) has argued that the overall Nubian values are low
in comparison to well-nourished modern children. Also, while modern children show a
decline after birth, the pattern is typically
reversed by 9 months of age. The continuing
decline among the Nubian children to age 3
appears to reflect the consequences of weaning stress (Hummert, 1983).
Following age 12, the midchildhood trend
toward an increase in percent cortical area
with age is reversed. Percent cortical area in
the 15-yearage group is on average 4% below
that of the 12-year group (72% compared to
from birth through age 16. Standardizing by
cortical area produced a Merent result.
Mineral density (g/cm3) undergoes a steady
increase to age 6 and then levels off through
the remaining age groups. The difference between the two techniques can be explained
in terms of the geometry of the tibia at midshaft. At birth and through the early years
of life, the tibia is basically tubular in shape.
Consequently, bone width measurements and
cortical area produce comparable estimates
of the bone actually present in the cross secw
tion. In the present data this is reflected in
Fig. 1. The relationship between age, tibial length, the basically parallel values from birth
and percent cortical area (PCA).
through age 6. However, as the geometry of
the bone changes in later childhood, bone
width measurements increasingly underes68%)and 2% below the 9-year age group (70% timate the amount of bone actually present.
compared to 68%).This change corresponds Thus, while BMC/BW continues to rise after
to a period of rapid longitudinal growth in age 6, BMC/CA levels off. In both cases, howlength off the tibial diaphysis (Hummert, ever, bone mineral content, as a measure of
1983). Huss-Ashmore et al. (1982) observed a tissue quality, does not undergo the negative
similar relationship between accelerated changes observed for percent cortical area. In
growth and cortical reduction in a sample of fact, bone mineral values by age 16 correancient Nubians from Wadi Halfa. According spond closely to values reported for modern
to Hummert, this early teenage reduction at populations. It appears, therefore, that reKulubnarti is the result of rapid periosteal duction in percent cortical area do not result
apposition associated with overall bone in a corresponding reduction in tissue qualgrowth offset by an even more pronounced ity as measured by bone mineral content.
Age changes in cross-sectional moments of
period of endosteal resorption and increased
inertia are presented in Figure 3. As indimedullary area.
Figure 2 presents bone mineral content cated, both AP and ML CSMI undergo pro(BMC) for the Kulubnarti sample. Inasmuch gressive increase from birth through age 12
as the bone mineral analyser measures bone with a dramatic increase from 12 to 16 years.
mineral additively across the antero-poste- In AP CSMI there is a 145%increase in bendrior and medio-lateral corticies, the BMC ing strength in the 4 years following age 12.
value must be standardized for bone size. There is a corresponding 130% increase in
One standard procedure has been to divide ML strength. While changes with age in the
BMC by the corresponding AP and ML bone AP and ML planes are basically similar, difwidths (BW). This method is limited, however, by the assumption that the bone is uniformly round in cross section. A second
method for standardizing BMC is to divide
by actual cortical area. Unlike the use of
bone width, cortical area makes no assumptions about the cross-sectional geometry of
the bone. For this reason, Ruff and Hayes
(1984) have argued that cortical area is a
superior measure for standardizing BMC
values even though it cannot be directly obtained from living subjects using radio.
graphic techniques. The Kulubnarti mate0
rials provide an opportunity to compare the
two methods directly.
As indicated in Figure 2, standardizing
Fig. 2. The relationship between age and bone minBMC to bone width creates a pattern of con- eral content (BMC) standardized to cortical area (CA)
tinuous gain in mineral mass (gramdcm2) and bone width (BW.
Fig. 3. The relationship between age and antero-postenor (AP)and mediolateral (ML) cross-sectional moments of inertia (CSMI).
ferences with age are again understandable
in terms of changing geometric patterns. As
previously observed for bone width and cortical area, the tibia begins as a tubular bone
with essentially equal AP and ML strength.
However, following age 6, the geometry of
the bone undergoes progressive change. As
the bone becomes increasingly elliptical in
the AF' plane, AP bending strength increases
relative to the ML plane. While differences
by sex cannot be assessed with this sample,
the overall pattern is similar to that reported
by Ruff and Hayes (1983).
As has been demonstrated for adults, age
changes in cortical bone in subadults must
be assessed in the context of geometric and
mechanical factors related to bone growth
and development. In the case of the Kulubnarti sample, periods of relative cortical bone
loss, expressed in percent cortical area, correspond to periods of rapid diaphyseal
growth. This is true for the period from birth
through age three as well as for the post-12
age period.
Two hypotheses may be generated to explain this relationship. First, periodic reductions in percent cortical area may be a
normal part of the modeling process associated with bone growth and development. The
reduction in percent cortical area observed in
modern infants between birth and 9 months
of age clearly reflects this kind of change.
Second. reductions in Dercent cortical area
during 'periods of rapid bowth may be stress
related. Garn and co-workers' comparison of
well nourished and proteincalorie malnourished Guatamalan children (Garnet al., 1969)
has demonstrated that reductions in percent
cortical area do occur as a result of nutritional stress while other aspects of bone development remain relatively unaffected.
From the standpoint of the second hypothesis, evidence for dietary stress on the Kulubnarti children is abundant. Van Gerven et al.
(1981)have described a close correspondence
between high mortality and cribra orbitalia
in the population and more recently Sandford et al. (1983)have demonstrated a direct
relationship between reduced iron levels
measured in hair samples from the subadults
and the presence of this skeletal lesion. Furthermore, Thorp (1983)has demonstrated a
delay in skeletal maturation relative to dental development consistent with protein
Percent cortical area values for the Kulubnarti children aged birth through 3 years
suggest that the modeling and dietary stress
hypotheses may not be mutually exclusive.
While an initial loss of bone is to be expected
given the normal process of skeletal modeling, the extension of loss beyond the first
year through age 3 is not typical of modern
well-nourished children (Garn, 1970)and appears related to nutritional stress.
An interpretation of the reduction in percent cortical area following age 12 in terms
of the modeling and dietary stress hypotheses is currently hampered by a lack of
comparative data. However, regardless of
whether this loss is due entirely or in part to
either normal modeling or nutritional stress,
tissue quality measured in terms of bone
mineral is not adversely affected. And, most
importantly, the organ quality of the tibia
measured by bending strength continues on
a rapid upward trajectory consistent with the
increased mechanical demands of advancing
age and physical activity. It appears particularly significant that the most rapid increase
in cross-sectional moments of inertia occurs
during the period of pronounced percent cortical bone reduction following age 12.These
adolescent children are behaving at the organ level much like the older postmenopausal women described by RUE and Hayes
(1983).That is, while their cortex becomes
relatively thinner, the greater diameter of
their tibia actually increases bending
The adaptive implications for the skeleton
Seem clear. As long as mechanisms are avail-
able to maintain adequate growth in bone
size (including length and periosteal diameter) periodic reductions in cortical bone,
whether due to modeling or dietary stress,
need not result in reduced organ or tissue
The results of the present analysis reflect
the continuing importance of archaeological
materials to the study of skeletal biology. By
providing whole bones directly measurable
by a variety of techniques, such materials
provide an excellent opportunity to assess
properties of internal and external morphology of vital importance to human growth and
This research was supported by National
Science Foundation Grant No. BNS-7800255. Special thanks to Dr.Christopher RufF
for his helpful comments.
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geometry, hajar, batn, prehistoric, cortical, maintenance, tibial, nubian, children, bones
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