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Dental indicators of growth disturbance in a series of ancient Lower Nubian populations Changes over time.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 60463-470(1983)
Dental Indicators of Growth Disturbance in a Series of Ancient
Lower Nubian Populations: Changes Over Time
JOEL D.RUDNEY
Carialngy Postdoetoral Program, School of Dentistry, University of
Minnesota, Health Sciences Unit A, Minneapolis, Minnesota 55455
KEY WORDS
disturbance
Nubia, Striae of Retzius, Meroitic, X-Group, Growth
ABSTRACT Previous studies of accentuated striae of Retzius in tooth enamel suggest that early childhood growth disturbance tends to be severe in
state-level agricultural societies. The present study investigates the diachronic
stability of levels of growth disturbance with a series of Lower Nubian agricultural states broadly similar in terms of mode of subsistence and way of life.
The sample consists of 114 first permanent molars from the Meroitic (100 B.C.
to 300 A.D.) and X-Group(300 to 600 A.D.) cultures. These teeth were sectioned
according to standard histological technique. Data on the frequency and severity of accentuated striae of Retzius were then used to derive estimates of the
magnitude of individual growth disturbance. Populations were compared by
means of a two-way ANOVA, with growth disturbance as the dependent variable, and age and population as the independent variables. The results show
that those dying in childhood experienced significantly higher levels of early
childhood growth disturbance than did those surviving to adulthood. The
results also show a decline in growth disturbance levels over time. Both XGroup children and X-Group adults experience significantly less early childhood growth disturbance than their Meroitic counterparts. These results suggest an improvement in child health status from Meroitic to X-Group times.
Tentative explanatory hypotheses imply an increase in village autonomy, an
increase in helminthic disease related to a change in irrigation technology, or
direct and indirect effects of consumption of naturally-occurring tetracyclines.
These hypotheses are not mutually exclusive, and further research is needed
before any of them can be tested.
Growth disturbance in early childhood is a
multifactorial syndrome. Its etiology is complex, incorporating both malnutrition and infectious disease (Scrimshaw et al., 1968).
Synergistic interaction between these components often leads to systemic disruption of
normal development, in which growth may
slow down or cease altogether (De Maeyer,
1976; Susskind, 1977; Sieber and Lippman,
1980). Records of such disruption are often
preserved in hard tissue, and that has made
it possible to study growth disturbance in
ancient populations. Such studies have employed a variety of skeletal and dental indicators of growth arrest, including Harris
lines, enamel hypoplasia, bone turnover
rates, and accentuated striae of Retzius (de-
0 1983 ALAN R.LISS, INC.
velopmental microdefects in tooth enamel)
(Rose and Boyd, 1978; Armelagos, Huss-Ashmore, and Martin, 1979; Clarke, 1980; Goodman et al., 1980; Rose et al., 1981). All of
these growth arrest indicators are useful, but
accentuated striae of Retzius have been
shown to have some particular advantages.
Enamel is unique among the hard tissues in
that it does not remodel (Osborn and Ten
Cate, 1976). Thus, a record of growth disturbance during the period of enamel formation
is preserved for as long as the tooth continues
to exist. That allows for the combination,
within a sample, of both children and adults,
which permits a more unbiased estimate of
Received May 14,1982; accepted September 27, 1982.
464
J.D. RUDNEY
the full extent of growth disturbance within
an ancient population (Rose, 1973; Molnar
and Ward, 1975; Rose, 1977; Rose and Boyd,
1978; Cook, 1981).
Previous accentuated striae studies have
shown a strong link between growth disturbance and cultural evolution. Diachronic
comparisons of hunting and gathering populations with village and state-level agriculturalists indicate that levels of growth
disturbance increase as the transition to agriculture is made, and peak at the state level
of social organization (Rose, 1973,1977;Rose
et al., 1978). These studies contribute to the
understanding of biological consequences of
major culture change, but give little attention to the possibility of fluctuation in levels
of growth disturbance in the absence of such
change. The purpose of the present research
is to investigate growth disturbance levels in
a series of populations broadly similar with
respect to culture and subsistence. An accentuated striae of Retzius data base is used to
evaluate the severity of growth disturbance
in two successive state-level agricultural
populations from ancient Lower Nubia. Biocultural interpretations of the pattern of variation between these two populations are
discussed, and resulting hypotheses are then
critically evaluated.
Archeological background
Lower Nubia is the portion of the Nile Valley immediately to the south of classical
Egypt, between the First and Second Cataracts. This study deals with material from
the Meroitic (100 B.C. to 300 A.D.) and XGroup (300 to 600 A.D.) cultural horizons
(Adams, 1977). These periods display extensive similarities in settlement pattern, diet,
food preparation techniques, and agricultural practices (Trigger, 1965; Adams, 1977).
Differences are primarily political and economic in nature. During the Meroitic period,
Lower Nubia is ruled by the Upper Nubian
empire of Meroe. During the X-Group period,
Lower Nubia becomes an autonomous kingdom, and trade also declines (Adams, 1977).
Throughout both periods, the subsistence
base consists of sorghum, supplemented by
legumes, dates, mutton, goat, and other fruits
and vegetables. Agricultural activity is intensive, with irrigation being provided by an
animal-powered lifiing device, the saqia (introduced at the beginning of the Meroitic
period) Chigger, 1965; Adams, 1977).
The skeletal biology of these Nubian populations has been a topic of intensive study.
Greene (19671, Carlson and Van Gerven
(1977, 19791, and Nielsen (1970) have shown
that the Meroitic and X-Group populations
are biologically continuous, while Armelagos
(1968,1969)and coworkers have given equal
attention to the paleopathology of these
groups. Reports have been published on mortality patterns (Meroitic and X-Group),gross
skeletal pathology (Meroitic and X-Group),
patterns of bone growth (X-Group),and bone
histology (X-Group)(Armelagos, 1968, 1969;
Armelagos et al., 1972; Martin and Armelagos, 1979). Of particular relevance to the
present study are findings of porotic hyperostosis (Meroitic and X-Group), and juvenile
osteoporosis (X-Group) (Carlson et al., 1974;
Armelagos et al., 1979). Both are symptomatic of conditions (iron deficiency and parasite-mediated anemia; protein-energy malnutrition) that can promote growth disturbance with concomitant accentuated striae of
Retzius formation (Kreshover, 1960;Roseand
Pasley, 1980; Rose et al., 1981).
MATERIALS AND METHODS
Sample selection
The sample was drawn from a collection of
Lower Nubian dental material recovered
from cemeteries in the vicinity of Old Wadi
Halfa, Sudan (Greene, 1967). Previous accentuated striae of Retzius studies have relied
primarily upon the canine, because its simple crown morphology makes it easy to section, and because its age 0.5 to age 4.5 period
of crown development encompasses the ages
at which growth disturbance typically occurs
(Rose, 1973; Clarke, 1978). However, in this
case, use of the canine was not feasible, because the Wadi Halfa dental collection consists mainly of posterior teeth. The first
permanent molar, which has also been employed by Cook (1981), was selected as the
most suitable alternative. This tooth is not
so easy to section (Rudney, 1981), but its
crown develops during the first 3 years of life
(Fanning and Brown, 19711, a period when
children are highly susceptible t o growth disturbance (Susskind, 1977; Thomson and Pollitt, 1977).
The sample selected consists of 105 first
permanent molars. The Meroitic cultural period is represented by 40 individuals from
GROWTH DISTURBANCE IN NUBIA: CHANGES OVER TIME
465
junction. Since ante-mortem loss of occluding teeth sometimes resulted in curtailment
of normal wear, it did prove possible to include a number of older adults in the sample
(due to differential wear across the buccal
and lingual cusps, most adults in the sample
are represented by only a single cusp-see
Table 1). The unavoidable exclusion of the
very young from the sample means that the
age-distribution within it may not be fully
representative of the Meroitic and X-Group
populations. However, the agedistributions
within the Meroitic and X-Group components of the sample were compared with the
Mann-Whitney U test and found not to be
significantly different (Table 1). Interpopulation comparisons within the sample are thus
not likely to be biased with respect to age.
Sample preparation and data collection
The teeth were bisected along a longitudinal plane running between the mesiobuccal
and distolingual cusps, and acid-etched
ground sections then made according to
TABLE 1. Agedistributwn ofthe sample’
standard histological technique (Rose, 1973;
Distolin a1
Mesiobuccal
Clarke, 1978; Rudney, 1981). The sections
Y
cusps3
cusps
were then examined for accentuated striae of
Age-group2
Meroitic X-Group Meroitic X-Group
Retzius (Rudney, 1981).A stria was classified
as accentuated on the basis of histological
0
1
0
1
3Y
evidence of unusually large fluctuation in
3
3
3
4
4Y
1
4
1
3
the shearing component of ameloblast mo5Y
4
3
4
4
6Y
tion. Such evidence is manifested as a gross
3
3
3
4
7Y
accentuation in the amplitude of prism cur0
0
0
0
8Y
vature across the crest of the stria. In more
1
3
0
2
9Y
1
2
1
2
severe cases, accentuation of prism curvature
10 Y
0
2
0
2
11 Y
is accompanied by blurring and obliteration
2
0
2
0
12 Y
of prism boundaries. These discontinuities
0
1
13 v
0
1
indicate an interruption of secretory activity
2
0
2
0
14 $
0
2
1
3
15 Y
so prolonged as to completely disrupt the nor16 y
0
2
1
2
mal pattern of enamel matrix flow (Osborn,
1
0
1
0
17 Y
1973;Osborn and Ten Gate, 1976;Rose, 1977,
1
3
0
3
18 Y
6
15
10
14
1979;Rudney, 1979,1980,1981).
19-30
v
_ _ _.
2
4
3
5
31-50
Such gradations in the severity of accen28
47
36
46
Totals
tuated striae were taken into account during
Mann-Whitney U test5:Age by population, Meaiobuccal cusps.
data collection. Striae displaying both accenU = 619.0; z = -0.4328; p = 0.6652.
tuated curvature and prism discontinuities
Mann-Whitney U test5: Age by population, Distolingual cusps.
were given a relative weight of 2, while striae
U = 819.5;z = 0.0806; p = 0.9358.
‘Data given aa number of individuals contributing a cusp to a
displaying only accentuated curvature reparticular agegroup. Persons contributing both a mesiobuccal
ceived a lesser weight of 1.The weights of all
and a distolingual cusp are represented twice.
aAge groups 3 years to 18 years represent dental ages. Age
accentuated striae found within each cusp of
groups 19-30 years and 31-50 years combine persons aged by
each
tooth were summed to generate a
subic, endmanial, and dental techniques.
Due to differential wear or damage during sectioning, four
“growth disturbance score” (Rudney, 1980,
Meroitic and 19 X-Group individuals are represented by a
1981). These scores provided an estimate of
mesiobuccal cusp alone.
the amount of growth disturbance experi‘Due to differential wear or damage during sectioning, 12
Meroitic and 18 X.Group individuals are represented by a
enced by individuals during the first 3 years
dwtolingual cusp alone.
of life, the period in which the M1 crown
6Siegel(1956).
cemetery 6B16 at South Argin. The remaining 65 are from X-Group cemeteries 2413
(Serra West) and NAX (North Argin) (Greene,
1967). The criterion for inclusion of a tooth
within the sample was the presence of a fully
developed and unworn dentinoenamel junction in the mesiobuccal and/or distolingual
cusp (see below). This criterion served to
maximize inter-tooth comparability within
the sample, although it did require the exclusion of very young and very old individuals
(Rudney, 1981). Ages within the sample
range from 3 to 50 years (Table 1). Those
younger than three were excluded due to immature enamel which was histologically distinct from fully developed enamel and also
subject to post mortem changes. Adults were
excluded when the mesiobuccal and distolingual cusps of all their first permanent molars
were worn below the tip of the dentinoenamel
466
J.D. RUDNEY
develops (Massler et al., 1941;Fanning and
Brown, 1971;Anderson et al., 1976).
To control for any intra-observer error in
the assessment of prism curvature, the scoring step was repeated until consistency was
achieved. Additional control for error is provided by independent analysis of growth disturbance scores for the mesiobuccal and
distolingual cusps (this step was mandated
by the inclusion of differentially worn teeth
in the sample). One-sample KolmogorovSmirnov tests indicate that the distribution
of scores for either cusp is not significantly different from normality (Siegel, 1956).On
that basis, it was deemed legitimate to use
parametric techniques to make population
comparisons. A two-way ANOVA was set up
for each set of cusps (all statistical tests were
run using the SPSS system of canned statistical programs) (Nie et al., 1975).Growth disturbance was taken as the criterion variable,
with Population and Age-at-Deathas the categorical variables. Meroitic and X-Group represented the categories in Population. In
order to provide adequate sample sizes for
analysis, the original age-groupswere pooled
into two categories, Children and Adults. Age
15 was made the dividing line between the
two.
RESULTS
The results of the analysis are the same for
both the mesiobuccal and distolingual cusps.
Table 2 presents the mean values for growth
disturbance scores within each category of
population and age. These values suggest a
difference in the level of growth disturbance
between age groups. Within each population,
those dying in childhood experience higher
levels of growth disturbance (during the first
3 years of life) than do those surviving to
adulthood. Moreover, there is also a clear
differencebetween populations in terms of the
magnitude of growth disturbance. X-Group
children experience less early childhood
growth disturbance than do Meroitic children, and X-Group adults experience less
early childhood growth disturbance than do
Meroitic adults. The ANOVA summary table
(Table 3) indicates that the differences between age groups and populations are highly
sisnificant (p gO.001) in all cases. It also
shows that the effects of age and population
on growth disturbance are independent and
additive. Together, both variables account for
about 30% of total variance in growth dis-
turbance scores (as indicated by the value of
R2).
DISCUSSION
The results show differences in the level of
growth disturbance both within and between
these ancient Lower Nubian populations. The
observed difference between age groups can
be related to mortality data collected for the
Wadi Halfa skeletal populations (Armelagos,
1968, 1969). The mortality curves for both
the Meroitic and X-Group population peak
during infancy and early childhood. Those
experiencing less growth disturbance in early
childhood would be expected to be more likely
to survive beyond that critical period. The
lower early childhood growth disturbance
scores seen in Meroitic and X-Group adults
would appear to be a reflection of this. Armelagos' (1968,1969)mortality data can also
be related to the decline in growth disturbance scores observed between the Meroitic
and X-Group populations, as his findings
show a corresponding decline in mortality
rates between the Meroitic and X-Group periods. Taken together, the mortality data and
the growth disturbance data strongly suggest an improvement in the relative health
status of Wadi Halfa area children during
the X-Group period. This change is difficult
to account for, in view of the extensive similarities between the Meroitic and X-Group
periods.
Two possible explanations for the X-Group
improvement in child health have thus far
been proposed. Armelagos (1968,19691,writing in reference to the Wadi Halfa mortality
data, has suggested that the improvement
may be related to an increase in local village
autonomy during X-Group times. A reduction in the demands of central authority could
have led to an increase in the amount of food
available for local consumption, and a similar effect might also have been engendered
by the decline in trade with Egypt (this trade
did involve an exchange of Nubian foodstuffs
for manufactured goods) (Adams, 1977).Such
changes might conceivably have led to a relative improvement in child nutrition (although a recent study of bone turnover rates
in X-Groupchildren does suggest that proteinenergy malnutrition was not unknown in XGroup times) (Armelagos, et al., 1979). A
question posed by this hypothesis pertains to
the degree of local autonomy actually experienced in the Wadi Halfa region. Sites found
467
GROWTH DISTURBANCE IN NUBIA: CHANGES OVER TIME
around Wadi Halfa include the X-Group royal
tombs at Ballana and Qustul, and a large
settlement at Faras believed by some to be
the X-Group capital (although others favor
the site of Qasr Brim, farther to the north)
(Adams, 1977).These sites suggest a substantial governmental presence in the Wadi Halfa
region during the X-Group period. The effect
such a presence may have had on the autonomy of local villages needs to be evaluated
before the autonomy hypothesis can be fully
accepted.
An alternative (though not antithetical) explanation for the X-Group improvement in
child health is based on endemic disease
(Rudney, 1981). The helminthiases hookworm and schistosomiasisare known to have
been present in Egypt for several millenia
(Foster, 1965;Ruffer, 19671,and high levels
of porotic hyperostosis strongly suggest their
presence in Lower Nubia during Meroitic and
X-Group times (Carlson et al., 1974). These
diseases are known to contribute growth
T ABU 2. ANOVA cell meam-growth disturbance by
disturbance in children, and a strong positive
population by age at death
relationship between high prevalences of
A. Mesiobuccal cusps
hookworm and schistosomiasis and yearPopulation
Age group
round irrigation has also been established
- Children
Adults
Memitic
x = 15.13(n = 16) = 12.08(n = 12) (May, 1958;Van der Schalie, 1960;Malek,
S.D. = 4.161
-S.D. = 5.282
1961;Scrimshaw et al, 1968;Miller, 1979).
X-Group
X = 11.09 (n = 23) X = 6.58(n = 24)
The intensification of Nubian agriculture
S.D. = 5.964
S.D. = 3.412
engendered by the introduction of the saqia
B. Distolingual cusps
at the beginning of the Meroitic period could
Population
Age P U P
thus have led to increased local prevalences
- Children
Adults
Meroitic
X = 16.18(n = 17)
= 12.47(n = 19) of hookworm and schistosomiasis (Rudney,
1981). A possible consequence of the deleteS.D. = 5.114
S.D. = 4.858
X = 11.82(n = 22) Z = 7.79 (n = 24)
X-Group
rious health effects associated with such a
S.D. = 5.491
S.D. = 3.867
shift could have been natural selection in
TABLE 3. ANOVA summary table-growth disturbance by population by age at &ath
A. Mesiobuccal cusps
sourceof
variation
sum of
squares
Main effects
737.087
386.606
Population
Age at death
292.400
9.253
Interactions:
Pop. with age
Explained
746.341
variance
1614.326
Residual
variance
Total
2360.667
variance
Multiple R = 0.559;Multiple R2 = 0.312
D.F.
Mean
square
2
1
1
1
368.554
386.606
292.400
9.253
16.209
17.003
0.407
0.001
0.001
0.001
0.526
3
248.780
10.942
0.001
71
22.737
74
F
12.860
R.
13.901
B. Distolingual cusps
718.4U
Main effects
414.094
Population
308.582
Age at death
0.528
Interactions:
Pop. with age
Explained
718.940
variance
Residual
1820.438
VarianCe
Total
2539.378
variance
Multiple R = 0.532;Multiple R2 = 0.283
2
1
1
1
359.206
414.094
308.582
0.528
15.391
17.743
13.222
0.023
0.001
0.001
0.001
0.881
3
239.647
10.268
0.001
78
23.339
81
31.350
468
J.D. RUDNEY
favor of those more resistant to these diseases (May and Anderson, 1979). The improvement in child health seen several
hundred years later in the X-Group period
might thus be related to a gradual increase
in the biological resistance of the Lower Nubian population to helminthic disease (Rudney, 1981).This hypothesis is not dependent
on the degree of local autonomy in the Wadi
Halfa region, but it in turn presents other
difficulties. One problem is that the biochemistry and genetics of innate mechanisms for
resistance to helminthic disease is not well
understood. There is strong evidence for the
existence of such resistance, but no accepted
means for the identification of genetically
resistant individuals (May, 1958; Malek,
1961;Wakelin, 1978;Miller, 1979).This lack
of specific information presently precludes
independent testing of the endemic disease
hypothesis through genetic analysis of living
Nile Valley populations differing in their exposure to helminthic disease.
The hypotheses considered above are complete in themselves, but a full discussion of
growth disturbance in Lower Nubia requires
mention of the Bassett et al. (1980)report of
tetracycline in labeling in bone sections from
Wadi Halfa X-Group remains. Exposure to
this antibiotic is thought to have occurred
through consumption of grain contaminated
by tetracycline-producingbacteria of the genus Streptomyces (Bassett et al., 1980).It can
be argued that tetracycline might have contributed to the X-Groupimprovement in child
health by ameliorating some bacterial, rickettsial, and chlamydia1 infections (tetracycline is not therapeutically effective against
viral or helminthic agents) (Kastrup and
Boyd, 1979). However, such an hypothesis
must be evaluated in light of the known capacity of pathogenic organisms to become resistant to tetracycline (Connamacher, 1976).
It can as easily be argued that any potential
benefits of tetracycline would have been nullified by the evolution of resistant bacterial
strains.
An additional complication is provided by
reports which suggest a deleterious effect of
tetracycline on dental development. Findings in experimental animals include ultrastructural changes in ameloblasts, which
may be accompanied by accentuated striae of
Retzius formation, or frank enamel hypoplasia. Such effects are dose dependent, and may
also vary according to the type of tetracycline
administered (Lofgren et al., 1968;Nylen et
al., 1972;Kruger, 1975).The effect of tetra-
cycline on dental development in humans is
not well understood, because it is difficult to
isolate the effect of the drug from that of the
disease it was used to treat. However, accentuated striae of Retzius have been reported
in association with tetracycline-labeledbands
in dentin, and the clinical literature contains
repeated suggestions that tetracycline may
act to compound effects of systemic disease
on dental development (Brearley, et al., 1968;
Baker and Storey, 1970; Baker, 1972; Primosch, 1980;Kotsanos, 1982). Thus, the results of the present study may be influenced
by a possible tetracycline effect on accentuated striae of Retzius formation (Rudney,
1981).A test of that hypothesis will require
at least minimal information on levels of tetracycline exposure in the dental tissues of
both the Meroitic and X-Group populations.
Research that is currently in progress may
supply some of the needed data. At present,
the most that can be said is that a tetracycline effect cannot be ruled out.
On the basis of current knowledge, all the
hypotheses discussed above are best regarded as tentative. Further research will be
needed to determine the relative strengths of
each. Since these hypotheses are not mutually exclusive, it is possible that each may
have a contribution to make to succeeding
stages of explanation. At present, the importance of the current study lies chiefly in the
finding of a significant difference in the level
of growth disturbance between two biologically continuous populations that are very
similar with respect to culture and environment. This finding suggests that the relationship between early childhood growth
disturbance and culture is complex and multifactorial. The Nubian data do nothing to
contradict the general impression that child
health tends to be poor in ancient state-level
agricultural societies (Cassidy, 1980). They
do, however, suggest that local epidemiological or historical factors may induce fluctuations in the level of growth disturbance seen.
Comparisons with diachronic series of populations from other areas may help elucidate
the extent to which such fluctuation in levels
of growth disturbance may be characteristic
of agricultural populations in general.
ACKNOWLEDGMENTS
An earlier version of this paper was presented at the 50th Annual Meeting of the
American Association of Physical Anthropologists, Detroit, Michigan, April 25,1981.The
author would like to thank Dennis P. Van
GROWTH DISTURBANCE IN NUBIA: CHANGES OVER TIME
Gerven and David L. Greene for their valuable advice and criticism during the course of
this research. Thanks are also due to Jerome
C. Rose and Steven K. Clarke for their advice
on the manufacture and observation of dental thin sections, and to George J. Armelagos, for access to data collected by the first
University of Colorado Nubia expedition. Finally, thanks to the University of Colorado
Department of Geology for use of their petrographic thin section lab, and to Geoff Reed
and Bob Lanham for instruction in the use of
the equipment.
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