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Ecology and ovarian function among Lese women of the Ituri forest Zaire.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 78519-526 (1989)
Ecology and Ovarian Function Among Lese Women of the
lturi Forest, Zaire
PETER T. ELLISON, NADINE R. PEACOCK, AND CATHERINE
T.AGER
Department of Anthropology, Harvard University, Cambridge, Massachusetts 02138 (P.T.E., C.L.); Department of Anthropology, University of California at Los Angetes, Los Angetes, California 90024 (N.R.P.)
KEY WORDS
Reproduction, Luteal function, Progesterone, Nutrition, Salivary steroids (methods)
ABSTRACT
Ovarian function is examined in 35 Lese women inhabiting
the Ituri Forest of northeastern Zaire over a period of 4 months through measurements of progesterone in saliva samples collected twice weekly. Ovulatory
frequency is found to be only 56%on average, with a pattern of age variation
similar to that observed in western women, though lower in level at each age.
Average luteal progesterone levels of the Lese women are lower than those of
Boston controls even if only ovulatory cycles are considered. Women with the
poorest nutritional status, inferred from longitudinal weight changes and
weight for height, show the greatest compromise of ovarian function, and the
average ovulatory frequency of the whole sample declines in parallel with a
period of weight loss over four months. It is suggested that low ovulatory frequency and luteal insufficiency contribute to the low fecundity of the Lese
population and that nutritional status is likely to be one of the ecological factors
modulating this effect.
Our study site in the northern part of
Zaire’s Ituri Forest lies in what has become
known as the “African infertility belt,” a
region stretching across the continent, along
and north of the equator, characterized by
isolated pockets of extremely low fertility and
high rates of secondary sterility (Belsey,
1976). Ordinarily these pockets have been
attributed to a high incidence of tubal sterility in women as a consequence of gonorrhea
infection, although this explanation h a s been
hard to verify. The Lese of our study area
show several features typical of the African
infertility belt. Among 119 postmenopausal
women the average number of live births is
only 2.4, with 37%reporting no live births and
10%reporting only one (Bailey, unpublished
data). Other features of individual reproductive histories, however, seem at variance with
the tubal sterility hypothesis, such as women
whose recent pregnancies prove them to be
still fecund, yet with interbirth intervals
much longer than would be expected given
their observed and traditional nursing behavior.
0 1989 ALAN R. LISS, INC
In this report we present evidence that
sheds new light on Lese fertility. I n particular, we show that suppressed ovarian function among Lese women may lead to a lower
monthly probability of conception than is
observed among western women. Further, we
show that one of the factors associated with
such ovarian suppression in this population
is nutritional status. Together these observations constitute a n important addition to our
knowledge of the ecology of human reproduction.
We have published elsewhere the results of
an initial study of ovarian function among
the Lese and Efe, conducted in the summer of
1983 (Ellison et al., 1986). This initial study
happened to occur at the end of a pronounced
hunger season during which the average
Lese woman lost 4.25 kg in 6 months. Based
on measurements of salivary progesterone
from 25 women with a history of recent infertility, we estimated that only 48%of our subjects ovulated during the month of observaReceived May 22, 1987; revision accepted April 29, 1988.
520
P.T.ELLISON ET AL.
tion. Because our data were limited, however,
we were unable to determine whether this low
ovulatory frequency was a consequence of
the period of weight loss or represented a
characteristic feature of the population.
Encouraged by the methodological success
of the initial study, a much more extensive
sample collection was undertaken from July
to November 1984, during the period of the
year immediately following the peanut harvest and honey season, when the nutritional
status of the population is ordinarily at its
highest.
MATERIALS AND METHODS
Once again our principal objective was to
measure progesterone in samples of saliva.
Progesterone is secreted in quantity in the
second, luteal half of the cycle, ordinarily as
a consequence of ovulation. Although luteinization of unruptured follicles is possible
(Stanger and Yovich, 1984),a significant elevation of luteal progesterone is generally
considered as reliable evidence of ovulation
(Riad-Fahmy, 1984; Walker et al., 1979). Adequacy of luteal progesterone production by
the corpus luteum appears to be a clinically
important determinant of the probability of
implantation and early viability of the trophoblast (Hamilton et al., 1987; Ftiddick et al.,
1983). Low levels of luteal progesterone and/
or shortened periods of progesterone secretion, collectively referred to as luteal phase
defects or luteal insufficiency, are chronically
associated with infertility (DiZerega and
Hodgen, 1981; Annos et al., 1980). Saliva
samples are easily collected under field conditions, and the progesterone concentrations
measured in saliva allow comparison of ovulatory frequency and luteal sufficiency with
data from other populations (Ellison, 1988).
From July through November 1984 saliva
samples were collected twice weekly from all
Lese women in the study area past menarche.
Of that sample, all women who were menstruating during the study period, hereafter
referred to as subjects, were included in the
analyses presented here. Three subjects became pregnant during the sampling, others
were occasionally absent from the study
area. None of the subjects was lactating during the sampling period or had children
under the age of 2 years. The total sample for
these analyses thus includes 89 cycles collected from 35 women, or a n average of 2.6
cycles per woman. Selected aspects of the
reproductive histories of these women are
included in Table 1.
Subjects were visited twice a week, in the
early morning, when a sample of 4-5 ml of
saliva was collected in a polystyrene tube.
Each woman was questioned at each visit
about recent menstruation. A colored bead
was added to a copper wire bracelet on each
occasion a s a simple quid-pro-quo and as a n
individual tally of samples given. Back in
camp 50 pl of sodium azide solution was
added to each sample as a preservative,
bringing the concentration to approximately
0.1%.Once a month all subjects were weighted
to the nearest 0.5 kg using a portable scale.
The samples were stored at ambient temperatures for up to a month before being frozen at
-20°C. Progesterone levels in saliva are
stable under these conditions when preserved
with sodium azide (Ellison, 1988; Ellison
et al., 1986).
In the laboratory, 2 ml of saliva from each
sample were extracted in ether and added to
a radioimmunoassay of progesterone. Details
of this assay procedure are published elsewhere (Ellison and Lager, 1986;Ellison et al.,
1986). Modifications of the assay since our
initial project in Zaire have improved the
sensitivity and precision of our measurements, the smallest measurable amount now
being 25 pmol/L and the coefficient of variation of sample determinations being less
than 10%. The time series of data from each
individual subject was analysed for evidence
of progesterone peaks using the program
PULSAR developed by Merriam and Wachter (1982) at NICHHD (Fig. 1). PULSAR
extracts a smooth baseline from the data series by a n iterative application of a robust
running averages procedure and identifies
peaks as significant departures from this
baseline. Identified peaks are excluded from
the next iteration until no further peaks are
detected. With this method, all cycles except
four could be categorized as ovulatory or not;
TABLE 1. Selected aspects of the reproductive
histories of Lese subiects
Average
interval since
last birth for Average
Age
group
%
%
parous women No. of
(years) N childless unmarried
(months) live births
4 2 2 11
23-35 19
236 5
54.5
26.3
20.0
27.3
5.3
0.0
39.8
56.6
132.7
0.7
1.6
2.8
521
OVARIAN FUNCTION AMONG LESE WOMEN
600
+ PROGESTERONE
0 BASELINE
400
1
500
P
400
>
300
5
200
;
m
0
20
40
60
80
100
120
DAYS
Fig. 1. Example of the use of PULSAR to analyse the
time series of progesterone data from a single subject.
Solid squares represent observed progesterone values,
open squares represent the extracted baseline, and asterisks represent the significant progesterone peaks identified by the program.
the four ambiguous cycles were examined
individually and subsequently included in
the ovulatory group.
The method of assaying salivary progesterone was originally developed by Walker and
colleagues at the Tenovus Cancer Institute in
Wales (Walker et al., 1979). Results from
assays performed in our laboratory at Harvard correspond closely with theirs (cf. Ellison et al., 1986). Samples collected from
cycling female researchers in the field also
demonstrate profiles comparable to the Boston and Welsh control values. In Figure 2,
profiles from three study subjects are depicted
illustrating the correspondence between salivary progesterone measurements and various reproductive states.
Statistical analyses of group differences in
progesterone levels are performed on logtransformed data unless otherwise noted, to
normalize distributions. Comparisons of ovulatory frequency are by chi-square statistic
unless otherwise noted.
RESULTS
Although the 1984 field season had been
planned to fall during a period of relative
food abundance, food supplies were not, in
fact, as bountiful as usual. Early and extended rains the previous December, January, and February had once again interfered
with the process of clearing and burning new
gardens, and many Lese families were compelled to rely solely on a replanting of the
previous years plots. In addition, the honey
season in June and July was the worst for
100
o
0
1'0
.
20
.
30
40
.
50
.
60
,
70
,
80
DAYS
Fig. 2. Sample salivary progesterone profiles of Lese
women in different reproductive states. Solid squares trace
the profile of a postmenopausal Lese woman. The rising
profile traced by the solid circles is that of a woman who
became pregnant during the sampling and who subsequently delivered a healthy baby girl. The open circles
trace the profile of a woman who bore twin boys prematurely at 6 months gestational age, both of whom died
within 12 hours. Notice that in the absence of lactation
normal cycles resume almost immediately.
Fig. 3. Distribution of net weight changes between
July and November 1984 in Lese subjects. (The three subjects who became pregnant during the study are not
included.)
many years, so that this normal infusion of
calories from the forest was virtually absent
for the Lese. Although by no means as severe
as the situation in the spring of 1983, there
was a steady decline in the average weight of
the study subjects between July and November, the average net change being a loss of
0.95 kg (Fig. 3).
522
P.T.ELLISON ET AL.
Once again ovulatory frequency was found
to be quite low: 54% weighting all cycles
equally, 56% weighting individual women
equally. Subdividing the subjects into three
age categories-522 years, 23-35 years, and
2 3 6 years-reveals a distinct age pattern
(Fig. 4): young women under 23 years of age
ovulate a mere 33% of the time on average
versus an ovulatory frequency twice as high
among older women aged 23 years and older
(P< .05). The slight decline in ovulatory frequency between subjects aged 23-25 years
and subjects aged 36 years and over is not
statistically significant, as is often reported
for western women (Doring, 1969). Although
comparable in shape to the age curves of ovulatory frequency available from western populations, the ovulatory frequencies of the
Lese women are substantially lower than
those of similarly aged women in the west.
For example, the ovulatory frequency we
found in a sample of 25 college undergraduates aged 18-22 years using the same method
was 58%(P< .01 compared to Lese sample),
and that among adult women was 100%(P<
.005 compared to Lese sample; Ellison et al.,
1987, Fig. 4).
Not only is the frequency of ovulation low
among the Lese women, the composite progesterone profile as a whole is low compared
to that of Boston women previously found
comparable to published standards from the
Tenovus Institute (Riad-Fahmy, 1984; Ellison et al., 1986). To some extent the low composite profile results from including progesterone levels from anovulatory Lese cycles.
Even if ovulatory cycles alone are considered,
16-22
23-35
36-50
AGE GROUP
Fig. 4. Ovulatory frequency by age for the Lese subjects compared to that of similarly aged Boston women.
however, the Lese composite profile is low
compared to that of Boston women (Fig. 5).
Nor does the inclusion of late adolescent
cycles in the Lese sample account for the difference from the Boston sample. Significant
differences can in fact be found between the
average luteal progesterone level of Boston
women and that of any of the following: the
entire Lese sample, only Lese women 2 2 3
years of age, only ovulatory cycles of Lese
women, and only ovulatory cycles of Lese
women 1 2 3 years of age (P< .05, one-tailed
t-tests, Fig. 6).
500
400
-mccNlw.s
+ OWLATORY
+ AULESE
300
200
100
0
-30
-20
-10
0
DAYS BEFORE MENSES
Fig. 5. Average salivary progesterone profiles of the
entire Lese sample, the subset of ovulatory Lese cycles,
and a sample of Boston women aged 23-35 years (Ellison
and Lager, 1986).
Fig. 6. Comparison of average luteal level of salivary
progesterone (+SE) among five sample groups: Boston
women aged 23-35 years, all Lese subjects, only ovulatory
cycles of Lese subjects, only cycles of Lese subjects over
age 23 years, and only ovulatory cycles of Lese subjects
over age 23 years.
OVARIAN FUNCTION AMONG LESE WOMEN
The women sampled in the initial study in
1983 correspond in age to the middle age
group of women in the present study. The
contrast between the 48% ovulatory frequency in 1983 and the 69% ovulatory frequency in this age group in 1984 may thus
reflect the more serious nutritional situation
in 1983, or it may represent differences in
the frequency with which reproductively
impaired women were included in the two
samples. We will return to the question of
sample bias in the discussion. The more
extensive data collection in 1984 allows us to
investigate the relationship between nutritional status a n d ovarian function, however, within the Lese sample. I n particular,
z
2.0
Kg
< 2.0 Kg
’
200
NET WEIGHT CHANGE (kg)
Fig. 7. Ovulatory frequency and average peak progesterone levels (SE) in L e e subjects (excluding three subjects who became pregnant during the study) subdivided
by net weight change July to November 1984.
523
three analyses provide evidence of a positive
relationship between these two variables.
First, the subjects can be subdivided on
the basis of their net weight change, July to
November (Fig. 7; the three subjects who
became pregnant during the study are excluded). Ovulatory frequency is slightly, but
not significantly, lower among those women
who lost more than 2 kg than among those
who lost less or gained weight. The average
peak progesterone level (ovulatory cycles
only) attained by the women who lost more
than 2 kg is significantly lower than that
attained by women who lost less or gained
weight (P< .05, one-tailed t-test). Second,
the subjects can be subdivided by weightfor-height at the start of the study as a n
index of current nutritional status (Fig. 8).
Once again ovulatory frequency (nonsignificantly) and peak progesterone levels (P<
.05, one-tailed t-test) are lower in the subjects with poorer nutritional status. These
results indicating that women with poorer
nutritional status also suffer impaired ovarian function do not appear to be artifacts of
age differences between the groups a n a lysed (see “Discussion”). Finally, monthly
ovulatory frequency declined steadily over
the course of the study, from 63%in JulyAugust to 30%in October-November (Fig. 9,
P < .001; significance of regression of ovulatory frequency against time, P < -005).
DISCUSSION
The results of the current study of Lese
ovarian function once again indicate that
ovulatory frequency and progesterone levels
500
0
-2
% OVUIATORY
+ PEAKPRCG
0
400
h
;
z
8
t-
v1
CI
300
p
Y
2
200
5 0.3
z
0.3
WEIGHTIHEIGHT (kglcrn)
Fig. 8. Ovulatory frequency and average peak progesterone (fSE) in Lese subjects subdivided by weight-forheight at the start of the study.
Fig. 9. Monthly ovulatory frequency of Lese subjects
over the course of the study.
524
P.T.ELLISON ET AL.
are low compared to western women. When
adjusted for age the ovarian suppression does
not appear to be as great as that observed in
1983 when the population was under more
severe nutritional stress. Close examination
of the 1984 data suggests that those women
in the population with the poorest nutritional
status initially and those who lost more
weight during the study show the greatest
compromise of ovarian function, particularly
as regards luteal progesterone levels. Neither
of these results appears to be a n artifact of
the distribution of young women, whose
ovarian function is much lower than that of
older women, between the groups analysed.
There is no significant difference in average
age between the subjects with a weight-forheight index less than 0.3 and those with a n
index over 0.3 (29.2 k 2.7 vs. 26.2 & 1.7 years,
mean k SE). The 11subjects in the under 23year age group, who show a significantly
lower level of ovarian function, are evenly
distributed between the two groups, six in the
group with a n index over 0.3 and five in the
group with a n index under 0.3. When women
are grouped by weight change, the group of
women who lost less than 2 kg is significantly older on average than the group of
women who lost more than 2 kg (29.3 k 2.0 vs
23.8 k 1.7 years, P < .05, two-tailed t-test). The
youngest age group is, however, also evenly
split in this case, the age difference being due
to the distribution of older women among
whom no difference in ovarian function was
detected.
These results together imply that Lese
ovarian function covaries with nutritional
status, in particular with the mild yet progressive weight loss associated with a period
of relative food shortage. Associations of
this kind have also been reported for western women. I n a study of nine normalweight women aged 20-29 years undergoing
voluntary weight loss through dieting, Pirke
et al. (1985) found no evidence of diminished
gonadotropin secretion after 6 weeks, but
significantly lowered levels of gonadal steroids, especially progesterone. Bullen et al.
(1985) found that among women undergoing
a prescribed exercise regimen, those who
were allowed to lose weight showed more
evidence of impaired ovarian function than
those who were not allowed to lose weight.
In our own studies we have found that Boston women undergoing voluntary weight
loss through dietary restriction show lower
ovulatory frequency and lower luteal pro-
gesterone levels than do similarly aged controls of stable weight (Lager and Ellison,
1987). The suppression of ovarian function
among such women was even more pronounced in the cycle following that in which
weight loss occurred than in the weight loss
cycle itself (Fig. 10). The results of our current study among the Lese are not out of line
with the findings of these previous studies.
Our results from the Lese, however, constitute the first evidence of a covariance of
nutritional status and ovarian function as
part of the natural ecology of a noncontracepting population.
Although the covariance of nutritional
status and ovarian function among the Lese
is comparable to that observed in the west
under more artificial conditions, it is not yet
clear whether nutritional status alone can
account for the dramatic difference in baseline level of ovarian function between the
Lese sample and western women of comparable age. Two other important possibilities are worth noting: first, that the sample
of Lese women studied is biased toward the
inclusion of women of impaired ovarian
function; and second, that the suppressed
ovarian function of Lese women is a chronic
feature of their reproductive ecology,perhaps
reflecting the impact of other ecological variables. Unlike the initial 1983 study, in which
subjects were chosen on the basis of a recent
history of infertility, all menstruating women
within the study area were included in the
500
1
-=-ccNrFa
+ WEIGKTLOSS
+ POST LOSS
fi
0 4
~ 3 0
I
-20
-10
0
DAYS BEFORE MENSES
Fig. 10. Comparison of the average salivary progesterone profiles from 19 cycles of normally menstruating
women, 14 cycles of weight loss in dieting women, and 9
cycles which followed a month of weight loss in dieting
women (Lager and Ellison, 1987).
OVARIAN FUNCTION AMONG LESE WOMEN
present study in a n attempt to minimize
selection bias.
Nevertheless, some overrepresentation of
women of diminished fecundity in our sample must be assumed. I n any natural fertility population that is heterogeneous with
respect to female fecundity, women of impaired fecundity will spend a greater proportion of their lives in the pool of menstruating women than fully fecund women.
This tendency will be exaggerated to the
extent that some women wean their infants
as a consequence of becoming pregnant
instead of the other way around, as is
reported by some Lese women. We fully
acknowledge that such a n overrepresentation of low fecundity women in our Lese
sample is likely. The noteworthy result of
our research is that such diminished fecundity is associated with suppressed ovarian
function, and in particular with low luteal
progesterone, which may therefore be a n
important contributing factor to the low fertility of the population.
It is possible that venereal disease may
produce such impaired ovarian function. In
particular, it is possible for gonorrhea infections to be so severe that the ovary becomes
scarred and ovulation is prevented (Svensson et al., 1983), but this result is rare in
western clinical experience and is always
accompanied by acute symptoms of pelvic
inflammatory disease. Furthermore, in our
sample evidence of luteal suppression persists even if anovulatory cycles are excluded.
These considerations suggest that the suppressed ovarian function observed is unlikely
to be a simple result of venereal disease.
It is also possible t h a t the suppressed
basal level of ovarian function in the Lese
sample is a chronic feature of their reproductive physiology, deriving from genetic,
developmental, or environmental causes
other than poor nutritional status. No evidence exists for strictly genetic differences
in reproductive physiology between populations, and the possibility of such a difference distinguishing the Lese seems unlikely.
A proper investigation of this question,
however, would require quite different data
from what are available to us. Development a l differences in ovarian function have
been demonstrated among western women,
with late-maturing women having a low trajectory of ovulatory frequency by age relative to early maturers (Apter and Vikho,
1983). The same factors that cause the Lese
525
to be a relatively late-maturing population,
with a n average menarcheal age of about 16
years, may result in suppressed ovarian
function throughout the average woman’s
life. Finally, other ecological factors, in particular heavy workloads and high disease
burdens, may combine with marginal nutritional status to suppress Lese ovarian function. Even a mild exercise regimen, if pursued regularly, is capable of suppressing
progesterone profiles and lowering ovulatory frequency to a degree comparable to
that observed in the Lese subjects. Boston
women who run a n average of 12.5 miles a
week for exercise show salivary progesterone profiles much like those of the Lese
with comparable ovulatory frequency and
average luteal levels (Ellison and Lager,
1986). Fairly heavy physical labor, such as
cultivating the gardens, or carrying firewood and children, is a regular feature of
the lives of Lese women. This possibility has
been the focus of a third field season in 1987
conducted by one of us (N.R.P.), which we
hope to report on soon.
In summary, we have shown that menstruating Lese women are characterized by
suppressed ovarian function, particularly
lower luteal progesterone levels, relative to
western women of the same age; we have
argued t h a t this suppression of ovarian
function is a likely contributor to the low
fertility of the Lese population; and we have
shown that within the sample of menstruating Lese women, level of ovarian function
covaries with nutritional status. As well as
adding to our understanding of Lese reproduction, these results illustrate the important contribution that the study of ovarian
function can make to the broader subject of
human reproductive ecology.
ACKNOWLEDGMENTS
We wish to thank Robert C. Bailey for the
use of his demographic data, and the many
members of our project who contributed to
the collection of anthropometric data. Our
special thanks to the Lese women of Malembi.
This work was supported by NSF grant BNS83-19629 to Irven DeVore and Peter Ellison.
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