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Circulating steroids and the relationship between ovarian and placental secretion during early and mid pregnancy in the baboon.

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American Journal of Primatology 7:357-366 (1984)
Circulating Steroids and the Relationship Between Ovarian
and Placental Secretion During Early and Mid Pregnancy
in the Baboon
MRC/ARC Comparative Physiology Rcworch Group, The Tnstitute of Zoology, T /
Socrety of London, Regen't's Park, London, lrnited Kingdom a n d 21nstitute of Primate Research,
National Museums ofKenyo, Nairobi, Kenya, Africa
Ovarian and placental steroid secretion was examined a t intervals
during early and mid-pregnancy in the olive baboon, Papio anubis.
Progesterone, androstenedione, testosterone, estrone, and estradiol170 were measured after celite chromatography in samples from
peripheral circulation and from utero-ovarian veins draining ovaries with and without corpora lutea at the following stages of
pregnancy: days 8-9 (unconfirmed pregnant), 10-19,34-40, 60-66,
and 104-106 after ovulation. The pattern of hormone levels in
peripheral and utero-ovarian vein samples indicated the following:
1)The corpus luteum was the principal source of progesterone until
at least day 19. Placental secretion was well advanced by days 3440 and provided the major contribution to circulating progesterone
levels by day 60. 2) There was a significant elevation in peripheral
concentrations of androstenedione and testosterone on days 10-19
and 34-40 of pregnancy; androgen levels in peripheral and uteroovarian vein samples declined to baseline values by day 60. 3)
Estrogens were secreted by the corpus luteum on days 10-19 but
not on days 34-40. Placental secretion of estradiol-17fi increased
markedly after days 60-66, whereas little, if any, placental secretion of estrone was apparent a t this time. These results provide
circumstantial evidence that progesterone secretion by the corpus
luteum of early pregnancy extends beyond the time when estrogen
secretion has declined and that the timing of the luteo-placental
shift in the baboon is intermediate between that in rhesus monkeys
and that in marmosets and humans. Increased secretion of androgens during the first 6 weeks of gestation may be useful in early
pregnancy diagnosis in the baboon, although the physiological significance of this event is not clear.
Key words: pregnancy, olive baboon, Pupio anribis, ovarian steroids, placental steroids,
progesterone, androstenedione, testosterone, estrone, estradiol-176
Received March 29, 1984, revision accepted July 4, 1984
Address reprint requests to J K Hodges, MKC ARC Comparative Physiology Research Group, Institute
of Zooloby, The Zoological Society of London, Rcgent's Park, London N W 1 4RY, Unlted Kingdom
0 1984 -41an R. Liss, Inc.
358 I Hodges, Tarara, and Wangula
The baboon has been the subject of detailed morphological studies on implantation and embryonic development [eg, Hendrickx, 1971; Pope, et al, 1982a1 as well as
proving a useful experimental primate in applied aspects of teratology and immunological inteiference with pregnancy [Hendrickx et al, 1975; Stevens, 1974, 19811.
Surprisingly little attention, however, has been paid to the hormonal control of early
pregnancy in the baboon and, in particular, the relationship between luteal and
placental endocrine function is poorly understood. Considerable information exists
on maternal and fetal endocrinology during mid to late gestation Leg, Townsley,
1974; Albrecht et al, 1980; Dawood & Fuchs, 19801, but there is only one report
relating to the hormonal control of early pregnancy, which describes changes in
peripheral plasma levels of total estrogens and progestins at intervals during the
first 25 days [Shaikh et al, 19761.
Studies in other nonhuman primates and humans have shown that the maintenance of early pregnancy depends upon a n initial and variable period of steroid
secretion by the corpus luteum, after which the placenta becomes the major source
of steroids and the corpus luteum is dispensible [Csapo & Pulkkinen 1978; Goodman
& Hodgen, 19791. There are, however, few details in any primate on the onset of
placental endocrine function and on the proportions of steroids secreted by the ovary
and placenta during the transition period. [Walsh et al, 1979; Hodges et al, 1983b).
The purpose of this study, therefore, was twofold: to determine changes in circulating
levels of steroid hormones at intervals during the first 100 days of pregnancy in the
olive baboon (Papio anubis) (gestation length 175-185 days); and to examine the
relative contribution of the ovary and placenta t o circulating steroid concentrations
during this period.
Adult female Olive baboons (Papio anubis), at least 5 years old and weighing
15-18 kg, were used in this study. Animals were maintained in sheltered outdoor
cages a t the Institute of Primate Research, Nairobi, Kenya. They were fed twice
daily with commercial primate cubes supplemented with fruit and vegetables and
provided with water ad libitum. Animals used for the collection of samples up to day
19 of pregnancy were kept in single cases (n = 11);samples during subsequent stages
of pregnancy were collected from different animals maintained in harem groups
(two males and approximately 25 females) in large corral-type cages (n = 16). These
animals were trained to enter smaller individual cages (attached to the side of the
main cage), normally used for collection of urine, where they were sedated with
ketamine-xylazine (see sample collection) before removal for sampling and surgery.
Mating Schedule
Female baboons in harem groups were in continuous contact with males and
were allowed to mate freely. Females housed individually were transferred to the
males cage for 6 hours daily for up to 5 days during the period of maximum sex skin
swelling (turgescence). The timing of the first day of mating within the period of
turgescence was based on the duration of maximum sex skin swelling in previous
menstrual cycles (known to be relatively constant within individuals). A vaginal
swab was taken a t the end of each 6-hour period and examined for the presence of
Timing of Pregnancy
Changes in sex skin swelling were carefully monitored each day in all females
in the study. The day of ovulation was estimated to be two days before the end of
Steroids and Raboon Pregnancy / 359
maximum turgescence (ie. onset of deturgescence), based on the findings of previous
studies [Wildt et al, 1977; Shaikh, 19821. This was also designated day 0 of pregnancy. Animals were divided into five groups, according to the stage at which blood
samples were collected. Group 1: day 8-9 (nonpregnant or unconfirmed pregnant,
n=4). These animals were mated as normal and surgery scheduled for the period
around implantation. However, blastocysts were not recovered after uterine flushing, and there was no evidence of a n implantation site. No other test for pregnancy
was carried out. Group 2: 10-19 days pregnant (n=7). Pregnancy was indicated by
the presence of a n embryo and implantation site, subsequently confirmed by histological examination (separate study). Samples were collected on day 10 (n = 11, day
11( n = l ) , day 13 (n=2), day 17 (n=1), and day 19 (n=2). Group 3: (34-40 days, n=6).
Group 4: (60-66 days, n=5). Group 5 : (104-106 days, n=5); pregnancy was confirmed
by the presence of an embryo or fetus. Blood sampling and laparotomy were performed once on each animal.
Sample Collection
Animals were anesthetised with a ketamine-xylazine mixture, 0.1 m l k g body
weight, i.m. (ketamine 70 mg/ml; xylazine 6 mg/ml) before removal from their cages.
Peripheral blood samples (10 ml) were taken by femoral venepuncture using a 21gauge needle and a nonheparinized syringe. Animals were then intubated and
maintained on gaseous anaesthesia using halothane (1.5-3%), nitrous oxide (0.5 L/
min), and oxygen (1.5 L/min). Laparotomy was performed by midventral abdominal
incision, and left and right utero-ovarian vein blood samples were collected using a
2-ml nonheparinized syringe fitted with a 25-gauge needle. Blood samples were
allowed to clot a t 4°C for 4-6 hours. Serum was collected after centrifugation at 400
g for 20 minutes at 4°C and stored at -20°C. Samples were shipped to London by
air and kept frozen with dry ice.
Steroids were separated by Celite chromatography [Anderson et al, 19761 before
assay. Tracer amounts (1,000 cpm) of 3H progesterone, 'H androstenedione, and 'H
testosterone, or 'H estrone and 3H estradiol-176 (Amersham International Ltd,
Bucks, England) with specific activities of 87, 98, 107, 92, and 102 Ciimmol, respectively, were added to the samples before extraction with ten volumes of redistilled
diethyl ether. Extraction for the measurement of estrogens was performed separately from that for the measurement of the other steroids. The extracts were
evaporated to dryness under nitrogen and allowed to reconstitute overnight in 1.0
ml iso-octane. Estrone and estradiol-17P were eluted from ethylene glycol columns
as described by Hodges et a1 [1983c]. Other steroids were eluted from propylene
glycol: celite (1:2 viw) columns with 2.5 ml isoctane (progesterone), 4.0 ml 8% ethyl
acetate in iso-octane (androstenedione), 3.0 ml 15%ethyl acetate in iso-octane (rinse),
and 4.0 ml 24% ethyl acetate in iso-octane (testosterone), based on the method
described by Nakakura et a1 [1982]. The fractions were dried under nitrogen and
reconstituted in 1.0 ml assay buffer for assay and recovery determination.
Radioimmunoassay of steroids was carried out according to the World Health
Organization procedure for matched reagents as described in detail by Hodges et a1
11983~1.The origins and cross-reactivities of the antiserum for estrone and estradiol176 have been reported by Hodges et a1 [1983c], and those for the antisera for
progesterone and testosterone by Harlow et a1 [1984] and Hodges et a1 [1983a],
respectively. Androstenendione was measured using an antiserum (Steranti Re-
360 Hodges, Tarara, and Wangula
search Ltd, St Albans, Herts, England) raised in a rabbit against androstenedione11-(succinyl)bovine serum albumin. Measured cross reactivities included androsterone l%, testosterone 0.5%, 5cr dihydrotestosterone, and dehydroepiandrostenedione
0.05%, CI8 and CZl steroids tested 0.01%. Dilution of antiserum was adjusted to give
approximately 30% binding in the absence of competing cold steroid.
Procedural losses were monitored individually. Mean recovery values for individual steroids after extraction and celite chromatography were between 65 and
84%. Assay sensitivity, calculated as the mass of hormone required to suppress the
binding of labelled hormone to 90% of the binding achieved in the absence of
unlabelled hormone, was between 5 and 10 pgltube depending on the steroid being
measured. The volume of serum taken for extraction varied according to the sample
volume available and the approximate hormone concentration expected (determined
previously in separate assays). Buffer blanks which were extracted and run through
celite gave values less than the assay sensitivities. The intraassay precision, expressed as the coefficient of variation, was below 10%for each hormone assay. Values
for the interassay coefficient of variation, based on repeated measurements of a pool
of monkey plasma were 11.1,11.6, 8.5, 12.1, and 14.7 for the estrone, estradiol-l7P,
progesterone, androstenedione, and testosterone assays, respectively.
Validation of the measurement of each hormone was achieved by performing
cochromatography on celite and comparing immunoreactivity and recovery of pure
tritiated steroid across the appropriate fractions at 0.5-ml intervals [Hodges et al,
1983~1.The elution profiles of immunoreactivity and radioactivity were similar for
individual hormones, indicating the absence of substantial contamination from
cross-reacting substances.
Statistical Analysis
Data for peripheral and utero-ovarian vein samples (including ratios) were
analysed separately using a one-way analysis of variance. Means were compared
post hoc by the Duncan Multiple Range Test.
The data for mean steroid concentrations in peripheral blood and in matched
samples from the utero-ovarian veins draining ovaries with and without a corpus
luteum are shown in Figures 1-5. All animals possessed a single corpus luteum.
Mean peripheral levels of progesterone rose significantly between days 10-19
and days 34-40 (p < 0.011, after which there was no further increase (Fig. 1).
Similarly, progesterone concentrations in the utero-ovarian vein not associated with
a corpus luteum also increased between days 10-19 and days 34-40 (p < 0.05),
without further significant change. In contrast, there were no significant differences
between progesterone levels in the utero-ovarian vein associated with a corpus
luteum. The mean ratio of progesterone levels in utero-ovarian veins with and
without a corpus luteum was significantly lower by day 60 and thereafter, compared
with days 8-9 (p < 0.01) and 10-19 (p < 0.05).
Mean concentrations of androstenedione in peripheral blood were significantly
higher on days 10-19 and days 34-40 (p < 0.01) than at the other three stages (Fig.
2). The levels in utero-ovarian vein samples associated with a corpus luteum were
also significantly higher between days 10 and 19 than levels a t other stages (p <
0.05, p < 0.01), while concentrations in the opposite utero-ovarian vein were significantly elevated on days 10-19 and 34-40 (p < 0.05) and were similar to each other.
Although the mean ratio of utero-ovarian vein levels fell from 1.85 between days 10
and 19 to 0.9 between days 34 and 40, the overall changes throughout the study
were not significant.
Steroids and Raboon Pregnancy / 361
The pattern of testosterone in peripheral circulation was similar to that of
androstenedione, although the absolute levels were lower (Fig. 3). Mean concentrations were significantly higher beween days 10-19 and 34-40 (p < 0.01) compared
with the other three stages, which were not significantly different from each other.
The apparent increase in testosterone in utero-ovarian vein samples over the same
period was not significant. This, however, is probably due to the extremely high
values in one animal in the 10-19-day group (utero-ovarian vein levels of 11.6 n g h l
and 12.4 ng/ml), since if these data were omitted, the adjusted means for uteroovarian vein levels with and without a corpus luteum were 1.25 ng/ml and 1.22 ngl
ml, respectively, and there was a significant elevation in testosterone levels in both
utero-ovarian veins between days 34 and 40 (p < 0.05). "here was no significant
change in the ratio of utero-ovarian vein testosterone levels over the period of study
before or after removal of the outlying data points mentioned above.
Mean peripheral levels of estrone (Fig. 4)rose between days 8-9 and 60-66 (p
< 0.05) with a further marked increase by days 104-106 (p < 0.01). In contrast,
there were no significant changes in mean levels of estrone in samples from either
utero-ovarian vein. However, the ratio between estrone levels in utero-ovarian veins
with and without a corpus luteum was significantly higher on days 10-19 compared
with all other stages (p < 0.01).
Estradiol-17P concentrations in peripheral blood increased progressively from
days 8-9 to 60-66, although due to large individual variation in the data, the mean
values were not significantly different (Fig. 5). There was, however, a highly significant increase after days 60-66 (p < 0,001). Similarly, the levels of estradiol-170
measured in samples from the utero-ovarian veins with and without a corpus luteum
also increased significantly at this time (p < 0.05, p < 0.01, respectively). The mean
ratio of estradiol-170 levels in utero-ovarian veins with and without a corpus luteum
was four- to sixfold higher on days 10-19 than a t subsequent stages, but the values
were not significantly different.
The present study examines the relationship between ovarian and placental
steroid secretion during early pregnancy in the baboon. The ratio of progesterone
levels in utero-ovarian veins draining ovaries with and without a corpus luteum
suggests that the corpus luteum is the major source of circulating progesterone until
a t least day 19 of pregnancy, whereas by day 60 placental progesterone secretion
has taken over. Although the onset of placental progesterone secretion is not clear
from the present data, the pattern of progesterone in utero-ovarian vein samples
without a corpus luteum indicates that secretion by the placenta is already well
advanced by the fifth week of pregnancy. Thus, the rise in peripheral progesterone
levels between days 10-19 and 34-40 of pregnancy reflects increasing placental
production rather than extended secretion by the corpus luteum. From the sampling
frequency used in this study it is difficult to compare the precise timing of the shift
from luteal to placental progesterone secretion in the baboon with that in other
primate species. In humans and marmoset monkeys, placental progesterone secret,ion begins around week 4-5 of pregnancy, although luteal secretion is still evident
at day 40 in marmosets [Hodges et al, 1983bl and, in humans, the corpus luteum is
not completely dispensible until week 6 [Csapo & Pulkkinen, 19781. In rhesus
monkeys, however, placental progesterone production begins as early as day 22
[Goodman & Hodgen, 19791, at a time when there is no longer a substantial contribution from the corpus luteum [Walsh et al, 1974; Sholl et al, 19771. Thus, from the
limited information available, the timing of the luteo-placental shift with respect to
progesterone secretion in baboons appears to be intermediate between that of hu-
362 I Hodges, Tarara, and Wanmila
7 .
0 12
Days after ovulation
Days after ovulation
Fig. 1. Upper portion. Concentrations or progesterone in the peripheral circulation ( A 1 and in uteroovarian veins draining ovaries with (*) and without (01 corpora lutea during early and mid pregnancy in
the bahoon. Samples in the day-8-9 group are from nonpregnant animals or animals in which pregnancy
4 (days 8-9) and 5-7 (all other slagesi. Lower portion.
was unconlirmed. Values are mean i s.e.m.. n :
Ratio of progesterone concentrations in utero-ovarian veins draining ovaries with and without corpora
lutea twithlwithout). Values are mean i s.e.m., n = 4 (days 8-91 and 5-7 (all other staged.
Fig. 2. Concentrations of androstenedione in peripheral and utero-ovarian vein blood and the ratio of
concentrations in utero-ovarian veins draining ovaries with and without a corpus luteum. See legend to
Figure 1for full details.
mans and marmosets and that of rhesus monkeys. Species differences in overall
gestation length should, however, be taken into consideration (baboon 185 days;
human 280 days; marmoset 144 days; rhesus monkey 165 days).
The fourfold elevation in mean androstenedione and testosterone levels in the
10-19-day group compared with levels a t days 8-9, in the absence of marked differences in the levels of other steroids, is of particular interest. Although the reproductive status (ie, pregnant or nonpregnant) of the animals in the 8-9-day fsroup is
uncertain, the levels of both androgens a t this time were similar to those reported
by Kling and Westfahl 119781 during the midluteal phase in Papzo cynocephah.
Irrespective of the composition of the 8-9-day group, however, the present data
clearly indicate a marked increase in the secretion of testosterone and androstenedione within the first 2-3 weeks of pregnancy. Sequential sampling during conception and noxiconception cycles would be needed to confirm this and to determine the
time course and magnitude of increased androgen secretion over the initial period
of gestation. Some support for the current observations is, however, provided in a
preliminary communication on P. qnorephalus by Castracane [1982], which reports
increased levels of androstenedione and testosterone during the conception cycle,
rising to maximum values around day 40; no data on hormone levels are given,
Although the stimulus for increased androgen secretion is not known, the period
of elevated levels approximates the time when chorionic gonadotrophin is detectable
in peripheral blood (12-55 days of pregnancy, [Tuller, 1974; Pope et al, 1982bj.
Indirect evidence that the increases in androgen secretion during early pregnancy
Steroids and Raboon Pregnancy I 363
Days after ovulation
Days after ovulation
Fig. 3. Concentrations of testostcrone in peripheral and utero-ovarian vein blood and the ratio of
concentrations in utero-ovarian veins draining ovaries with and without a corpus lutcuni. See legend to
Figure I for full details.
Fig. 4. Concentrations of cstrone in peripheral and utero-ovarian vein blood and the ratio of concentrations in utero-ovarian veins draining ovaries with and without a corpus luteum. See legend to Figure 1
for full details.
2.g 4
60-66 104-106
Days after ovulation
Fig. 5. Concentrations of estradiol-178 in peripheral and utero-ovarian vein hlood and the ratio of
concentrations in utero-ovarian veins draining ovaries with and without corpus luteum, *, **, =**; mean
s.e.m. values for pcripheral samples 0.032 i 0.009 n g h l , 0.07 ? 0.02 ng/ml, and 0.11 0.02 ngiml,
respectively. See legend to Figure 1for full details.
364 I Hodges, Tarara, and Wangula
may be related to the onset of CG production is provided by Castracane [1982] who
showed that hCG administration during the nonpregnant luteal phase results in a n
increase in circulating levels of both testosterone and androstenedione. However, it
is not clear why, in the present study, secretion of androgens increased in the
absence of any marked change in the circulating levels of estrogens or progesterone.
The data shown in Figures 2 and 3 provide circumstantial evidence for luteal
secretion of androstenedione between days 10 and 19 and for nonluteal (possibly
placental) secretion of both androgens between days 34 and 40. If placental secretion
of androgens does occur at this time, it is difficult to explain why it is limited to the
early stages of pregnancy, since by day 60 both peripheral and utero-ovarian vein
levels have declined to nonpregnant values. One possible explanation, supported by
the increase in estrone and estradiol-17P between days 3 4 4 0 and 60-66, might be a
feedback mechanism whereby androgen secretion is regulated by estrogens. Alternatively, a n increase in placental aromatisation of androgens may occur a t this
stage of pregnancy. Clearly, further studies are required to clarify the control and
physiological importance of androgen secretion during early pregnancy in the baboon.
Circulating levels of estrone and estradiol-17P on days 8-9 and 100-106 were
comparable to those measured a t equivalent stages in other species of baboon [Kling
& Westfahl, 1978; Albrecht & Townsley, 1978) but considerably lower at days 60-66
than those (3.5 ng/ml estradiol-17P 1 reported in I? papio by Albrecht and Townsley
[1978]. This discrepancy is unlikely to be due to differences in assay methodology
(levels a t day 100 were similar) but most probably reflects a species difference with
respect to the onset of increased estradiol-17P secretion. The utero-ovarian vein
estrone concentration ratios indicate that the corpus luteum secretes estrone between days 10 and 19 but not at other stages. Luteal secretion of estradiol-176 on
days 8-9 and 10-19 may also be inferred from the elevated utero-ovarian vein ratios
a t these times, although due to individual variation in the levels of estradiol-l7/3,
this could not be demonstrated statistically. There was, however, no evidence of
luteal secretion of either estrogen by days 34-40 of pregnancy. Since days 34-40
represent a transitional period between luteal and placental secretion of progesterone, the corpus luteum of early pregnancy in the baboon may continue to secrete
progesterone beyond the time when estrogen secretion has declined, which is similar
to recent findings in the marmoset monkey [Hodges et al, 1983131.
The origin of circulating estrone after days 34-40 is unclear, since the marked
increase in peripheral levels occured in the absence of a rise in utero-ovarian vein
concentrations. This observation suggests that during midpregnancy in P anubis,
circulating estrone may derive largely from peripheral conversion and that there is
little, if any, direct secretion from the placenta. Further studies are, however, needed
to support this interpretation which a t present is purely speculative.
In contrast to estrone, the marked elevation in circulating estradiol-17P levels
by day 104 pregnancy appears to be directly related to increased placental secretion
as evidenced by the rise in estradiol-17p concentrations in both utero-ovarian veins.
Estradiol production during late pregnancy in P: papio is known to occur principally
in the placenta from dehydroepiandrosterone (DHEA) secreted by the maternal and
fetal adrenal glands [Townsley & Pepe, 1977: Schut ct al, 19781. The elevation in
circulating estradiol-17P between days 66 and 104 of pregnancy may therefore be
related to changes in the secretion and/or placental utilization of DHEA at this time.
Although this would not seem to be supported by the pattern of DHEA in peripheral
circulation, which does not show a significant increase until after day 150 [Townsley
& Pepe, 19771, increased availability of DHEA or its sulphate for placental conversion may not necessarily be reflected by changes in concentrations in the peripheral
Steroids and Baboon Pregnancy / 365
1. Comparison of progesterone concentrations in peripheral and utero-ovarian
vein samples indicated that the corpus luteum is the major source of progesterone
until at least day 19 of pregnancy and that the onset of placental progesterone
secretion occurs before day 34.
2. Peripheral concentrations of testosterone and androstenedione were significantly elevated on days 10-19 and 34-40 compared with other stages. The increase
in androgen levels during the first 6 weeks of pregnancy appears to reflect ovarian
and possibly early placental secretion which declines by day 60. Measurement of
testosterone or androstenedione may be useful in early pregnancy diagnosis in the
3. The corpus luteum secretes estrogens until at least day 19 of pregnancy but
not a t day 34. Circulating estradiol-17P concentrations rise sharply between days
60-66 and 104-106, reflecting increased placental secretion. In contrast, very little
placental secretion of estrone was evident at any of the stages observed.
We are grateful to the colony management staff of the Institute of Primate
Research for care and maintenance of the animals; Dr. N. Gulemhusein for assistance with surgery; the World Health Organisation for standards and antisera for
the testosterone and estradiol-17P assays; and to Dr. D.H. Abbott and Mr. D. Harris
for advice on statistical analysis. The work was supported by the World Health
Organisation Special Programme on Human Reproduction, a Medical Research
Council (U.K.) Programme Grant to Professor J. Hearn, and a core support grant
from the A.B.R.C. to the Institute of Zoology.
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pregnancy, steroid, mid, baboons, ovarian, secretion, placental, relationships, early, circulating
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