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Circulating and excreted hormones during the ovarian cycle in the cotton-top tamarin Saguinus oedipus.

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American Journal of Primatology 31:55-65 (1993)
Circulating and Excreted Hormones During the Ovarian
Cycle in the Cotton-Top Tamarin, Saguinus oedipus
TONI E. ZIEGLER, DANIEL J . WITTWER, AND CHARLES T. SNOWDON
Department of Psychology and Wisconsin Regional Primate Research Center, University of
Wisconsin, Madison
Five parous, cycling cotton-top tamarin females were used to compare
circulating and urinary profiles of the major reproductive hormones during the ovarian cycle. Blood samples were collected on unanesthetized,
hand restrained females three times per week for 25 days and first morning void urine was collected daily for 30-40 days including the serum
sampling period. Serum and urine samples were analyzed for estrone,
estradiol, and bioactive LH. Additionally, serum was analyzed for progesterone and urine for estrone conjugates (ElG) and immunoreactive LH.
Both serum and urinary hormonal profiles revealed ovarian cyclicity in
four females; the fifth one stopped cycling during the study. All hormones
were referenced to the urinary immunoreactive LH peak. Urinary estrone
conjugates followed similar profiles to serum progesterone. Progesterone
levels increased two- to threefold on the day of the urinary immunoreactive LH peak. Peak levels of circulating bioactive LH occurred on the same
day or the day preceding the urinary bioactive and immunoreactive LH
peak for all four cycling females. Serum estradiol levels rose during the
follicular phase and peaked prior to or on the day of the urinary LH peak
while urinary estradiol levels did not rise until the day of the urinary LH
peak. Serum and urinary estrone levels did not rise until the day of the
urinary LH peak and remained high throughout the luteal phase. The
measurement of urinary LH corresponded well with serum LH, establishing urinary LH as an important hormone for monitoring the ovulation in
the tamarin. The highest circulating estradiol concentrations were found
in the follicular phase of the cycle, but estradiol did not appear in urine
during the follicular phase of the cycle. Elevated estrone levels occur during the luteal phase following the progesterone pattern, and therefore
elevated urinary concentrations of estrone and estrone conjugates may be
indicative of luteal function. o 1993 Wiley-Liss, Inc.
Key words: ovarian cycle, serum hormones, urine hormones, tamarins
Received for publication October 5, 1992;revision accepted March 1, 1993.
Address reprint requests to Dr. Toni E. Ziegler, Department of Psychology, 1202 W. Johnson St., University of Wisconsin, Madison, Wisconsin 53706.
0 1993 Wiley-Liss, Inc.
56 1 Ziegler et al.
INTRODUCTION
Reproductive events are best detected and timed while monitoring hormonal
concentrations, especially in species of primates that do not exhibit external signs
of ovulation and conception. Traditionally, reproductive events have been described through measurement of circulating hormones which allow for precise
timing of ovulation and early detection of pregnancy. However, when monitoring
the reproductive events in endangered, excitable, or very small animals, urinary
assays for reproductive hormones have proven to be reliable and less stressful
[Hodges et al., 1979; Shideler et al., 1983; Lasley et al., 1985; Dahl et al., 1987;
Ziegler et al., 1987a,bl.
While many primate species have been examined for reproductive function
using urinary assays, with very few species have the patterns of urinary hormones
been compared directly to circulating hormones to determine their effectiveness in
timing ovulation and early detection of pregnancy. To date, this comparative information is only available for the human [Munro et al., 1991; Dahl et al., 1987;
Beitins et al., 19801, the cynomolgus monkey [Mehta et al., 19861, the rhesus
macaque [Monfort et al., 19871, the common marmoset [Eastman et al., 1984;
Hodges et al., 19831, and the owl monkey [Bonney et al., 19791. Most of these
studies were limited to a comparison of only one or two hormones.
Most of our knowledge of the reproductive hormones in the cotton-top tamarin
comes from measurements of urinary hormones [Brand, 1981; French et al., 1983;
Ziegler et al., 1987a,bl. Both urinary estrone and estradiol show elevated levels
following the LH surge, paralleling progesterone concentrations, without a preovulatory urinary estrogen rise. Since the major urinary estrogens show a luteal
instead of follicular rise and only 5% of progesterone is excreted into the urine
[Ziegler et al., 19891, a comparative study on circulating and urinary hormones is
essential for the interpretation of the urinary hormonal patterns.
The present study documents the patterns of hormone secretion in the peripheral circulation and compares the serum hormonal profiles to urinary metabolites.
MATERIALS AND METHODS
Subjects and Sampling
Five cycling cotton-top tamarins ranging in age from 20 months to 9 years
were used as subjects. All but one female (the youngest) had given birth to live
infants. One female lived alone in a pair cage, three females were paired with a
male and two of these females were hysterectomized with ovaries intact while the
other one lived with a vasectomized male, and one female was the breeding female
in a large family (five offspring in the cage) where the breeding male had died.
Thus, all five females were unable to conceive during the study. Sizes of pair and
family cages, husbandry, and diet have been reported [Snowdon et al., 1985; Ziegler et al., 1987bl.
Blood and urine samples were collected from the tamarins for 25-30 days.
Three times per week between 1300 and 1400, the females were caught from their
cages and hand restrained while 0.5-0.9 ml of blood was collected by venipuncture
of the femoral vein on the unanesthetized females. The collected blood was stored
in serum separator tubes (Microtainer, Becton Dickinson, Rutherford, NJ) for 30
min, then centrifuged for 10 min, and the serum portion stored at -20°C until
hormonal assay analyses. Once a week, an aliquot of the whole blood collected from
each female was used to monitor hematocrit levels. Hematocrit levels decreased
15-18% over the four week bleeding period falling from a mean of 54 to a mean of
47. Urine was collected as first morning void daily between 0800 and 0900 when
Serum and Urinary Hormones in Cotton-Top Tamarins / 57
TABLE I. Parallelism, Recovery of Extracted Steroid, Assay Sensitivities, and
Precision for the Hormones Measured in the Serum and Urine of Cotton-Top Tamarins
Sensitivity
Hormone
~
Parallel
Recoveryb
pg/tubeb
Serum'
80.55 2 0.95
0.21 rt 0.01
10.6
pg/ml
6.5
pg/ml
26
ng/ml
0.14
ng/ml
15.82
mIUf
Assay precision"
Urine'
Intra
Inter
~~~
estrone
yes serum
yes urine
estradiol
yes serum
yes urine
estrone
no serum
conjugates yes urine
progesterone yes serum
yes urine
bioLH
yes serum
yes urine
immunoLH
yes urine
82.30
* 2.89
0.56
* 0.01
-
3.10 ? 0.91
87.70 ? 0.21
1.06 5 0.51
103.6 t 2.60
1.04 0.28
ng/mlTd
0.29 C 0.01
Flltube
-
*
-
17.61 4.32' (3) 13.44 (7)
ng/ml
3.9
5.43 (3) 11.78 (7)
ng/ml
196
2.78 (3) 10.68 (7)
ng/ml
2.92 (3)
3.53 (3)
23.07
mIU
8.0
bum1
3.36 (3)
13.72 (4)
2.66 (3)
8.88 (3)
"Expressed as coefficient of variation.
'Values are mean s.e.m.
'Based on dilutions used for assay.
dT = testosterone.
"Numberin parentheses = n.
'mIU = milli-international units of purified human chorionic gonadotropin.
*
lights were turned on in the rooms. A collection container was held directly underneath the female of interest while she urinated. A detailed description of the
collection technique has been described [Ziegler et al., 1987a,bl. Collected urine
was centrifuged and stored at -20°C until hormonal analyses were performed.
Ovarian cycling that is not followed by conception rarely occurs in paired
cotton-top tamarins. We therefore assessed all previous complete ovarian cycles
that have been monitored in our colony by measuring daily urinary estrone conjugates and LH. These were analyzed for ovarian cycle length and for length of the
follicular and luteal phase of the cycle. The seven females who had shown ovulatory cycles were between 1 and 10 years of age and represented all aspects of
reproductive condition (i.e., nulliparous to multiparous, paired or living alone after
a mate had been removed).
Assays
Both serum and urine samples were analyzed for estrone, estradiol, and bioactive LH. Additionally, serum was analyzed for progesterone and urine for immunoreactive LH and estrone conjugates. The methods and validation of urinary
hormones for these assays have been described [Ziegler et al., 1987a,bl but brief
descriptions of the assays and the modifications for serum analyses are reported
below. Table I gives information on parallelism, recoveries, sensitivity, and precision for the various assays.
Serum samples (60-100 pl) analyzed for estrone and estradiol were measured
by ether extraction, chromatography separation using LH-20 Sephadex columns
and a dich1oromethane:methanol solvent system with individual RIA of each steroid. This method separates estrone and estradiol from each other as well as from
other steroids. The estrone antiserum crossreacted < 0.1%with other steroids but
the estradiol antisera crossreacted 5.8%with estrone, 0.3% with estriol, and 0.82%
58 / Ziegler et al.
for testosterone. Serial dilutions of a serum pool with the addition of 50 pgI100 p1
of estrone and 75 pg/lOO p1 of estradiol were parallel to the standard curve and
gave recoveries of each added steroid at 80.6% and 82.3%, respectively. Urine
samples were assayed at volumes between 0.1 and 1pl using a 1:lOO dilution of the
samples with an additional dilution of 1:25 for estrone after chromatographic separation. To measure total estrone and estradiol, urine was hydrolyzed overnight
with 25 p1 beta-glucuronidase (Type H2, containing sulphatase activity as well,
Sigma Chemical Co., St. Louis, MO) a t 37°C prior to column chromatography.
Serum and urine samples were run in the same RIA for each female. The intra- and
interassay coefficient of variations are reported in Table I.
Measurement of estrone conjugates (ElGI in the urine was accomplished by
adding 0.01-0.1 p1 of sample and direct assay with estrone-3-glucuronide antibody
and trace. Validation and description of this assay has been reported [Ziegler et al.,
1987bl. Serum samples were not analyzed for E1G since serial dilutions of a serum
pool were not parallel to the standard curve.
Serum samples were analyzed for progesterone concentration using 10 p1 of
serum. Samples were extracted with 5 ml of petroleum ether to separate progestins
from other steroids, dried under air, and measured by RIA using a progesterone
antiserum a t 1:2,800 in 100 p1 (HH, P-1, Holly Hill Biologicals, Inc., Hillsboro, OR)
and [1,2,6,7-3Hl-progesterone
a t 7,500 cpm in 100 pl (P4:New England Nuclear,
Boston, MA) as ligand. The antiserum crossreacted 14.4%with 5a-pregnane-3,20dione, 1.6%with pregnenolone, 0.6% with 5P-pregnane-3,20-dione, 0.2% with 17ahydroxyprogesterone, 0.2% with 20P-dihydroprogesterone,and 0.2% with 20adihydroprogesterone. Progesterone (Sigma) was used as standards in the range
from 5-250 pg/ml. Five serial dilutions of pooled tamarin serum were parallel to
the standard curve.
Bioactive LH (bioLH) was measured by the use of the mouse interstitial cell
bioassay using the methods already reported [Ziegler et al., 1987al. Serum and
urine samples were added as 5 p1 of sample diluted with 95 pl of tissue culture
medium 199 with 0.2% BSA. Pooled tamarin serum with the addition of serial
dilutions of human chorionic gonadotropin (0.1,0.25,0.5 mlU) were parallel to the
standard curve and yielded an accuracy of 103.6 ? 2.6%.
Immunoreactive LH was measured in urine using a heterologous LH RIA
which measures LH and CG in the tamarin. Methods and validations have been
reported [Ziegler et al., 1987al.
All urinary hormonal concentrations were expressed as milligrams of creatinine to compensate for variability in fluid intake. The creatinine assay was performed according to the methods in Tietz [19761.
RESULTS
Four of the five tamarins displayed hormonal cyclicity during the blood and
urine sampling. The fifth female ceased cycling and all her hormone levels dropped
to basal levels during the sampling period. Ovarian cycle lengths as defined by
successive urinary immunoreactive LH peaks ranged from 15-24 days for the four
females with a mean level of 20 & 2.5 SEM. LH peaks were defined as two- to
fivefold increases in basal LH for 1-2 days before declining to near basal levels.
Levels of hormones were determined for the four cycling females and adjusted for
day from the urinary LH peak. Figure 1A presents the serum LH and progesterone
profiles and Figure 1B presents the corresponding urinary LH and E1G profiles in
one representative female. Highest elevations of LH in both serum and urine
occurred on the same day in two of the females, while highest elevations in serum
LH may have occurred the day before the urinary LH peak in the two females
Serum and Urinary Hormones in Cotton-Top Tamarins / 59
A
- 15
-E
60
E
SO-
.
2
-E
-
-
Ol
-10
=
n
I
A
40
-
30
-
5
L
al
E
2al
u)
-5
.
-
' I
'
'
'
' 1
10 I , I '
, '
-10-9 - 8 - 7 - 6 - 5 - 4 - 3 - 2 - 1
.
.
0
'
1
1
'
'
2
1
. .
4
3
)
8
I
5
6
.
'
7
I
8
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'
9
. 1- 0
10
Days from urinary LH peak
B
30
6
6
.
E
m
PI
E
1
20
C
2
0
5
F
W
P
0
.-C
10
L
f
0
I . , . , . , . , . , . , .
I . ,
- 1 0 - 9 - 8 - 7 - 6 - 5 - 4 - 3 - 2 - 1
.
,
0
.
,
1
.
,
2
.
,
3
.
,
4
.
,
5
P
0
.c
5
. ,.,.,.,.,0
6
7
8
9
10
Days from urinary LH peak
Fig. 1. Serum and urinary hormonal profiles for a representative female cotton-top tamarin during the ovarian
cycle. A: Circulating levels of serum bioactive LH (bioLH, expressed in mIU/human chorionic gonadotropin
reference preparation) and progesterone (P). B Urinary levels of immunoreactive LH and estrone conjugates
(ElG). All graphs are normalized to the day of the urinary LH peak and urinary hormones are expressed per
milligram of creatinine (Cr).
where a matched serum sample was not obtained on the day of highest urinary LH
levels. Serum progesterone and urinary E1G showed similar profiles of basal levels
of hormone prior to the LH peak, increasing the day before or the day of the LH
peak and remaining elevated following the presumed ovulation. Thus, ovulation in
60 / Ziegler et al.
100
t
80
cn
E
.
2
E
I
60
50
F
m
.-C
-
L
40
0
. , . , . , . , . , . ) . 1 . r . , .
- 1 0 - 9 - 6 - 7 - 6 - 5 - 4 - 3 - 2 - 1
a
20
0
1
2
3
4
5
6
7
8
9 10
Days from urinary LH peak
Fig. 2. Serum and urinary bioactive LH levels (bioLH, expressed &s mIUlml human chorionic gonadotropin
reference preparation) from a representative female cotton-top tamarin during the ovarian cycle. Data are
normalized to the day of the urinary LH peak.
the tamarin may best be reflected by a serum LH peak coincident with increased
progesterone and a urinary LH peak coincident with increased E1G. The follicular
phase for the females was described by basal levels of serum progesterone (< 5
ng/ml) and urinary E1G (< 10 pg/mgCr) for 5 days prior to the urinary and serum
LH peak.
Based on the data revealing serum progesterone and urinary E1G patterns to
be similar, we examined eleven females for ovarian cycle length by assessing
urinary LH and E1G. There was a mean cycle length of 21.36 f 1.05 SEM. days
(range 15-24 days). Follicular and luteal phases of the cycle were identified by
basal E1G for the follicular phase and elevated E1G for the luteal phase. The
follicular phase was an average of 5 2 0.45 days with a coefficient of variation (c.v.)
of 8.94%. The luteal phase was found to be a mean of 16.36 f 3.64 days with a C.V.
of 22.25%indicating that the majority of variance in cycle length between females
was due to the variation in length of the luteal phase.
Serum and urinary bioactive LH profiles are shown in Figure 2 for an individual female. Although serum samples were not collected daily, the highest concentrations of the hormone appeared to coincide in serum and urine or else the
serum LH peak preceded the urine peak by a day. Serum and urinary bioactive LH
concentrations were highly correlated for all females, r = 0.83, n = 43, P < 0.01.
Comparisons of serum estrogens to urinary estrogens are shown in Figure
3A,B for one representative female. All females showed comparable profiles. Serum estradiol levels were elevated during the follicular and ovulatory phases, but
urinary estradiol did not increase until the day of the LH peak. Neither serum nor
urinary estrone concentrations showed follicular increases, but they were both
elevated on the day of the LH peak and throughout the luteal phase of the cycle.
Even though serum and urinary estrone followed similar patterns, t b b viere not
Serum and Urinary Hormones in Cotton-TopTamarins I 61
A
500T+
I'800
serumE2
-E
-E
.
.
0
0
n
P
(Y
W
-10
- 5
0
5
10
15
B
t
.
E"
0
C
hl
w
Q)
.-c
L
a
Fig. 3. Serum and urinary levels of estrone (El)and estradiol (E2)in one representative cotton-top tamarin
female. A: Serum estradiol and serum estrone are measuredas days from urinary LH peak. B: Urinary estradiol
and urinary estrone measured as days from urinary LH peak. Urinary estrogens were expressed per milligram
of creatinine (Cr).
highly correlated for any of the four females. The ratio of estrone:estradiol was
higher in the urine by a mean factor of 20.5 times than in serum, indicating a shift
to increased estrone secretion in the urine.
The female who stopped cycling during the serum collection time had elevated
62 I Ziegler et al.
levels of serum progesterone, estradiol, estrone, and urinary E1G for the first 10
days of collection. Levels then dropped and remained low for the next 15 days.
After the blood collection stopped, E1G levels remained low for approximately 10
days and then the female resumed cycling.
DISCUSSION
The measurement of circulating hormones documented the ovarian cycle in
the cotton-top tamarin. The patterns of the reproductive hormones indicated normal ovarian function and resembled the hormonal profiles of other New World
primates. Although it was impossible to collect daily samples from these small
primates, the increase in follicular estradiol and elevated LH was detected in all
four cycling females. The follicular phase of the cycle was short, lasting only 5 days
with the luteal phase varying considerably. Although the present data are limited,
it appears that cotton-top tamarins differ from humans, great apes, and Old World
monkeys where follicular and luteal phases are usually of comparable lengths
[Knobil & Hotchkiss, 19881. Data from the common marmoset have indicated a
similar profile to the cotton-top tamarin where the follicular phase is shorter than
the luteal phase (mean of 8 days follicular phase: mean of 21 days luteal phase)
[Harlow et al., 1983, 19841.
Serum patterns in the cotton-top tamarin were similar to those reported in the
common marmoset with a few exceptions. Both the common marmoset and the
cotton-top tamarin show follicular increases in estradiol with peak concentrations
occurring the day before or the day of the LH peak and elevated estrone levels
occurring during the luteal phase of the cycle. However, the onset of increased
circulating progesterone appears to occur when LH is elevated in the cotton-top
tamarin, whereas the progesterone increase occurs 1-2 days following the LH peak
in the common marmoset [Harlow et al., 19841. It is not possible to make direct
comparisons between the present data on serum profiles with the data presented
by Preslock et al. [19731 on serum estrogen and progestin profiles due to the
non-specific assays that were used for that early study. However, estrogen levels
did appear to precede progestin levels in the earlier study.
The urinary profiles of immunoreactive LH and E1G paralleled the serum
profiles of bioactive LH and progesterone. It is therefore feasible to define the
ovulatory period in the cotton-top tamarin from the urinary LH peak and onset of
elevated estrone. This comparison means that urinary hormones can be used to
monitor ovarian function without the need of collecting serial blood samples in this
small and excitable primate. With the ability to collect daily urine samples reliably, we can examine social and behavioral effects on fertility at times that require
minimal disturbances to the female and her social group. This also enables us to
collect long-term data that would be impossible with serial blood sampling.
Even without daily blood sampling in the four cotton-top tamarins, it was
possible to see that the serum and urine LH levels were elevated during the same
time frame. It is possible that serum LH levels may peak the day before the
urinary LH peak in some females, but the highly elevated serum LH on the same
day as the urinary LH peak seen in two of the four females suggests that the serum
LH peak may also occur on the same day. Human LH and FSH have a fairly rapid
clearance rate through the hepatic system due to a lower sialic acid content and
may be excreted rapidly into the urine [Ashwell & Morell, 19741.
Previous investigations examining urinary estrogens in tamarins have all
revealed similar profiles of urinary estrogens increasing a t the time of the ovulatory LH peak and remaining elevated during the luteal phase of the cycle [Ziegler
et al., 1987a,b, 19891. Serum profiles from the present study indicated that the
Serum and Urinary Hormones in Cotton-TopTamarins / 63
cotton-top tamarin, as in other primates, showed follicular increases in circulating
estradiol that peak before or on the day of the LH peak. Only serum estrone showed
the urinary pattern of elevated levels beginning a t the time of the LH peak and
extending through the luteal phase. There appears to be either a delay in estradiol
excretion into the urine or estradiol is converted to nonhydrolyzable forms since
there are no increases in urinary estradiol until the time of the LH peak. It also
appears that estradiol is partially metabolized to estrone in the urine since serum
levels are comparable for the two estrogens while urine levels are considerably
higher for estrone than estradiol. Ziegler et al. [19891reported that approximately
half of injected radiolabelled estradiol was converted to estrone in the cotton-top
tamarin and that estrone is excreted a t a slower rate than estradiol.
Circulating estrone and urinary estrogens are following a progesterone-like
pattern. This may suggest that some estrogens are produced by the corpus luteum.
Elevated levels of estrogens are produced by the corpus luteum in many primates,
including humans, gorillas, chimpanzees, and orangutans, but in lesser amounts
in the Old World monkeys such as the rhesus, baboon, and cynomolgus monkeys
[see Knobil & Hotchkiss, 19883.Both the common marmoset [Harlow et al., 19841
and the cotton-top tamarin display elevated circulating levels of estrone during the
luteal phase of the ovarian cycle. An alternative explanation may be peripheral
conversion of another luteal steroid to estrone. The active interstitial gland tissue
found in tamarins of all ages after puberty may also contribute to the elevated
estrone levels [Mansdotter et al., 1992;Tardif & Ziegler, 19921.
One of the five females from which repeated serum samples were taken ceased
ovulating and showed basal hormone levels. This female was the only one living in
a large family cage where repeated capture took longer than 5 min and involved
extended chasing of the tamarins before capture occurred. Since the entire group
(six tamarins) was highly agitated, it is possible that the stress of the extended
capture experience adversely affected ovarian cyclicity. The female did return to
ovulatory cyclicity 10 days following the cessation of capture and bleeding.
In summary, the ovarian cycle of four female cotton-top tamarins was evaluated by both serum and urinary hormones. Serum estradiol levels were elevated
during the follicular phase of the cycle when progesterone levels were a t basal
levels as is typical of primates. The pattern of urinary LH and E1G followed the
same pattern of serum LH and progesterone in defining the periovulatory events.
This allows us to continue to monitor reproductive functioning by using urinary
measurements that can be collected daily with minimal intervention.
CONCLUSIONS
1. Serum LH levels were at highest elevations the day before or the day of the
urinary LH peak.
2. Urinary estrogens follow the same profile as serum progesterone and can be
used to indicate the luteal phase in ovarian cycling cotton-top tamarins.
3. Serum and urine estradiol profiles differ during the ovarian cycle with
serum estradiol indicating a preovulatory peak and urinary estradiol showing
luteal elevations.
ACKNOWLEDGMENTS
We are extremely grateful to G.Scheffler and F.Wegner for technical advice
concerning assays, P. Cofta, L. Converse, and T. Dreyfus for assisting in the
capture and bleeding of tamarins, J. Scheffler and Dr. D. Houser for veterinary
advice, and R. Roush and T. Porter for colony management. We also acknowl-
64 I Ziegler et al.
edge Dr. John Mara of Hill Pet Products, Topeka, KS, for donation of Zu-Preem
Marmoset Diet. This research was supported by grant MH 35,215 to C.T. Snowdon,
RR 00167 to the Wisconsin Primate Research Center, and The University of Wisconsin Graduate School Research Committee. This is publication 32-049 of the
Wisconsin Regional Primate Research Center.
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