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Correlation between urinary pregnanediol glucuronide and basal body temperature in female orangutans Pongo pygmaeus.

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American Journal of Primatology 34:275-281 (1994)
BRIEF REPORT
Correlation Between Urinary Pregnanediol Glucuronide
and Basal Body Temperature in Female Orangutans,
Pongo pygmaeus
CHERYL S. ASA', FRANK FISCHER', EMILEE CARRASCO', AND
CYNTHIA PURICELLI'
' S t . Louis Zoological Park, St. Louis, Missouri; 'The Population Council, New York,
New York
Changes in basal body temperature (BBT) in relation to the menstrual
cycle were investigated in three adult female orangutans (Pongo pygmaeus). In particular, the relationships of BBT to urinary estrone conjugates (EC) and to pregnanediol glucuronide (PDG) were examined using
two of the females during two cycles each. Radiotelemetry transmitters
were implanted peritoneally to record core body temperatures. Radio signals were received approximately every 2 min, 24 h per day. Because
temperatures during the period 0300-0400 h were most stable (i.e., were
less likely to be affected by confounding variables such a s activity), a mean
of these values was used to calculate daily BBT. BBT showed a highly
significant positive correlation with PDG but not with EC. Menstrual
phases were associated with declining or trough levels of BBT. Although
changes in BBT were not sufficiently distinct to predict or to precisely
identify the time of ovulation, the strong association between BBT and
PDG suggests that radiotelemetry of BBT may be useful in monitoring
ovarian cycles, especially the luteal phase, in this species.
0 1994 Wiley-Liss, Inc.
Key words: body temperature, pregnanediol, telemetry, orangutan, ape,
menstrual cycle
INTRODUCTION
The cyclicity of body temperature during the ovulatory cycle, first recognized
almost a century ago [Giles, 18971, has been ascribed to the thermogenic property
of progestins [Barton & Wiesner, 1945; Buxton & Atkinson, 19481. However, factors other than progesterone can influence body temperature, including activity,
arousal, handling [Balin & Wan, 19683, anesthesia [Wixson et al., 19871, and
circadian rhythms in basal metabolic rate and sleep [Aschoff, 19821. Peripheral
measurement (e.g., rectal or oral) may not reflect the more stable core basal body
Received for publication September 17, 1993; revision accepted January 25, 1994.
Emilee Carrasco's current address is Biopsychology Subprogram, Hunter College, 692 Park Avenue,
New York, NY 10021.
Address reprint requests to Cheryl Asa, St. Louis Zoological Park, Forest Park, St. Louis, MO 63110.
0 1994 Wiley-Liss, Inc.
276 I Asa et al.
temperature (BBT). In addition, vaginal temperature is affected by changes in
blood flow [Abrams & Bazer, 19731, also related to the reproductive cycle, but
correlated with estradiol [Abrams et al., 19731, not progesterone.
Thus, it is not surprising that earlier investigations that were unable to control for these variables produced variable results. In particular, studies to detect or
predict ovulation for timed intercourse or inseminations have met with limited
success (e.g., human: Bauman [1981]; gibbon, Hylobates lar: Carpenter [1941];
rhesus, Macaca mulatta: Erikson [1960]; dog, Canis familiaris: Christie & Bell
[1971]), perhaps because they require more precision than peripherally measured
temperature can provide, and because the cyclic increase in progesterone occurs
after ovulation in most species, with highest pregnancy rates following artificial
insemination the day prior to temperature rise [Newill & Mauricekatz, 19821.
However, biotelemetry can remotely monitor temperature during periods of
sleep from a n intra-peritoneal transmitter to control most variables, and thus,
more closely approximate true BBT. This study evaluated the ability of temperature telemetry to monitor the menstrual cycle of the orangutan as compared to
urinary estrone and pregnanediol-glucuronide levels and presence of menstrual
blood.
MATERIALS AND METHODS
Two females (#78217: 13 years; #75201: 16 years) were nulliparous, due to
deficits in the species-specific social responses necessary for mating resulting from
human rearing. The others (#911006: 22 years; #921216: 24 years) had at least
one infant. They were housed with a n adult male, also sexually incompetent due to
rearing condition, in a n indoor enclosure (approximately 62 x 30 m) during the
day (0900-1645 h) but singly overnight in sleeping quarters (8 x 12 m or 6 x 10
m) so that morning urine could be collected.
Urine was aspirated by syringe each morning from the drains of females 75201
and 78217 from 16 May to 6 July 1991 (Julian days 136 to 187), and held at -80°C
until assay. Between 1December 1991 and 25 April 1992 (Julian days 335,1991,
to 115, 1992), urine was tested for menstrual blood (Ames Hemastix; Miles, Inc.,
Elkhart, IN). Urine was also collected and tested with Hemastix, but not assayed,
from female 911006 from 6 December 1991, and from 921216 from 1 May 1993
through 28 December 1993.
On 8 May 1993, the synthetic progestin medroxy-progesterone acetate (DepoProvera; Upjohn Co., Kalamazoo, MI) was administered by intramuscular injection
(10 mg/kg body weight) to females 911006 and 921216.
Estrone conjugates (EC) and pregnanediol glucuronide (PDG) were measured
as in Chaudhuri e t al. [19881, modified for the orangutan (PDG antiserum: Department of Biochemistry and Molecular Biology, University College, London,
UK). Serial dilutions of orangutan urine had displacement curves parallel to that
obtained with increasing amounts of estrone sulfate (31.25-500 pg) or PDG (622,000 pg). Assay sensitivity was 7.5 pg/tube (EC) and 31.25 pglml (PDG); intraassay and inter-assay (n = 4) coefficients of variation (CVs) based on replicates of
a n orangutan urine pool werg 2.6% and 24.8% (EC) and 4.7% and 26.9% (PDG),
respectively. (Although standard curves were consistent, relatively high interassay CVs were due to a shift in values of pooled urine reference samples.) Steroid
values are expressed relative to urinary creatinine concentrations [Taussky, 19541.
Temperature transmitters (Wildlife Materials, Inc., Carbondale, IL; coated
with a n inert material, 7 x 3.8 x 1.8 cm, 50 g, 2 year battery life) were inserted
via a 5 cm incision into the abdominal cavities of females 75201 and 78217 under
general anesthesia (isoflurane) on 16 May 1991 (Julian day 136), into female
Orangutan Body Temperature and Progestin I 277
ORANGUTAN 782 17
r
25
r
300
4
250
TI
z
m
200!3
15OP
3
09
100,
q
140
150
160
170
180
190
200
210
JULIAN DATE 1991
menstrual phase
I
300
-
250
-
200 =
,-
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-
150y
-
-
100
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911006 on 8 September 1992 (Julian day 2521, and into female 921216 on 7 January 1993 (Julian day 737).
The automatic data collection system, consisting of a Commodore computer
and receiver (Wildlife Materials, Inc.), continuously sampled temperatures at approximately 2 min intervals. One antenna was directed toward the communal
enclosure and another toward the sleeping quarters.
Quantatative comparison of hourly standard errors on 24 h circadian temperature graphs showed 0300-0400 h to be most stable. Thus, daily means generated
from that hour were used as the BBT. Daily concentrations of EC and PDG were
compared to BBT using Pearson Product Moment Correlation (Number Cruncher
Statistical System, Kaysville, UT).
RESULTS
Concentrations of PDG, but not those of EC, were significantly correlated with
BBT (female 78217: P 5 0.001; r2 = 0.65, df = 61; female 75201: P 5 0.001; r2 =
0.60, df = 58, one-tailed test). There were more fluctuations in the BBT curve for
female 78217 than those for female 75201 (Fig. l ) , as reflected in differences in
cycle minima and maxima (1.53"C: 78217; 1.29"C: 75201).
Sustained increases in PDG were preceded by EC peaks and followed by menstrual flow (Fig. 1).A second, more attenuated elevation in EC was seen during
278 I Asa et al.
38
ORANGUTAN 75201
1
333
I
I
1
352
7
28
-
1
-
52
1
76
-
I
I
97
119
JULIAN DATE 1991-92
38
ORANGUTAN 70217
1
333
352
7
28
- I
.
I
d
52
76
97
119
JULIAN DATE 199 1-92
menstrual phase
-
menstrual phase #9llOOS
-
Fig. 2. Cyclic changes in basal body temperature of two female orangutans in relation to the menstrual phase.
periods of increased PDG excretion. Menstrual flow was first detected a s BBT,
PDG, and EC declined. Although BBT appeared to increase several days before
PDG, decreases were coincident. PDG was undetectable in this assay system during apparent inter-luteal phases, but, despite the strong correlation between these
parameters, BBT showed some fluctuation during these periods, especially in female 78217.
using only BBT and menstrual
Continued cycle monitoring of three fem:
flow revealed menstrual phases associated witl%Iecreases in BBT (Figs. 2,3). An
menstrual cycle appeared to
exception occurred in female 78217 (Fig. 21, w t
phase-shift in association with that of female 9ilh)06. Mean menstrual cycle
lengths for the three females (day 1 = first day of enstrual flow) were 34 ? 2
days (n = 5 cycles) for female 78217, 31.7 f 0.6 days (n = 6 cycles) for female
75201, and 27 f 3.3 days (n = 9 cycles) for female 911 96.
Depo-Provera treatment resulted in immediate, sustained temperature elevation in both females (Fig. 4).
-
DISCUSSION
The highly significant correlation between PDG in this study contrasts with
results for the langur, Presbytis entellus [Lohiya et al., 19881, and the chimpanzee,
Pan troglodytes [Graham et al., 19771, perhaps attributable to differences in methodology. Langur temperatures, measured vaginally with a thermometer during
Orangutan Body Temperature and Progestin I 279
37
ORANGUTAN 9 11006
I
-
u
v
z2
36 -
ffi
4
w
a
2
35 -
E-
260
280
300
320
340
360
JULIAN DATE 1992
menstrual phase
-
Fig. 3. Cycle changes in basal body temperature of female 911006 in relation to the menstrual phase.
FEMALE 9 1 1006
1
37.5
37.0 W
5c
2a
5+
36536.0
-
35535.0
-
'
34.5
,
I
I
I
I
I
I
I
I
I
1
1120
1140
1160
1180
1200
1220
1240
1260
1280
1300
1320
FEMALE 921216
37.5
w
-
370-
K
3
+
4
cx
w
a
365-
W
I
+
36.0
Depo-Provera
-
I
restraint, may have been elevated from handling. In addition, vaginal temperatures can be affected by estrogen-stimulated local blood flow increases [Abrams &
Bazer, 1973; Abrams et al., 19731. The chimpanzee temperatures, although measured remotely, used transmitters placed intra-muscularly that may have been
affected by muscle-generated heat.
Although White et al. [1973] did not measure PDG or progesterone, they did
find a sustained luteal increase in BBT for the pigtail macaque, Macaca nemestrzna, using subdermal radiotransmitters. Likewise, in chimpanzees [Graham et
al., 19771, BBT and PDG were not correlated, but there was a sustained BBT
increase during the luteal phase.
280 I Asa et al.
In the present study, in three of four cycles, BBT also appeared to rise with the
EC peak and then dip before exhibiting the sustained luteal increase. Periovulatory changes in BBT reported for other species include a decrease a t the time of the
serum estradiol peak in the langur [Lohiya et al., 19881, a decrease and then a n
increase at ovulation in the rhesus [Balin & Wan, 19681, a decrease the day after
the urinary estrone peak in the chimpanzee [Graham et al., 19771, a decrease the
day of the luteinizing hormone peak in the human [Morris et al., 19761, and a spike
the day of estrus for domestic cattle, Bos taurus [Wrenn et al., 1958; Zartman et al.,
19831. Because little if any preovulatory progesterone has been detected in these
species, hyperemia associated with the estrogen spike or a n as-yet-unsuspected
factor may be responsible.
The absence of a n absolute correspondence between the menstrual phases and
changes in BBT shown by female 78217 was possibly due to the influence of female
911006 (Fig. 2). BBT for female 78217 declined slightly at the time of her own
menstrual phase, rose briefly, and then declined again with the menstrual phase
of Female 911006. During subsequent cycles, the menstrual phases of the two
females were synchronized and the BBT curve of female 78217 once again appeared regular. Although there has been no study of tendencies toward menstrual
cycle synchrony in orangutans, one report suggests that introduction of a new
female can affect cycles and perhaps fertility in this species [Zucker et al., 19871.
The ability of Depo-Provera, a synthetic progestin, to stimulate a sustained
BBT elevation confirms the positive association between body temperature and
both endogenous and exogenous progestins. The duration of the effect is surprising,
however. The absence of menstrual cycles during this entire period suggests that
circulating levels of progestin were sufficient to suppress ovarian activity as well
as to maintain elevated BBT.
In conclusion, although based on only two cycles from each of two females, the
correlation between BBT and urinary PDG was highly significant. In addition,
during continued monitoring of multiple cycles in these and a third female, BBT
was elevated during the predicted luteal period, defined by dates of menstrual
blood in urine. Exogenous, synthetic progestin administration also produced sustained BBT elevation.
ACKNOWLEDGMENTS
We thank M. White and R. Rouggly for urine collection, Dr. R. Junge for
surgical installation of transmitters, G. London, S. Taylor, P. Monk, K. Kearns,
and K. VanKoevering for computer data transcription, and I. Porton and Dr. W.J.
Boever for advice. This work was supported in part by a grant from the NixonGriffis Fund for Zoological Research.
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correlation, urinary, temperature, female, body, pygmaeus, glucuronides, pongo, pregnanediol, orangutans, basal
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