The Journal of Clinical Endocrinology & Metabolism Vol. 84, No. 2 623-626
Copyright © 1999 by The Endocrine Society
Stress and the Menstrual Cycle: Short- and Long-Term Response to a Five-Day Endotoxin Challenge during the Luteal Phase in the Rhesus Monkey1
Ennian Xiao,
Linna Xia-Zhang and
Michel Ferin
Department of Obstetrics and Gynecology and The Center For
Reproductive Sciences, College of Physicians and Surgeons, Columbia
University, New York, New York 10032
Address all correspondence and requests for reprints to: Dr. Michel Ferin, Department of Obstetrics and Gynecology, College of Physicians and Surgeons, Columbia University, 630 West 168 street, New York, New York 10032. E-mail: mf8{at}columbia.edu
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Abstract
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Previously, we reported that in the rhesus monkey a 5-day
inflammatory-like stress during the early-mid follicular phase acutely
stimulates the hypothalamic-pituitary-adrenal axis and exerts effects
on the hypothalamic-pituitary-gonadal axis, delays folliculogenesis and
in some animals decreases luteal function in the post-treatment cycle.
Because the endocrine environment at the time of the stress may
influence the response to the stress, we now investigate the acute and
long-term responses to a similar stress challenge during the luteal
phase of the menstrual cycle, at a time of progesterone dominance. Nine
monkeys with normal cycles were injected with endotoxin
(lipopolysaccharide; LPS, 150 µg iv) twice a day for 5 days starting
on days 4–8 after the LH peak. Blood samples were taken at hour 3 and
hour 8 after each morning LPS injection to monitor the acute
gonadotropin and cortisol responses. To verify cyclicity, menses were
checked every day, and daily blood samples were taken for estradiol and
progesterone measurement. Two control cycles, the LPS treatment cycle,
and two post-treatment cycles were documented. Endotoxin activated the
adrenal axis: mean (±SE) cortisol secretion was
significantly increased at hour 3 after the first morning LPS injection
(74.1 ± 4.9 vs. 24.1 ± 1.8 µg/dL in the
control; P < 0.05) and remained elevated at
hour 8. This response decreased progressively with time: on day 5 of
LPS treatment, the cortisol level was still significantly higher than
control at hour 3 (38.5 ± 5.0 µg/dL; P <
0.05) but had returned to the control concentration by hour 8 (days
3–5 of LPS). Mean integrated progesterone through the luteal phase of
the LPS treatment cycle was significantly decreased (33.5 ± 3.3
ng/ml vs. 48.9 ± 3.7 and 54.0 ± 4.9 in the
two control cycles; P < 0.05), but luteal phase
length remained unchanged. When compared with control levels on the
same day of the luteal phase, about one third of LH and FSH values were
lower than one SD below mean control levels. LPS
administration had no effect on the two post-treatment cycles, except
that integrated luteal progesterone in 3 out of 9 monkeys was still
reduced in post-treatment cycle 1. There were no differences in
follicular phase length and preovulatory estradiol peaks between
control cycles and post-treatment cycles. When compared with our
previous study, the results illustrate specific responses to stress at
different phases of the menstrual cycle and support the notion that a
moderate short-term inflammatory-like stress episode has the potential
to subtly alter critical aspects of cyclicity.
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Introduction
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A LINK BETWEEN stress and reproductive
dysfunction is well accepted (1, 2, 3, 4, 5, 6). However, there are few data in the
literature that directly connect a specific stress with a disturbance
of the menstrual cycle. Previously, we reported that, in a nonhuman
primate, a 5-day inflammatory-like stress episode during the follicular
phase of the menstrual cycle which acutely activates the
hypothalamic-pituitary-adrenal (HPA) axis also influences the
hypothalamic-pituitary-gonadal (HPG) endocrine axis and interferes with
cyclicity (7). Treatment and post-treatment menstrual cycles were
characterized by a prolonged follicular phase and instances of
decreased luteal function. Ovarian steroids, specifically estradiol,
have been reported to modulate the endocrine response to stress
(8, 9, 10, 11, 12). In this study, we have administered endotoxin during the
luteal phase of the cycle at a time of enhanced progesterone secretion
and have hypothesized that this different endocrine environment will
modify the HPG response to this acute adrenal axis activation.
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Materials and Methods
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Nine adult female rhesus monkeys (5.5–7.5 kg) were used in this
study. Animals were housed in individual cages, fed, and handled as
described previously (7). The protocols were in accordance with the NIH
guide for the care and use of laboratory animals and approved by the
Institutional Animal Care and Use Committee of Columbia University.
After two normal cycles, lipopolysaccharide (LPS) (WE.coli
055:B5, Difco Laboratories, Detroit, MI) (150 µg in 0.5 ml normal
saline) was given iv at 0900 h and 1700 h for 5 days during
the luteal phase, starting on day 4–8 after the LH peak. To monitor
the gonadotropin and adrenal responses to the LPS injections, blood
samples were taken at hour 3 and hour 8 after each morning LPS
injection. To verify cyclicity, menstruation was checked daily by
vaginal swabbing and daily blood samples for hormone measurements were
obtained by venipuncture. Two control cycles, the treatment cycle, and
the two post-treatment cycles were documented. To compare cycle
quality, the following parameters were used: the length of the
follicular and luteal phase, the follicular phase estradiol peak, and
the integrated progesterone levels during the luteal phase, as
calculated by trapezoidal analysis.
Blood samples were centrifuged and sera were kept frozen until assay.
FSH and LH were measured with recombinant homologous RIAs described
previously (8). Assay sensitivity (95% binding) was 0.06 ng/ml for LH
and 0.045 ng/ml for FSH. Intraassay and interassay coefficients of
variation (CV) were 5.0 and 6.1% for FSH and 7.0 and 13.1% for LH,
respectively. Estradiol and progesterone concentrations were measured
by chemiluminescent immunoassay using the Immulite system
(Diagnostic Products Corp., Inc., Los Angeles, CA).
Interassay CVs were 11.9% and 11.1% for estradiol and progesterone,
respectively. Cortisol was measured using a solid-phase
125I RIA (Coat-A-Count, Diagnostic Products Corp., Inc., Los Angeles, CA). Intraassay and interassay CVs were 2.9%
and 6.1%, respectively.
The data were analyzed statistically by multiple ANOVA, followed by the
Tukey test. The significance level was established at P
< 0.05.
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Results
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Acute effects of LPS treatment
Endotoxin treatment resulted in the activation of the HPA axis.
Cortisol secretion was increased after each morning LPS injection. On
day 5 of LPS treatment, mean (±SE) cortisol concentration
at 1200 h (hour 3 after LPS) was 38.5 ± 5.0 µg/dL
vs. 24.1 ± 1.8 µg/dL in the control luteal phase
(P < 0.05). This increase on day 5 was significantly
lower than that at 1200 h on the first day of LPS injection
(74.1 ± 4.9, P < 0.05). Cortisol was still
significantly increased at hour 8 after LPS injection on days 1 and 2,
but not 3–5, of treatment. A similar cortisol response profile was
observed in all animals. Symptoms related to endotoxin injection
resembled a mild flu-like illness and included nausea, decreased food
intake, and general sluggishness. In the majority of animals, these
symptoms were limited to the first day of treatment.
Mean (± SE) integrated progesterone concentration during
the luteal phase of the treatment cycle was significantly decreased by
LPS injection (33.5 ng/ml ±3.3 vs. 48.9 ± 3.7 and
54.0 ± 4.9 for control cycles 1 and 2, respectively;
P < 0.05) (Fig. 1
).
Compared with control LH levels on the same day of the luteal phase, 58
out of 90 LH values during the 5-day LPS treatment were below the
control mean while 28 values were lower than 1 SD from the
mean. For FSH, 69 out of 90 values were below control mean levels while
31 values were lower than 1SD from the mean (Fig. 2).
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Figure 1. Integrated progesterone concentrations
throughout the luteal phase during the two control cycles, the LPS
treatment cycle and the two post-LPS treatment cycles. During the
luteal phase of the treatment cycle, monkeys (n = 9) received a
5-day endotoxin (LPS) treatment. Note the significantly lower
integrated luteal progesterone in the treatment cycle, compared with
the two control cycles and the post-treatment cycle 2 (*,
P < 0.05).
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Figure 2. LH (upper panel) and FSH
(lower panel) concentrations during the 5-day LPS
treatment in the luteal phase. Each black dot represents
daily individual values measured at hour 3 and hour 8 after the first
of two daily LPS injections. The shaded areas represent
mean ±1 SD in control cycles during the luteal phase. Day
0 is the day of the preovulatory gonadotropin surge. Note that the
majority of gonadotropin values during LPS treatment are below the mean
control levels.
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Effects of LPS treatment on cyclicity
The length of the follicular and luteal phase remained unchanged
in the treatment as well as in the two post-treatment cycles as
compared with the two control cycles (Table 1). The integrated luteal progesterone
secretion in post-treatment cycle 1 was still lower in 3 out of 9
monkeys (49.8 ± 10.2% of their own control); however, as a
group, the mean luteal progesterone levels in the 2 post-treatment
cycles were not significantly different from the control cycles
(post-treatment cycle 1: 39.2 ± 6.4; post-treatment cycle 2:
48.8 ± 4.2 ng/ml) (Fig. 1
). There were no differences in the
preovulatory estradiol peak between control and post-treatment cycles
(control cycle 1: 219.1 ± 35.7; control cycle 2: 230.7 ±
22.0; post-treatment cycle 1: 242.4 ± 31.1; cycle 2: 229.4
± 38.9 pg/ml).
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Table 1. Effects of a 5-day LPS iv treatment during the
luteal phase on the length (mean days ± SE) of the
menstrual cycle in rhesus monkeys (n = 9)
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Daily estradiol and progesterone levels over a five-cycle period in two
individual monkeys are illustrated in Fig. 3. In monkey RUZ1 (upper
panel), integrated progesterone during the luteal phase of control
cycles1 and 2 were 46.2 and 49.5 ng/ml. LPS treatment decreased
progesterone secretion to 22.7 while in the two post-treatment cycles
progesterone secretion was still lower than in control cycles (27.8 and
39.7). In monkey 53–124 (lower panel), progesterone
secretion was 42.3, 45.0, 23.2, 41.8, and 47.8, respectively.
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Figure 3. Daily estradiol (lines) and
progesterone (shaded areas) concentrations throughout
two control cycles, the treatment cycle during which LPS
(arrow) was given for a 5-day period in the luteal
phase, and the two post-LPS cycles in two monkeys. The time scale is
identical for both animals. There was a decreased integrated
progesterone during the luteal phase of the treatment cycle in both
monkeys and in post-treatment cycle 1 in monkey no. RUZ1. Integrated
progesterone values in the individual luteal phases are noted in the
text.
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Discussion
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The results from this study in rhesus monkeys with normal
ovulatory cycles demonstrate that an acute stimulation of the HPA axis,
as induced by a 5-day inflammatory stress episode, during the luteal
phase is accompanied by a decrease in luteal progesterone secretion
without alteration in the length of the luteal phase. The
post-treatment recovery cycles were normal in regard to cycle length,
the preovulatory estradiol peak and integrated luteal progesterone
levels in most, but not all, monkeys.
As expected, endotoxin injection elevates cortisol release, the result
of an activation of the HPA axis. Although data in the literature
suggest that ovarian steroids may modulate the HPA response to stress
(13, 14, 15, 16, 17), the overall cortisol response pattern in this study in the
luteal phase did not differ from that observed in the follicular phase
(7). In both studies, there was a robust response of cortisol after the
first LPS injection, but a progressive decrease in that response with
time in all monkeys. This observation probably reflects adaptation to a
prolonged stress challenge, a phenomenon described in the rodent (18).
Whatever specific mechanism is responsible for this process in our
animals remains to be investigated. The mild flu-like symptoms induced
by endotoxin, likewise, were most prominent on day 1 and disappeared in
the majority of monkeys thereafter.
The exact mechanism(s) whereby endotoxin administration decreases
luteal progesterone secretion remain to be determined. One hypothesis
is that endotoxin may directly interfere with progesterone production
and secretion by the corpus luteum. There are several reports that
suggest that endotoxin may alter gonadal steroidogenesis by a direct
gonadal effect (19). Such an effect may be mediated by various
mechanisms including the activation of local macrophages and the local
release of cytokines such as interleukins and TGF
(19, 20, 21, 22, 23) or of
nitric oxide (24, 25). Alternatively, the decrease in luteal
progesterone during the treatment cycle may be the result of the
inhibition of gonadotropin secretion by LPS administration during that
luteal phase. Indeed, LH is known to be the main endocrine signal in
support of luteal progesterone synthesis and secretion (26, 27). Our
results show that, during the 5-day LPS treatment period, about 2/3 of
LH values were below the mean control level at a similar stage of the
luteal phase while 1/3 were lower than 1 SD from the
control mean. These data indicate that endotoxin injection may have
resulted in a decrease in LH secretion, a probable mechanism for the
decrease in progesterone. Unfortunately, we could not demonstrate a
statistical difference in LH levels between control and treatment
periods with our twice a day sampling. Such a demonstration will
require a more frequent blood sampling schedule to take into account
the characteristic pulsatile LH pattern during the luteal phase.
The gonadotropin response during the endotoxin treatment period in the
luteal phase differs markedly from previously reported data obtained
after this stress challenge was given during the early-mid follicular
phase (7), even though the same LPS injection regimen was used. After
LPS injection in the follicular phase, both LH and FSH secretion
increased (7). Such a positive gonadotropin response had also been
observed acutely after central interleukin-1 administration in the
follicular phase (9) or in the ovariectomized monkey replaced with
follicular levels of estradiol (8). In contrast, the gonadotropins did
not increase after LPS administration in the luteal phase and the
majority of LH and FSH values were below control levels. This result is
similar to the inhibition of LH and FSH secretion observed in the
ovariectomized animal after central interleukin (28, 29) or peripheral
LPS injection (1, 30). The mechanisms responsible for these
differential effects of endotoxin on gonadotropin secretion under these
different endocrine conditions are presently under study.
Effects of endotoxin administration in the luteal phase were in most
animals confined to decreased luteal progesterone secretion in the
treatment cycle in the absence of luteolysis. However, three of the
nine animals also showed a relative secretory insufficiency during the
luteal phase of the first post-treatment cycle. The overall cortisol
response profile in these animals, however, was similar to that of the
other monkeys. In contrast, when endotoxin was given during the
early-mid follicular phase, its effects appear to be more extensive: a
permanent damage to folliculogenesis was observed in half of the cycles
and long-term effects on luteal secretory capability were observed in
all animals (7).
In summary, these data, together with results from a companion paper
(7), illustrate specific differences in the response to stress at two
phases of the menstrual cycle. They also support the notion that a
moderate short-term stress episode has the potential to subtly alter
critical aspects of cyclicity. Importantly, they also suggest that,
even though a stress episode is not sufficient to induce amenorrhea, it
may impact on fecundity potential during the cycle in which it occurs
and perhaps also in the ensuing cycles depending on its timing. The
stress used in these two studies was an inflammatory challenge which
produced a mild flu-like syndrome and activated the HPA axis. Whether
other types of stress stimuli would induce similar effects on the
menstrual cycle following HPA activation remains to be
investigated.
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Acknowledgments
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The authors thank Jun Zhu and Alinda Barth for performing the
hormone assays and Dr. A. F. Parlow (Harbor-University of
California-Los Angeles Medical Center, Torrance, CA) for providing the
reagents required for the monkey LH and FSH radioimmunoassays.
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Footnotes
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1 This work was supported in part by NIH Grant DK-39144. 
Received September 8, 1998.
Revised October 27, 1998.
Accepted November 2, 1998.
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Top
Abstract
Introduction
