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Assessment of circadian rhythms throughout the menstrual cycle of female rhesus monkeys.

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American Journal of Primatology 70:19–25 (2008)
Assessment of Circadian Rhythms Throughout the Menstrual Cycle of Female
Rhesus Monkeys
Section of Neurobiology, Physiology and Behavior, University of California, Davis, California
Reproductive cyclicity has a significant influence on the regulation of circadian rhythms in rodents.
Studies have suggested that there are changes in body temperature rhythms between the follicular and
luteal phases in human females. This study examined the effects of menstrual cyclicity on physiological
and behavioral circadian rhythms in female rhesus monkeys (Macaca mulatta), an acknowledged
biomedical model. Seven unrestrained subjects were implanted with a biotelemetry transmitter to
measure body temperature and heart rate and an accelerometer was used to measure physical activity.
Water was available ad libitum and drinking was measured via an electronic circuit attached to a water
lixit. A video-based task system, the Psychomotor Test System, provided environmental enrichment
and delivered a pelletized diet. Mean, phase, and amplitude of each rhythm were calculated. Estrogen
and progesterone conjugates were assayed and quantified from daily urine samples to identify follicular
and luteal phases of the menstrual cycle. Average circadian variables were then compared between
these phases. Heart rate was significantly (Pr0.05) delayed in the luteal phase. Albeit non-significant,
analysis showed a trend toward decreased circadian amplitude of body temperature in the luteal phase.
Am. J. Primatol. 70:19–25, 2008. c 2007 Wiley-Liss, Inc.
Key words: luteal; follicular; body temperature; heart rate; phase; activity
Living organisms exhibit a circadian (24 hr)
rhythm virtually in all physiological and behavioral
variables. In primates, these endogenous circadian
rhythms are regulated by a pacemaker in the
hypothalamus, the suprachiasmatic nucleus. The
pacemaker and thus circadian rhythms can be
influenced by external factors such as light [Czeisler
& Wright, 1999], gravity [Fuller et al., 1994], and
other non-photic cues [Klerman et al., 1998].
Circadian rhythms in mammals co-exist with
other ultradian (o24 hr) and infradian (424 hr)
rhythms. Prominent infradian rhythms regulate
reproductive cyclicity in females. For example, in
some rat strains that typically have a 4-day estrous
cycle, the reproductive cycle can be lengthened to 5
days by increasing the period of light exposure
[Hoffman, 1968]. The human reproductive cycle or
menstrual cycle with a period of approximately 28
days may influence daily circadian rhythms and may
be an important consideration when studying female
circadian rhythms. Some human studies evaluating
the effect of the menstrual cycle on the circadian
rhythm of body temperature (Tb) have shown mean
Tb increases during the luteal phase of the menstrual
cycle [Cagnacci et al., 1996, 1997, 2002; Driver et al.,
1996; Lee, 1988; Severino et al., 1991], whereas
others have reported that the amplitude of the Tb
r 2007 Wiley-Liss, Inc.
rhythm decreases during the luteal phase in humans
[Cagnacci et al., 1996, 1997, 2002; Lee, 1988;
Nakayama et al., 1997; Severino et al., 1991].
Human circadian research is necessarily limited
by practical constraints. For example, to evaluate the
effects of the menstrual cycle on circadian rhythms,
physiological variables must be recorded over at least
one cycle (28 days) in a highly controlled environment (i.e., controlled for light, social cues, ambient
temperature). Facilities available to perform such
studies in humans for long duration are few.
Consequently, an animal biomedical model may be
a useful tool for understanding changes in circadian
rhythmicity occurring throughout the approximately
28-day period of the menstrual cycle.
Contract grant sponsor: National Aeronautics and Space Administration; Contract grant number: NNJ04HF44G; Contract grant
sponsor: NASA’s Graduate Student Research Program; Contract
grant number: NFT-51417; Contract grant sponsor: Zonta
International Amelia Earhart Fellowship.
Correspondence to: Charles A. Fuller, Section of Neurobiology,
Physiology and Behavior, One Shields Avenue, University of
California, Davis, CA. E-mail:
Received 10 January 2007; revised 6 April 2007; revision
accepted 17 April 2007
DOI 10.1002/ajp.20451
Published online 23 May 2007 in Wiley InterScience (www.
20 / Barger et al.
The rhesus monkey (Macaca mulatta) is a useful
biomedical model because it is a menstrual animal
like the human and has a similar 28-day cycle
[Abbott et al., 2004]. The effect of the menstrual
cycle on circadian rhythmicity in rhesus has not yet
been characterized. This study was performed to
examine the interaction between the menstrual cycle
and the circadian timing system in female rhesus.
Specifically, this study tested the hypothesis that
circadian rhythms will be altered as a function of the
phase of the menstrual cycle.
electrocardiogram (ECG) leads and an antenna were
attached to the transmitter body. Under general
anesthesia, the transmitter was implanted subcutaneously and under a non-active muscle layer on the
left side of the abdomen. The ECG leads and antenna
were routed subcutaneously and secured to the
muscle in the left, right, and center of the chest.
In all cases, animals were allowed at least two
weeks recovery from surgery before data collection
Data Collected
(5.4870.02 years,
6.570.4 kg; mean7SEM) were studied for 36 days
with continuous physiological data recording. All
animal care met the NIH Guidelines for Animal Care
and Use. All procedures complied with protocols
approved by the University of California Davis
Institutional Animal Care and Use Committee and
adhered to the legal requirements of USA.
Housing and Husbandry
This study was performed at the California
National Primate Research Center as part of the
doctoral dissertation research of LKB (awarded
1999). All subjects were individually housed in
standard primate cages. Animals were visually
isolated from each other, except when standard
husbandry tasks (approximately 1 hr per day) were
performed. Husbandry was performed on a non-24 hr
Illumination was provided by a 12-inch, 8-Watt
cool white fluorescent bulb mounted outside of the
animal’s cage (Il 5 90–400 lux depending on the
animal’s position inside of the cage). Lighting
schedule (LD 16:8) was computer controlled. Mean
room temperature during data collection was maintained at approximately 221C.
Animals were fed via the Psychomotor Test
System, a computer-based task system that rewards
successful completion of a video task with a 190-mg
pellet of a nutritionally complete diet (P.J. Noyes,
Lancaster, NH). The Psychomotor Test System also
provided the environmental enrichment mandated
by the Animal Welfare Act. Water was available ad
libitum through a lixit system (AnCare, Bellmore,
Biotelemetry Surgery
Each animal was surgically implanted with a
battery operated biotelemetry unit to allow collection
of body temperature and heart rate (HR) data from
unrestrained subjects (T4E; Koningsberg Instruments, Pasadena). The temperature sensor was
contained within the body of the implant. Two
Am. J. Primatol. DOI 10.1002/ajp
Menstrual cyclicity
To identify menstrual phase, we tracked the
individual menstrual cycles of each animal by daily
observation of the cage for menses. Additionally,
urine was collected daily and a 5 ml of aliquot was
frozen for latter assay for estradiol and progesterone
Body temperature and heart rate
Each implant had a unique FM modulated signal
which the TI20-C Temperature/Biopotential Demodulator (Koningsberg Instruments, Pasadena, CA)
decoded allowing continuous monitoring of Tb. ECG
leads provided continuous ECG recording, which was
converted to HR by an R wave detector. An in-cage
antenna system maximized signal reception and all
data, sampled at 1-sec intervals, were saved to a
computer hard disk. In-house software translated Tb
and HR telemetry files into a form that could be
analyzed for circadian rhythmicity.
Each animal was fitted with a mesh jacket that
included a dorsal pocket to accommodate an activity
(ACT) monitor (Individual Monitoring Systems,
Baltimore, MD). The ACT monitor was an accelerometer that recorded an ACT count as velocity and/
or direction of movement changed. ACT data were
summed in 2-min bins.
Drinking was monitored with an electric contact
circuit on the lixit (Data Sciences, St. Paul, MN).
Drink counts were stored on microcomputer hard
disk and summed in 10-min bins.
Using a procedure developed at the Center for
Health and the Environment at the University of
California, Davis [Shideler et al., 1990], enzyme
immunoassays were used to determine the quantity
of the estradiol and progesterone metabolites in the
urine. Shideler et al. [1990] have shown a significant
correlation between estrone sulfate and estrone
glucuronide (both together referred to as E1C) and
Female Rhesus Rhythms / 21
Physiological data (Tb, HR, ACT, drinking, and
feeding) were edited, to exclude times when animals
were disturbed during daily husbandry. Circadian
analysis was completed using in-house software
(EPL, Davis, CA), which uses a Fourier-based
phase-fitting algorithm. The daily mean, rhythm
amplitude (calculated as the mean to maximum of
the best fit curve), and acrophase (calculated as the
time of the maximum of the best fit curve) were
calculated for each variable. Telemetry data from
seven animals and ACT data from six animals were
aligned by the E1C peak. Means for each circadian
variable were calculated for both the follicular and
luteal phases. Analysis of variance (ANOVA) with
repeated measures was used to compare differences
in circadian variables between menstrual phases and
between days of each phase and Tukey’s test was
used for post hoc analysis. An a of 0.05 was
considered significant. All results are presented as
mean7standard error.
It has been reported that female rhesus are
seasonal with ovulatory cycles restricted to fall and
winter [Walker et al., 1984] and because menstrual
records of our subjects showed that many ceased
menstruating or had abnormally long cycles during
the summer months, this study was conducted
during the winter when all subjects were menstruating regularly. The menstrual cycle was defined from
the first day of menses until the next menses. All
subjects had menstrual cycles of normal length
ranging from 27 to 35 days (30.373.6 days). The
results of the hormone assays were used to first
divide each animal’s data into follicular and luteal
phases. The follicular phase was defined as the first
day of menses up to and including the day of the E1C
peak. Luteal phase was defined as the day following
the E1C peak until the day of the next menses.
The hormone distribution had to meet several
criteria to be considered a legitimate menstrual
cycle. First, the follicular phase was required to
show a rise in E1C. Second, a true luteal phase was
ng E1C / mg Cr
Data Analysis
ng PdG / mg Cr
serum estradiol, and between pregnanediol-3-glucuronide (PdG) and serum progesterone in rhesus
monkeys. Urine samples were diluted 1:20 instead
of the standard 1:50 to compensate for dilute urine
samples obtained from the rhesus. To account for
variation in the concentration of urine, all assay
results were indexed by creatinine (Cr) using
methods described by Taussky [1954]. When Cr
levels were not reliable (i.e., Cr value r0.07 mg/ml),
daily E1C and PdG levels were discarded and zero
was substituted when a negative number indicated
that a sample contained no detectable E1C/PdG.
Fig. 1. Average cycle of estrone sulfate and estrone glucuronide
(E1C) and pregnanediol-3-glucuronide (PdG) of seven animals.
Follicular phase is defined as day 1 of menses up to and including
the E1C peak. All animals cycled regularly throughout this study
with cycle lengths ranging from 27 to 35 days.
characterized primarily by a sustained increase in
PdG and finally, PdG had to fall before the next
reported menses. The day of E1C peak was usually
chosen as the day with the highest E1C values. In
two subjects, there were missing data or no single
distinguishable high point, thus the day with the
highest E1C followed by a sustained rise in PdG was
selected as the day of E1C peak [Giardi et al., 1997].
Average hormone data are shown in Figure 1.
Representative raw data of all physiological variables
are presented in Figure 2.
In this rhesus study, mean Tb was not different
between follicular (36.9870.121C) and luteal
(36.8970.161C) phases. Likewise, minimum Tb was
(37.7370.171C) and luteal (37.7170.201C) phases.
There was a significant (Po0.05) increase in mean
Tb 2 days before the E1C peak (Fig. 3a). There were no
differences in the phase or amplitude of Tb between the
follicular and luteal phases. Mean, acrophase, and
amplitude of all physiological variables for the follicular
and luteal phases are summarized in Table I.
There was no difference in mean HR between the
follicular phase and the luteal phase (Fig. 3b). The
phase of the HR rhythms was significantly (P 5 0.007)
delayed in the luteal phase (14.9370.54 hr) versus the
follicular phase (14.3070.56 hr). There was no difference detected in HR amplitude between the follicular
and luteal phases. The circadian rhythms of ACT (Fig.
3c) and drinking (Fig. 3d) did not change significantly
between phases of the menstrual cycle.
This study characterized the circadian rhythms
of multiple physiological variables through the
menstrual cycle of rhesus monkeys. We observed an
increase in mean Tb before the E1C peak, and some
Am. J. Primatol. DOI 10.1002/ajp
22 / Barger et al.
T o(C)
Tb (oC)
HR (beats/min)
Heart Rate (Beats/Min.)
Drink (Counts/10-min)
Drink (Counts / 10-min.)
Activity (counts/2-min)
Activity (Counts/10-min.)
E1C L+1
Time (days)
Fig. 2. Body temperature (Tb) (a), heart rate (b), activity (c), and
drinking (d), data from a representative rhesus monkey during
the transition from follicular to luteal phases.
Fig. 3. Average of mean body temperature (Tb) (a), heart rate
(HR) (b), activity (c), and drinking (d), for all animals across the
menstrual cycle. There is a significant (Po0.05) increase in Tb
2 days before E1C peak.
changes in rhythm variables that are somewhat
similar to those reported in the human literature.
Tb is one of the most commonly studied markers
of circadian rhythmicity in humans. Some of the
current human literature reports an increase in
mean Tb following ovulation, in the luteal phase of
the menstrual cycle [Cagnacci et al., 1996, 1997;
Driver et al., 1996; Lee, 1988; Severino et al., 1991].
In fact, the increase in basal Tb following ovulation is
used as one of the markers for family planning [De
Leizaola-Cordonnier, 1995]. The increase in serum
estradiol, as reflected in the E1C peak, invokes a
Am. J. Primatol. DOI 10.1002/ajp
Female Rhesus Rhythms / 23
TABLE I. Summary
Menstrual Phase
36.9870.12 36.8970.16
Tb (1C)
HR (beats/min)
121.2974.26 120.6273.91
ACT (counts/2 min)
24.2573.56 24.7773.95
Drink (counts/10 min)
Tb (hr)
HR (hr)
ACT (hr)
Drink (hr)
14.9370.54 0.007
13.8070.49 0.095
Tb (1C)
HR (beats/min)
ACT (counts/2 min)
Drink (counts/10 min)
0.7270.05 0.0581
Tb, body temperature; HR, heart rate; ACT, activity.
indicates significant difference between follicular and luteal phases.
sudden increase in luteinizing hormone, (LH) which
induces ovulation to occur usually 24–36 hr later
[Prior et al., 1990]. Therefore, ovulation should occur
the 1 or 2 days after the E1C peak. Our data
indicated that rhesus also have a periovulatory
increase in mean Tb , albeit earlier in the menstrual
cycle than humans (i.e., 2 days before the E1C peak,
which is 2–3 days before ovulation). Additionally, in
contrast to the human literature [Cagnacci et al.,
1996, 1997, 2002; Driver et al., 1996; Lee, 1988;
Severino et al., 1991] there was no difference in
mean Tb between the follicular and luteal phases. An
increase in progesterone during the luteal phase is
generally thought to be the cause of the increase in
human body temperature [Cagnacci et al., 1997].
Cagnacci et al. [1997] reported that a woman’s body
temperature was related to her progesterone:estradiol ratio. Although the rhesus lack the luteal rise in
E1C seen in human menstrual cycles, there was no
significant relationship found in this rhesus study
between Tb and level of progesterone, or between Tb
and progesterone:E1C ratio.
The differences between this rhesus and previous human studies may be explained by the
different methodologies utilized. For example, studies investigating human circadian rhythms generally measured only one variable (Tb) using rectal
[Baker et al., 2002], vaginal [Cagnacci et al., 1996,
1997, 2002], or tympanic [Wright & Badia, 1999]
probes or thermister pills that were swallowed
[Coyne et al., 2000]. In this study, the thermistor
location was consistent between subjects and
throughout the study period. On the basis of the
pattern of the circadian temperature rhythm, we
believe the temperature data reported in this study
were reflective of deep body rather than skin
temperature. Body temperature was high during
the day and low at night with the rise to daytime
levels beginning before lights on. This is the common
pattern seen in diurnal primates in brain, rectal, and
axillary temperature and it differs from the pattern
of skin temperature [Fuller et al., 1996]. However, it
is possible that the different site of Tb measurement
could potentially account for our different results.
Another methodological difference between this
study and previous ones using human subjects is
that the human studies varied in their definition of
phases of the menstrual cycle and examined a limited
number of days in each defined phase of the
menstrual cycle. Using the rhesus model allowed us
to record data continuously over an entire cycle. To
our knowledge, this is the first study examining
rhesus circadian rhythms across the menstrual cycle.
We divided the cycle into follicular and luteal phases
only and report average data for each of these
phases. However, post hoc analysis of select days in
each phase of the menstrual cycle, similar to the
methodology used in human studies, did not alter
our results. Alternatively, the differences between
rhesus and humans may be explained physiologically. For example, the lack of increase in mean Tb
during the luteal phase in rhesus could be owing to
decreased sensitivity to progesterone in rhesus. This
hypothesis would require further investigation.
The acrophase of HR was significantly delayed
in the luteal phase as compared with the follicular
phase. Minor, non-significant delays were observed
in the other rhythms monitored. Some human
studies have also reported a delay in Tb acrophase
during the luteal phase [Cagnacci et al., 1996, 1997;
Coyne et al., 2000; Nakayama et al., 1997], however,
some have reported no difference in acrophase
between menstrual phases [Lee, 1988]. The human
data are more difficult to interpret because ambient
lighting, which was not controlled in some of these
studies, influences circadian acrophase [Czeisler
et al., 1986]. Wright and Badia [1999], using a
‘‘constant routine’’ that carefully controls for external influences such as light and ambulation,
reported no difference in Tb acrophase between the
follicular and luteal phases.
In our study, the amplitude of the Tb rhythm
showed a decreasing trend in the luteal phase, but
the decrease was not statistically significant. Tb
amplitude in human subjects has shown significant
decreases in the luteal phase [Cagnacci et al., 1996,
1997; Coyne et al., 2000; Lee, 1988; Nakayama et al.,
1997]. Interestingly, Nakayama et al. [1997] reported
a decreased amplitude during the follicular phase in
patients with premenstrual syndrome. If a rhesus
counterpart to premenstrual syndrome exists, this
phenomenon could be explored in future rhesus
Am. J. Primatol. DOI 10.1002/ajp
24 / Barger et al.
In this study, we recorded ACT using an
accelerometer mounted in a pocket located in the
back of a jacket worn by each subject. Using this
methodology, rhesus showed no difference in the
amount of ACT between menstrual phases. These
results mirror those of a human study that used wrist
actigraphy as a measure of ACT [Severino et al.,
1991]. A different approach was used in the study by
Wright and Badia [1999]. Rather than quantifying
ACT, these authors controlled ACT by having their
subjects follow a constant routine. ACT levels of our
subjects were, presumably, lower than would have
been seen in free-ranging rhesus.
There are several limitations that must be
addressed. This study analyzed multiple circadian
variables of seven subjects over one menstrual cycle
and found minimal differences in physiological
variables between the follicular and luteal phases of
the menstrual cycle. First, although sufficiently
powered to detect a difference in the mean Tb, we
were underpowered to detect differences in phase
and amplitude of the body temperature rhythm.
Therefore, the lack of consistent changes in mean,
amplitude, and phase among the various physiological rhythms may be reflective of inadequate power
rather than dissociation among rhythms. Second,
this study did not measure basal rhythms, but
rhythms were investigated with normal ACT under
controlled environmental conditions; thus, we cannot exclude the possibility that environmental/ACT
masking affected some of our variables.
These results are somewhat consistent with
human studies reported in the literature. Most
notably, there was a periovulatory rise in Tb although
there was no difference in Tb between the follicular
and luteal phases of the menstrual cycle in the rhesus.
Rhesus data showed a trend toward a delayed
acrophase, similar to some human studies that
reported a delayed acrophase of Tb in the luteal phase.
Finally, there was a trend, albeit non-significant,
toward decreased amplitude in the circadian rhythm
of Tb in rhesus, similar to most human studies where
the decreased amplitude of Tb is significant.
The differences noted between the human
literature and the data we collected in the rhesus
monkey do not indicate weaknesses of the rhesus as a
biomedical model. On the contrary, the use of rhesus
monkeys in research eliminates environmental and
social influences inherent in human investigations.
Indeed, rhesus monkeys have been successfully
utilized as biomedical model in reproductive research
including protocols investigating infertility [Abbott
et al., 2004, ILAR journal] and menopause [Roberts
et al., 1997].
The authors would like to thank Peter Takeuchi
and the staff at the California National Primate
Am. J. Primatol. DOI 10.1002/ajp
Research Center (CNPRC) for their invaluable
assistance during this study. All animal care met
the NIH Guidelines for Animal Care and Use and
complied with applicable US laws. We would also like
to thank Dr. Bill Lasley for his guidance and Heather
Todd for her assistance with the laboratory analyses.
This study was supported by NASA grant
NNJ04HF44G to CAF and NIH NCRR grant
P51RR000169 to CNPRC. Dr. Barger was supported
by NASA’s Graduate Student Research Program
(NFT-51417) and a Zonta International Amelia
Earhart Fellowship.
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