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Higher Sweating Rate and Skin Blood Flow during the Luteal Phase of the Menstrual Cycle

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Evaporation by sweating is the most effective way to remove heat from the body. Sweat rates increase under both local and whole-body heat stress. Men and women differ in how they respond to heat, because sexual steroids alter resting body core temperature and the threshold for sweating and skin blood flow (SBF) during heating. The purpose of the present study was to compare local sweat rates and cutaneous vasodilatation during heat exposure in women with a regular menstrual cycle. The cutaneous vasodilatation was judged by measuring the SBF. Eight female and nine male subjects participated in this study, and their age range was 24-29 years. Female subjects were tested twice throughout one full menstrual cycle: once during the middle follicular phases and once during the luteal phase. Subjects remained in a temperature-regulated room at 41°C and 21% of relative humidity for 40 minutes. Sweat rate was recorded from the forehead, forearm, and thigh, and skin temperature and SBF were measured on the thigh and forehead. We found that the sweating rate and SBF were greater in the luteal phase compared to follicular phase (p < 0.05). Since both SBF and sweating were controlled by the sympathetic nerve system, the sympathetic outflow was greater during whole body heat exposure in the luteal phase. In contrast, for men, there was no significant difference in sweating and SBF over the same calendar period (p > 0.05). We propose the enhanced sympathetic activity in the luteal phase with a regular menstrual cycle.
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Sweating and Skin Blood Flow in Women 117Tohoku J. Exp. Med., 2014, 234, 117-122
117
Received July 30, 2014; revised and accepted September 3, 2014. Published online September 17, 2014; doi: 10.1620/tjem.234.117.
Correspondence: JongEun Yim, Department of Physical Therapy, Sahmyook University, Hwarangro 815, Nowon-gu, Seoul 139-742,
Republic of Korea.
e-mail: jeyim@syu.ac.kr
Higher Sweating Rate and Skin Blood Flow during the Luteal
Phase of the Menstrual Cycle
Haneul Lee,1 Jerrold Petrofsky,1 Nirali Shah,1 Abdulaziz Awali,1 Karan Shah,1
Mohammed Alotaibi1 and JongEun Yim2
1Department of Physical Therapy, Loma Linda University, Loma Linda, CA, USA
2Department of Physical Therapy, Sahmyook University, Seoul, Korea
Evaporation by sweating is the most effective way to remove heat from the body. Sweat rates increase
under both local and whole-body heat stress. Men and women differ in how they respond to heat, because
sexual steroids alter resting body core temperature and the threshold for sweating and skin blood flow
(SBF) during heating. The purpose of the present study was to compare local sweat rates and cutaneous
vasodilatation during heat exposure in women with a regular menstrual cycle. The cutaneous
vasodilatation was judged by measuring the SBF. Eight female and nine male subjects participated in this
study, and their age range was 24-29 years. Female subjects were tested twice throughout one full
menstrual cycle: once during the middle follicular phases and once during the luteal phase. Subjects
remained in a temperature-regulated room at 41°C and 21% of relative humidity for 40 minutes. Sweat rate
was recorded from the forehead, forearm, and thigh, and skin temperature and SBF were measured on the
thigh and forehead. We found that the sweating rate and SBF were greater in the luteal phase compared
to follicular phase (p < 0.05). Since both SBF and sweating were controlled by the sympathetic nerve
system, the sympathetic outflow was greater during whole body heat exposure in the luteal phase. In
contrast, for men, there was no signicant difference in sweating and SBF over the same calendar period
(p > 0.05). We propose the enhanced sympathetic activity in the luteal phase with a regular menstrual
cycle.
Keywords: cutaneous vasodilatation; estrogen; menstrual cycle; progesterone; sweat rate
Tohoku J. Exp. Med., 2014 October, 234 (2), 117-122. © 2014 Tohoku University Medical Press
Introduction
Evaporation by sweating is the most effective way to
remove heat from the body (Petrofsky et al. 2005). Sweat
rates increase under both local and whole-body heat stress.
This is reex in nature to maintain body core temperature
(Shibasaki et al. 2006; Wingo et al. 2010). But, women’s
heat response from whole-body heat stress or during exer-
cise is different than that of men (Avellini et al. 1980;
Gagnon and Kenny 2012). It is well documented that body
core temperature uctuates during the menstrual cycle in
women due to female reproductive hormones, especially,
progesterone. Progesterone concentration peaks during the
luteal phase whereas it decreases during the follicular phase
(Petrofsky et al. 1976, 2005; Simao et al. 2012). The con-
centration of progesterone is correlated with elevated core
temperature and also the threshold for sweating and skin
blood ow (SBF) during exercise (Stephenson and Kolka
1985; Charkoudian and Johnson 2000; Inoue et al. 2005).
Inoue and colleagues have shown that mean body tempera-
ture and SBF are greater during the luteal phase where pro-
gesterone is higher compared to the follicular phase (Inoue
et al. 2005; Kuwahara et al. 2005). Oral contraceptive pills
(OCP) are active in suppressing pituitary production of fol-
licle-stimulating hormone and luteinizing hormone and pre-
venting ovulation from occurring (Kenny et al. 2008).
Combined estrogen and progesterone as synthetic steroids
are the main components of OCP and this exogenous source
of synthetic forms of the hormones, prevents ovulation by
maintaining consistent hormone levels (Krishnan and Kiley
2010). The effect of progesterone and estrogen on body
core temperature is well established. It is interesting that
many for the changes in muscular blood ow and endur-
ance are not seen in women on oral contraceptives, showing
the impact of the hormones in non OCP users (Petrofsky et
al. 1976). Therefore, the effect of menstrual cycle on sweat
rate and cutaneous vasodilatation is probably a complex
interaction between progesterone and estrogen. Thus, in
the present study, we compared local sweat rate and cutane-
ous blood flow from whole-body heat stress between
H. Lee et al.
118
women with a regular menstrual cycle and men.
Methods
Subjects
Eighteen young healthy adults between the ages of 24 and 29
years old participated in this study. Subjects were divided into two
groups: female subjects with a regular menstrual cycle and male
group. All subjects were physically inactive with a body mass index
(BMI) between 15 and 30. Subjects had no history of pregnancy, car-
diovascular disease, hepatic disease, diabetes, and were not taking
any medication would affect sex hormones. All methods and proce-
dures were approved by the Institutional Review Board of Loma
Linda University, and all subjects signed a statement of informed
consent before participating the study.
Procedures
Female subjects were tested twice throughout one full menstrual
cycle; once during the middle follicular phases (6 to 9 days after the
onset of menstruation) and once during the luteal phase (21 to 24
days after the onset of menstruation). Since these phases do not occur
in the male group, testing occurred at match days. Female subjects
were asked to report the days of their cycle at the beginning of the
study. Since body core temperature uctuates during the day, the var-
ious tests performed at the same time period each day (between 9 am
to 11 am).
On the rst day, before beginning the experiment, height,
weight, BMI, skin thickness, and fat thickness were measured. On
each day, after the subjects arrived at laboratory, they rested comfort-
ably in a regulated temperature room at 25°C for 20 minutes to stabi-
lize their body temperature in a neutral environment. Each subject
wore short sleeve T-shirts and shorts during the tests. Subjects
remained in a temperature regulated room at 41°C and 21% of rela-
tive humidity (RH) for 40 minutes. Sweat rate at 3 different areas
(forehead, forearm, and thigh), skin temperature, and SBF were mea-
sured throughout the test. Subjects were allowed to drink water dur-
ing heat stress.
Measurements
Local sweat rate: Three different local sweat rates were mea-
sured with a Q-Sweat measuring system (WR Medical Electronics,
Stillwater, MN). The system provided a constant source of air pres-
sure being applied through sweat capsules mounted on the skin. The
constant source of air to each capsule was rst dried in Dri-rite and
by applying air at a constant ow rate; outgoing air from the capsules
could be assessed for humidity. By knowing the temperature of the
air, the ow rate and humidity in the capsule, sweat rate were calcu-
lated. Three sweat capsules were used, on the forehead, calf, and on
the forearm.
Skin temperature: Skin temperature was measured with a therm-
istor (SKT RX 202A) manufactured by Bio Pac systems (Bio Pac
Inc., Goleta, CA). The SKT 100 thermistor amplier (Bio Pac Inc.,
Goleta, CA) sensed the thermistor output. The output, which was a
voltage between 0 and 10 volts, was sampled with an analog-to-digi-
tal converter at a frequency of a 1,000 samples per second with a res-
olution of 24 bits using a Bio Pac MP150 analog-to-digital converter.
The converted data was then stored on a desktop computer using
Acknowledge 4.1 software for later analysis. Data were analyzed
over a 5-second period for mean temperature. The temperature was
calibrated at the beginning of each day by placing the thermistors in a
controlled temperature water bath calibrated against a standard ther-
mometer.
Skin blood ow (SBF): The SBF was measured with a Moor
Laser Doppler ow meter (VMS LDF20, Oxford, England). The sys-
tem uses a red laser beam (632.8 nm) to measure SBF using the
Doppler Effect. After warming the laser for 15 to 30 minutes prior to
use, the laser was applied to the skin through a VP12B ber optic
probe placed above the forearm. The Moor Laser Doppler ow unit
measured SBF through most of the dermal layer of the skin. The SBF
was then calculated in a unit called Flux, based on the red cell con-
centration and red cell velocity with a stated accuracy of ± 10%.
Statistical analysis
Data were summarized as means and standard deviations.
Baseline characteristics and sweat rates of two groups was compared
using an independent t-test. Skin temperature and SBF were com-
pared by a mixed factorial analysis of variance (ANOVA) with
repeated measures. The level of signicance was set at α = 0.05.
Results
Nine subjects were enrolled in each group. However,
one subject from the female group was excluded because
the subject started taking OCP during the study. The sub-
ject’s menstrual phase was determined by their self-report-
ing. General characteristics of 17 subjects are shown in
Table 1.
Skin temperature
The skin temperature measured over the 40-minute
period is shown in Fig. 1 in the female subjects in the fol-
licular and luteal phases of the menstrual cycle. As shown
in Fig. 1, the skin temperature was higher by about 2.5°C in
the luteal than the follicular phase ( p < 0.01). For the
males, the skin temperature remained at 32.1°C throughout
the exposure to heat.
Sweat rates
The sweat rates in the women during the two phases of
the menstrual cycle are illustrated in Figs. 2, 3 and 4 for the
Table 1. General characteristics of 8 female and 9 male subjects.
Age (years) Height (cm) Weight (kg) BMI
women Mean 25.00 161.47 56.81 21.78
s.d. 1.85 6.34 7.99 2.73
men Mean 26.90 176.63 82.69 26.52
s.d. 2.08 5.80 10.92 3.34
Sweating and Skin Blood Flow in Women 119
Fig. 1. Thigh skin temperature in the women in the two phases of the menstrual cycle. Each point is the mean of 8 female
subjects.
Fig. 2. Forearm sweat rate in the women in the two phases of the menstrual cycle. Each point is the mean of 8 female sub-
jects ± the standard deviation.
*Signicant increases from baseline.
#Signicant difference between luteal and follicular phase.
Fig. 3. Forehead sweat rate in the women in the two phases of the menstrual cycle. Each point is the mean of 8 female sub-
jects ± the standard deviation.
*Signicant increases from baseline.
#Signicant difference between luteal and follicular phase.
H. Lee et al.
120
forearm, forehead and thigh respectively. As shown in
these gures, the sweat rate rose steadily throughout the
exposure period. This increase on each area in sweat was
signicant ( p < 0.01) comparing the initial sweat rate to the
sweat rate after 40 minutes of heat exposure. In all 3 cases,
the sweat rate in the luteal phase was signicantly greater
than the follicular phase ( p < 0.05).
Skin Blood Flow (SBF)
The blood ow in the skin for the forehead and thigh
is illustrated in Figs. 5 and 6 respectively for the 8 women.
As illustrated here, the blood ow increased for both phases
of the menstrual cycle at both sites. The increase in SBF
was signicant over the 40 minutes for both phases of the
menstrual cycle ( p < 0.01). While resting SBF at either site
was not statistically different (p > 0.05), by 15 minutes of
exposure the SBF was signicantly higher in the women
during the luteal phase of the menstrual cycle ( p < 0.05).
Male subjects
For the male subjects, the sweat and SBF data was sig-
nicantly higher than that which was found for the women
in either phase of their menstrual cycles. A typical example
is shown in Fig. 7. The forehead sweat data is shown in
this gure. The sweat rate at each area in the men was sig-
nicantly greater than that seen in the women ( p < 0.01).
While there was a signicant increase in SBF and sweat
over exposure, there were no signicant differences in these
measures between the two measurements ( p > 0.05). The
SBF followed a similar response with SBF higher in the
men than the women throughout the heat exposure.
Fig. 4. Thigh sweat rate in the women in the two phases of the menstrual cycle. Each point is the mean of 8 female subjects
± the standard deviation.
*Signicant increases from baseline.
#Signicant difference between luteal and follicular phase.
Fig. 5. Forehead skin blood ow in the women in the two phases of the menstrual cycle. Each point is the mean of 8 female
subjects ± the standard deviation.
*Signicant increases from baseline.
#Signicant difference between luteal and follicular phase.
Sweating and Skin Blood Flow in Women 121
Discussion
Estrogen and progesterone in women have well docu-
mented effects on the body. One of the most apparent
effects is on body temperature and the thermoregulatory
system (Charkoudian and Johnson 2000; Charkoudian
2001, 2003). Beta estrogen receptors are found throughout
the body including the central nervous system (Paterni et al.
2014). These receptors control a variety of functions
including tissue synthesis, tissue blood ow and body tem-
perature (Petrofsky et al. 1976). In this respect, estrogen
and progesterone have an antagonistic role where the
effects of estrogen on beta receptors are opposed by proges-
terone (Silva et al. 2000; Stachenfeld et al. 2000).
In the present investigation, data supported the concept
that there are not just changes in body temperature during
the second half of the menstrual cycle, but changes in vaso-
motor and sudomotor activity as well. Skin temperature
was higher, sweating greater and skin circulation greater in
the luteal phase of the menstrual cycle. The fact that men
who were measured at the same time did not have a change
sweat rates or blood ow when comparing the two measur-
ing points separated by 2 weeks supports the concept that
this is not environmental but physiological. Interestingly,
the sweat rates and cutaneous vasodilation was greater in
men than women. But women have a smaller mass and
greater surface are to sweat from and therefore, potentially,
sweat rates and SBF per meter skin surface area may not be
very different.
It has been reported that sweat rates and cutaneous
vasodilatation increases in the luteal phase of the menstrual
cycle (Kolka and Stephenson 1997; Dzeletovic et al. 2012),
but such a fact seems counterintuitive. During the luteal
phase when progesterone is high, the body’s thermostat is
reset to a higher temperature (Stephenson and Kolka 1999).
This is accomplished by reducing skin vasodilation so that
Fig. 6. Thigh skin blood ow in the women in the two phases of the menstrual cycle. Each point is the mean of 8 female
subjects ± the standard deviation.
*Signicant increases from baseline.
#Signicant difference between luteal and follicular phase.
Fig. 7. Forehead sweat rate in the men in the two different measurements. Each point is the mean of 9 male subjects ± the
standard deviation.
*Signicant increases from baseline.
H. Lee et al.
122
metabolism warms the body. But by the same mechanism,
the higher body temperature seems to make the body more
sensitive to heat stress and increases autonomic activity to
the thermoregulatory system. Recent studies do not show
an increase in sympathetic activity during the luteal phase
of the menstrual cycle (Tenan et al. 2014). In fact, analysis
of heart rate variability shows that heart rate increases dur-
ing the luteal phase compared to the follicular phase due to
a withdrawal of parasympathetic tone (Tenan et al. 2014).
No such change was seen in sympathetic tone. Thus the
general increase in SBF and sweat rates in the heat must be
centered in hypothalamic control and not due to a general
increase in sympathetic activity; the parasympathetic sys-
tem exerts no inuence on sweat glands and SBF. While
many studies have examined either SBF or sweating during
the menstrual cycle, there is some controversy on the nd-
ings. Some report little to no change in SBF and others do
with the menstrual cycle (Stephenson and Kolka 1999;
Stachenfeld et al. 2000; Dzeletovic et al. 2012). But SBF
was measured in the whole limb or on the skin. Sometimes
it was measured together with sweat rates during local heat
and sometimes exercise (Freedman and Subramanian 2005;
Garcia et al. 2006; Janse et al. 2012). Here, unlike most
studies, the subjects were kept in a temperature-controlled
room at the same time of the day and same phase of the
menstrual cycle. In this respect this study removes some of
the variables that have plagued previous studies. Further
investigation is warranted.
Conict of Interest
The authors declare no conict of interest.
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... A total of nine studies that included 102 women satisfied the inclusion criteria regarding SBF and the menstrual cycle [12,19,20,[37][38][39][40][41][42]. Women who participated in these studies varied in characteristics related to oral contraceptive use, age, and level of physical activity. ...
... It was measured at varying locations including the thigh, forehead, forearm, and finger. Four out of the nine studies, with a total of 33 subjects, showed a statistically significant increase in SBF during the luteal phase compared to the follicular phase [19,20,39,40]. The reported increases varied by study. ...
... We found slight evidence for an effect in the opposite direction as expected: women wore more skinrevealing clothes in the luteal phase. There are several explanations for this finding: higher basal temperature when in the luteal phase (Lee et al., 2014), less risky behaviour when fertile (Bröder & Hohmann, 2003;Chavanne & Gallup Jr, 1998) and stronger protection against intra-sexual aggression (Krems et al., 2021). Given that these effects were not robust and not replicated in the other studies, we refrain from further interpretation before replication in independent samples. ...
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To assess potential mechanisms responsible for the lower sudomotor thermosensitivity in women during exercise, we examined sex differences in sudomotor function and skin blood flow (SkBF) during exercise performed at progressive increases in the requirement for heat loss. Eight men and eight women cycled at rates of metabolic heat production of 200, 250, and 300 W/m(2) of body surface area, with each rate being performed sequentially for 30 min. The protocol was performed in a direct calorimeter to measure evaporative heat loss (EHL) and in a thermal chamber to measure local sweat rate (LSR) (ventilated capsule), SkBF (laser-Doppler), sweat gland activation (modified iodine-paper technique), and sweat gland output (SGO) on the back, chest, and forearm. Despite a similar requirement for heat loss between the sexes, significantly lower increases in EHL and LSR were observed in women (P ≤ 0.001). Sex differences in EHL and LSR were not consistently observed during the first and second exercise periods, whereas EHL (348 ± 13 vs. 307 ± 9 W/m(2)) and LSR on the back (1.61 ± 0.07 vs. 1.20 ± 0.09 mg·min(-1)·cm(-2)), chest (1.33 ± 0.06 vs. 1.08 ± 0.09 mg·min(-1)·cm(-2)), and forearm (1.53 ± 0.07 vs. 1.20 ± 0.06 mg·min(-1)·cm(-2), men vs. women) became significantly greater in men during the last exercise period (P < 0.05). At each site, differences in LSR were solely due to a greater SGO in men, as opposed to differences in sweat gland activation. In contrast, no sex differences in SkBF were observed throughout the exercise period. The present study demonstrates that sex differences in sudomotor function are only evidenced beyond a certain requirement for heat loss, solely through differences in SGO. In contrast, the lower EHL and LSR in women are not paralleled by a lower SkBF response.
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This study investigated the effects of the menstrual cycle on prolonged exercise performance both in temperate (20°C, 45% relative humidity) and hot, humid (32°C, 60% relative humidity) conditions. For each environmental condition, 12 recreationally active females were tested during the early follicular (day 3-6) and midluteal (day 19-25) phases, verified by measurement of estradiol and progesterone. For all four tests, thermoregulatory, cardiorespiratory, and perceptual responses were measured during 60 min of exercise at 60% of maximal oxygen consumption followed by an incremental test to exhaustion. No differences in exercise performance between menstrual cycle phases were found during temperate conditions (n = 8) despite a higher resting and submaximal exercise core temperature (Tc) in the luteal phase. In hot, humid conditions (n = 8), however, prolonged exercise performance, as exercise time to fatigue, was significantly reduced during the luteal phase. This finding was not only accompanied by higher resting and submaximal exercise Tc but also a higher rate of increase in Tc during the luteal phase. Furthermore, submaximal exercise HR, minute ventilation, and RPE measures were higher during the luteal phase in hot, humid conditions. No significant differences were found over the menstrual cycle in heat loss responses (partitional calorimetry, sweat rate, upper arm sweat composition) and Tc at exhaustion. In temperate conditions, no changes in prolonged exercise performance were found over the menstrual cycle, whereas in hot, humid conditions, performance was decreased during the luteal phase. The combination of both exercise and heat stress with the elevated luteal phase Tc at the onset of exercise resulted in physiological and perceptual changes and a greater thermosensitivity, which may explain the decrease in performance.
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Sweat rate (SR) is reduced in locally cooled skin, which may result from decreased temperature and/or parallel reductions in skin blood flow. The purpose of this study was to test the hypotheses that decreased skin blood flow and decreased local temperature each independently attenuate sweating. In protocols I and II, eight subjects rested supine while wearing a water-perfused suit for the control of whole body skin and internal temperatures. While 34°C water perfused the suit, four microdialysis membranes were placed in posterior forearm skin not covered by the suit to manipulate skin blood flow using vasoactive agents. Each site was instrumented for control of local temperature and measurement of local SR (capacitance hygrometry) and skin blood flow (laser-Doppler flowmetry). In protocol I, two sites received norepinephrine to reduce skin blood flow, while two sites received Ringer solution (control). All sites were maintained at 34°C. In protocol II, all sites received 28 mM sodium nitroprusside to equalize skin blood flow between sites before local cooling to 20°C (2 sites) or maintenance at 34°C (2 sites). In both protocols, individuals were then passively heated to increase core temperature ~1°C. Both decreased skin blood flow and decreased local temperature attenuated the slope of the SR to mean body temperature relationship (2.0 ± 1.2 vs. 1.0 ± 0.7 mg·cm(-2)·min(-1)·°C(-1) for the effect of decreased skin blood flow, P = 0.01; 1.2 ± 0.9 vs. 0.07 ± 0.05 mg·cm(-2)·min(-1)·°C(-1) for the effect of decreased local temperature, P = 0.02). Furthermore, local cooling delayed the onset of sweating (mean body temperature of 37.5 ± 0.4 vs. 37.6 ± 0.4°C, P = 0.03). These data demonstrate that local cooling attenuates sweating by independent effects of decreased skin blood flow and decreased local skin temperature.