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Thermal and Mountain Medicine Division, United States Army Research Institute of Environmental Medicine, Natick, Massachusetts 01760-5007
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Kolka, Margaret A., and Lou A. Stephenson. Effect of
luteal phase elevation in core temperature on forearm blood flow during
exercise. J. Appl. Physiol. 82(4):
1079-1083, 1997.
Forearm blood flow (FBF) as an index of skin
blood flow in the forearm was measured in five healthy women by venous
occlusion plethysmography during leg exercise at 80% peak aerobic
power and ambient temperature of 35°C (relative humidity 22%;
dew-point temperature 10°C). Resting esophageal
temperature (Tes) was 0.3 ± 0.1°C higher in the midluteal than in the early follicular phase of
the menstrual cycle (P < 0.05).
Resting FBF was not different between menstrual cycle phases. The
Tes threshold for onset of skin
vasodilation was higher (37.4 ± 0.2°C) in midluteal than in
early follicular phase (37.0 ± 0.1°C; P < 0.05). The slope of the FBF to
Tes relationship was not different between menstrual cycle phases (14.0 ± 4.2 ml · 100 ml
1 · min1 · °C1
for early follicular and 16.3 ± 3.2 ml · 100 ml1 · min1 · °C1
for midluteal phase). Plateau FBF was higher during exercise in
midluteal (14.6 ± 2.2 ml · 100 ml1 · min1 · °C1)
compared with early follicular phase (10.9 ± 2.4 ml · 100 ml1 · min1 · °C1;
P < 0.05). The attenuation of the
increase in FBF to Tes occurred when Tes was 0.6°C higher and
at higher FBF in midluteal than in early follicular experiments
(P < 0.05). In summary, the FBF response is different during exercise in the two menstrual cycle phases
studied. After the attenuation of the increase in FBF and while
Tes was still increasing, the
greater FBF in the midluteal phase may have been due to the effects of
increased endogenous reproductive endocrines on the cutaneous
vasculature.
body temperature regulation
INTRODUCTION THE CHANGING HORMONAL PATTERN during the human
menstrual cycle may affect skin blood flow during exercise or heat
stress, as it is well established that various estrogenic hormones
influence vascular activity (1, 11, 28). In a "normal" menstrual cycle, circulating estradiol is elevated immediately before the luteinizing hormone "surge" preceding ovulation (late follicular phase) and, again, in the midluteal phase when progesterone is also
increased (7, 9, 23). In a previous investigation (27), we described an
increased esophageal temperature
(Tes) for the onset of skin
vasodilation during exercise in the midluteal phase of the menstrual
cycle when both circulating progesterone and estradiol were elevated.
Other laboratories have reported increased threshold for the onset of
finger vasodilation during exercise (17) or increased threshold for
cutaneous vasodilation during passive heating or cooling in the luteal
phase of the menstrual cycle (13, 15, 16); the result being altered
thermoregulatory control in the luteal phase associated with increased
core temperature. These conclusions were supported by studies showing
increased body temperature in humans after progesterone administration
(2, 5, 23, 26), and in animals by decreased firing rate of preoptic
warm-sensitive neurons and increased firing rate of preoptic cold-sensitive neurons after intravenous progesterone (24). These data
support the hypothesis that there is an increased thermoregulatory set-point temperature during the midluteal phase of the menstrual cycle
(3).
Forearm blood flow measurement provides an index of skin blood flow
that is important in the assessment of thermoregulatory effector
function (18, 20). As core temperature increases during exercise or
heat stress, blood flow to the cutaneous vasculature increases
proportionately. Exercise places limits on the cutaneous vasculature to
dilate and, as core temperature approaches 38°C, skin blood flow
levels off even as core temperature continues to increase (4, 18, 19,
20). It is this relationship that was of interest in the present study.
The purpose of this study was to characterize possible differences in
the skin blood flow responses in women during an exercise-heat stress
in both the early follicular and midluteal phases of the menstrual
cycle. We hypothesized that the leveling off of forearm blood flow
would occur at different core temperatures in the two menstrual cycle
phases studied. The approach (relatively intense exercise and heat)
stimulated prolonged and fairly high cutaneous vasodilation, which
allowed for the characterization of adaptive skin blood flow responses.
The elevation in resting core temperature was the a
priori criterion for the midluteal-phase experiments.
METHODS Five healthy women completed two experiments each at an exercise
intensity of 80% of peak aerobic power at 35°C (relative humidity
22%; dew-point temperature 10°C) after they were verbally apprised
of the nature and risks of the study. The average age was 27.6 ± 4.4 (SD) yr, height was 1.68 ± 0.05 m, mass was 65.9 ± 7.0 kg,
DuBois surface area was 1.75 ± 0.06 m2, and peak aerobic power was
2.87 ± 0.54 l/min. Exercise lasted 25-30 min.
Each volunteer had a normal menstrual cycle as defined by regular
periodicity and was not taking oral contraceptives. To verify ovulatory
menstrual cycles, daily basal body temperature (BBT; oral) was recorded
by each subject on awakening. Data from an entire menstrual cycle were
collected before inclusion in the study to determine whether BBT
increased after ovulation (21). Higher BBT is closely correlated with
higher plasma progesterone concentration in the luteal phase of the
menstrual cycle (5). Consequently, elevated BBT in the luteal phase was
an adequate post hoc method of determining that
ovulation occurred and enabled us to schedule experiments in the
appropriate menstrual cycle phase. From additional experiments in our
laboratory and others, higher midluteal phase
Tes readings occur when
circulating estradiol and progesterone are elevated significantly, and
Tes does not increase in the
midluteal phase in the absence of elevated estradiol and progesterone
(26). Testing in the midluteal phase was done on days when the resting
core temperature was elevated (approximate days
19-22), consistent with elevated serum estradiol
and progesterone (26). Testing in the early follicular phase was done
on days 3-6 (day
1 = 1st day of menstrual flow).
Before testing, volunteers were thoroughly familiarized with all
experimental techniques. On test days, preexperiment body weights were
within 1% of the mean baseline body weight measured during preliminary
testing to avoid dehydration. In all experiments, each subject sat in a
chair positioned behind the cycle ergometer, such that during leg
exercise the legs were parallel to the floor. The subject swallowed a
catheter containing a thermocouple that was adjusted to approximate
heart level based on 25% of each subject's height. Surface
thermocouples were placed at eight skin sites, one site being the
forearm adjacent to the strain gauge, to estimate mean skin temperature
(25). A mercury-in-Silastic strain gauge was placed on the forearm for
the measurement of forearm blood flow by venous occlusion
plethysmography (VOP; 10, 29). The strain gauge was placed around a
section of forearm distal to the main mass of the muscles to decrease
the proportion of muscle in the whole arm cylinder measured. The
forearm was suspended by the wrist, with a sling apparatus anchored at
two points, minimizing movement artifact during exercise as the arm and
gauge moved in translation with the torso and the strain gauge position
on the arm was near the height of the heart. During seated exercise, any increase in forearm blood flow is an accurate index of an increase
in skin blood flow (18). Heart rate (HR) was measured from the
electrocardiogram.
Temperatures and forearm blood flow were measured twice each minute. HR
was recorded every 2.5 min, and metabolic heat production was estimated
from oxygen utilization (open-circuit spirometry) at rest and during
exercise. The Tes threshold for
onset of cutaneous vasodilation and the slope of this relationship
during exercise were determined by calculation of a linear-regression
equation from the Tes and VOP
data, when both parameters were increasing at the beginning of exercise
("a" on Figs. 1, 2, 3). In addition, the relationship of forearm blood flow and
Tes, after the increase in forearm
blood flow was attenuated during exercise, was also characterized by
least squares regression ("b" and "c" on Figs. 2, 3). Data from VOP and temperatures
at rest, during exercise, and the
Tes threshold for onset of
cutaneous vasodilation were analyzed by analysis of variance procedures
with repeated measures.
RESULTS Resting Tes averaged 36.84 ± 0.21 (SD) °C in the early follicular phase experiments and 37.13 ± 0.23°C in the midluteal phase experiments
(P < 0.05). Mean skin temperature
averaged 35.87 ± 0.27°C in the early follicular phase
experiments and 36.18 ± 0.27°C in the midluteal phase
experiments (P < 0.05). There was no
difference in forearm blood flow, HR, or metabolic rate at rest between
the menstrual cycle phases studied. The
Tes pattern (mean ± SD) is shown in Fig. 1 with the midluteal phase elevation in core temperature observed throughout exercise (P < 0.05). The forearm blood flow pattern (mean ± SD) is shown in Fig.
2. There is a clear attenuation in the increase of forearm blood flow
after 12-13 min of exercise in the early follicular phase and
after 15 min in the midluteal phase, even as
Tes continues to increase. Forearm
blood flow was significantly higher during exercise after the plateau
in the midluteal phase (14.6 ± 2.2 vs. 10.9 ± 2.4 ml · 100 ml The relationship of forearm blood flow, as an index of skin blood flow,
to increasing Tes during the
initial rapid rise of both variables ("a" in Figs. 1, 2, 3)
indicated that the Tes threshold for onset of skin vasodilation during exercise averaged 37.0 ± 0.1°C in the early follicular phase and 37.4 ± 0.2°C in the
midluteal phase (P < 0.05). The
slope for the forearm blood flow to
Tes relationship during the
exercise transient averaged 14.0 ± 4.2 ml · 100 ml The relationship after the attenuation of the increase in forearm blood
flow is presented in Table 1. The
Tes at the attenuation of the
forearm blood flow increase was higher in the midluteal experiments
than in the early follicular experiments
(P < 0.05). This attenuation of the
increase in forearm blood flow occurred at a significantly higher skin
blood flow in midluteal experiments than in early follicular
experiments (P < 0.05). HR during
the attenuation in forearm blood flow ("c" on Figs. 2 and 3)
averaged 150 ± 11 beats/min in the early follicular phase
experiments and 161 ± 9 beats/min in the midluteal phase
experiments. Metabolic rate and mean skin temperature were not
different during exercise in the two menstrual cycle phases studied.
Table 1.
Characteristics of skin blood flow and Tes at attenuation
of the increase in FBF and Tes during high-intensity
exercise
Fig. 1.
Pattern of esophageal temperature (means ± SD) during exercise in
early follicular (
) and midluteal phase (
) experiments in which
subjects exercised at 80% peak aerobic power. Mean skin temperature
averaged 35.3 and 35.4°C in early follicular and midluteal phase
experiments, respectively. a, Exercise transient. Midluteal > early follicular, P < 0.05.
[View Larger Version of this Image (19K GIF file)]
Fig. 2.
Pattern of forearm blood flow (means ± SD) during exercise in early
follicular () and midluteal phase () experiments in which
subjects exercised at 80% peak aerobic power. Midluteal > early
follicular, P < 0.05. a, Exercise
transient; b, attenuation of forearm blood flow increase; c, leveling
off or plateau of forearm blood flow.
[View Larger Version of this Image (22K GIF file)]
Fig. 3.
Relationship of forearm blood flow to esophageal temperature during
exercise (80% peak aerobic power) in early follicular () and
midluteal phase () of menstrual cycle. a, Exercise transient; b, attenuation of forearm blood flow increase; c, leveling off or
plateau of forearm blood flow.
[View Larger Version of this Image (17K GIF file)]
1 · min1;
P < 0.05).
1 · min1 · °C1
in early follicular experiments and 16.3 ± 3.2 ml · 100 ml1 · min1 · °C1
in midluteal experiments. After this initial exercise transient, the
relationship between forearm blood flow and
Tes was attenuated as is the
pattern for forearm blood flow (see Figs. 2 and
3). This relationship between forearm
blood flow and Tes is shown graphically in Fig. 3.
Phase
Slope, Post-Attentuation
Tes, °C
FBF, ml · 100 ml
1 · min1 HR, b/min
°C
Early
follicular
1.5 ± 0.5 37.5 ± 0.2
10.9 ± 2.4
150 ± 11
35.25 ± 0.41
Midluteal
1.0 ± 0.5 38.1 ± 0.2*
14.6 ± 2.2*
161 ± 9*
35.41 ± 0.45
Data are calculated at "b" and "c" on Figs. 1, 2, 3.
Tes, esophageal temperature; FBF, forearm blood flow; HR,
heart rate;
sk, mean skin
temperature.
Units for skin blood flow-to-Tes slopes
are ml · 100 ml1 · min1 · °C
1.
*
P < 0.05.
DISCUSSION
This study presents evidence that the "equilibrated" forearm blood flow (when the rapid increase in forearm blood flow is attenuated) is increased when the Tes is elevated during the midluteal phase of the menstrual cycle compared with the early follicular phase. Additionally, at any Tes >37.5°C, forearm blood flow is higher during exercise in the midluteal phase of the menstrual cycle compared with the early follicular phase of the menstrual cycle. The results also confirm previous work from our laboratory and others (13, 15, 16, 27) that increased resting core temperature during the midluteal phase affects, or is related to, a higher core temperature for the onset of skin vasodilation during exercise.
Forearm blood flow was 40-50% higher after the attenuated increase or equilibration during our luteal phase experiments. If there were a similarly increased blood flow extrapolated to the entire skin surface (assuming that cutaneous blood flow of other areas responds like the forearm), a significant increase in blood volume to the skin occurred. This redistribution would require increased cardiac output to maintain muscle perfusion during the high-intensity exercise as well as additional perfusion of the cutaneous circulation. No measurement of cardiac output was made during these experiments; however, HR was significantly increased in association with higher forearm blood flow during the luteal phase experiments, which may indirectly indicate higher cardiac output.
Evidence for reduced vasodilator activity as opposed to sympathetic restraint of skin blood flow has been presented (19, 20) to explain attenuation of the increase in skin blood flow. The current data indicate that forearm blood flow was significantly higher at the point of attenuation or equilibration during the midluteal phase experiments. It is not possible to determine from the current study whether this observation results from modulation of the vasodilatory, vasoconstrictor, or a combination of the two broad inputs to the cutaneous vasculature. It does show that forearm blood flow equilibration during an exercise-heat stress is different between menstrual cycle phases.
Little insight is provided from previous literature into the possible mechanisms for the increased forearm blood flow at the point of attenuation for a given Tes (Fig. 3) observed in the present study. Previous conclusions (15-17, 27) were that the onset of vasodilation and cutaneous vasodilatory threshold temperature were altered between the early follicular and midluteal phases of the menstrual cycle in eumenorrheic women during exercise or heat stress. However, the finding that postural vasoconstriction was attenuated in the midluteal phase, compared with late follicular (preovulatory) and early follicular phase experiments (14), is consistent with the present study in that both responses could be explained by either increased vasodilatory signal(s), dampened vasoconstrictor signal(s), or a combination of both. In opposition, however, is the report that skin conductance, calculated from experiments conducted in a human calorimeter, was lower in the midluteal phase of the menstrual cycle compared with the follicular phase (12). It is difficult to compare the latter results (12) with the current experiments, as the follicular phase experiments were actually run during late follicular phase/preovulatory phase (day 9 ± 1) when the hormonal environment is characterized by high estrogen levels and low progesterone levels (7). In the present study, there was no significant difference in forearm blood flow between menstrual cycle phases when the subjects were resting in a warm environment (35°C).
The increased equilibrated forearm blood flow observed in women
exercising in a hot environment during the midluteal phase in the
present study is likely associated with changes in the reproductive
endocrines characteristic of that menstrual cycle phase. Taken together
with other data (19, 20), it is suggested that neuroendocrine,
endocrine, or paracrine influences on the cutaneous vasculature that
modulate vasodilatory and/or vasoconstrictor responses are
activated by a signal resulting from the increased concentration of
circulating 17
-estradiol and progesterone, which occurs in the
midluteal phase. For example, 17-estradiol has a vascular protective
effect as it induces both prostacyclin and nitric oxide synthesis (8).
This vascular protective effect is also apparent in postmenopausal
women who receive hormone replacement therapy (11, 22). It is unknown
whether progesterone plays any role in eliciting the increased
equilibrated forearm blood flow in exercising eumenorrheic women during
the midluteal phase, other than its proposed effect on the
thermoregulatory set-point temperature (6, 15, 17, 27). Clearly,
further studies are necessary to characterize the mechanisms altering
cutaneous vasodilation during the midluteal phase in exercising women.
ACKNOWLEDGEMENTS
The views, opinions, and/or findings contained in this report are those of the authors and should not be construed as official Department of the Army position, policy, or decision, unless so designated by other official documentation. Human subjects participated in these studies after giving their free and informed consent. Investigators adhered to Army Regulation 70-25 and United States Army Medical Research and Development Command Regulation 70-25 on the Use of Volunteers in Research.
FOOTNOTES
Address for reprint requests: M. A. Kolka, TMMD/USARIEM, Kansas St., Natick, MA 01760-5007.
Received 12 February 1996; accepted in final form 13 November 1996.
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