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Human Performance and Protection, Defence and Civil Institute of Environmental Medicine, Toronto, Ontario, Canada M3M 3B9
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ABSTRACT |
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Eleven women (age = 24.4 ± 6.3 yr,
mass = 65.0 ± 7.8 kg, height = 167 ± 8 cm, body
fatness = 22.4 ± 5.9%, mean ± SD) were immersed to
neck level in 18°C water for up to 90 min for comparison of their
thermal responses with those of men (n = 14) in a
previous similarly conducted protocol. Metabolic rate increased about
three times resting levels in men and women, whereas the rate of rectal temperature cooling (
Tre/
t) in women
(0.47°C/h) was about one-half that in men. With use of all data,
Tre/
t correlates with the ratio of body
surface area to size and the metabolic rate of shivering correlates
inversely to the square root of body fatness. No significant gender
differences in total metabolic heat production normalized for body mass
or surface area were found among subjects who completed 90 min of
immersion (9 women and 7 men). Nor was there a gender difference in the
overall percent contribution (~60%) of fat oxidation to total heat
production. Blood concentrations of free fatty acids, glycerol,
-hydroxybutyrate, and lactate increased significantly during the
90-min immersion, whereas muscle glycogen sampled from the right
quadriceps femoris vastus lateralis decreased (free fatty acids,
glycerol, and
-hydroxybutyrate were higher in women). When the
subjects were subgrouped according to similar body fatness and 60 min
of immersion (6 women and 5 men), no significant gender differences
emerged in
Tre/
t, energy metabolism, and
percent fat oxidation. These findings suggest that no gender
adjustments are necessary for prediction models of cold response if
body fatness and the ratio of body surface area to size are taken into
account and that a potential gender advantage with regard to
carbohydrate sparing during cold water immersion is not supported.
body cooling; shivering; prediction; model; substrate utilization
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INTRODUCTION |
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PREDICTION MODELS of survival time for cold exposure (30, 31) are in use as a decision aid in search-and-rescue operations. Such predictions are largely based on the physiological factors that affect the rate of heat production within the body and physical factors that affect heat loss from the body. These models were subsequently calibrated against data involving male responses to cold. Although data regarding female responses to cold are limited, the evidence suggests that differences in thermoregulation between genders are mostly due to anthropometric differences in body fatness and the body surface area (SA)-to-size ratio (19, 26, 37). If this is the case, then models that factor these variables into account might be valid as gender invariant.
Another important factor for prediction modeling of survival time for
cold exposure is substrate utilization. A greater dependence on the
contribution of fat oxidation (fatox) to fuel shivering thermogenesis could be advantageous by preserving carbohydrate (CHO)
stores and thereby potentially extending shivering endurance. This
benefit of CHO sparing has been demonstrated during exercise when the
endurance time during cycling at 80% of maximal aerobic power
(
O2 max) was extended in active women
compared with men because of a greater reliance on lipid and,
consequently, a lower reliance on muscle glycogen (8).
Although shivering thermogenesis occurs at low levels relative to
O2 max, it has been proposed that
shivering endurance depends not on the absolute intensity of shivering
but its value relative to maximal shivering and is glycogen dependent
(38). Use of intramuscular glycogen reserves to fuel
intensive thermogenic activity has been reported by Martineau and
Jacobs (17).
The proportion of specific energy substrates utilized during exercise depends on a number of factors, including exercise intensity and duration, cardiorespiratory function, hormonal components, and diet. Several studies (11, 12, 24, 28, 29) have reported that women utilize more fat than men during exercise at the same relative intensity. More recently, Pettit et al. (23) examined the contributions of fatox and CHO oxidation (CHOox) in eight men and nine women during a 2-h resting exposure to 5°C air. They found that these respective substrates contributed 53 and 47% to total heat production in men compared with 64 and 36% in women (P < 0.05), consistent with the exercise studies. Although expected, it is uncertain whether this relationship also holds for higher metabolic levels observed during shivering in cold water, rather than in cold air.
Validation of a model prediction of survival time for men and women requires comparative data of thermoregulatory responses and substrate utilization to cold exposure. The prediction of survival time is not necessarily limited to extreme cold strain, since it also involves calculations that encompass conditions from thermoneutrality through lethal hypothermia. Consequently, if differences in thermoregulatory responses between genders are found under conditions of mild cold strain, such as at the beginning of a cold exposure, then these differences might propagate and ultimately impact survival time predictions. Hence, this investigation is focused on experimental conditions that involve a level of cold stress that might be considered moderate during the initial exposure but is potentially lethal in the long term. Furthermore, the aforementioned survival time prediction model (30, 31) assumes that casualties are in a sedentary posture; therefore, this study will also be limited to resting individuals exposed to cold.
The aims of the present study involving cold water immersion are to
confirm that the rates of body cooling and metabolic heat production
(
) are gender invariant when corrected for anthropometric differences and to determine gender differences in substrate
utilization. As a result, this study will explore any adjustments that
might be necessary to improve the accuracy of prediction models of cold exposure survival time. More specifically, we followed the experimental protocol developed by Martineau and Jacobs (17, 18) for
men to test women. The hypotheses of the present study are as follows: 1) women and men exhibit similar changes in body cooling and
metabolism during cold exposure when subject responses are corrected
for body fatness (BF) and size, and 2) in women, a higher
percentage of
during cold water immersion would be due to
fatox than was previously observed for men.
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MATERIALS AND METHODS |
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The experimental procedure has been described in detail by Martineau (16) and Martineau and Jacobs (17, 18). The primary differences are that women were used in the present study, and they were immersed in a different water tank for ease of operation, yet the level of water agitation was moderate in both cases. All data cited for men were obtained from the work of Martineau (16). Data on all 14 subjects (17), as well as the rectal temperature (Tre) response for a subgroup of 8 subjects (18), have been reported previously.
Subjects.
Eleven women completed the study conducted in accordance with a
protocol approved by the Human Ethics Committee. Subjects signed an
informed consent and underwent a preexperimental assessment, during
which height and weight were measured, %BF was estimated (27) after determination of body density by hydrostatic
weighing, and
O2 max was determined
through a standard exercise test to exhaustion on a treadmill. The body
SA-to-size ratio will be represented by the SA-to-volume (mass/density)
ratio (SA/vol) instead of the conventional measure of SA/mass, since
the ratio is intended to reflect the exposure area relative to overall
body size.
Protocol. At least 1 wk before the experimental trial, subjects were immersed in 18°C stirred water for 15 min to familiarize them with the laboratory setting and test procedures. On the day of the experimental trial, subjects reported to the laboratory at the same time of day to avoid possible diurnal effects. They were asked to abstain from alcohol for 48 h and to fast for 12 h before the trial and not to exercise within 24 h of the trial; otherwise there were no dietary or mobility restrictions. No attempt was made to standardize the menstrual cycle phase for the cold water immersions. After the subject dressed down into a two-piece bathing suit and self-inserted a rectal probe, she was instrumented with bipolar electrocardiogram skin electrodes and an intravenous catheter. The subject then lay quietly on an open mesh cot in a supine position for 30 min at 23°C air temperature so that her resting metabolic rate could be measured. Then the subject, while remaining in the same position on the cot, was lowered into the water bath at a water temperature that averaged ~18°C (within 0.2°C) during the immersion. There the subject remained in a supine position immersed to the neck level until one of the following criteria was reached: 90 min elapsed, Tre decreased to 35.5°C, or the subject asked to be removed.
Measurements.
Tre (measured at 15 cm past the anal sphincter) was
measured continuously (Pharmaseal 400 Series, Baxter Healthcare) during the immersion and averaged each minute. Respiratory gases were monitored using a semi-automated metabolic cart system (model OCM-2,
Ametek, Pittsburg, PA) during the last 10 min of the thermoneutral rest
period before immersion and continuously throughout the immersion, with
the exception of a 5-min break for recalibration purposes after 25 min
of immersion. During monitoring, the subject was connected to a
mouthpiece, breathing valve, and hose assembly, which directed the
expired gases to a 5-liter mixing box connected in series to a
ventilation module that measured the expired ventilation rate (VMM
Ventilation Measurement Module, Interface Associates, Irvine, CA). A
sample line directed gases from the mixing box to O2 and
CO2 analyzers (models S-3A11 and CD-3A, respectively, Ametek, Applied Electrochemistry, Paoli, PA). Commercially available microcomputer-based software (Vista/Turbofit Software, version 3.10, Vacumetrics, Ventura, CA) was used to register the data each minute and
to convert the values of O2 consumption
(
O2) and CO2 production into
STPD units.
8 h. Glycogen
was assayed as glucose units after hydrochloric acid hydrolysis with
use of a fluorometric enzymatic method (14).
Venous blood samples (10 ml) were scheduled to be drawn before
immersion and after 5, 30, 60, and 90 min of immersion from an
antecubital vein with use of a 20-gauge 1-in. catheter and heparin lock
(10 U/ml). A waterproof dressing (Tegaderm) was placed over the site
where the catheter pierced the skin to help stabilize the catheter. Two
milliliters of the blood sample were dispensed into heparin-treated
tubes for subsequent determinations of glucose, lactate,
-hydroxybutyrate (
-OH), hematocrit, and Hb; 4 ml were dispensed
into a tube treated with EGTA (90 mg/ml) and glutathione (60 mg/ml) for
subsequent determinations of catecholamines; 2 ml were dispensed into
an EDTA-treated tube for subsequent determinations of free fatty acids
(FFA), glycerol, and insulin; and 2 ml were dispensed into an
EDTA-treated tube containing Trasylol for subsequent determination of
glucagon. All samples were centrifuged, and the plasma was stored at
70°C until assayed.
Hematocrit was determined by centrifugation (Autocrit Ultra3
Centrifuge, Clay Adams, Parsippany, NJ). Commercially available kits
were used to measure concentrations of plasma glucagon (Glucagon RIA
kit, Diagnostic Products, Los Angeles, CA), plasma insulin (Pharmacia
Insulin RIA 100, Pharmacia, Uppsala, Sweden), and FFA (WAKO NEFA kit,
Osaka, Japan). Glucose and Hb were assayed using automated
spectrophotometric techniques (Hemocue, Mission Viejo, CA). Plasma
samples were analyzed for glycerol concentration after deproteinization
(3), lactate, and
-OH (21). Plasma
epinephrine and norepinephrine levels were measured using negative ion
chemical ionization gas chromatography-mass spectrometry
(40). Changes in plasma volume were calculated from the
changes in hematocrit and Hb concentration (6).
Calculations.
The subject's body SA (in m2) was estimated using the
following formula regressed specifically for women from the data of
Jones et al. (13)
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(1) |
(in W) was calculated from the respiratory gas exchange
measurements of
O2 (in l/min) and the
respiratory exchange ratio (RER via the CO2 production)
according to Peronnet and Massicotte (22)
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(2) |
O2 and RER. Details on these
calculations and justification for use of the nonprotein RER are found
in the report of Vallerand et al. (36).
Data analysis. The thermoregulatory variables measured were Tre and the metabolic responses to cold water immersion. Because subjects were immersed in water up to the neck level, it was assumed that skin temperature and its effect on thermoregulatory responses were not different between the men and women.
The data involving all subjects (All) were analyzed for the duration of immersion (
t), the rate of change of Tre over
the immersion period (
Tre/
t), the
at the lowest common Tre attained by all subjects, percent
contribution of fatox to total heat production, and the
proportionality constant (A) for the prediction of the metabolic rate due to shivering (
shiv). According to
Tikuisis and Giesbrecht (32),
shiv is
inversely proportional to
for given core and mean skin
temperatures
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(3) |
shiv ·
. The value of
shiv was determined from the difference between the
subject's metabolic rates measured at the lowest common Tre and at rest.
Additionally, the data of all subjects who completed 90 min of
immersion (subgroup S90) were separately analyzed for
Tre/
t, the total heat production, percent
contribution of fatox to total heat production, and muscle
glycogen depletion (
Gly). This discrimination allows a direct
comparison of substrate utilization between men and women over the
maximum period of immersion.
For comparative purposes, a second subgroup involved subjects of
similar body fatness (subgroup SBF) who completed
60 min of
immersion. Data from this subgroup were specifically selected to allow
a direct comparison of results with those of McArdle et al.
(19), whose male and female subjects were immersed in 20°C water for 60 min and subgrouped according to %BF of 15-18 and 15-21%, respectively (n = 4 in each). Hence,
our data analyses involved
Tre/
t and mean
O2 over 60 min but also included
%fatox and muscle
Gly. Male and female subjects were
selected on the basis of whether their %BF was higher or lower than
the respective mean values for the All group.
A t-test was applied to test for gender differences within
each group at P < 0.05. Statistical analyses of
substrate utilization, muscle glycogen content, and blood metabolites
were conducted using a mixed ANOVA design with a between-subject
variable (gender) and repeated measures for within-subject comparisons.
A Hunyh-Feldt score of <0.05 was applied for significance testing.
Multiple linear regressions were performed on the All data to identify significant parameters, with acceptance at P < 0.05.
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RESULTS |
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Table 1 summarizes the subject
characteristics in each group. When data were used from all subjects
(group All), gender differences were observed for height and BF. Gender
differences were found in all subject characteristics except age in
those subjects who were immersed for 90 min (subgroup S90). Body mass,
SA, and SA/vol were significantly different between men and women of
comparable BF that were immersed for 60 min (subgroup SBF). Whereas
SA/vol was significantly different between genders in subgroups S90 and SBF, SA/mass (not shown) was significantly different in all groups.
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Figure 1 shows the mean Tre
profile of all the female subjects immersed in the cold water. All but
three subjects responded with an initial transient rise in
Tre, and none reached the cutoff criterion of 35.5°C. Two
subjects requested early withdrawal after 60 min of immersion. Net
decreases in Tre ranged from 0.27 to 1.47°C. Figure
2 shows the mean
of all female
subjects, which increased to ~3.2 times the resting metabolic rate
after 30 min of immersion. Also shown in Figs. 1 and 2 are the mean
responses of all the male subjects, of whom six reached 35.5°C before
90 min of immersion and one requested early withdrawal (16,
17).
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Table 2 summarizes all the subjects'
thermoregulatory responses grouped by gender. The only significant
gender difference was in the rate of change of Tre. No
significant differences were found in
when further normalized
against lean body mass (LBM). Nor was there any gender difference in
the resting metabolic rates (48.5 ± 14.1 and 43.7 ± 6.8 W/m2 for men and women, respectively) used to determine
shiv.
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Although the female trials were not controlled for menstrual cycle, the above analysis was repeated with women subgrouped according to their menstrual cycle phase [follicular (n = 4) and luteal (n = 7)]. There were no differences between these subgroups in any of their physical characteristics or thermoregulatory responses listed in Tables 1 and 2. The only difference was in their immediate preimmersion Tre [36.85 ± 0.07 and 37.12 ± 0.15°C (P = 0.01) for women in follicular and luteal phases, respectively], yet this had no impact on their subsequent thermoregulatory responses.
The regression of the pooled data of
Tre/
t
against the physiological variables listed in Table 1 yielded SA/vol as
the only significant independent variable
[
Tre/
t (°C/h) = 3.36
0.144 · SA/vol; P = 0.04, r = 0.42]. The regression of
shiv (by use of data at
the lowest measured common value of Tre = 36.8°C) yielded BF as the only significant independent variable
[
shiv (W/m2) = 160.8
3.49 · %BF; P = 0.00, r = 0.56]. The fit of A (see Eq. 3) against the
pooled data yielded a closer fit:
shiv
(W/m2) = 371.5/
(root mean square
error = 1,542 vs. 1,757 with use of the above linear regression).
Table 3 summarizes the responses by
gender of the subjects who completed 90 min of cold water immersion
(subgroup S90). The only significant gender difference was in the
absolute total heat production. However, when normalized against total
body mass, LBM, or body SA, no significant differences in heat
production emerged. If these data were further confined to subjects of
similar BF (by use of the selection criterion in subgroup SBF resulting in 5 subjects/gender group), there were also no differences in any of
the heat production variables, including the absolute value.
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There was no significant gender difference in substrate utilization in those subjects who completed 90 min of immersion (subgroup S90). To examine whether the pattern of substrate utilization was different over this period of immersion, the relative contributions of %fatox and %CHOox were determined during 30-min intervals. Men showed a significant increase in %fatox (from 54 to 66%) and a corresponding significant decrease in %CHOox (from 46 to 34%) from 30 to 60 min, which leveled off during the last 0.5 h of immersion. Women, on the other hand, showed no significant changes over time (%fatox and %CHOox were 64 and 36%, respectively).
For additional comparisons to other published studies, subgroup S90 was
further segregated (subgroup S90Rel) to involve only subjects with similar relative intensities of shivering heat production compared with their
O2 max. No
significant gender difference in contributions of substrate utilization
was found among the subjects in this subgroup [5 women
(
O2 max = 41.1 ± 6.6 ml · min
1 · kg
1) and 5 men
(47.0 ± 3.9 ml · min
1 · kg
1),
P > 0.05] whose relative shivering intensities were
31 ± 2 and 29 ± 6% of
O2 max, respectively. Yet, the same
shift in substrate utilization with time from CHO to fat occurred in the men in subgroups S90Rel (Fig.
3) and S90.
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Muscle glycogen samples were obtained from all but two women in subgroup S90. Concentrations decreased significantly between the pre- and postimmersion samples (from 493 ± 132 to 382 ± 76 mmol glucose/kg). Compared with the corresponding decrease in the male sample concentrations (from 405 ± 64 to 312 ± 42 mmol glucose/kg), no main effect of gender was found.
Difficulty was encountered in obtaining blood samples from several
subjects during the immersion and was attributed to cold-induced vasoconstriction in the subject's forearm. Consequently, the
statistical analysis was limited to comparison of the pre- and
postimmersion values. Blood analyses for the men were further limited
to FFA,
-OH, glycerol, glucose, and lactate (Table
4). FFA,
-OH, glycerol, and lactate
concentrations increased significantly during the immersion in subgroup
S90. Gender comparisons in subgroup S90 revealed a greater increase in
FFA (119.7 vs. 36.2%), glycerol (255 vs. 54.8%), and glucose (15.9 vs.
3.7%) in women than in men. There was no significant gender
difference in the magnitude of plasma volume change (Table 4).
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The following results pertain to the four to five women in subgroup S90
from whom pre- and postimmersion blood samples were obtained (Table 4).
Although cold water immersion did not affect the levels of
-OH,
epinephrine, and glucagon, significant increases were observed in all
other metabolite and hormone concentrations (i.e., FFA, glycerol,
glucose, insulin, lactate, and norepinephrine). The decrease in plasma
volume (19.3 ± 4.7%) may be partly responsible for the increased
blood metabolite levels of glucose and norepinephrine. However, the
changes in the concentrations of FFA (120%), glycerol (255%), insulin
(41%), and lactate (163%) were too large to be attributed only to the
change in hemoconcentration.
Table 5 summarizes the responses by
gender of the subjects selected to have similar BF and to have
completed
60 min of immersion (subgroup SBF). The variables were the
same as those reported by McArdle et al. (19) for
comparative purposes and also include %fatox and muscle
Gly. No significant gender differences were found in any of these
variables. However, the analysis for
Gly (on the basis of values
before and 90 min after immersion) excluded one woman who was immersed
for only 60 min. In addition, an analysis of the blood samples taken
for all subjects in subgroup SBF before and after 60 min of immersion
indicated metabolite concentrations that mirrored those shown in Table
4. Specifically, similar gender differences were found in FFA,
glycerol, glucose, and lactate, and a main effect of time was found in
the same components except for glucose. These results, however, must be
weighed against the small number (i.e., 2-5) of blood samples
involved.
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DISCUSSION |
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Although no difference in the rate of shivering heat production
between genders emerged in our study, the pooled data indicated a
significant correlation between
shiv and BF. That an
improvement in fit was further obtained by the attenuation of
(Eq. 3) confirms the earlier finding of such
a dependency (32). Because no difference was found in the
proportionality constant A between genders (Eq. 3), it is concluded that the shivering metabolic drive was not
different, at least when Tre = 36.8°C during
immersion to neck level in 18°C water.
Cold exposure has been shown to be a significant stimulus for lipolysis
and glycogenolysis (17, 18, 35). These earlier findings
are substantiated in the present study by the changes observed in FFA,
glycerol,
-OH, lactate, and muscle glycogen content during cold
water immersion. Furthermore, the assessment of fatox and
CHOox supports the contention that the increased metabolic
demand during cold exposure is fueled by fatox and
CHOox.
Despite gender differences in body size, BF, total heat production, and the relative intensity of shivering, there were no gender differences in the relative contributions of fat and CHO to fueling metabolism over the 90-min immersion period (Table 3). Similar changes in muscle glycogen concentration during immersion also suggest that men and women relied on CHO to a similar extent during shivering.
The gender difference in plasma FFA, glycerol, and glucose might appear
to contradict the absence of a significant gender difference in
fatox. However, gender differences in these metabolite responses may reflect the greater relative intensity of shivering in
women (34 ± 5 and 26 ± 7%
O2 max for women and men, respectively)
rather than an inherent difference in the type of energy substrate that
is preferentially oxidized. To support this contention, statistical
analysis of the blood metabolites was performed on subjects in subgroup
S90Rel (subjects with similar relative shivering
intensities), and only glucose showed a significant gender difference,
although blood data were available only for three women and five men in
subgroup S90Rel. Furthermore, there was no gender
difference in muscle glycogen utilization in subgroup S90Rel.
Yet these results are in contrast to those reported by Pettit et al.
(23) involving 5°C air exposure. In that study involving nine women and eight men (mass = 55.6 and 76.6 kg, height = 165 and 178 cm, SA/mass = 0.0290 and 0.0254 m2/kg, and
BF = 23.2 and 19.5%, respectively; mass, height, and SA/mass are
significantly different), the ratio of %fatox to
%CHOox was 1.84 for women and only 1.19 for men. In the
present study, the ratio was similar for both genders (1.76 and 1.58, respectively, in subgroup S90 and 1.41 and 1.30, respectively, in
subgroup S90Rel). The greater cold stress during the entire
90 min of water immersion at 18°C in contrast to the 2 h of cold
air exposure at 5°C might account for the differences in substrate
utilization between the two studies. Indeed, Pettit et al. reported a
mean increase in
O2 of only 80% during
2 h of the cold air exposure compared with a >200% increase in
O2 during 90 min of immersion in our study. Total heat production for women and men in subgroup
S90Rel was twice that reported by Pettit et al. (1,213 vs.
681 kJ for women and 1,897 vs. 904 kJ for men), although the ratio of
total heat production in women to that in men was similar in both
studies (0.75 reported by Pettit et al. and 0.73 in the present study). Furthermore, when substrate utilization was analyzed during 30-min intervals, our data indicate that substrate selection in men shifted toward more fat and less CHO with time in subgroups S90 and
S90Rel (%fatox-to-%CHOox ratios
at the end of the first 30 min of immersion were 1.17 and 0.89, respectively, closer to the value of 1.19 reported by Pettit et al.).
Other explanations for the differences between the two studies may be
possible differences in the relative shivering intensities and/or
O2 max, although neither
O2 max nor subject training status was
reported in Pettit et al. (23). As is the case with
exercise, subjects shivering at a higher fraction of their
O2 max should demonstrate an increased
CHOox. Also, there is evidence that gender differences in
substrate utilization during exercise may be attenuated by physical
training (5, 7, 25). Such findings are not universal,
inasmuch as Tarnopolsky et al. (28) reported that
well-trained female endurance athletes demonstrated a preference for
lipid metabolism during submaximal exercise compared with male athletes.
Our results also contrast with those of Blatchford et al.
(2), who studied substrate utilization in six women and
six men during a 90-min walk at 35%
O2 max and reported a greater level of
fat utilization in the women. Although cold exposure was not involved,
their study was similar to the present investigation in terms of
duration and energy expenditure of the subjects. The disparity in
%fatox between the two studies raises the question of
whether it is valid to expect substrate utilization of exercising muscle to be similar to that of involuntarily shivering muscle when
O2 rates are the same as those addressed
by Tipton et al. (33).
Aside from the shift in substrate utilization observed in men, the only
other difference between responses of men and women related to the
rates of deep body cooling. Interestingly, although BF was different
between the two genders, it did not emerge as the dominant regressor
with regard to the rate of body cooling. Instead, SA/vol (which was not
different between the genders) did emerge as the dominant, although
weak, regressor. This seemingly anomalous result can be explained
through a closer inspection of the individual thermoregulatory
responses. The subjects (both genders) with the lowest SA/vol also
responded with the lowest
Tre/
t. In
subjects with the highest SA/vol,
Tre/
t
values were near the highest observed, yet %BF values were near the
average in their gender group. On the other hand, in subjects with the lowest %BF,
shiv values were the highest, which
would mitigate heat debt and body cooling rate. A striking example of
this was the male subject having the lowest %BF at 3.5%. This
individual (72.0 kg, 187 cm) responded to the water immersion with an
overall heat production of 2,466 kJ (or 34.2 kJ/kg, 35.5 kJ/kg LBM,
1,319 kJ/m2), which was markedly higher than the average
(Table 3).
Toner at al. (34) provided an alternative explanation regarding enhanced heat loss with an increasing SA/vol. Essentially, they found that differences in heat loss diminished with exercise (vs. during rest) in men immersed in 26°C water. These investigators hypothesized that the increased blood perfusion to the muscles attenuated the insulative value of the larger relative muscle mass of the low SA/vol group. This hypothesis helps explain why differences in the rates of deep body cooling were not observed between the same subjects used by McArdle et al. (19) when they exercised in cold water (20). Regardless of the mechanism involved, SA/vol nevertheless provides a valid index of the susceptibility to heat loss in resting individuals, as previously concluded by McArdle et al. (19).
Graham et al. (10) found no significant differences in
Tre/
t and an increase in
O2 relative to
Tre
between men and eumenorrheic women exposed to 5°C air for 60 min.
Subject characteristics of mass, SA, and BF were significantly
different between the genders. Although not provided, the mean SA/mass
values were ~0.0256 and 0.0281 m2/kg for the men and
women, respectively. Despite these physical differences, the lack of
differences in the subjects' cold response is consistent with our own
study if we consider subgroup S90, where the same physical
characteristics cited above were also significantly different between genders.
Few studies have reported the effects of the menstrual cycle on
thermoregulation in the cold. In a recent study, Gonzalez and Blanchard
(9) exposed six resting women (60.9 kg, 165 cm, 23.9% BF)
with clothing protection to a ramped decrease in air temperature during
the follicular and midluteal phases. Their finding of a higher
preexposure deep body temperature during the midluteal phase in the
lightly clothed trial is consistent with our findings. However, the
attenuation in shivering thermogenesis as a function of mean body
temperature during the midluteal phase compared with the follicular
phase was not evident in our study (through
shiv).
It is possible that the greater level of cold stress imposed on our
female subjects, in whom shivering thermogenesis was at least twice as
high, overwhelmed the effects observed by Gonzalez and Blanchard. In
fact, the predictive equations of shivering thermogenesis that these
investigators regressed are not applicable to conditions where mean
skin temperature is <31°C, as in our study.
The results of the responses of subgroup SBF (Table 5) contrast with those of McArdle et al. (19), who reported considerably higher rates of decrease in Tre in both genders having similar BF in addition to a significantly higher rate of decrease in Tre in their female than in their male subjects (1.6 vs. 1.1°C/h). The higher rate in women was attributed to a larger SA/mass, and the overall rates for both genders were probably the result of the lack of transient rise in Tre. The absence of a transient rise seems unusual given that cutaneous vasoconstriction, which normally causes a transient rise in Tre (4), should have occurred despite the slightly warmer water temperature (20°C) used. Indeed, the data reported by Martineau (16) and Young et al. (39) for men immersed to neck level in 18°C stirred water support this expectation. A transient rise in Tre (mean ~0.07°C) was observed in the former study in all but one man [n = 14; time to maximum Tre = 31.6 ± 23.2 (SD) min after the start of immersion]. Young et al. showed a mean (n = 7) transient increase of ~0.4°C after 30 min of immersion. On the other hand, Kollias et al. (15) showed no transient increase in women of average BF (n = 3, 22.2% BF) immersed to neck level in 20°C stirred water, whereas obese women (n = 7, 34.0% BF) showed a transient rise. There is no obvious explanation for these disparities other than subject variability, possible differences in subject preparation before the immersion, and/or different degrees of cold stress due to differences in water temperature and turbulence level. Finally, no difference in the rate of deep body cooling was found between genders among all the subjects who completed 90 min of immersion in our study (subgroup S90), indicating a consistency in the cooling response during the latter stage of the immersion.
Furthermore, the metabolic responses of the SBF subjects were higher
than those reported by McArdle et al. (19).
O2 rates averaged 0.78 and 0.60 l/min
for the respective studies (pooled data). The lower rate for the latter
study helps explain the reported higher rate of deep body cooling
(average respective values of
Tre/
t were
0.36 and
1.35°C/h). However, these large differences cannot be
easily explained by differences in body characteristics [respective
average values for our subjects (n = 11) and those of
McArdle et al. (n = 4) were as follows: mass = 73.6 and 68.7 kg, height = 175 and 170 cm, SA/mass = 0.0263 and 0.0267 m2/kg, and BF = 16.9 and 17.7%]. Gross
methodological differences in subject preparation and immersion
conditions are not readily apparent between the two studies, aside from
the small difference in water temperatures used (18 vs. 20°C).
Despite these disparities, including differences in the rate of body
cooling, both studies are in agreement that thermoregulatory variations
are explainable by anthropometric variations.
The aims of this study were to compare the rates of body cooling and
energy metabolism of women and men immersed in cold water and to
determine whether gender-related adjustments are necessary for
prediction models of cold exposure survival time. On the basis of the
above findings, we accept the first hypothesis that women and men
exhibit similar changes in body cooling and
during cold water
immersion at rest when subject responses are corrected for BF and size.
On the other hand, we must reject the hypothesis that women metabolize
a higher percentage of fat during cold water immersion lasting 90 min.
The consequences of these findings with regard to modeling survival
time for sedentary cold exposure is that no adjustments are necessary
if BF and SA/vol are taken into account. That the %fatox
was not different between women and men refutes a potential gender
advantage with regard to CHO sparing during shivering thermogenesis.
| |
ACKNOWLEDGEMENTS |
|---|
The authors gratefully acknowledge the US Army Medical Research and Materiel Command (Ft. Detrick, Frederick, MD) for support in this research (carried out under Contract DAMD17-96-C-6128). The authors also acknowledge the expert assistance of I. Smith, D. Kerrigan-Brown, LCDR R. Bordeleau, R. Limmer, and A. Keefe (Defence and Civil Institute of Environmental Medicine) during the experimental phase of this work. Special appreciation is also extended to Dr. J. Zamecnik for the analysis of blood catecholamine concentrations.
| |
FOOTNOTES |
|---|
The views, opinions, and/or findings contained in this manuscript are those of the authors and should not be construed as an official Department of National Defence (Canada) or Department of Defense (United States) position, policy, or decision, unless so designated by other official documentation. This manuscript has been approved for public release; distribution is unlimited.
Address for reprint requests and other correspondence: P. Tikuisis, Defence and Civil Institute of Environmental Medicine, 1133 Sheppard Ave., West, PO Box 2000, Toronto, ON, Canada M3M 3B9 (E-mail: peter.tikuisis{at}dciem.dnd.ca).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 22 November 1999; accepted in final form 27 May 2000.
| |
REFERENCES |
|---|
|
|
|---|
1.
Bergstrom, J.
Muscle electrolytes in man.
Scand J Clin Invest
68 Suppl:
1-110,
1962.
2.
Blatchford, FK,
Knowlton RG,
and
Schneider DA.
Plasma FFA responses to prolonged walking in untrained men and women.
Eur J Appl Physiol
53:
343-347,
1985[ISI][Medline].
3.
Boobis, LH,
and
Maughan R.
A simple one-step enzymatic fluorometric method for the determination of glycerol in 20 µl of plasma.
Clin Chim Acta
132:
173-179,
1983[ISI][Medline].
4.
Burton, AC,
and
Edholm OG.
Man in a Cold Environment. New York: Hafner, 1969, p. 132.
5.
Costill, DL,
Fink WJ,
Getchell LH,
Ivy JL,
and
Witzmann FA.
Lipid metabolism in skeletal muscle of endurance-trained males and females.
J Appl Physiol
47:
787-791,
1979
6.
Dill, DB,
and
Costill DL.
Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration.
J Appl Physiol
37:
247-248,
1974
7.
Friedmann, B,
and
Kinderman W.
Energy metabolism and regulatory hormones in women and men during endurance exercise.
Eur J Appl Physiol
59:
1-9,
1989.
8.
Froberg, K,
and
Pedersen PK.
Sex differences in endurance capacity and metabolic response to prolonged, heavy exercise.
Eur J Appl Physiol
52:
446-450,
1984.
9.
Gonzalez, RR,
and
Blanchard LA.
Thermoregulatory responses to cold transients: effects of menstrual cycle in resting women.
J Appl Physiol
85:
543-553,
1998
10.
Graham, TE,
Viswanathan M,
Van Dijk JP,
Bonen A,
and
George JC.
Thermal and metabolic responses to cold by men and by eumenorrheic and amenorrheic women.
J Appl Physiol
67:
282-290,
1989
11.
Green, HJ,
Fraser IG,
and
Ranney DA.
Male and female differences in enzyme activities of energy metabolism in vastus lateralis muscle.
J Neurol Sci
65:
323-331,
1984[ISI][Medline].
12.
Horton, TJ,
Pagliassotti MJ,
Hobbs K,
and
Hill JO.
Fuel metabolism in men and women during and after long-duration exercise.
J Appl Physiol
85:
1823-1832,
1998
13.
Jones, PR,
Wilkinson S,
and
Davies PSW
A revision of body surface estimations.
Eur J Appl Physiol
53:
376-379,
1985.
14.
Karlsson, J.
Lactate and phosphagen concentrations in working muscle of man.
Acta Physiol Scand
358 Suppl:
7-21,
1971.
15.
Kollias, J,
Barlett L,
Bergsteinova V,
Skinner JS,
Buskirk ER,
and
Nicholas WC.
Metabolic and thermal responses of women during cooling in water.
J Appl Physiol
36:
577-580,
1974.
16.
Martineau, L.
Substrate Availability and Temperature Regulation During Cold Water Immersion in Humans (PhD thesis). Toronto, ON, Canada: University of Toronto, 1990.
17.
Martineau, L,
and
Jacobs I.
Muscle glycogen utilization during shivering thermogenesis in humans.
J Appl Physiol
65:
2046-2050,
1988
18.
Martineau, L,
and
Jacobs I.
Muscle glycogen availability and temperature regulation in humans.
J Appl Physiol
66:
72-78,
1989
19.
McArdle, WD,
Magel JR,
Gergley TJ,
Spina RJ,
and
Toner MM.
Thermal adjustment to cold-water exposure in resting men and women.
J Appl Physiol
56:
1565-1571,
1984
20.
McArdle, WD,
Magel JR,
Spina RJ,
Gergley TJ,
and
Toner MM.
Thermal adjustment to cold-water exposure in exercising men and women.
J Appl Physiol
56:
1572-1577,
1984
21.
Maughan, R.
A simple, rapid method for the determination of glucose, lactate, pyruvate, alanine, 3-hydroxybutyrate and acetoacetate on a single 20-µl blood sample.
Clin Chim Acta
122:
231-240,
1982[ISI][Medline].
22.
Peronnet, F,
and
Massicotte D.
Table of nonprotein respiratory quotient: an update.
Can J Sport Sci
16:
23-29,
1991[ISI][Medline].
23.
Pettit, SE,
Marchand I,
and
Graham T.
Gender differences in cardiovascular and catecholamine responses to cold-air exposure at rest.
Can J Appl Physiol
24:
131-147,
1999[ISI][Medline].
24.
Phillips, SM,
Atkinson SA,
Tarnopolsky MA,
and
MacDougall JD.
Gender differences in leucine kinetics and nitrogen balance in endurance athletes.
J Appl Physiol
75:
2134-2141,
1993
25.
Powers, SK,
Eilwy W,
and
Howley ET.
Comparison of fat metabolism between trained men and women during prolonged aerobic work.
Res Q Exerc Sport
51:
427-431,
1980[ISI][Medline].
26.
Rennie, DW,
Covino BG,
Howell BJ,
Hong SH,
Kang BS,
and
Hong SK.
Physical insulation of Korean diving women.
J Appl Physiol
17:
961-966,
1962
27.
Siri, WE.
Body composition from fluid spaces and density: analysis of methods.
In: Techniques for Measuring Body Composition, edited by Brozek J,
and Henschel A.. Washington, DC: Natl. Acad. Sci. Natl. Res. Council, 1961, p. 223-244.
28.
Tarnopolsky, LJ,
MacDougall JD,
Atkinson SA,
Tarnopolsky MA,
and
Sutton JR.
Gender differences in substrate for endurance exercise.
J Appl Physiol
68:
302-308,
1990
29.
Tarnopolsky, MA,
Atkinson SA,
Phillips SM,
and
MacDougall JD.
Carbohydrate loading and metabolism during exercise in men and women.
J Appl Physiol
78:
1360-1368,
1995
30.
Tikuisis, P.
Predicting survival time for cold exposure.
Int J Biometeorol
39:
94-102,
1995[ISI][Medline].
31.
Tikuisis, P.
Prediction of survival time at sea based on observed body cooling rates.
Aviat Space Environ Med
68:
441-448,
1997[Medline].
32.
Tikuisis, P,
and
Giesbrecht GG.
Prediction of shivering heat production from core and mean skin temperatures.
Eur J Appl Physiol
79:
221-229,
1999.
33.
Tipton, MJ,
Franks GM,
Meneilly BS,
and
Mekjavic IB.
Substrate utilization during exercise and shivering.
Eur J Appl Physiol
76:
103-108,
1997.
34.
Toner, MM,
Sawka MN,
Foley ME,
and
Pandolf KB.
Effects of body mass and morphology on thermal responses in water.
J Appl Physiol
60:
521-525,
1986
35.
Vallerand, AL,
and
Jacobs I.
Rates of energy substrate utilization during human cold exposure.
Eur J Appl Physiol
58:
873-878,
1989.
36.
Vallerand, A,
Zamecnik J,
and
Jacobs I.
Plasma glucose turnover during cold stress in humans.
J Appl Physiol
78:
1296-1302,
1995
37.
Wagner, JA,
and
Horvath SM.
Influences of age and gender on human thermoregulatory responses to cold exposures.
J Appl Physiol
58:
180-186,
1985
38.
Wissler, EH.
Mathematical simulation of human thermal behaviour using whole-body models.
In: Heat Transfer in Medicine and Biology, edited by Shitzer A,
and Eberhart RC.. New York: Plenum, 1985, vol. 1, p. 347-355.
39.
Young, AJ,
Muza SR,
Sawka MN,
Gonzalez RR,
and
Pandolf KB.
Human thermoregulatory responses to cold air are altered by repeated cold water immersion.
J Appl Physiol
60:
1542-1548,
1986
40.
Zamecnik, J.
Quantitation of epinephrine, norepinephrine, dopamine, metanephrine and normetanephrine in human plasma using negative ion chemical ionization GC-MS.
Can J Anal Sci Spectrosc
42:
106-112,
1997.
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