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1 Département de Biologie and 3 École des Sciences de l'Activité Physique, Université d'Ottawa, Ottawa, Ontario K1N 6N5; 2 Département de Kinésiologie, Université de Montréal, Montréal, Québec H3C 3J7; 4 Département de Kinanthropologie, Université du Québec à Montréal, Montréal, Québec H3C 3P8; and 5 Département des Sciences de l'Activité Physique, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada G9A 5H7
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The relative roles of circulatory glucose, muscle glycogen, and lipids in shivering thermogenesis are unclear. Using a combination of indirect calorimetry and stable isotope methodology ([U-13C]glucose ingestion), we have quantified the oxidation rates of these substrates in men acutely exposed to cold for 2 h (liquid conditioned suit perfused with 10°C water). Cold exposure stimulated heat production by 2.6-fold and increased the oxidation of plasma glucose from 39.4 ± 2.4 to 93.9 ± 5.5 mg/min (+138%), of muscle glycogen from 126.6 ± 7.8 to 264.2 ± 36.9 mg glucosyl units/min (+109%), and of lipids from 46.9 ± 3.2 to 176.5 ± 17.3 mg/min (+376%). Despite the observed increase in plasma glucose oxidation, this fuel only supplied 10% of the energy for heat generation. The major source of carbohydrate was muscle glycogen (75% of all glucose oxidized), and lipids produced as much heat as all other fuels combined. During prolonged, low-intensity shivering, we conclude that total heat production is unequally shared among lipids (50%), muscle glycogen (30%), plasma glucose (10%), and proteins (10%). Therefore, future research should focus on lipids and muscle glycogen that provide most of the energy for heat production.
energy metabolism; shivering thermogenesis; heat loss; plasma glucose oxidation; stable isotopes
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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DURING ENVIRONMENTAL
COLD exposure in adult humans, a decrease in core temperature is
prevented by increasing heat production (
prod) via shivering thermogenesis.
Involuntary muscle contractions during shivering are mainly fueled by
carbohydrates (CHO) and lipids, whereas the contribution of protein
oxidation remains minor (~10%) (16, 36, 42).
However, the respective importance of CHO and lipid oxidation has not
been clearly established. For example, some researchers imply that CHO
is the preferred fuel in the cold (~60% of total
prod) (12, 13, 20, 36, 37, 39,
41-43), whereas others show a greater reliance on lipids (~60% of total prod)
(21-23, 33, 45). Possible reasons for such
discrepancies between studies are differences in shivering intensity
(but see DISCUSSION), cooling protocol, and/or nutritional state. Over the last decade, most studies of fuel selection during shivering have focused on CHO metabolism as a probable limiting factor
for prod. However, two important issues
remain unresolved: 1) the relative contributions of hepatic
glucose and muscle glycogen to total CHO oxidation have not been
quantified, and 2) the potentially important role of
triacylglycerol stores (adipose tissue, liver, and muscle) has often
been underrated, particularly during prolonged, low-intensity shivering.
Plasma glucose and muscle glycogen have both been shown to play
significant roles in prod during cold
exposure (16). Vallerand et al. (42, 43)
calculated that plasma glucose and muscle glycogen would contribute
equally to total CHO oxidation, assuming that 100% of hepatic glucose
production (Ra Glu) is oxidized. However, as pointed out by
these authors, at such low rates of oxygen consumption
(
O2), this assumption is probably not
met because nonoxidative glucose disposal could be important. Studies in which measurements of Ra Glu and plasma glucose
oxidation were carried out simultaneously indicate that nonoxidative
disposal ranges between 25% Ra Glu during submaximal
exercise [45% maximal O2
(O2 max)] and 70% Ra Glu
at rest (11).
A series of studies have shown that 90 min of cold-water immersion cause a reduction of glycogen concentration in biopsies from the vastus lateralis (17, 21-24, 47). Unfortunately, estimating total use of muscle glycogen, at the whole organism level, from small biopsy samples is inaccurate at best, because 1) glycogen content varies greatly between and within individual muscles and 2) the specific muscles involved in heat generation and their level of recruitment are unknown. Therefore, the exact contributions of plasma glucose and muscle glycogen are presently unclear because their rates of oxidation have never been measured directly during shivering.
The purpose of this study was to quantify the respective contributions
of plasma glucose, muscle glycogen, and lipid oxidation to total
prod during prolonged, low-intensity
shivering by using a combination of stable isotope and indirect
calorimetry methods. In human subjects exposed to low-intensity
shivering [10°C for 2 h with a liquid conditioned suit (LCS)],
we hypothesize that plasma glucose oxidation will play a lesser role
than previously suggested (42, 43) and that lipid
oxidation will be a major pathway for heat generation because of the
small change in metabolic rate observed in the cold.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects.
Six healthy and trained men volunteered for this study, which was
approved by the Health Sciences Ethics Committee of the University of
Ottawa, and written consent was obtained from the participants. Percent
body fat [underwater weighing; Brosek et al. (5)] and
O2 max were measured with a progressive treadmill protocol 5-7 days before the experiments. Physical
characteristics of the subjects are presented in Table
1.
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Experimental protocol. Experiments were conducted between 900 and 1300 after 36 h without heavy physical activity. The last evening meal was standardized (~988 kcal, ~52% CHO, ~18% lipids, ~30% proteins), and subjects were asked to report to the laboratory the next morning (900) after a 12- to 14-h fast. Ingestion of CHO from plants naturally rich in 13C (C4 photosynthetic cycle) was avoided to maintain low 13C background enrichment in plasma glucose and expired CO2. Care was taken to minimize thermal stimuli between awakening and the start of the experiment (i.e., avoid exposure to hot or cold temperatures, very-low-intensity exercise during transit from home to the laboratory). On their arrival in the laboratory, subjects were instrumented with thermal probes and an indwelling catheter (18-gauge, 32 mm, Medical, Arlington, TX) placed in an antecubital vein (left arm) for blood sampling and were fitted with a LCS (Three Piece Delta Temax, Pembroke, ON). Subjects were then asked to empty their bladder [time (t) = 0 min] and sit quietly for 2 h at 28.1 ± 0.3°C (758 ± 4 mmHg, 20-30% relative humidity). After this habituation period, they were transferred to an environmental chamber (11.1 ± 0.1°C, 760 ± 4 mmHg, 40-57% relative humidity), and a 10°C water perfusion was started through the LCS by using a temperature-controlled circulation bath (Endocal, NESLAB; and model 200-00, Micropump, Vancouver, WA). Thermal response, metabolic rate, and fuel utilization were measured at 28°C and during the subsequent 2-h cold exposure.
Thermal response.
Central body temperature [esophageal temperature (Tes)]
was monitored continuously by using a pediatric Tes probe
(Mon-a-therm general purpose, Mallinckrodt Medical, St. Louis, MO),
which was inserted through the nose to a depth placing the tip of the
thermocouple at the level of the left atrium, or one-fourth of the
standing height of the subject (25). Heat flux transducers
(Concept Engineering, Old Saybrook, CT) were used to estimate skin
temperature and nonevaporative heat flux from the forehead, chest,
biceps, forearm, abdomen, lower and upper back, front and back calf,
quadriceps, hamstrings, and finger. Mean skin temperature
(
) and
convective heat exchange (
). Respiratory evaporative
(
resp) and convective heat exchanges
(resp) were determined from ventilation
(E) measurements by estimating water loss via the
respiratory tract (2,411.3 J heat/g evaporated water) (4).
It was assumed that evaporative heat loss
(loss) from the skin was negligible under the LCS. Whole body loss (in watts) was
calculated as follows
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(1) |
Metabolic rate and fuel utilization.
E, O2, and carbon
dioxide production (CO2) were determined
by open-circuit spirometry (250 liters, chain-compensated gasometer,
Warren Collins, Braintree, MA). All expired gas collections were made
at ambient temperature outside the experimental chamber. A mouthpiece,
a unidirectional valve (2700 series, Hans Rudolph, Kansas City, MO),
and a 44-mm plastic tube were used to direct all expired gases to the
collection tank. Expired gases were collected for 5 min every 30 min at
28°C and during cold exposure. E (l/min, BTPS) was calculated from the displacement of the cylinder
and corrected for temperature and pressure. Oxygen and carbon dioxide concentrations in dry expired gases (CaSO4, Drierite, 8 mesh, Fisher Scientific, Ottawa, ON) were determined directly from the spirometer by using calibrated electrochemical gas analyzers (AMETEK model S-3A/1 and CD 3A, Applied Electrochemistry, Pittsburgh, PA).
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(2) |
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(3) |
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(4) |
CO2 and
O2 (Eqs. 2 and 3)
were corrected for the volumes of O2 and CO2
corresponding to protein oxidation (1.010 and 0.843 l/g, respectively),
and Ureaurine is urinary urea excretion.
Estimates of RPox (Eq. 4) were made
by measuring Ureaurine from urine samples
collected for a period of 120 min at 28 and 10°C. A correction for
urea accumulation in plasma was not required because plasma levels did
not change during cold exposure (P = 0.28; paired
t-test) (18). Urinary and plasma urea
concentrations were determined on a Synchron Clinical System (CX7,
Beckman, Anaheim, CA). Respective contributions of glucose, lipid, and
protein oxidation to total prod were
calculated by using energy potentials of 16.3, 40.8, and 19.7 kJ/g,
respectively (9, 28).
Plasma glucose oxidation. For the measurement of plasma glucose oxidation, the subjects ingested 10 g of glucose [7 × 1.4 g in 100 ml of water; corn sugar, with a ratio of 13C to C (13C/C) = 0.01098] artificially enriched with 13C ([U-13C]glucose, 13C/C >99%, Isotec, Miamisburg, OH) to obtain a final 13C/C of 0.0476 isotopic composition of exogenous glucose solution (Rexo).
After baseline 13C/12C in plasma and expired CO2 (t = 30 min) were measured, subjects ingested the first dose of [13C]glucose. Subsequent doses were then taken every 30 min until the end of the experiment. Isotopic composition of plasma glucose and expired CO2 were determined in blood and expired gas samples every 30 min before the ingestion of the next dose. On collection, blood samples were put on ice, spun in a refrigerated centrifuge, and separated, and the plasma was kept frozen at
20°C until analysis.
The isotopic composition of plasma glucose (Rglu) was
measured as previously described (29). Briefly,
plasma samples (1 ml) were deproteinized (BaOH: 1.5 ml, 0.3 N; and
ZnSO4: 1.5 ml, 0.3 N) and centrifuged to precipitate the
proteins. Double-bed ion exchange chromatography with superimposed
columns (resins: AG 50W-X8 H+, 200-400 mesh, and AG
1-X8 chloride, 200-400 mesh) was used to isolate plasma glucose.
After evaporation, glucose was combusted (60 min at 400°C) in the
presence of CuO, and CO2 was recovered. Measurements of
13C/12C in expired CO2 and in
CO2 obtained from glucose combustion were determined in a
prism mass spectrometer (VG, Manchester, UK). Isotopic composition was
expressed as 
difference (
) compared with Pee Dee Belemnitella-1
(PDB-1) Chicago standard with the equation of Craig (6)
![&dgr;<SUP>13</SUP>C‰<IT>=</IT>{[(<SUP>13</SUP>C<IT>/</IT><SUP>12</SUP>C<SUB>sample</SUB>)<IT>/</IT>(<SUP>13</SUP>C<IT>/</IT><SUP>12</SUP>C<SUB>standard</SUB>)]<IT>−</IT>1}<IT>×</IT>10<SUP>3</SUP>](/content/vol93/issue1/fulltext/77/img006.gif)
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(5) |
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(6) |
CO2 is in l/min
(STPD), Rref is the isotopic composition of
expired CO2 at 28°C before ingestion of the first
[13C]glucose dose, k1 (0.7426 l/g) is the
volume of CO2 produced from the complete oxidation of
glucose (28), and k2 is the fractional recovery
at the mouth of CO2 produced in tissues. A fractional recovery of 13CO2 at the mouth (k2)
of 0.8 and 1 was used at 28°C and during cold exposure, respectively
(46). Because of the large size of the bicarbonate pool,
only values in the last 30 min at 28°C and at 10°C were used in the
calculation of plasma glucose oxidation rate (RGox-plasma).
This delay allows sufficient time for equilibrium of the
13C/12C to be attained in the bicarbonate pool
(27).
Plasma glucose oxidation was calculated from
13CO2 excretion and the isotopic enrichment of
plasma glucose by using the following equation (7, 46)
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(7) |
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(8) |
Blood analysis. Plasma glucose and lactate concentrations were measured spectrophotometrically at 340 nm on a Beckman DU 640 (2), whereas total plasma nonesterified fatty acid (NEFA) concentration was determined by using an analytic assay kit (NEFA C, Wako Chemicals, Osaka, Japan). Insulin concentration was measured by using a radioimmunoassay (#KTSP-11001, Medicorp, Montréal, PQ).
Statistical analyses.
Overall changes in Tes, 
sk,
loss, prod,
blood metabolite concentrations, expired CO2 and plasma
glucose isotopic enrichments, and gas exchange over time were assessed
by using a one-way ANOVA with replication. For each sampling time, a
Bonferroni t-test was used to detect potential differences
with control values observed at 28°C. Differences in metabolic fuel
utilization for CHO (RGox, RGox-exo,
RGox-plasma, RGox-mus, RGox-liver),
lipids (RFox), and proteins (RPox) over the
last 30 min at 28°C and during cold exposure were determined by using
two-tailed paired t-tests. Statistical differences
were considered significant when P 
0.05. All values given
are means ± SE (n = 6).
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Thermal response.
Changes in Tes and sk are presented in
Fig. 1. Whereas Tes remained
constant at 36.4 ± 0.1°C throughout the experiment, sk decreased from 34.0 ± 0.02 to 27.2 ± 0.02°C in the initial 90 min of cold exposure and did not change for
the last 30 min. Absolute loss and
prod increased by a maximum of 3.3-fold (77.7 ± 0.6 to 258.4 ± 10.6 W) and 2.6-fold (95.3 ± 2.2 to 243.8 ± 4.2 W), respectively (Fig.
2). After reaching a maximum 20 min after
the onset of cold exposure (t = 140 min),
loss decreased by 16% over the next 100 min (238.3 ± 0.6 W). Maximal prod
was reached after 90 min of cold exposure and stayed constant for the
remainder of the experiment. Observed shivering activity appeared minimal over the first 60 min of cold exposure but increased
progressively in the last hour.
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Metabolic response and fuel utilization.
Changes in E, O2, and
respiratory exchange ratio (RER) are shown in Fig.
3. E and
O2 increased by 2.4- and 2.6-fold, respectively (Fig. 3, A and B). A small decrease
in RER was observed during cold exposure, but it did not reach overall
statistical significance (one-way ANOVA with replication;
P = 0.075), averaging 0.84 ± 0.01 throughout the
experiment (Fig. 3C; 0.86 ± 0.01 at 28°C and
0.83 ± 0.02 between 150 and 180 min at 10°C).
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prod
throughout cold exposure are plotted in Fig.
4. Total lipid and CHO utilization
increased 3.8-fold (Fig. 4A; 39 ± 2 mg fatty acids/min
at 28°C to 177 ± 17 mg fatty acids/min at 10°C) and 2.2-fold
(Fig. 4B; 165 ± 9 mg glucose/min at 28°C to 358 ± 41 mg glucose/min at 10°C), respectively. Protein utilization was
not affected significantly by the change in temperature and averaged
62.1 ± 3.1 mg/min at 28°C and 77.7 ± 5.0 mg/min at
10°C. A trend toward an increase in the relative contribution of
lipids and a decrease in the relative contribution of CHO during cold exposure was noticed in the cold. However, these observed changes failed to reach statistical significance (Fig. 4B;
P = 0.10). In contrast, the relative contribution of
protein oxidation to total prod decreased
significantly throughout cold exposure, from 21.2 ± 0.8% at
28°C to 10.7 ± 0.8% at 10°C.
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Plasma concentrations.
Changes in plasma concentrations of insulin, glucose, lactate, and NEFA
during cold exposure are presented in Fig.
5. Insulin and glucose concentrations
were not affected by the change in temperature (Fig. 5, A
and B). After 90 min of cold exposure, plasma lactate and
NEFA concentrations were increased 1.8-fold (0.90 ± 0.11 to
1.61 ± 0.15 mM, Fig. 5C) and 2.5-fold (0.21 ± 0.03 to 0.52 ± 0.01 mM, P < 0.001; Fig.
5D), respectively, over control values at 28°C.
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CHO oxidation: plasma glucose vs. muscle glycogen.
The amount of [13C]glucose administered provided a strong
signal in CO2 and plasma glucose to quantify circulatory
glucose oxidation (Fig. 6, A
and B). The change in isotopic enrichment of expired CO2 and plasma glucose ([-13C]PDB-1), as
well as the calculated values of RGox-plasma and RGox-exo obtained throughout the experiment are plotted in
Fig. 6. At 28°C, 60 min after glucose ingestion,
RGox-plasma averaged 39.4 ± 2.4 mg/min
(RGox-liver was 37.7 ± 2.3 mg/min and
RGox-exo only 2.1 ± 0.4 mg/min) and increased
progressively throughout cold exposure to reach a maximal value of
107.3 ± 6.1 mg/min (RGox-liv was 84.0 ± 6.0 mg/min and RGox-exo only 9.6 ± 5.5 mg/min; Fig. 6C).
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prod did
not change when subjects were exposed to the cold, whereas that of
RFox increased 1.5-fold and that of RPox
decreased twofold.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Even though plasma glucose oxidation is strongly stimulated during
low-intensity shivering (+138%), we show that this fuel only plays a
minor role in total prod (10%
prod). Also, muscle glycogen oxidation
doubled during mild cold exposure, providing 75% of total CHO
oxidized. Interestingly, lipids are the most important fuel, showing
close to a fourfold increase in oxidation rate and accounting for the
production of as much heat as all other metabolic substrates combined.
This study quantifies the RGox-plasma during cold exposure.
It shows that RGox-plasma is stimulated in direct
proportion to metabolic rate (Table 2, Fig. 3B) and that its
relative contribution to total prod
remains constant and low. During low-intensity shivering, the
contribution of plasma glucose is as minor as that of proteins (Table
2). In contrast, muscle glycogen stores play a more prominent role,
providing three times more glucose units for oxidation than the
circulation (Table 2).
The [13C]glucose ingestion technique selected for this study allowed us to quantify the role of circulatory glucose as an oxidative fuel to support shivering. Results show that, during mild cold exposure, circulatory glucose plays a more minor role than previously suggested when oxidation was estimated from measurements of Ra Glu (42, 43). As anticipated, neglecting to subtract nonoxidative glucose disposal from Ra Glu caused a significant overestimation of glucose oxidation rates. Under conditions of steady state (i.e., when plasma glucose concentration remains constant over time), Ra Glu and glucose disposal were matched. However, the disposal of glucose can take place through two distinct metabolic pathways: oxidation (RGox-plasma) and storage (or nonoxidative disposal). At low metabolic rates (rest, mild exercise, or low-intensity shivering), nonoxidative disposal represents a significant fraction of Ra Glu, and, therefore, a direct measurement of oxidation is necessary to quantify the role of plasma glucose as an oxidative fuel.
The stimulation of circulatory glucose utilization in the cold was not accompanied by changes in plasma glucose or insulin concentrations (Fig. 5, A and B), as previously observed in several other studies (23, 34, 38, 42, 43). Constant glycemia shows that Ra Glu and glucose disposal were both increased in parallel. The increase in glucose uptake taking place during cold exposure is, therefore, not dependent on changes in plasma insulin. However, it may be the consequence of a cold-induced increase in insulin sensitivity and/or GLUT translocation, as previously proposed for humans (35, 40) as well as animals (32, 44). An insulin-independent control of glucose uptake may allow an increase in glucose delivery specifically to shivering muscles rather than indiscriminately to all insulin-sensitive tissues.
The major source of CHO was muscle glycogen, providing three-fourths of
all of the glucose oxidized in the cold (Table 2). Even though whole
body glycogen stores only represent 1% of total energy stores,
shivering studies in humans have shown that glycogen availability,
modified through diet or exercise, affects fuel selection (22,
33, 47) and possibly body cooling rate (22). In
these studies, whereas prod was the same
among depleted glycogen, loaded glycogen, and normal glycogen controls
immersed in 18°C water, RER values were significantly lower for
depleted glycogen than for loaded glycogen and glycogen controls,
indicating a compensatory shift to a greater relative use of lipids
when glycogen reserves are depleted (22, 33, 47). However,
these studies do not provide information on the effect of glycogen
availability on the relative importance of RGox-plasma and
RGox-mus to total CHO oxidation.
Oxidizing lipids to generate heat.
The dual role of lipids as a heat insulation layer and as a large,
energy-dense metabolic fuel (>95% of total energy stored) has been
recognized for a long time (31). However, the quantitative importance of lipids as a substrate to support prolonged, low-intensity shivering has been somewhat neglected because, over the last decade, most studies have focused on CHO-dependent
prod (16). Our results show
that RFox provides 50% of all of the heat produced (Table
2). The relative importance of lipid oxidation measured here is
consistent with several studies (15, 21-23, 33, 45), whereas many others found that CHO oxidation is dominant (12, 13,
20, 36, 37, 39, 41-43). In all of these studies, it is very
interesting to note that the reported dominance of either CHO or lipids
has no clear link with differences in shivering intensity but seem to
be correlated with the cooling protocol. Whereas subjects exposed to
cool air used CHO preferentially (~60% of
prod; Refs. 12,
13, 20, 36, 37,
39-43), those cooled by water immersion or by LCS
favored lipid utilization (~60% of prod; Refs. 15,
21-23, 33, 45).
Physiological reasons for such a difference are unclear, and further
research will be needed to explain it.
O2 max),
the observed utilization of lipids is not that surprising. Exercise
studies reveal that lipid oxidation predominates for prolonged work at all intensities <50% O2 max (1,
4, 30). Therefore, even at the highest possible metabolic rates
reached during maximum shivering [~5 times resting metabolic rate or
~40% O2 max (10)],
lipids may still play a significant role in heat generation, if fuel
selection patterns are identical between exercise and shivering.
The large increase in lipid utilization observed here during
low-intensity shivering (Table 2) is a strategy to spare limited CHO
reserves. Any increase in the relative use of lipids allows the
maintenance of prod for longer and,
therefore, improves chances of survival in the cold. We can estimate
theoretical values for maximum cold endurance under the conditions of
our experiments, assuming that the relative use of the different fuels
remains the same as measured after 2 h of mild shivering. An
average adult man would be able to shiver at 245 W (Fig. 2) for ~20 h
under the specific conditions of the present study before depleting muscle glycogen reserves (assuming that 80% of muscle glycogen is
available for oxidation; mean muscle glycogen concentration = 100 mmol glucosyl units/kg wet mass; actively shivering muscle mass = 70% of 36 kg; RGox-mus = 18.4 µmol · kg
body mass
1 · min1; Table 2).
The stimulation of RFox (Table 2) found here was
accompanied by a twofold increase in circulatory NEFA levels (Fig.
5D) as observed in other studies (34, 37, 38, 42, 43,
45). Vallerand et al. (43) found that men exposed
to 5°C for 3 h showed a parallel increase in NEFA concentration
and NEFA disappearance rate. Together, these observations
suggest that the oxidation of circulatory NEFA increased throughout
cold exposure. However, the relative contributions of NEFA from the
circulation (adipose and liver) and from muscle triacylglycerols to the
fourfold increase in total fat oxidation remain to be established.
In conclusion, this study shows that total
prod during prolonged, low-intensity
shivering is unequally shared among lipids (50%), muscle glycogen
(30%), circulatory glucose (10%), and proteins (10%). Therefore, the
importance of plasma glucose oxidation is only minor, and future
research should focus on lipid and muscle glycogen stores that provide
most of the energy for prod.
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ACKNOWLEDGEMENTS |
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The authors acknowledge the excellent technical assistance provided by Caroline Proulx, Marie-Catherine Lamoureux, Martin Milot, Charlotte Weber, and Kevin Litchfield. We also thank the subjects of this study for their collaboration.
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FOOTNOTES |
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This work was funded by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC Canada) (to J.-M. Weber, G. P. Kenny, D. Massicotte, F. Péronnet, and C. Lavoie). F. Haman is the recipient of a NSERC scholarship.
Address for reprint requests and other correspondence: J.-M. Weber, Biology Dept., Univ. of Ottawa, 30 Marie Curie, Ottawa, Ontario, Canada K1N 6N5 (E-mail: jmweber{at}science.uottawa.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.
First published March 1, 2002;10.1152/japplphysiol.00773.2001
Received 23 July 2001; accepted in final form 19 February 2002.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Significantly different from maximal value reached during
cold exposure, P 
, Eq. 
, Eq. 
;
B) at 28°C and during whole body 10°C. FFA, free fatty
acid. Values are means ± SE. * Significantly different from
values at 28°C, P 
