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1 Rehabilitation and 2 Neurology, Department of Medicine, McMaster University, Hamilton, Ontario, Canada L8N 3Z5
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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We investigated the effect of endurance
training on whole body substrate, glucose, and glycerol utilization
during 90 min of exercise at 60% peak O2 consumption
(
O2 peak) in males and females.
Substrate oxidation was determined before and after 7 wk of endurance
training on a cycle ergometer, with posttesting performed at the same
absolute (ABS, W) and relative (REL,
%O2 peak) intensities.
[6,6-2H]glucose and [1,1,2,3,3-2H]glycerol
tracers were used to calculate the respective substrate tracee flux.
Endurance training resulted in an increase in
O2 peak for both males and females of
17 and 22%, respectively (P < 0.001). Females
demonstrated a lower respiratory exchange ratio (RER) both pretraining
and posttraining compared with males during exercise (P < 0.001). Glucose rate of appearance (Ra) and rate of
disappearance (Rd) were not different between males and
females. Glucose metabolic clearance rate (MCR) was lower at 75 and 90 min of exercise for females compared with males (P < 0.05). Glucose Ra and Rd were lower during
exercise at both ABS and REL posttraining exercise intensities compared
with pretraining (P < 0.001). Females had a higher
exercise glycerol Ra and Rd compared with males
both pre- and posttraining (P < 0.001). Glycerol
Ra was not different at either the ABS or REL posttraining
exercise intensities compared with pretraining. We concluded that
females oxidize proportionately more lipid and less carbohydrate during
exercise compared with males both pre- and posttraining, which was
cotemporal with a higher glycerol Ra in females.
Furthermore, endurance training resulted in a decrease in glucose flux
at both ABS and REL exercise intensities after endurance exercise training.
carbohydrate utilization; lipid utilization; training adaptations
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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ENDURANCE EXERCISE
TRAINING results in adaptive changes in muscle metabolic function
characterized by a decrease in carbohydrate utilization and an increase
in lipid oxidation when tested at the same absolute exercise intensity
(21, 28, 34). The reduction in the reliance on
carbohydrate oxidation during exercise includes a sparing of muscle
glycogen (27, 33, 34) and a decrease in the rates of
appearance and oxidation (13, 28, 34) of plasma glucose.
There is consistency in the observed increase in mitochondrial
potential and 
-oxidation maximal enzyme capacity (21,
33), yet controversy exists regarding the source of the oxidized
free fatty acids (FFA). For example, some studies have found an
increase in intramuscular triglyceride utilization (21, 33,
34), whereas others have found an increase in plasma FFA uptake
(1, 25) and peripheral adipocyte lipolytic sensitivity (6, 7). Although the metabolic adaptations to endurance exercise have been extensively reproduced (13, 27, 28,
32-34), almost all of these adaptations have been reported
in studies involving exclusively or predominantly male participants.
Consequently, less is known about the response of females to endurance
exercise training.
Cross-sectional studies have found gender differences in the metabolic response to submaximal endurance exercise characterized by a lower respiratory exchange ratio (RER) (14, 20, 31, 41) and attenuated muscle glycogen depletion (10, 40) for females compared with males. Although the results from these studies are generally consistent, there remains a controversy regarding the most appropriate method of matching the genders on the basis of oxygen consumption (i.e., relative to total vs. fat-free mass) and training history. A longitudinal design eliminates the issue of potential gender differences in training background by exposing males and females to a similar training stimulus.
McKenzie et al. (27) found that leucine and total carbohydrate oxidation was higher in males compared with females during exercise both before and after endurance exercise training. Another study reported that, compared with males, females had a higher glycerol rate of appearance and lower carbohydrate oxidation during exercise than were present before and after endurance exercise training (14). These latter studies suggested that there may be gender differences in the metabolic response to exercise before and after training (14, 27); however, this remains an incompletely characterized area of investigation.
The purpose of the present study was to investigate the effect of endurance training on whole body substrate oxidation and glucose and glycerol turnover during 90 min of exercise at 60% of peak oxygen uptake in both males and females. The longitudinal design allowed for the comparison of the metabolic response of males and females in the untrained as well as the trained state.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects.
Sixteen healthy volunteers (8 males and 8 females) participated in the
study (Table 1). Informed consent was
obtained after a description of the study and advisement of the risks
and benefits of participation, in accordance with and prior approval of
the Research Ethics Committee.
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Protocol.
A progressive exercise test on an electronically braked cycle ergometer
was used to determine peak oxygen consumption
(O2 peak), as previously described
(42). The O2 peak test
took place in the 2 wk before the initiation of the study.
O2 peak was used to estimate
the workload required to elicit 60% of the subject's
O2 peak for subsequent testing.
Detailed metabolic, dietary, and anthropometric data were collected
before (PRE) and after (POST) a 7-wk endurance exercise training
program. Exercise testing was completed at 60%
O2 peak PRE training and at the same
workload POST training (ABS; absolute trial). In addition, we completed
a posttraining exercise testing session at 60% of the new POST
training O2 peak (REL; relative trial). The order of the POST trials was randomized for each individual, and
trials were completed within 3-5 days of each other to ensure that
the females were tested in the early to midfollicular phase of the
menstrual cycle. The exercise program consisted of 7 wk of cycle
training with a 5:2 (exercise-rest day) protocol. Each session was 60 min in duration at an intensity of 60%
O2 peak. After 3 wk of training, a
second progressive exercise test was administered to reevaluate
O2 peak, and adjustments were made to
training intensities to ensure a progressive training stimulus for each subject.
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90 min) for the determination of the
natural background isotopic enrichment of glucose and glycerol. A
priming dose of glucose (17 µmol/kg) and glycerol (1.5 µmol/kg)
tracers were given, followed by a constant infusion at the rates of
~0.22 µmol · kg
1 · min1
and ~0.05
µmol · kg1 · min1 for
glucose and glycerol tracers, respectively. Subjects were infused for
90 min at rest, before the onset of exercise. At the onset of exercise,
the infusion rates were increased in a stepwise fashion to ~0.55 and
~0.125
µmol · kg1 · min1,
respectively, for glucose and glycerol tracers, as previously described
(4). The infusion rate remained at ~0.55 and ~0.125 µmol · kg1 · min1 for
glucose and glycerol tracers for the remainder of the 90 min of
exercise. Blood samples were drawn at 75 min after the initiation of
the constant infusion (15 min), at rest (0 min), and at 30, 60, 75, and 90 min during exercise. (Thus the first blood sample for tracer
kinetic determination was taken at 4 h and 15 min after the
consumption of the high-CHO snack drink described above.) Blood samples
were collected into heparinized tubes and centrifuged immediately, and
the plasma was stored at 50°C for subsequent analysis. For
catecholamine determination, 5 ml of whole blood were added to a tube
containing 100 µl of EDTA and reduced glutathione. The tube was
centrifuged at 2,000 g for 10 min, and the plasma was stored
at 80°C for subsequent analysis. Blood samples collected for
hormone analyses were allowed to stand for 10 min in untreated tubes
and then were centrifuged, and the serum was stored at 50°C for
subsequent analysis.
Respiratory measurements were made using a computerized open-circuit
gas collection system as described previously (42). Respiratory gases were collected at rest and at 30, 60, 75, and 90 min
of exercise. Heart rate was also monitored continuously throughout the
90 min of exercise and was recorded at the same time points as
respiratory gases. The proportions of CHO and lipid utilized were
calculated using the RER corrected for protein oxidation (11). Protein oxidation rates were estimated from leucine
oxidation rates measured in a previous study in our laboratory
(27), with the assumption that tissue protein contains 590 µmol of leucine/g.
Analysis. Plasma lactate and glucose concentrations were analyzed with a blood glucose and lactate analyzer (YSI model 2300 STAT Plus, Yellow Springs Instrument, Yellow Springs, OH). Plasma glycerol concentration was determined by using an enzymatic colorimetric assay [Triglyceride (GPO-Trinder), Sigma Diagnostics, St. Louis, MO].
Resting serum samples were analyzed for 17-estradiol, progesterone,
testosterone, and insulin. Insulin was also analyzed during exercise.
17-Estradiol, progesterone, testosterone, and insulin
were analyzed using a single incubation radioimmunassay (Coat-a-Count:
kit nos. TKE22, TKEP1, TKTE1, and TKIN5; Diagnostics Products, Los
Angeles, CA). Serum FFA concentrations were determined at rest and
during exercise using an enzymatic colorimetric assay (NEFAC-ACS, Wako
Chemicals, Richmond, VA). Catecholamines (epinephrine and
norepinephrine) were analyzed using high-performance liquid chromatography (injector WISP 710B and pump model 570, Waters, Milford,
MA) with electrochemical detection (Coulochem II, ESA, Chelmsford, MA),
as previously described (4).
Isotopic enrichment of glucose and glycerol was determined using gas
chromatography-mass spectrometry (GC model 6890 and MS model 5973, Hewlett-Packard, Fullerton, CA) of the pentaacetate and
tris-trimethylsilyl derivatives, respectively, as previously described
(4). Mass analysis was performed in the electron impact
ionization (Ei+) mode to monitor selected ions with a
mass-to-charge ratio (m/z) of 200 and 202 atomic mass units
(amu) for glucose enrichment and an m/z of 205 and 208 amu
for glycerol enrichment.
Rates of appearance (Ra) and disappearance (Rd)
of glucose and glycerol were calculated according to the Steele
equation (38), which was modified for use with stable
isotopes according to Romijn et al. (35), because the
amount of tracer infused is no longer considered negligible. Enrichment
and concentration data were fitted to curves by use of spline fitting
(35); then the kinetics were calculated as described in
the previous paragraph. The volume of distribution was assumed
to be 100 ml/kg for glucose and 230 ml/kg for glycerol
(35). We attempted to minimize the changes in enrichment
by increasing the infusion rate in step increments when exercise was
initiated, as previously described (4).
Statistical analysis.
The physical characteristics of the participants and the hormone
concentrations were analyzed using a two-way analysis of variance
(ANOVA). All other data were analyzed using a three-way ANOVA, with
gender being the between-factor variable, condition (PRE, ABS, and REL)
being the first within-factor variable, and time (t = 0, 30, 60, 75, 90 min) being the second within-factor variable. When
significance was obtained, the location of the difference was
determined using Newman-Keuls post hoc analysis. The level of
significance was set at P 
0.05. Values are presented as
means ±SE.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Physical characteristics.
Males had a significantly higher absolute
O2 peak than the females; however,
there was no significant difference between the genders in
relative O2 peak when expressed per kilogram of fat-free mass (FFM). Training resulted in a significant increase (P < 0.001) in
O2 peak for both males and females (Table 1). Male participants were heavier, taller, and leaner than the
female participants. Body mass and FFM were unchanged, whereas fat mass
and percent body fat decreased (P < 0.01) after training for both males and females (Table 1).
Diet. Total energy intake was not altered by training (Table 2). The proportion of energy derived from CHO was not changed, whereas that derived from fat was decreased and that from protein was increased, after training. Males had a higher total energy intake compared with females, yet the proportion of energy derived from fat, CHO, and protein was not different between males and females (Table 2).
Basal hormone levels.
Seven weeks of endurance training had no effect on resting serum
testosterone concentration in males (19.3 ± 1.8 
21.5 ± 2.8 nmol/l) or females (1.6 ± 0.3 1.3 ± 0.3 nmol/l),
and males had a significantly higher testosterone concentration
compared with females (P < 0.001). Endurance training
did not alter resting serum 17-estradiol concentration (males = 96.3 ± 13.9 161.2 ± 20.9 pmol/l; females = 119.3 ± 31.6 139.5 ± 40.4 pmol/l). Because the females
were tested during the early to midfollicular phase of their menstrual
cycle, resting serum 17-estradiol concentrations were not
significantly different between the genders. Serum progesterone concentrations were not different for females before and after training
(PRE = 3.5 ± 0.5 nmol/l, POST = 2.1 ± 0.4 nmol/l), which ensured that they were tested in the early to
midfollicular phase of their menstrual cycle.
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Exercise trial (90-min).
By design, the percentage of O2 peak
elicited in the REL exercise trial was not different from that elicited
in the PRE-training exercise trial, yet the absolute power output (in W) was higher. Oxygen consumption (O2)
was greater in the REL exercise trial compared with both the PRE and
ABS trials (Fig. 1A). At 75 and 90 min, O2 was lower for the ABS
compared with PRE trial (P < 0.001) despite the
workloads being the same (Fig. 1A). Females had a lower
absolute O2 during the exercise trial compared with males (Fig. 1B). Endurance training resulted
in a lower RER in the ABS trial, but not in the REL trial, compared with PRE (P < 0.001). RER increased from rest at the
onset of exercise in all exercise trials (Fig. 1C), and
females had a lower exercise RER compared with males (P < 0.01; Fig. 1D). Heart rate was lower during exercise in
the ABS trial compared with both the PRE and REL trials
(P < 0.001; data not shown). Resting heart rate was
significantly lower after endurance training in both the ABS and REL
compared with the PRE trial (P < 0.001; data not shown). Males had a lower resting heart rate compared with females (P < 0.05; data not shown).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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We found that females oxidized proportionately more fat than males
during all exercise trials. There was no gender difference in glucose
Ra; however, females had a lower MCR at later exercise time
points compared with males. Endurance training resulted in an increase
in O2 peak of similar magnitude for
both males and females. CHO utilization was lower after endurance
training during exercise at the same ABS exercise intensity; however,
glucose Ra and MCR were lower after endurance training at
both the ABS and REL exercise intensities.
Gender differences. Before and after training, females had a lower RER than males. These findings support the observations that females oxidized a greater proportion of fat compared with males during acute exercise at the same REL intensity (20, 31, 41). Females were also found to have a higher glycerol Ra compared with males. The higher glycerol Ra in females suggested that females have an increased rate of lipolysis compared with males, although the source of the lipid remains unclear. Similar findings have been reported in one training study in which males (15) were compared with data previously reported by the same group in female subjects (12). Studies investigating gender differences in the metabolic response to a single bout of prolonged submaximal exercise have found that females have a lower RER (20, 31, 41), attenuated muscle glycogen utilization (10, 40), and lower leucine oxidation (27) compared with males. The overall conclusion is that females oxidize a greater proportion of fat and less CHO and amino acids compared with males.
Although there was no gender difference in glucose Ra before or after training at either exercise intensity, glucose MCR was lower in females compared with males at later time points during endurance exercise. Females were also found to have a strong trend toward a higher plasma glucose concentration (P = 0.056) compared with males. These findings demonstrated that females have a lower skeletal muscle glucose uptake compared with males for a given glucose concentration. Two studies have found that 17-estradiol administration can decrease glucose Ra
during submaximal exercise in humans (4, 37). We have
previously shown a better maintenance of plasma glucose and a lower
glucose MCR and Rd during endurance exercise in males given
17-estradiol (4).
Another example of the effect of 17-estradiol on plasma glucose
maintenance comes from experiments using peroxisome
proliferator-activated receptor-
double-knockout (PPAR /)
mutant mice (8). This group found that all male, but only
25% of female, PPAR / mice given etomoxir (an inhibitor of
carnitine palmitoyl transferase I) developed fatal hypoglycemia
(8). The hypoglycemic effect of the PPAR /
genotype + etomoxir was prevented entirely when the male mice were
pretreated with 17-estradiol (8). These findings
indicate that 17-estradiol can mediate glucose Ra and the maintenance of plasma glucose during metabolic stress situations. Given that the plasma 17-estradiol concentration was identical in
the current study between males and females at the time of testing, a
potential role for 17-estradiol would not be occurring acutely.
Previously, we also found that transdermal 17-estradiol
administration had no effect on skeletal muscle glycogen utilization in
males (43). The marked hepatic glycogen sparing (23,
24) and the lack of an effect on GLUT-4 content
(39) suggest that 17-estradiol has a more significant
effect on hepatic glucose production than on skeletal muscle glucose
uptake. These observations are similar to animal data demonstrating
muscle and hepatic glycogen sparing (23, 24) and increased
lipid oxidation (18) in 17-estradiol-supplemented male
or oophorectomized female rats.
In the present study, the lower epinephrine concentration in females
was cotemporal with a lower glucose MCR at 90 min compared with males.
This observation is similar to the results of Ruby et al.
(37), who demonstrated that the provision of
17-estradiol to amenorrheic females reduced plasma epinephrine
concentration during endurance exercise. It is also similar to previous
findings from our laboratory, in which the 17-estradiol administered
to males resulted in a significantly lower glucose Ra and
MCR and a trend (P = 0.09) toward a decrease in plasma
epinephrine concentration (4).
Training.
There was a decrease in total CHO utilization during exercise after
endurance training when tested at the same ABS workload compared with
pretraining. However, there was no change in the proportion of CHO
utilized during exercise at the same REL intensity posttraining. Our
results are similar to those of others (21, 34) who have
found a decrease in CHO utilization (2, 28, 34) and an
increase in fat utilization (21, 27, 34) during prolonged
exercise at the same ABS workload after endurance exercise training.
Friedlander and colleagues (13, 14) also did not find a
decrease in CHO oxidation for either men or women during exercise at
the same REL intensity after 10-12 wk of endurance training.
Together, these data demonstrate that, despite an increase in fat
utilization after endurance exercise training when subjects were tested
at the same ABS exercise intensity (which is a lower percentage of the
O2 peak posttraining), there is no increase in the proportion of fat utilized at the same REL intensity. It is possible that the duration of training was not sufficient for
seeing adaptations in lipid oxidation with a longitudinal study design,
for cross-sectional studies have shown that well trained endurance
athletes have a lower RER compared with untrained persons at the same
REL-intensity exercise (5, 22).
O2 peak, whereas those in the previous
exercise trials (13, 14) were performed at a higher intensity (~65 O2 peak). Furthermore,
at higher exercise intensities the proportion of CHO oxidation
increases (3, 35, 36), which may supersede any
training-induced attenuation of glucose Ra.
In the present study, the decrease in glucose Ra and MCR,
in conjunction with a similar RER during exercise at the same REL intensity after training, illustrated that there was not a net decrease
in CHO utilization but rather a shift in the source of CHO utilized. If
there is a decrease in plasma glucose uptake and no change in RER, then
there must be a compensatory increase in skeletal muscle glycogen
utilization. With endurance exercise training there is an increase in
resting skeletal muscle glycogen concentration (22, 27, 33,
34) and an increased rate of glycogen resynthesis after exercise
(16, 19). Although many studies have found an attenuation
of skeletal muscle glycogen utilization at the same ABS exercise
intensity after endurance training, there is limited research on the
glycogen utilization before and after endurance exercise training at
the same REL intensity. McKenzie et al. (27) found that
the absolute change in glycogen concentration was similar during
exercise at the same REL intensity before and after training. Another
important consideration in the evaluation of the data is that a
significant decrease in glucose Ra may amount to an
increase in glycogen use that is not measurable with the muscle biopsy
technique. It is also possible that whole body RER does not reflect
tissue-specific respiratory quotient (RQ). For example, Bergman et al.
(2) reported that working muscle RQ and whole body RER can
be disparate during endurance exercise (i.e., a reduction in whole body
RER with no change in muscle RQ); however, this discrepancy has not
been consistently found (30).
Glycerol Ra and Rd were not affected by
training at rest or during exercise at either the same ABS or REL
intensity. Although an increase in glycerol Ra is sometimes
found at rest after training (34), this is not always the
case (14). However, when glycerol Ra was
compared between trained and untrained individuals, trained individuals
were found to have a greater glycerol Ra compared with
untrained individuals during exercise (5). Although plasma glycerol concentration is considered an indicator of changes in whole
body lipolysis, this is based upon the concept that glycerol can only
be taken up by the liver and kidney. A recent study (26) has illustrated that only ~50% of circulating glycerol is taken up
by the liver and kidney, suggesting that there is glycerol kinase
present in extraliver and extrakidney tissues. Together with the data
by Elia et al. (9), which indicated that glycerol may not
always be released by skeletal muscle and that glycerol taken up by
skeletal muscle may be used for the synthesis of intramuscular triglycerides (17), small changes in whole body
lipolysis after 7 wk of endurance training may not be detected with
glycerol Ra measurements. As a consequence, although our
data demonstrate a higher glycerol Ra in females than in
males, both before and after training, it is difficult to speculate on
the mechanism(s) behind this observation.
Endurance training resulted in a lower plasma norepinephrine
concentration at the same ABS exercise intensity; however, there was no
effect of endurance training on plasma norepinephrine concentration at
the same REL exercise intensity. Plasma epinephrine was lower at 90 min
after subjects trained at the same ABS exercise intensity. The plasma
epinephrine concentration at 90 min of exercise paralleled the lower
glucose MCR that was observed in females at the later time points
during endurance exercise. Our data are similar to those of previous
training studies with male participants (21, 34)
demonstrating a decrease in plasma norepinephrine and epinephrine concentrations after endurance exercise training when the participants were tested at the same ABS exercise intensity. However, the data are
not in complete agreement with those of other investigators (14), who found change in plasma norepinephrine
concentration in males, yet females had lower concentrations at both
the ABS and REL exercise intensities after training. They also found
no change in plasma epinephrine concentration in women;
however, males had a higher plasma epinephrine concentration after
training at both the ABS and REL exercise intensities
(14). As previously addressed, the differences between our
data and those of Friedlander et al. (14) may be due to
the lower exercise testing intensity in the present study.
In conclusion, we found that there is a shift toward an increase in fat
utilization and a decrease in CHO utilization after training at the
same ABS exercise intensity. However, there was not an increase in fat
utilization after training at the same REL exercise intensity. There is
a decrease in plasma glucose uptake during exercise after training
during exercise at both ABS and REL exercise intensities. Finally,
females have an increased rate of lipolysis and utilize proportionately
more fat during endurance exercise compared with males, regardless of
training state.
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ACKNOWLEDGEMENTS |
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We thank Jack Rosenfeld and Doug Mahoney for assistance in HPLC analysis of catecholamines, and Brian Roy for assistance with the GC-MS analysis of glucose and glycerol.
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FOOTNOTES |
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This study was funded by the Natural Science and Engineering Research Council of Canada.
Address for reprint requests and other correspondence: M. A. Tarnopolsky, Dept. of Neurology, Rm. 4U4, McMaster Univ. Medical Centre, 1200 Main St. West, Hamilton, Ontario, Canada L8N 3Z5 (E-Mail: tarnopol{at}mcmaster.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 17 July 2000; accepted in final form 14 February 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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significantly different from
REL (P < 0.001). B: gender difference in
glucose Ra during 90 min of exercise. C: glucose
metabolic clearance rate (MCR) during 90 min of exercise before (ABS)
and after (ABS and REL) training. *Significantly different from PRE
(P < 0.001). D: gender difference in
glucose MCR during 90 min of exercise. 
Significantly different from
males (P < 0.05). E: glucose concentration
during 90 min of exercise before (ABS) and after (ABS and REL)
training. Main effect for condition: §P < 0.05 (REL > PRE and ABS). F: plasma lactate concentration
during 90 min of exercise. *Significantly different from PRE
(P < 0.001); 