Department of Nutrition, University of Montreal, and Centre hospitalier de l'Université de Montréal, Montreal, Quebec, Canada, H2W 1T8
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ABSTRACT |
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The thermogenic response to food (TRF) and substrate oxidation
were studied in 12 endurance-trained and 13 untrained female subjects.
Energy expenditure and substrate oxidation were calculated by indirect
calorimetry before and for 6 h after an oral test meal and after
the same meal given intragastrically on a separate occasion. The TRF
was calculated after the oral meal, the obligatory component after the
intragastric meal (OTRF), and the facultative component from the
difference between the two. O2 max was
measured on a treadmill and body composition by underwater weighing.
The TRF and OTRF were significantly higher in trained than in untrained
subjects: 223 ± 63 vs. 185 ± 50 kJ/6 h (P < 0.03) and 174 ± 38 vs. 131 ± 37 kJ/6 h
(P < 0.01) for the TRF and OTRF in trained vs.
untrained subjects, respectively. Multiple regression analysis showed
that maximum O2 consumption
(
O2 max), but not percentage of body
fat, was significantly related to OTRF (r =0.68,
P < 0.01). Trained subjects had higher fatty acid
oxidation than untrained subjects before (0.6 vs. 0.4 mg · kg
1 · min
1,
P < 0.05) and after the oral meal (13 ± 6 vs.
8 ± 4 g/6 h P < 0.05). These results demonstrate
that 1) TRF is higher in trained than in untrained women;
2) this is due to a higher cost of nutrient digestion,
absorption and storage; 3) the difference is related to
higher
O2 max; and 4) fatty
acid oxidation is greater in trained women in both the postabsorptive
and postprandial states. These observations suggest that endurance
training induces metabolic changes that favor leanness.
energy expenditure; endurance training; women
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INTRODUCTION |
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THE THERMOGENIC RESPONSE to food (TRF) is an increase in resting energy expenditure (REE) after ingestion of food. In rats and dogs, TRF has two components, an obligatory component, which includes the process of digestion, absorption, and storage of nutrients, and a facultative component, which is linked with oropharyngeal stimulation (11, 12, 15). In humans, we have shown that 30-40% of TRF is related to oropharyngeal stimulation (10) and that this component is under the control of the sympathetic nervous system (9). These observations support the concept that a facultative component of the TRF exists in humans and that it is regulated in a manner similar to that in rodents. We have postulated that the existence of these two components of the TRF in humans may explain some of the discrepancies observed in the literature when only the whole thermic response to feeding is studied. Factors that have been found to influence TRF, such as energy content of the meal, obesity, or exercise may affect either component. If only one component is affected, analytical variability arising from the nonaffected component may impair the ability to show a difference between individuals. For instance, we have found that only the facultative component of TRF was affected by obesity (13).
The effects of exercise training on the TRF are poorly understood. Some research suggests higher TRF in trained subjects (8, 14, 37, 43), whereas other studies have found lower TRF (21, 22, 39) or no difference between trained and sedentary individuals (4, 28, 38). Understanding the relationships between physical training and TRF is important for the evaluation of long-term benefits of exercise for weight regulation. Although TRF represents a small proportion of 24-h energy expenditure, a permanent increase in this component of the energy balance equation is likely to be significant.
The objective of this study was, therefore, to measure both components
of the TRF in trained and untrained women and to calculate the
relationship of these measurements to
O2 max and body fat.
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SUBJECTS AND METHODS |
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Subjects.
Twenty-five (12 trained and 13 untrained) young (aged 18-35 yr),
healthy female subjects were recruited for this study. The trained
subjects were distance runners or triathletes currently performing 8
h/wk of aerobic exercise, who had been training for at least two years
previously, and who had engaged in provincial and national
competitions. This group was selected from three university sports
centers in Montreal. The untrained subjects had not performed aerobic
exercise more than 1.5 h/wk during the previous two years and had never
been enrolled in any athletic competition involving endurance
activities; they were selected through city newspaper ads and ads in
local universities. All subjects were nonsmokers, were weight stable
(±2.5 kg during the 6 mo before the study), were not taking any
medication known to affect metabolic rate, did not present any family
history of diabetes or obesity, and had a regular menstrual cycle
(28-35 days). Trained and untrained groups were matched for body
size [body mass index (BMI) 18-22 kg/m2]. This was
done to facilitate analysis of the effect of body composition on TRF.
Informed consent was obtained from each subject, and the ethics
committee of our institution approved the study.
Procedures for admission into the study. Before their engagement in the study, all subjects went through a preliminary session, during which they were informed of all the investigation procedures. During this session, a nasogastric tube (Flexiflo no. 8 enteral feeding tube, Ross Laboratories, Columbus, OH) was inserted into the stomach without nasal anesthesia and left in place for ~10 min. The participants were also familiarized with the measurement of indirect calorimetry and had a physical examination.
Glucose tolerance test. Because insulin resistance is associated with inhibition of the TRF (33), serum glucose and insulin concentrations were measured as markers of insulin sensitivity during a 75-g oral glucose challenge in all subjects.
Subjects arrived at the clinic after a 12-h fast, and a first blood sample was taken; then they ingested 75 g of glucose (Glucotrol, Rougier, Chambly, Canada), and a second blood sample was collected 120 min later. Serum glucose was measured by the glucose oxidase method. Insulin level was quantified by radioimmunoassay (SERONO RIA kit, Immunocorp, Montreal, Canada).Body composition. Body fat was assessed by densitometry and skinfold measurements. Body density was measured by underwater weighing (18); a maximum of seven trials was performed for each subject. Three trials with the least variability and providing the highest body density were averaged to obtain final body density. Residual lung volume was measured using the closed-circuit helium-dilution method (26). Skinfold thicknesses were measured at 10 sites on the left side of the body with a Lange caliper (Cambridge Scientific Industries, Cambridge, MD); the average of triplicate measurements was used to calculate body density. Fat-free mass (FFM) and fat mass (FM) were calculated from body density values according to the equations of Siri (34) and from skinfold values with the equations of Allen et al. (2).
Maximal treadmill exercise test.
Maximal aerobic capacity was measured on a treadmill (Quinton Q65); the
Léger and Boucher (23) protocol was selected using the modified formula of Léger and Mercier (24). All
subjects were asked to abstain from drinking alcohol or products
containing caffeine 24 h before the test and not to eat a large
meal 3-4 h before the evaluation; trained subjects were instructed
to abstain from intense exercise 24 h before the test. The test
began with a 5-min run at 8 km/h, after which the speed was increased
by 1 km/h every 2 min until exhaustion. Expired gases were measured using a breath by breath system (mass spectrometer, Marquette 1100 medical gas analyzer with a ventilation measurement module and the
Marquette Calcul O2 software). Heart
rate (HR) was monitored continuously with a portable chest strap
monitor (Polar CIC, Port Washington, NY).
REE and TRF tests.
REE was measured for 30 min before each test meal. The test meals were
assigned randomly (see test meal composition in Table 1).
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Calculations and statistics.
Energy expenditure was calculated from
CO2,
O2,
and urinary nitrogen by the Weir equation (42)
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RESULTS |
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Subjects.
The average duration of aerobic exercise in trained subjects was
13.6 ± 2.8 h/wk, and the average time since involvement in competitive activities was 4.3 ± 1.6 yr. The physical
characteristics of the trained and untrained subjects are shown in
Table 2. There was no difference in age,
weight, height, and BMI between the groups. Body fat, FM, and resting
HR were lower in trained subjects; FFM was higher in trained subjects.
REE was higher in trained subjects: 101 ± 12 vs. 93 ± 7 kJ · kg1 · day
1
(P < 0.05), and the difference was still significant
after adjustment by ANCOVA of REE for FFM: 100 ± 10 and
92 ± 10 kJ · kg
1 · day
1 for trained
and untrained subjects, respectively (P < 0.05).
O2 max was significantly greater in
trained subjects. There were no significant differences in plasma
insulin and glucose concentrations (data not shown).
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Thermogenic response to food.
Figure 1, A and B,
presents the response of each group (trained and untrained) to oral
and tube feeding. Both groups exhibited significantly lower energy
expenditure after tube feeding (22.2 and
29.0%, respectively,
P < 0.01 for both comparisons).
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Substrate oxidation.
Results of substrate oxidation are presented in Table
3. At rest and after a 12-h
fast, fatty acid oxidation was significantly higher in trained subjects
(+37% between the average values of both study days): 0.40 ± 0.2 vs. 0.55 ± 0.3 mg · kg1 · min
1 in
untrained and trained subjects, respectively. Glucose oxidation was not
different between groups.
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DISCUSSION |
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The results of this study show that TRF is higher in endurance-trained than in sedentary women. In addition, they show that the obligatory component of TRF, not the facultative one, is responsible for this effect. We believe that intragastric feeding results in the blunting of the facultative component of TRF, because we have found that intravenous administration of propranolol, an inhibitor of the sympathetic nervous system, eliminates the difference in TRF between intragastric and oral feeding and has no effect on TRF after intragastric feeding (9). Indeed, it was shown by Acheson et al. (1) that facultative thermogenesis induced by the intravenous administration of glucose can be suppressed by propranolol infusion. Taken together with our findings, these results suggest that intragastric feeding abolishes a component of TRF that is dependent on the autonomic nervous system. Insulin secretion is unlikely to be responsible for the facultative component of TRF, because no difference was found in the area under the curve of plasma insulin after intragastric vs. oral feeding (10).
Previous investigations measuring TRF in trained and untrained subjects at rest presented discrepant data. Methodological issues, such as heterogeneity of the group, the small number of subjects studied, "mixed" gender, various time lapses between testing and the last bout of exercise, inconsistent duration of TRF measurement, and variable quantity and composition of test meals may explain these discrepancies (8, 14, 21, 22, 29, 36, 41). The literature is limited and controversial concerning TRF in female athletes, as well (4, 28, 43).
In this study, the trained and untrained subjects were matched for age, weight, height, and BMI to minimize the possible influence of these parameters on TRF, which resulted in recruiting control subjects with low body fatness, and these subjects may not represent the general sedentary population. Because excess body fatness is associated with decreased insulin sensitivity (33) and lower TRF, our subject selection is likely to have led to a smaller between-group difference than would have been expected from a sedentary group with more body fat. In addition, subjects followed a specific nutrient partitioning for 3 days before testing. This was done to avoid the possible influence of an inhabitual pretest diet on TRF. Whether TRF is influenced by the energy partitioning of a meal is controversial, and there are no data on the influence of diet composition before measuring TRF. The difference between the two groups of subjects regarding food energy partitioning was small and is unlikely to have affected the results.
Our results show a significantly higher TRF (+22%) in trained subjects, and when both TRF components are taken into consideration, the obligatory but not the facultative component is higher (+32%) in these subjects than in the untrained controls. Our data on the TRF are in agreement with those of authors who measured TRF in athletes 36 h or more after the last exercise bout (8, 14, 43) and in contradiction with those where the TRF was measured 12-16 h after exercise (21, 39). The importance of the length of time without exercise before measuring TRF in trained subjects has been stressed (30), but only one study has specifically addressed this issue. In that investigation (41), the thermogenic response to an oral glucose load was significantly higher 3 days after the last exercise bout compared with 16 h. These results suggest that a detraining phenomenon may have the same effect as a stressful situation on TRF in athletes and favor a 24-h lag time between the last bout of exercise and TRF measurements in trained individuals. On the other hand, it is possible that TRF would also be influenced by an exercise bout close to the time of measurement. The lower TRF found in trained subjects 12-16 h postexercise might represent an adaptive phenomenon with increased efficiency of nutrient storage during this period of time. The phenomenon must be transient, however, because our study and investigations with TRF measurements performed more than 24 h postexercise showed heightened TRF in trained subjects.
In addition to demonstrating a higher TRF in trained women, our data suggest that this difference is related to an enhancement of the cost of digestive absorption and metabolic storage of nutrients (i.e., the "obligatory component") and not through an increment of the "facultative component" of the TRF. Whether this increased cost of metabolic digestion, absorption, and storage of nutrients is related to carbohydrate or protein metabolism, or both, cannot be evaluated from our data. In the postabsorptive state, no difference in leucine turnover was found between endurance-trained and sedentary subjects (19), but postprandial measurements of protein turnover have not been made under these circumstances.
We found a strong correlation between %body fat and
O2 max, (
0.68, P < 0.005); the correlation between OTRF and
O2 max did not change with %body fat
as a covariate. This indicates that, at least in subjects of comparable
body fatness, body composition does not influence the energy cost of
nutrient storage. In the literature, investigations looking at
O2 max and TRF have conflicting
results, with observations of an increase in both parameters in trained
subjects (8, 14) as well as an inverse relationship
between the TRF and
O2 max in trained
subjects (22, 30). Poehlman et al. (30),
studying male subjects, proposed a curvilinear relationship between
O2 max and TRF, with highly trained
subjects having a lower TRF when
O2
exceeded 70 ml · kg
1 · min
1. These
discrepancies may be related to the methodological issues already
discussed, but they may also arise from the fact that both components
of TRF were not measured in these experiments.
The finding of a relationship between
O2 max and the cost of nutrient
metabolism and storage deserves further investigation. Consistent with
our findings of a positive relationship between
O2 max and TRF is the observation that
O2 max is positively and independently
related to insulin sensitivity (7). Indeed, low insulin
sensitivity has been reported to be an independent factor related to
low TRF (33). The influence of the genetic background of
an individual vs. the effect of endurance training on
O2 max cannot be inferred from our
data, because the relationship between
O2 max and OTRF was correlated in our
subjects irrespective of their training status. Whether endurance
training increases the obligatory component of TRF remains to be studied.
In addition to higher TRF, we found that athletes had a higher resting
metabolic rate (RMR), even after the data were adjusted for FFM. We
used FFM as a covariate instead of dividing RMR by FFM, because the
regression line between the two variables did not intercept zero. Most
studies on the relationship between the RMR and endurance training have
been conducted in men, and the results of those that have investigated
women are conflicting. No difference was observed in RMR between
trained and untrained women by LeBlanc et al.
(22) and Owen et al. (28), but exercise training in combination with weight reduction has been found to increase RMR in women (20, 25). Basal metabolic rate was
reported to be higher in four female cross-country skiers measured at
39-h postexercise compared with control subjects matched for lean
body mass (35). These discrepancies may be related to the
time elapsed after the last exercise bout, phase of the menstrual cycle
(36), physical activity, or food intake, all of which may
influence RMR. We attempted to minimize these factors by controlling
for body size and composition, pretest food intake, and phase of the menstrual cycle. As these factors are likely to influence RMR, optimal
experimental conditions for such studies should measure either small
numbers of subjects with strictly standardized settings or large
numbers of subjects allowing for multivariate analyses.
In the present investigation, differences in FFM were accounted for by ANCOVA, and it was shown that RMR was higher in trained subjects after this correction. Thus our data indicate that endurance training per se increases RMR in women.
Studies of RMR in healthy men suggest that strenuous exercise (i.e.,
>70% O2 max) can augment RMR up to
24 h postexercise (30), but the relationship between
aerobic fitness and RMR in men is not clear. A positive relationship
between RMR and aerobic fitness was found in some investigations
(3, 30, 40) but not in others (9, 14, 21).
The conflicting results on relationships between the RMR and physical
fitness observed in both men and women suggest that longitudinal
studies are warranted in subjects showing large variations in
O2 max through physical training.
The data on substrate oxidation show that fatty acid oxidation was 37% higher in trained than in untrained subjects in the postabsorptive state. This difference was more pronounced during the postprandial phase, with the average value for fatty acid oxidation in trained subjects being 65% above that of untrained subjects. The physiological regulation of fatty acid oxidation at rest and the effects of endurance training have not been well characterized. Calles-Escandon and Driscoll (5) found no difference in fatty acid oxidation in the postabsorptive state between 12 trained subjects and 14 sedentary controls. In their investigation, both men and women were explored, and there is no analysis of a possible gender effect. Similarly, Roy et al. (32), studying six sedentary and six trained men, found that athletic status had no influence on fatty acid oxidation measured for 24 h in a respiration chamber. This conflicts with our data, because an increase in fatty acid oxidation during both the postabsorptive and the postprandial periods should elicit higher 24-h oxidation rates. On the other hand, Calles-Escandon et al. (6) reported that exercise training increased fatty acid oxidation at rest, independent of changes in energy intake and body composition. In their study, the duration of the experimental periods was short (10 days), and the results may be attributed to an acute effect of exercise on fatty acid oxidation. Finally, two cross-sectional investigations of large groups of men and women reported gender differences in fat oxidation; one found lower fat oxidation in women (27), and the other found different effects of aging on fat oxidation between sexes (16). The effect of endurance training on fat oxidation at rest and after a meal may not be the same in men and women. Trained and untrained subjects of our study did not show the same pattern of substrate oxidation during the two modes of feeding; untrained subjects oxidized less glucose and more fatty acids after intragastric feeding, suggesting that the facultative component of TRF may be related to an increase in glucose oxidation. Trained subjects showed no such differences in substrate oxidation with oral vs. intragastric feeding.
In conclusion, this study shows that trained women have higher resting
and postprandial energy expenditure than untrained women of similar
body size. The greater TRF in trained subjects is related to a higher
cost of nutrient metabolism, and this energy expenditure is correlated
with O2 max. Fat oxidation is also
higher in trained women after an overnight fast and postprandially. These findings have important implications for understanding the relationships between physical fitness, body weight regulation, and the
efficiency of nutrient digestion, absorption and storage.
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ACKNOWLEDGEMENTS |
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This work was supported by the Hotel-Dieu Foundation and by the Department of Nutrition of the University of Montreal.
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FOOTNOTES |
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Address for reprint requests and other correspondence: D. R. Garrel, Centre hospitalier de l'Université de Montréal, Hôtel-Dieu 3840 St-Urbain, Montreal, Quebec, Canada H2W 1T8 (E-mail: garreld{at}ere.umontreal.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. §1734 solely to indicate this fact.
Received 10 August 1999; accepted in final form 20 April 2000.
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