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Original Studies |
Department of Pediatrics, University of Verona, 37134 Verona, Italy; and Institute of Physiology, University of Lausanne (Y.S.), 1011 Lausanne, Switzerland
Address all correspondence and requests for reprints to: Claudio Maffeis, M.D., Department of Pediatrics, University of Verona, Polyclinic, 37134 Verona, Italy. E-mail: maffeis{at}borgoroma.univr.it
| Abstract |
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| Introduction |
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3% of energy content of fat ingested) than after
carbohydrate or protein intake (
67 and
25%, respectively)
(11). Contrasting data are available on the extent to which diet composition and fat intake play important roles in the development of childhood obesity (12, 13, 14). However, in the long run, just a few grams of fat ingested every day over fat requirements (oxidation) may theoretically lead to significant fat gain. The lower thermogenesis induced by a fat diet may be a contributing factor to fat gain. At present, no data on the role of diet composition on thermogenesis are available for obese and nonobese children. Therefore, the purpose of this study was to investigate the relationship between the thermogenesis induced by isocaloric meals with different fat contents in a group of obese and nonobese girls. In particular, we tested the hypothesis that a mixed meal rich in fat could elicit energy saving compared with an isocaloric and isoproteic meal rich in carbohydrate.
| Subjects and Methods |
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Twelve girls, 6 obese and 6 nonobese, participated in the study.
One nonobese girl was excluded in the final analysis of the data
because of the anxiety she showed during the indirect calorimetric
test, leading to unrealistic respiratory exchange recording.
Therefore, the results obtained from 11 girls who successfully
performed the tests are included herein. The physical characteristics
of the girls are given in Table 1
. None
of the girls had any overt disease other than obesity. Obesity was
defined as a body mass index (BMI) above the 95th percentile for age
and sex, and normal weight was defined as a BMI lower than the 85th
percentile (15). The BMI percentiles reported by Must
et al. were used as a reference (16). None of
the obese girls was dieting at the time of the study, and all of the
girls had an essentially stable body weight for at least 1 month before
the study. None was taking medication. The girls arrived at the
Department of Pediatrics at 0830 h in the morning accompanied by
their parents. Informed consent was obtained before taking part in the
study. The protocol was in accordance with the 1975 Declaration of
Helsinki as revised in 1983.
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The study was designed as a cross-sectional study for repeated
measures. The study lasted 6 consecutive h during which the girls were
under medical supervision. During the days preceding the test, no
attempt was made to influence the usual diet of each girl (who had
access to a free diet), but none of them was on a hypocaloric diet. The
day immediately before the test, they did not perform any intense
physical activity. Each girl arrived at the Department of Pediatrics at
0830 h on the day of the calorimetric test. The girls consumed
their last meal at 2000 h. After 30 min of resting in a
comfortable temperature (
24 C)- and humidity-controlled environment,
continuous respiratory exchange measurements were made by indirect
calorimetry at 0900 h.
One week after the first test, each girl came back to the Department of Pediatrics at 0830 h and repeated the indirect calorimetric test with a different menu. The two menus were given at random.
Anthropometry and body composition
Anthropometric assessments (weight, height, and four skinfold thicknesses at the biceps, triceps, suprailiac, and subscapular sites) were carried out on each girl. Skinfold thickness was measured to the nearest millimeter in triplicate with a Harpenden skinfold caliper (CSM Weighing Equipment Ltd., London, UK). The formulas reported by Deurenberg et al. for this age category were used to estimate relative body fat (17). Body fat mass was obtained by multiplying the percentage of body fat by body weight. Fat-free mass was calculated by subtracting body fat from body weight.
Dietary intakes
On the day of the study, after a 30-min baseline calorimetric
period, the children were given a test meal. Two different menus were
served on the 2 days of the experiment. The two menus were calculated
to have the same energy (2500 kJ or 600 Cal), a different carbohydrate
to fat ratio, and a similar protein content. The energy and nutrient
contents of the two menus were calculated using the tables of food
composition of the National Institute of Nutrition (18).
Expressed as a percentage of total energy value, the two test meals
contained 1) low fat (LF): 12% protein, 20% fat, and 68% of
carbohydrate energy; and 2) high fat (HF): 12% protein, 48% fat,
and 40% carbohydrate energy. A detailed description of the two
menus is given in Table 2
. Each meal was
eaten under supervision between 09301000 h.
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After 30 min of absolute rest, considered to be an adaptation period during which the procedure was explained to each child as well as to their parents, respiratory exchanges were measured continuously for 30 min on five different occasions during the study period. During the measurement, the child rested quietly while watching unexciting cartoons. Special attention was given to prevent extra body movements, which would contribute to increasing energy expenditure.
The postabsorptive resting energy expenditure (REE) measurement was made at 0900 h (preprandial baseline). Postprandial calorimetric measurements took place at 1030, 1145, 1300, and 1415 h and lasted 30 min each. Respiratory exchange measurements were determined by means of an open circuit computerized indirect calorimeter (Deltatrac, Datex, Inc., Finland) using a transparent ventilated hood system, as previously described (19). REE was calculated from oxygen production (VO2) and carbon dioxide production (VCO2) using Weirs formula (20).
Macronutrient oxidation rate
The macronutrient oxidation rate was calculated from VO2 and VCO2 using the following formulas (21): Fox (g/min) = 1.67 VO2 (L/min) - 1.67 VCO2 (L/min) - 0.307 Pox; and Gox (g/min) = 4.55 VCO2 (L/min) - 3.21 VO2 (L/min) - 0.459 Pox, where Fox is fat oxidation, Gox is glucose oxidation, and Pox is protein oxidation.
Protein oxidation was estimated as follows: Pox (g/min) = [REE (kJ/min) x 0.15]/16.74 kJ. We assumed that protein oxidation covered 15% of REE in both obese and nonobese girls. Postprandial changes in macronutrient oxidation were quantified calculating the areas under the respective 300 min plots.
Statistical analysis
All results presented are expressed as mean and SEM. Variables were not normally distributed; therefore, comparisons of physical characteristics and postabsorptive and postprandial REE and RQ of obese and nonobese girls were made using a two-tailed Mann-Whitney test. A two-tailed Wilcoxon test was used to compare the postprandial energy expenditure, macronutrient oxidation rates, and respiratory quotient measured after a HF vs. a LF meal. The degree of association was quantified between two variables using the Spearman correlation analysis. P < 0.05 was used to indicate statistical significance. Statistical analyses were performed using JMP 2.0 software (SAS Institute, Inc., Cary, NC).
| Results |
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Postabsorptive REE and RQ
Postabsorptive REE and postabsorptive RQ measured before a high
fat meal and a low fat meal, respectively, are shown in Table 3
. Postabsorptive REEs measured before a
HF meal and a LF meal were significantly different when the two groups
were pooled, although the mean difference between the two was only
2 ± 1%. The obese girls showed significantly lower
postabsorptive RQ than the nonobese girls, whereas postabsorptive REE
was not significantly different in the two groups (Table 4
).
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During the first 3045 min after meal ingestion, energy
expenditure increased rapidly and then progressively decreased during
the following hours. In the total sample, postprandial thermogenesis,
expressed in absolute values (kilojoules per 5 h), as a percentage
of postabsorptive REE or as a percentage of energy intake
(test meal), was significantly higher after a LF meal than after a HF
meal (Table 3
). Postprandial REE measured after both meals was not
significantly different between the two groups (Table 4
).
A high fat/low carbohydrate meal induced a rise in RQ comparable to a low fat/high carbohydrate meal during the first 40 min after food ingestion. Afterward, RQ decreases more readily to baseline with a LF than with a HF meal. Postprandial RQ was significantly lower in obese than in nonobese girls after both meals.
Pre- and postprandial macronutrient oxidation rates
Carbohydrate and fat oxidation rates measured in postabsorptive
conditions and after meal intake (HF and LF) are shown in Fig. 1
. The high fat/low carbohydrate meal
induced a significantly lower increase in carbohydrate oxidation
(P < 0.001) than the low fat/high carbohydrate meal in
both obese and nonobese girls (Table 5
).
On the contrary, the fat oxidation rate measured in the 5 h after
meal intake was significantly (P < 0.01) higher after
a HF than after a LF meal in both obese and nonobese girls.
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| Discussion |
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When the percentage of fat in the diet increases, the organism may respond in two ways to maintain energy and fat balance. First, it may oxidize a larger amount of fat to maintain fat balance or, second, it may promote a subsequent reduction of lipid intake as a compensatory mechanism. Experimental studies have not confirmed these hypotheses. In particular, fat intake is not able to stimulate fat oxidation, as is the case with carbohydrates and proteins. In fact, in young men, fat oxidation remained unchanged despite the addition of 106 g fat to a maintenance diet containing 35% calories as fat (4). Moreover, slower thermogenic responses were found after fat intake than after isoenergetic meals of protein or carbohydrate (3). A self-regulating effect after high fat meals, which promotes compensatory lower energy fat intake, has not been demonstrated. On the contrary, a voluntary reduction of fat intake was accompanied by a lower energy intake and promoted weight and fat loss in humans as well as in animals (23, 24, 25).
The results of this study, the first to investigate the effects of
isocaloric-isoproteic meals with different fat/carbohydrate ratios on
thermogenesis in children, demonstrate that diet composition affects
meal-induced thermogenesis in both lean and obese girls. A high fat
meal may induce a significantly lower thermogenesis than a isocaloric,
isoproteic, low fat meal. A higher fat/carbohydrate ratio in the meal
was able to elicit an approximately 30% lower meal-induced
thermogenesis expressed in absolute values compared with a diet with a
lower fat/carbohydrate ratio. However, it should be pointed out that
the impact of this lower energy expenditure induced by a higher fat
meal on the total energy expenditure remains fairly limited (
2%).
Similar results were found in a recent study of macronutrient disposal
during acute overfeeding with different macronutrients in five obese
and eight nonobese women (26). The total energy
expenditure was 2% lower with fat diet overfeeding compared with the
carbohydrate overfeeding (glucose), but this difference failed to reach
statistical significance. Therefore, the clinical consequences of diet
composition on 24-h thermogenesis do not seem relevant at least over
the short-term and in adults.
In the 5 h after meal intake, the girls oxidized a higher amount of fat with the HF than with the LF meal (14.6 ± 1.7 vs. 11.4 ± 1.8 g fat; P < 0.001), but they oxidized less than 50% of the fat taken with the high fat meal (HF vs. LF, 31.9 vs. 13.3 g fat). As a result, fat storage was 8-fold higher after a HF meal than after a LF meal (17.2 ± 1.7 vs. 1.9 ± 1.8 g; P < 0.001). Although the design of our study is not longitudinal, and therefore a cause and effect relationship is not present, it clearly demonstrates for the first time in children that regardless of the level of adiposity, a HF meal is promoting a significantly larger fat storage than an isocaloric, isoproteic LF meal. Conversely, an isocaloric change in the amount of fat in the diet is known to result in a change in body weight and body fat, as reviewed by Astrup et al. (27) in a meta-analysis including several intervention studies in man; a reduction in dietary fat concomitant to an increase in carbohydrate without restriction of total energy produced progressive weight (fat) loss in overweight individuals, suggesting that part of this effect may be metabolic, i.e. mediated by an improvement in thermogenesis and a lower postprandial fat storage, as demonstrated in our study.
Fat intake is just one of the two factors of the fat balance equation: an increase in fat mass and/or energy expenditure for physical activity may increase fat oxidation, reestablishing fat balance and opposing further fat gain. In particular, studies conducted in children showed that the fat oxidation rate is higher in fatter subjects in both postabsorptive and postprandial conditions (13, 28, 29). However, this compensatory fat mass-dependent increase in fat oxidation is a slow process. Moreover, the results of a recent longitudinal study (30) showed that over the long term, spontaneous metabolic adaptations to weight changes in both energy expenditure and fat oxidation are modest when adjusted for body composition. Finally, McDevitt et al. recently showed that acute fat overfeeding was associated with limited increase in fat oxidation in women compared with carbohydrate overfeeding (26).
The relationship between adiposity and dietary fat has been frequently reported in both prepubertal children and adolescents (12, 13). This relationship may be also stronger if the selective underreporting of fat intake, recently demonstrated by Goris et al. (31) in obese adults, also occurs in obese children. It is well known that the obese children tend to prefer a fatter diet than their nonobese counterparts (12), and this preference seems to be present in preobese children also. In fact, the results of a longitudinal study support the hypothesis that fat intake plays a role in promoting fat gain in children independently of other risk factors (14).
In the past, a potential thermogenetic defect in preobese subjects had been suggested as a risk factor for obesity in humans (32). However, several studies performed on children have failed to demonstrate a clear thermogenic defect in obese or postobese subjects, especially after a mixed solid meal (33, 34, 35, 36). However, as shown by the results of this study, diet composition is likely to influence, although moderately, the magnitude of thermogenic response independently of the adiposity level of the individual. Although in a real-life setting, the thermogenic response to fat and carbohydrate is difficult to differentiate, under ad libitum free-living conditions fat is still the more fattening substrate because of its increased energy density, which promotes passive overconsumption, even when palatability is constant, as recently demonstrated by many researchers (26, 37, 38, 39).
In conclusion, diet composition constitutes an important factor in the regulation of oxidative metabolism in children. In particular, a high fat and low carbohydrate diet is able to induce a lower thermogenesis compared with an isoenergetic, isoproteic low fat diet. Over the long term and together with other critical powerful factors, such as the high energy density, palatability of fatty foods, etc., the reduced postprandial thermogenesis following the high lipid meals may contribute to the progressive development of weight (fat) gain and the maintenance of obesity in children.
| Footnotes |
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2 The contribution of other sources of energy such as
dietary fiber can be considered quantitatively negligible for current
average fiber intake. Alcohol (29.3 kJ/g or 7 Cal/g), because it is an
unusual food at least in young children, is negligible. ![]()
Received December 30, 1999.
Revised June 2, 2000.
Revised September 26, 2000.
Accepted October 3, 2000.
| References |
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