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The Journal of Clinical Endocrinology & Metabolism Vol. 86, No. 1 214-219
Copyright © 2001 by The Endocrine Society


Original Studies

Meal-Induced Thermogenesis and Obesity: Is a Fat Meal a Risk Factor for Fat Gain in Children?1

Claudio Maffeis, Yves Schutz, Alessandra Grezzani, Silvia Provera, Giorgio Piacentini and Luciano Tatò

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
 Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Diet composition, in particular fat intake, has been suggested to be a risk factor for obesity in humans. Several mechanisms may contribute to explain the impact of fat intake on fat gain. One factor may be the low thermogenesis induced by a mixed meal rich in fat. In a group of 11 girls (10.1 ± 0.3 yr), 6 obese (body mass index, 25.6 ± 0.6 kg/m2), and 5 nonobese (body mass index, 19 ± 1.6 kg/m2), we tested the hypothesis that a mixed meal rich in fat can elicit energy saving compared with an isocaloric and isoproteic meal rich in carbohydrate. The postabsorptive resting energy expenditure and the thermic effect of a meal (TEM) after a low fat (LF; 20% fat, 68% carbohydrate, and 12% protein) or an isocaloric (2500 kJ or 600 Cal) and isoproteic high fat (HF; 48% fat, 40% carbohydrate, and 12% protein) meal were measured by indirect calorimetry. Each girl repeated the test with a different, randomly assigned menu (HF or LF) 1 week after the first test. TEM, expressed as a percentage of energy intake was significantly higher after a LF meal than after a HF meal (6.5 ± 0.7% vs. 4.3 ± 0.4%; P < 0.01). The postprandial respiratory quotient (RQ) was significantly higher after a LF meal than after a HF meal (0.86 ± 0.013 vs. 0.83 ± 0.014; P < 0.001). The HF low carbohydrate meal induced a significantly lower increase in carbohydrate oxidation than the LF meal (20.3 ± 6.2 vs. 61.3 ± 7.8 mg/min; P < 0.001). On the contrary, fat oxidation was significantly higher after a HF meal than after a LF meal (-1.3 ± 2.4 vs. -15.1 ± 3.6 mg/min; P < 0.01). However, the postprandial 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). These results suggest that a high fat meal is able to induce lower thermogenesis and a higher positive fat balance than an isocaloric and isoproteic low fat meal. Therefore, diet composition per se must be taken into account among the various risk factors that induce obesity in children.


    Introduction
 Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBESITY IS THE most common nutritional disorder in children living in industrialized countries (1). Several genetic and environmental factors are involved in the development of obesity, although, for thermodynamic reasons, overweight is necessarily caused by a positive energy balance (2). Energy balance is the result of the sum of the balance of three macronutrients: protein, carbohydrate, and fat.2 Evidence exists in humans that carbohydrate balance and protein balance are efficiently self-regulated (3, 4). In fact, carbohydrate and protein oxidation are promoted by carbohydrate and protein intake. On the contrary, fat oxidation is not stimulated by fat intake (5). Moreover, the intake of other energy substrates has been shown to have a reducing effect on fat oxidation (6). There is also evidence that other features of lipid metabolism, such as the greater dependence of fat oxidation on the stimulation by the sympathoadrenal system compared with protein and carbohydrate utilization and the absence of metabolic pathway other than lipogenesis to buffer a significant fraction of excess fat intake, are contributing factors to fat gain (7). Finally, a high fat diet may favor fat gain, based on certain characteristics of fatty foods. First, ingestion of fatty foods promotes food consumption by means of the high energy density and palatability of this diet (8, 9); second, satiation is lower with fat than with protein and/or carbohydrate intake, and self- compensation by adjusting subsequent intake is less likely after a high fat meal (9, 10); and third, meal-induced thermogenesis is lower after fat intake (~3% of energy content of fat ingested) than after carbohydrate or protein intake (~6–7 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
 Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Subjects

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 1Go. 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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Table 1. Physical characteristics of the 11 girls

 
Experimental design

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 2Go. Each meal was eaten under supervision between 0930–1000 h.


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Table 2. Composition and energy content of high fat/low carbohydrate and low fat/high carbohydrate test meals, respectively

 
Measurements of resting energy expenditure

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 Weir’s 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
 Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
The physical characteristics of the obese and nonobese girls are shown in Table 1Go. As expected, weight, BMI, waist circumference, fat mass, and fat-free mass were significantly greater for the obese than for the nonobese girls.

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 3Go. 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 4Go).


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Table 3. Postabsorptive and postprandial resting energy expenditure (REE) and respiratory quotient (RQ) in the total sample measured before and after high fat and low fat meals

 

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Table 4. Postabsorptive and postprandial resting energy expenditure (REE) and respiratory quotient (RQ) in obese and nonobese girls measured before and after high fat and low fat meals

 
Postprandial REE and RQ

During the first 30–45 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 3Go). Postprandial REE measured after both meals was not significantly different between the two groups (Table 4Go).

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. 1Go. 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 5Go). 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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Figure 1. Nutrient oxidation rate (milligrams per min) measured in postabsorptive conditions and after a test meal intake (high fat/low carbohydrate meal on the left and low fat/high carbohydrate on the right) in obese girls (top) and nonobese girls (bottom). Data are the mean and SEM.

 

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Table 5. Variation of carbohydrate and fat oxidation (postprandial - postabsorptive) after high fat and low fat meal in obese, nonobese girls and in the total sample

 

    Discussion
 Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
The chronic excess fat intake with regard to fat requirement is the common final mechanism by which the different factors promoting obesity cause fat deposition. Evidence exists that fat content in the diet is a promoting factor of energy intake (8, 9), although a genetic predisposition of the subject seems to be necessary (22). In other words, exposure to a high fat diet per se is not sufficient to promote weight gain if there are no genetic predisposing factors.

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
 
1 This work was supported by National Research Council (Rome, Italy) Contract 96.03441.CT04 and by Nestlè Italiana Spa, Italy. Back

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. Back

Received December 30, 1999.

Revised June 2, 2000.

Revised September 26, 2000.

Accepted October 3, 2000.


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 Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals