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1 From the Pennington Biomedical Research Center, Baton Rouge, LA.
2 Supported by US Department of Agriculture grant 96034323-3031.
3 Address reprint requests to SR Smith, Pennington Biomedical Research Center, 6400 Perkins Road, Baton Rouge, LA 70808. E-mail: smithsr{at}mhs.pbrc.edu.
ABSTRACT
Background: Dietary fat contents are highly variable. Failure to compensate for the positive fat balance that occurs during the shift to a high-fat, low-carbohydrate diet by increasing energy expenditure or by decreasing food intake may result in the gain of fat mass.
Objective: The objective of this study was to investigate the time course of fat oxidation during adaptation to an isoenergetic high-fat, low-carbohydrate diet.
Design: After a 5-d control diet, dietary fat was increased from 37% of energy to 50% of energy for 4 d in 6 healthy, young lean men. Respiratory quotient and substrate macronutrient oxidation and balance were measured in a respiratory chamber. Fasting concentrations of insulin, glucose, and triacylglycerol; maximal oxygen consumption (
Key Words: Respiratory chamber • physical fitness • insulin • macronutrient oxidation • dietary fat • fat oxidation • physical activity • macronutrient oxidation • fat balance • high-fat diet • obesity • men
INTRODUCTION
The prevalence of obesity is increasing at a rapid rate in Western societies and in societies that are adopting a Western pattern of food intake (1). Multiple factors are likely to be involved in the development of this epidemic, including increased dietary fat and decreased levels of physical activity. Public health efforts have emphasized the role of preventing weight gain as a means of preventing the complications of obesity.
High fat intakes (or low carbohydrate intakes) may also contribute to weight gain (1, 2). Dietary fat varies from day to day (3) and a shift from a high-carbohydrate to a high-fat diet results in a transiently positive fat balance (4–7). This occurs because it takes several days for fat oxidation to match the increased fat intake. After several days, fat oxidation rises to match fat intake and fat balance is achieved. Failure to compensate for the positive fat balance that occurs during the shift to a high-fat, low-carbohydrate diet by increasing energy expenditure (EE) or by a decrease in food intake results in the gain of fat mass.
Physical activity appears to be effective in preventing weight gain (8–10), although the exact mechanisms are not entirely clear. This may be partly because physical fitness is associated with an increase in the cellular machinery necessary to oxidize fat (11). In an earlier study, we examined the effects of both a high- and a low-carbohydrate diet in sedentary men and in 2 groups of athletes, 1 group with aerobic training and the other with weight training (12). In that study, there was a trend toward an effect of physical fitness level on fat oxidation after 7 d of a high-fat, low-carbohydrate diet. This suggested that differences in habitual activity or physical fitness may influence the adaptation to a high-fat, low-carbohydrate diet. Interpretation of substrate balances in that study was confounded because all of the men were in positive energy balance (12). Improved control of energy balance now allows us to reduce this difference between energy intake and EE to less than half that in the earlier study (13).
We hypothesized that the ability of an individual to adapt to a high-fat diet might be related to their level of physical fitness as assessed by maximal oxygen consumption (
SUBJECTS AND METHODS
Study volunteers
Six male volunteers were recruited via print advertising and completed comprehensive laboratory and physical examinations before signing an informed consent document. Men who were smokers, taking medications, or who performed >2 h of weekly aerobic activity were excluded. The study protocol was approved by the local Institutional Review Board.
Protocol
Before the 5-d stay in the respiratory chamber, volunteers were fed a standard weight-maintenance diet that provided 37% of energy as fat for 4 d. The first day in the metabolic chamber the dietary fat content was also 37% of energy; this was raised to 50% for the next 4 d in the chamber.
Prediction of energy requirements before entry into the metabolic chamber
The resting metabolic rate (RMR, kJ/24 h) and respiratory quotient (RQ) of subjects in a semirecumbent position who had fasted overnight were measured with a metabolic cart by using a ventilated-hood system (model 2900Z metabolic cart; Sensormedics, Yorba Linda, CA). A triaxial activity monitor (Tritrac model 3RD; Hemokinetics, Madison, WI) was used to estimate energy requirements and treadmill time within the metabolic chamber by using the following equation:
RESULTS
The study population included healthy, but sedentary, young men with similar anthropometric characteristics (Table 1). A factor of 1.4 x resting EE was used to calculate energy intake. As shown in Figure 1, energy intake was actually closer to 1.5 x RMR. This was because the metabolizable energy content of the diet was closer to 93% than to 90%, which was used to predict energy requirements (see Eqs 1 and 2 in Methods). The diet composition measured in the laboratory is shown in Table 2. Overall, dietary fat and carbohydrate intakes were similar to the target values. EEs during the 5 d in the respiratory chamber are also shown in Figure 1. Energy intake was closely matched to EE (Table 3). Energy balance on days 2 and 3 was <800 kJ/d. The rise on day 4 reflected an uncompensated decrease in EE.
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TABLE 1.. Characteristics of the study population1
FIGURE 1. . Mean (±SEM) ratios of daily metabolizable energy intake (EI: food energy - fecal energy) to resting metabolic rate (RMR) measured by indirect calorimetry, ratios of daily energy expenditure (EE) in the metabolic chamber to RMR measured by indirect calorimetry, and daily energy balances (metabolizable EI - EE) at baseline (B) and on days 1–4 of a high-fat, low-carbohydrate diet. n = 6.
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TABLE 2.. Diet composition1
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TABLE 3.. Energy intake, energy expenditure, fecal energy, and energy balance
The increase in dietary fat resulted in the expected fall in nonprotein RQ (npRQ) (Figure 2; P < 0.05 by repeated-measures ANOVA). The individual values for each chamber day are also presented in Figure 2. The interindividual variability in the rate of change in npRQ was large. It is notable that one individual did not appear to increase fat oxidation under sedentary conditions, as evidenced by a lack of change in npRQ (Figure 2, •; bottom panel).
FIGURE 2. . Mean (±SEMs) and individual (bottom panel) changes in 24-h nonprotein respiratory quotient (npRQ) during adaptation to an isoenergetic high-fat (low carbohydrate) diet expressed as for the high-fat, low-carbohydrate diet for 4 d. Dietary fat at baseline (B) was 37% of energy. *Significantly different from baseline, P < 0.05. The arrow represents the expected change in RQ with the high-fat diet if fat oxidation and fat intake were equal. n = 6.
Daily macronutrient balances are shown in Table 4. As expected from the significant changes in npRQ (Figure 2), there was a trend toward an increase from baseline in fat balance when subjects ate the isoenergetic high-fat diet. Carbohydrate balance became negative during the first day of isoenergetic high-fat feeding and remained negative for the remainder of the 4 d of the high-fat diet. Nitrogen balance became positive during the high-fat diet. Protein oxidation decreased as a result of isoenergetic high-fat feeding (P < 0.05 for comparison of baseline fat balance to that for days 1, 2, 3, and 4; Table 4).
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TABLE 4.. Macronutrient intake, oxidation, and balance1
Next, we explored the sources of interindividual variability in fat balance during high-fat feeding under sedentary conditions. Free-living
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TABLE 5.. Simple correlation coefficients (r) between baseline population characteristics and cumulative fat balance (g/4 d) over the 4-d feeding period1
FIGURE 3. . Regression plot of the relation of cumulative fat balance to the fasting insulin concentration, postabsorptive respiratory quotient (RQ), and maximal oxygen consumption (
In an attempt to determine the best correlate of fat balance, insulin concentration,
FIGURE 4. . Regression plot of the relation of fat balance to carbohydrate balance during the shift to a high-fat diet expressed as the cumulative (4 d) fat and carbohydrate balances for each of the 6 male volunteers. Cumulative fat balance (MJ/d) = 6.4 – 0.77 x cumulative carbohydrate balance (r2 = 0.88, P < 0.05).
DISCUSSION
In this study, we showed that lean, sedentary young men differed in their response to a diet that is lower in carbohydrate and higher in fat than their usual diet while living in a respiratory chamber for 5 d. Some men came closer to achieving fat balance than did others. Nitrogen balance also became positive when the subjects ate the higher-fat diet. Baseline insulin concentrations, postabsorptive RQ, and
A high baseline RQ, ie, increased carbohydrate oxidation, has been identified as a predictor of weight gain or weight regain in several studies (15–18). In our study, the individuals with the highest baseline RQs also had the highest baseline insulin concentrations and lowest baseline
Fat oxidation in muscle can be modulated by several factors. Exercise increases fat oxidation in muscle by increasing the activity of lipoprotein lipase (11) and carnitine O-palmitoyltransferase I (23) and the number of mitochondria (24). Physical fitness is correlated with the concentrations of enzymes needed to oxidize fatty acids (11). Collectively, these processes enhance the availability of fatty acids, their transport into mitochondria, and their rate of oxidation by muscle.
When interpreting the current data from the viewpoint of fat oxidation, we note that 76% of the variance in fat balance could be accounted for by the
Previous studies identified several factors that alter the rate of adaptation to high-fat diets. First, in young women who were restrained eaters, fat balance was more positive after 3 d of eating a isoenergetic high-fat diet than in nonrestrained women eating the same diet (27). Second, obesity may also play a role. Although lean individuals eventually adjust fat oxidation to match fat intake, obese individuals adapt slowly to high-fat feeding (2). Obese subjects showed no relation between the amount of dietary fat consumed and the amount of fat oxidized. On the other hand, lean subjects, like those in our study and the study of Schrauwen et al (7), increased their fat oxidation to match intake. These interindividual differences may translate into differences in weight gain over time when individuals are exposed to a high-fat diet. Thomas et al (2) pointed out that "it is possible that individuals differ in how quickly equilibrium between food quotient (FQ) and respiratory quotient (RQ) is achieved...and that time course differences may be important in determining susceptibility to dietary obesity."
Impaired fat oxidation is a characteristic of the formerly obese population. Astrup et al performed a series of studies in which the adaptation to a high-fat diet was studied in formerly obese women. These women, who had reduced their weight to within 10% of ideal body weight and had been weight stable for 2 mo, were compared with age- and BMI-matched never-obese women. The rate of fat oxidation was then measured acutely after a high-fat (50% of energy) meal (28) or after a 3-d high-fat diet (29, 30). Under both the acute and chronic conditions, fat oxidation was suppressed in the formerly obese women. This suggests that these women had a low capacity to oxidize fat.
High-fat foods are energy dense and palatable, potentially increasing their overall consumption (31, 32). In the present study, altered intake was not permitted because the experimenters manipulated EE and energy intake. When diets with different fat contents are fed covertly, adaptation is slow (33). However, when subjects are familiar with the available foods dietary adaptation may be more effective (34) and may also be related to the perceived carbohydrate content of the foods. One component of the adaptation to energy-dense and highly palatable foods may be the rate at which carbohydrate oxidation is inhibited and the rate at which fat oxidation can be increased. The present study suggests that this response time is highly variable.
Genetic factors may also play a role in these differential responses to lower-carbohydrate diets. Several animal models have been used to map genes related to the susceptibility to increases in body fat when animals eat a high-fat diet (35). Although the individual genes have not been identified (36), the fact that these differences exist in animals is consistent with the observations of individual differences noted here.
In summary, this study showed a delay in the rise in fat oxidation when healthy lean young men were shifted from a 37%-fat diet to a 50%-fat diet. Individuals in whom carbohydrate oxidation decreased had a less positive fat balance during the high-fat feeding. There was a striking degree of variability between subjects in fat balance over the 4-d feeding period. Fat balance was negatively correlated with the degree of physical fitness (measured by
ACKNOWLEDGMENTS
We acknowledge the expert participation of the volunteers and Susan Mancuso for her detailed study coordination.
REFERENCES