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Nutrient Requirements

Increasing the Protein Content in a Carbohydrate-Free Diet Enhances Fat Loss during 35% but Not 75% Energy Restriction in Rats

Institut National de la Recherche Agronomique, Unité INRA-INAPG de Physiologie de la Nutrition et du Comportement Alimentaire, Institut National Agronomique Paris-Grignon, F75231 Paris cedex 05, France and ^* ENSIA, Département Science de l’Aliment, Laboratoire de Chimie des Substances Naturelles, 91744 Massy cedex, France

¹To whom correspondence should be addressed. E-mail: fromenti{at}inapg.fr.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The purpose of the present study was to test the influence of the amount of protein in a carbohydrate-free diet during a weight reducing program using severe (75%) or more moderate (35%) energy restriction in rats. In Expt. 1, 3 groups (n = 6) consumed ad libitum a high-carbohydrate, low-fat diet [P21C69L10 containing 21% of energy as protein (P21), 69% carbohydrate (C69) and 10% lipids (L10)], a high-carbohydrate, high-fat diet (P21C34L45), or a carbohydrate-free, high-fat, high-protein diet (P55L45). In Expt. 2, 7 groups (n = 7) were studied. For 20 d, groups 1–4 consumed ad libitum diets containing macronutrients at the proportions indicated in their designations [P14C56L30 (control diet), P30L70, P50L50, and P90L10]. Groups 5–7 were pair-fed the same diets at the level of the spontaneous intake of the P90L10 group on the previous day (35% energy restriction). In Expt. 3, 5 groups (n = 7) were fed 1 of the following diets for 20 d. Group 1 consumed the control diet (P14C56L30) ad libitum. Groups 2–5 were energy restricted to 25% of the daily energy intake of group 1 with diets varying in their protein and lipid concentrations (P14C56L30, P50L50, P70L30, and P90L10). A high-fat content in the diet devoid of carbohydrate did not increase energy intake and body adiposity and neither body weight nor body composition was significantly affected by the protein to lipid ratio when energy restriction was 75%; however, a protein content > 50% preserved lean body mass at the expense of fat mass when energy restriction was 35%. Our results show that the absence of carbohydrates from the diet induces a low energy intake and the preferential deposition of protein.

KEY WORDS: • obesity • body composition • high-protein carbohydrate-free diet • high-fat diet • rats

Diet composition is believed to influence total energy intake and long-term changes to body weight and body composition, but the precise role of different macronutrient combinations, i.e., the relative importance of carbohydrate, fat, and protein, remains unclear (1–5). Usually, most diets are relatively low in protein (i.e., 10–15% of energy); in this context, the so-called "high-fat" diets under which body weight, body fatness, and insulin resistance are increased, are in fact diets containing high levels of both fat and carbohydrate. In this framework, different processes may play crucial roles in the negative effects on energy balance of these high fat, high carbohydrate diets, including 1) the high palatability and increased energy density of such fat- and carbohydrate-rich diets, favoring energy intake (6,7); 2) the simultaneous ingestion of carbohydrates that stimulate insulin secretion and fat that can be readily stored at low energy cost under the condition of high insulin level (8,9); and 3) the concomitant apparent lack of stimulation of fat oxidation by fat intake, at least in obesity-prone subjects (10,11). In contrast, high-protein diets seem to reduce energy intake, reduce body weight, and favor protein rather than lipid deposition (12–15). Accordingly, the use of high-protein diets has been advocated during weight reducing therapies using very low-energy diets to favor simultaneously the maintenance of body protein and the loss of fat (16–18). In addition, the lowered insulin secretion resulting from the absence or low levels of carbohydrate in the diet can be expected to reduce postprandial fat deposition. Thus, the purposes of the present study were as follows: 1) to determine whether a high-fat diet per se or only the combination of high-fat and high-carbohydrate levels in the diet would have a detrimental effect on the energy balance, and 2) to test the influence of the amount of protein in carbohydrate-free diets on body weight and adiposity in rats with ad libitum consumption and during 35 or 75% energy restriction.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Animals and diets. Wistar (Iffa Credo, n = 18) or Sprague-Dawley (Harlan, n = 84) male rats, individually housed in stainless steel cages located in a temperature-controlled room (23 ± 1°C) with a 12-h light:dark cycle (lights on 0600–1800 h), were studied during these experiments. All of the diets were AIN 93M modified diets [(19); Table 1] and were prepared by the "Feed Preparation Laboratory" (INRA). Water was freely available throughout the experiments. Vitamins and minerals were not adjusted in the restricted diets.

    Expt. 2. Sprague-Dawley rats (n = 49) were acclimated to the laboratory conditions for 10 d while consuming ad libitum a control diet containing by energy: milk proteins 14%, carbohydrates 56%, and lipids 30% (P14C56L30). They were then distributed among 7 groups of 7 rats with similar mean body weights (270 ± 2 g). Thereafter, they consumed ad libitum the same P14C56L30 diet for another 9 d (baseline period). They then were fed the following diets for 20 d: 4 groups consumed P14C56L30, P30L70, P50L50, or P90L10 ad libitum, and 3 groups were fed the designated diets but pair-fed an amount based on the spontaneous intake of the P90L10 group on the previous day (P14C56L30-PF, P30L70-PF, P50L50-PF).

    Expt. 3. Sprague-Dawley rats (n = 35) were acclimated to the laboratory conditions for 10 d while consuming ad libitum the same control diet (P14C56L30), as in Expt. 2. They were then distributed among 5 groups of 7 rats with similar mean body weights (390 ± 5 g). They consumed ad libitum the same P14C56L30 diet for a further 9 d (baseline period). Thereafter, they were fed the following diets for 20 d: 1) one group consumed the P14C56L30 diet (control) ad libitum and 4 groups were food restricted to 25% of the mean daily energy intake of the control group with each of the experimental diets: P14C56L30-R, P50L50-R, P70L30-R, P90L10-R.

    Food intake and body composition. During the experimental periods, body weight and spontaneous food intake were measured daily. An energy efficiency ratio was calculated as the weight gain (g) during the experimental period divided by the cumulative energy intake over the same period (kJ). Carcass analysis was performed at the end of the 3 experiments. After overnight food deprivation, the rats were weighed, anesthetized with an overdose of sodium pentobarbital (45 mg/kg), and heparinized. Blood was collected from the vena cava. The following tissues and organs were then dissected and weighed to the nearest 0.01 g: skin, stomach, intestine, spleen, liver, heart, kidneys, brain, carcass (muscles with skeleton), scapular brown adipose tissue (SBAT), epididymal, retroperitoneal, mesenteric, and subcutaneous white adipose tissues (WAT). Lean body mass was defined as sum of the weight of the internal organs plus the carcass and the brain. An adiposity index (AI) was calculated by dividing total WAT weight by the weight of the stripped carcass.

    Statistics. Results are expressed as means ± SEM. Data were evaluated by ANOVA or ANOVA for repeated measures (SAS, version 6.11). When appropriate, a post-hoc Tukey’s Honestly Significant Difference was used to compare between-group means when the ANOVA test was significant. Statistical significance was set at P < 0.05.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Expt. 1. Energy intake and body composition of rats that consumed ad libitum high-fat diets with or without carbohydrate. During the baseline period (until d 0), all of the rats (n = 18) consumed an amount of energy (500 ± 4 kJ/d) similar to the P21C69L10. Body weight gains were also similar (6.7 ± 0.6 g/d). After the 60-d feeding period with the experimental diets, rats fed the P21C34L45 diet ate more (group effect P < 0.05, time effect, P < 0.0001; group x time effect P < 0.0001), weighed more, and had a greater proportion of body fat than those in the other 2 groups (Table 2). This was the result of both a higher energy intake and a higher energy efficiency ratio. These results indicated that the association of high fat and high carbohydrate but not high fat per se increased energy intake and adipose tissue development and that eating a high-protein diet decreased energy intake.

View larger version (34K): [in this window] [in a new window]   FIGURE 1 Body weight (upper panel) and daily energy intake (lower panel) of rats consuming different carbohydrate-free diets ad libitum or 35% energy restricted. Values are means ± SEM, n = 7. Means without a common letter differ, P < 0.05.

View larger version (19K): [in this window] [in a new window]   FIGURE 2 Adiposity index of the rats as a function of the protein concentration of the diet. Black circles: Ad libitum consumption of rats in Expt. 2. Crosses: rats restricted to 65% of ad libitum intake in Expt. 2. Open squares: rats restricted to 25% of ad libitum intake in Expt. 3.

The weight of SBAT was lower in P30L70- and P50L50-fed rats than in rats fed P14C56L30 and was the lowest in P90L10-fed rats (Table 3). In pair-fed rats, SBAT weight was more uniform; it was lower only in the P30L70-PF-fed rats than in the other groups (Table 4).

    Expt. 3. Energy intake and body composition of 75% energy-restricted rats. During the baseline period, all rats consumed the high-fat diet (P14C56L30) ad libitum and had similar energy intakes (493 ± 4 kJ/d). During the experimental period, the unrestricted control group consuming the P14C56L30 diet ad libitum maintained its level of energy intake (446 ± 5 kJ/d) and gained weight regularly (3.9 ± 0.5 g/d). All restricted rats lost weight at a similar rate (5 g/d) so that at the end of the 20 d of energy restriction, body weight loss was similar in all 4 restricted groups (P14C56L30-R, –113.4 ± 3.3 g; P50L50-R, –103.7 ± 15.1 g; P70L30-R, –126.6 ± 13.7 g and P90L10-R, –119.0 ± 2.9 g). In rats consuming ad libitum the P14C56L30 diet, all tissues and organs other than kidneys weighed more, with a lower lean body mass, and a higher AI than energy-restricted rats (P < 0.0001) (Table 5). In contrast, all energy-restricted rats, whatever diet they were fed, had similar weights of all their organs and tissues except for kidneys, similar indices of muscle mass, and similar AIs, showing that the composition of the diet fed during severe energy restriction did not influence body composition.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

These studies were designed to test the hypothesis that a "high-fat" diet leads to overfeeding and obesity only when the diet is also rich in carbohydrates because we anticipated that mixing fat and carbohydrates would favor insulin secretion and consequently lipid storage, whereas in the absence of carbohydrate, a lower insulin response to feeding would favor lipid oxidation rather than storage. The results confirmed this hypothesis by showing that in rats consuming food ad libitum, only 30% of lipids in a diet that also contained carbohydrates (56%) increased energy intake and adiposity more than diets containing up to 50 or 70% of lipids but devoid of carbohydrates. This demonstrated that the high fat content of a diet per se is not sufficient to promote hyperphagia and obesity. On the basis of this result, it seems that carbohydrates are necessary to stimulate the effect of dietary fats on energy intake and adiposity. These findings agree with recent observations that a carbohydrate-free, high-fat, high-protein diet was as efficient or even more efficient than a high-carbohydrate, low-fat diet in reducing weight and fat tissue in humans (20).

The results of this study also indicated that reduced energy intake and AI were associated mainly with protein content rather than lipid and carbohydrate content. It was observed previously that increasing the level of protein in a high-carbohydrate, low-fat diet usually decreased energy intake (21–23). During the present study, rats with free access to the P50L50 diet also reduced their spontaneous energy intake, thus showing that the anorectic response to a high-protein diet does not require the presence of carbohydrates in the food. In addition, during both the ad libitum and energy restriction studies, AI was associated with the protein content rather than with the lipid content of the diet because the P14C56L30 diet was the one that most increased adiposity. This hypothesis is reinforced by numerous previous observations of carbohydrate-containing diets, showing that rats fed high-protein diets, or spontaneously selecting a high-protein intake during dietary self-selection, were leaner than rats fed or selecting lower levels of protein, a phenomenon observed whatever the fat to carbohydrate ratio is selected in parallel (4,14,15,21,24,25). However, it is also possible that a lower carbohydrate intake or the complete absence of carbohydrate after a higher intake of protein may have reduced insulin secretion and thus favored the utilization rather than the storage of ingested lipids (26). In other words, low-carbohydrate rather than high-protein diets may be the main factor responsible for reducing adiposity when the protein content of the diet is increased. The decrease in adiposity was also observed in the 35% energy-restricted rats in this study, but instead of an inverse relation between dietary protein and adiposity, 2 distinct groups emerged, one in which the adiposity index was 15% (P14C56L30 and P30L70 rats), and another in which the adiposity index was lower, i.e., 10% (P50L50 and P90L10 rats). The P14C56L30 diet led to a higher AI than expected given its lipid content, a result that may be due to its high-carbohydrate content.

Another result of this study was that the energy efficiency ratio did not vary as a function of the protein content of the diet, but rather was affected by the carbohydrate to fat ratio in the diet. Because the thermic effect of protein is high and the conversion of protein to glucose via gluconeogenesis is usually considered a costly process, we anticipated that the pair-fed groups of Expt. 3, rats that were fed the diets with the highest protein contents, i.e., P90L10 and P50L50, would exhibit a reduced energy efficiency. Because food intake was controlled, this would have resulted in a lower final weight and/or lower AI than that in rats fed the other diets, in particular the well-balanced P14C56L30 diet, but this was not the case. In addition, during Expt. 3, after the 20 d of severe energy restriction, the main differences in body composition involved a deficit of 10 g of lipid in rats fed diets with the highest protein content, or an energy deficit of 0.5 g or 4.5 kJ/d for a mean intake of >250 kJ/d. In other words, the excess energy cost of ingesting these diets was <2%, which is far below the extra cost that might have been anticipated from the expected specific dynamic effect of amino acids. Thus, the present results indicate that the energy cost of ingesting and metabolizing different foods with protein contents differing by as much as 60% was virtually identical, suggesting that using amino acids as an energy substrate was not more costly than using carbohydrates. This agrees with other previously published reports that energy efficiency is not decreased when the protein content of the diet is increased (27,28), but indeed, that high-fat diets generally increase energy efficiency (27). This is a challenge to the concept of an obligatory high thermogenic effect of protein, which is also disputed by the fact that the thermic effect of feeding is increased and energy efficiency is decreased in rats fed low-protein diets (29,30).

The final important observation was that in severely energy-restricted rats, body weight loss and body composition were not affected by diet. These results are in agreement with others (18,31). Whatever the diet, the body weight loss of restricted rats was more the consequence of a loss of white adipose tissue (60%) than of lean body mass (26%), without significant improvement to the maintenance of lean body mass in those fed the protein-rich P90L10 diet. In a situation of severe energy restriction, subjects are constantly in a state of negative energy balance, i.e., no net lipid storage occurs. The macronutrients provided by the meals are thus completely oxidized after ingestion, and diet composition cannot affect the metabolic fate of nutrients. The present observations indicate that the role of the macronutrient composition of a diet should be taken into account when mild-to-moderate energy restriction and refeeding after food restriction occur, rather than during very low-energy diets.

The diets used in this study were more carnivorous than omnivorous as used in modern human nutrition. If the absence of carbohydrate in the diets used in this study indeed played an important role in decreasing body fat and AI in rats with ad libitum consumption and 35% energy restriction, it will be necessary in future studies to test the influence of the ratio of protein to energy concomitantly with the fat to carbohydrate ratio in the diet and the resulting AI under conditions of ad libitum consumption and energy restriction (32). This would help to establish the composition of the diet most appropriate to favoring the maintenance of lean body mass at the expense of body fat. The issue of palatability should also be addressed because it may apply to human "low-carb" diets. In rats fed monotonous diets, however, palatability affects food intake only in the short term. For instance, when rats are allowed to choose the food they consume, they initially select carbohydrate and fat rather than protein because of their higher palatability, but within days, they establish their preference for protein (15) probably because as time passes, the postingestive metabolic responses take precedence over the initial palatability effect.

In conclusion, taken together with previous studies (18,33, 34) the present results illustrate the potential efficacy of energy restriction programs used in combination with manipulations of the macronutrient composition of diets. We advanced the hypothesis that an absence of carbohydrates from the diet and the expected high satiety value of proteins would induce a low energy intake and the preferential deposition of protein. Despite being poorly balanced, diets containing only protein and fat satisfied the hypothesis under conditions of ad libitum consumption and energy restriction, but the advantage of this approach did not persist when the energy intake was very low.

The present results suggest future experiments that include direct measurements of energy metabolism in rats fed these diets and in measurements of glucose and insulin metabolism to test directly the hypothetical explanations presented for the body composition changes. Further experiments would also involve diets that are more realistic for humans, i.e., use 20% protein and vary the fat to carbohydrate ratios compared with 35% protein with varied fat to carbohydrate ratios.

	FOOTNOTES

 
² Abbreviations used: AI, adiposity index; P21C69L10: 21% protein, 69% carbohydrate, and 10% lipids; P21C34L45: 21% protein, 34% carbohydrate, and 45% lipids; P55L45: 55% protein, 45% % lipids; P14C56L30: 14% protein, 56% carbohydrate, and 30% lipids; P30L70: 30% protein and 70% lipids; P50L50: 50% protein and 50% lipids; P90L10: 90% protein and 10% lipids; PF, pair-fed; R, energy restricted; SBAT, scapular brown adipose tissue; WAT, white adipose tissue.

Manuscript received 22 April 2004. Initial review completed 22 May 2004. Revision accepted 21 July 2004.

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TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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