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Unité INRA 914 de Physiologie de la Nutrition et du Comportement Alimentaire, Institut National Agronomique Paris-Grignon, 75231, Paris cedex 05, France
1To whom correspondence should be addressed. E-mail: even{at}inapg.fr.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • meal pattern • energy intake • dietary self-selection • protein to energy ratio
Rats that are allowed to select their diets [dietary self- selection (DSS)2] are able to regulate their daily energy intake, body weight gain, and reproductive cycle (1–4). Broad variations in macronutrient selection nonetheless occur. In the case of protein, the intake required to maintain a stable nitrogen balance and protein turnover in human adults and rats has been established at 10–15% of total energy, and a high protein intake is often considered an unnecessary burden, particularly for the liver and kidneys (5–7) With DSS, rats spontaneously ingest up to 30% or even 50% of their total energy intake in the form of protein. Such high-protein intakes occur more frequently when the macronutrients are available separately than when two or more mixed diets that contain different proportions of all macronutrients are offered (8–20). In the latter case, the reason for the lower protein intake may be that it cannot occur without the simultaneous ingestion of carbohydrate and fat, and thus may be limited by the mechanisms regulating energy and/or carbohydrate and fat intake (8). On the other hand, the broad variability in protein selection may be because the mechanisms controlling protein intake are limited; rats are able to recognize when they are consuming insufficient or excessive amounts of protein (11,21). However, several studies have shown that protein intake is tightly controlled (8,22,23). In particular, compared with carbohydrate-restricted rats that do not develop an appetite for carbohydrate (24), those that have been protein restricted do increase their protein intake when protein is made available (18,25–29). Exercise, which increases protein requirements (30) also increases protein intake in humans and rats (31–33). In addition, rats selecting a high-protein diet (8), as well as those fed a high-protein diet (34), do not grow more rapidly than rats fed a maintenance diet containing 20% protein. This suggests that the high protein intake has a more complex rationale than simply achieving nitrogen balance. It was also recently reported that male rats fed a high-protein (50%) composite diet from weaning until maturity had lower basal insulin levels and reduced amounts of gonadal and retroperitoneal fat (19), suggesting improved control of body weight and glucose homeostasis.
Humans, like rats, tend to ingest more protein than is required to simply achieve nitrogen balance, and protein intake may reach 30–35% in specific groups (35,36). In this context, it is important to understand more clearly the motivations underlying the spontaneous ingestion of a high proportion of the daily energy intake in the form of protein. In the present study, we examined the meal pattern of rats allowed to select their protein intake separately from a fat-carbohydrate mixture. This intermediate design between macronutrient selection and selection between mixed diets was chosen to give the rats an opportunity to ingest protein independently of fat and carbohydrate, and also to establish the fat to carbohydrate ratio at that formulated according to AIN93 recommendations, thereby avoiding any variability associated with differences in the relative preference for fat and carbohydrates. We investigated the possible occurrence of any specific common feeding strategies that would indicate that selection of a high-protein diet during DSS was indeed the result of a finely tuned control of the protein intake, and might highlight potential physiologic mechanisms motivating the choices. Complementary experiments were conducted to confirm that the amount of protein consumed was not dependant on a particular type of protein, and that protein selection was not due to the higher palatability of the protein diet.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Diets.
Six diets were used during this study (Table 1). The P14 diet was an AIN-93M modified diet (37), but with 140 g total milk protein/kg diet in place of casein. The P50 diet was also an AIN-93M modified diet containing 500 g total milk protein/kg diet. The additional protein replaced an equivalent amount of sucrose and starch. The dietary self-selection (DSS) regimen comprised two diets, a fat-carbohydrate mixture (FC) and total milk protein (P), whey proteins (W) or casein (C), depending on the study. An FC mixture with a fixed fat to carbohydrate ratio was chosen to prevent any interactions between the relative intake of fat and carbohydrate and the intake of protein, thus allowing the study to focus on protein selection. In addition, the fat to carbohydrate ratio in the FC diet was adjusted to equal the ratio in the AIN-93-based P14 diet (1:18 by weight). All diets were supplemented with vitamins, minerals, and fiber. They were rendered semiliquid by moistening with water (1:1) to prevent spillage. When calculating the energy intake, dilution (by dividing the energy value of the powder in half) and water evaporation [by keeping additional food cups in the room and measuring water loss (usually 
2%) during the period of measurement] were taken into account.
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Male adult Wistar rats (n = 18; Harlan), weighing 160–190 g at the start of the experiment were housed individually in a quiet, temperature-controlled room (22 ± 2°C). They were maintained under an artificial 12-h light:dark cycle (lights on at 0600 h) and had free access to food and water. After adaptation to the laboratory conditions while consuming the P14 diet, they were offered a choice between the FC-mix and P (n = 6), W (n = 6), or C (n = 6). The relative 24-h intakes of FC-mix and protein in the three groups were measured after 2 wk of adaptation to the choice procedure, i.e., at a time when the selection between the FC-mix and protein was established and stable.
Expt. 2: relative palatability of the FC-mix and whole-milk protein.
Male adult Wistar rats (n = 10; Harlan), weighing 220–240 g at the start of the experiment were housed as in Expt. 1. After adaptation to the laboratory conditions while consuming the P14 diet, all food was removed from the cages at 1200 h and the rats were offered a choice between the FC-mix and P at the onset of night (1800 h). The relative intakes of the two foods were measured 15, 30, 60, 90, and 120 min after the initial presentation of the two diets.
Expt. 3: analysis of meal pattern with DSS between a FC-mix and whole-milk protein.
Male adult Wistar rats (n = 12; Harlan), weighing 160 g at the start of the experiment were housed as in Expts. 1 and 2. Because one rat never adapted to the choice procedure, results were analyzed for only 11 of these rats. Eight of the 11 rats were housed in cylindrical Plexiglas cages equipped to monitor the meal patterns (see below). The other three were kept in stainless steel wire cages throughout the study; only their 24-h energy intake was recorded by the daily weighing of food cups. After adaptation to the laboratory conditions, the rats were fed the P14 diet for 2 wk (P14 period), then allowed a free choice between the FC and P diets for 2 wk (DSS period), and finally fed the P50 diet for 10 d (P50 period). Energy intake and body weight were measured daily between 1700 and 1800 h. Meal patterns were recorded on d 13 and 14 of the P14 period, on d 1, 2, 3, 4, 5, 13, and 14 of the DSS period, and on days 1, 2, 3, and 10 of the P50-period. Meal pattern recordings started at 1800 h and ended at 1700 h on the next day (23 h). Energy intake was recorded by means of strain-gauges placed under the food cups (AHA500, Phimesure, accuracy of 0.1 g) and connected to a 34970A data acquisition/switch unit (Agilent Technology) plugged into a personal computer that was programmed to record data every 10 s via the DAC Express software (Agilent Technology). For each rat, the exact feeding pattern was established according to the following criteria: eating bouts were a minimum of >0.1 g and lasted for >10 s. Two feeding bouts were considered to be two separate meals when the interval between them was >10 min (38). The amount of food ingested was converted into kJ of metabolizable energy as a function of its composition and digestibility (Table 1). During the DSS period, several types of meals were defined as follows according to the order in which FC and P were ingested: 1) simple meals, during which rats ingested a single diet, either P or FC; ii) mixed meals, during which rats ingested both P and FC. Mixed meals were further broken down into four categories, depending on the sequence of FC and P ingestion: P-FC (meals beginning with the ingestion of P and ending with FC), FC-P (meals beginning with the ingestion of FC and ending with P) and based on the same definitions, P-FC-P and FC-P-FC meals.
Expt. 4: analysis of body composition after 15 d of DSS.
This study was performed to supplement Expt. 3 by analyzing the effects of DSS on body composition. Male adult Wistar rats (n = 12; Harlan), weighing 160–190 g at the start of the experiment were housed individually, as in the other studies. They were fed the P14 maintenance diet for 2 wk, after which 6 rats were switched for 2 wk to self-selection between the FC-mix and P, and the other 6 rats continued to consume the P14 Diet. Body weight was recorded periodically and the protein intake in DSS rats was measured during wk 2 of the DSS period. At the end of the study, the rats were killed by an overdose of anesthetic (pentobarbital, 40 mg/kg) and their body composition was measured by dissecting and weighing the main tissues.
Statistical analysis.
Values are expressed as means ± SEM. Comparisons between 2 group means were performed using the bilateral Student’s t test. ANOVA (SAS program, SAS Institute) was used for between-group comparisons of more than two means and repeated measures ANOVA was used for between-group comparisons during DSS. ANOVAs were followed when required by Tukey’s post-hoc test. Within-group changes in energy intake vs. the Control P14 period were analyzed by bilateral paired t test with Bonferroni corrections to take into account the repetitions in the comparisons. The distribution of the meal sequences during DSS was analyzed with the 
2 test. A probability of P< 0.05 was chosen as the criterion for significance.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Body weight. During the P14 period, rats gained weight at a constant rate of 8.4 ± 0.3 g/d (Fig. 3). Body weight decreased on d 1 of the DSS period but increased again as early as d 2. Daily body weight gain during the DSS period (4.8 ± 0.2 g) was lower than during the P14 period, however (P < 0.001). The switch to the P50 diet did not affect body weight gain compared with the DSS period (4.4 ± 0.3 g).
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70% of mixed meals, indicating a clear preference for meals terminated by the ingestion of protein (n = 142 meals, 2 = 23.7, P < 0.001 vs. a 50–50 distribution).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The observation that rats ingested >40% of their energy in the form of protein when given the option of selecting independently from several nutrient sources was in line with numerous previous studies (8–20). The most meaningful demonstration of the elevated protein intake of rats was made in the very detailed examination by Musten et al. (8), who showed that rats offered a choice between a fat-carbohydrate mixture and composite diets with various protein contents, consumed the protein-containing diet almost exclusively for as long as the protein level in the composite diet remained <40%; when the protein content of the composite diet was >60%, they stabilized their protein intake at 35–40% of their energy intake, ingesting both the protein diet and the fat-carbohydrate mixture. It was also shown that earlier food restriction specifically increases non-protein intake (14,39), thus supporting the interpretation that the level of protein selection is adjusted to adapt the P/E ratio of the diet to physiologic requirements. In the present study, we also verified that the high protein intake was not strictly dependent on the whole-milk protein used in the DSS study but occurred also with casein, as well as with whey protein; all three of these proteins qualify as "high quality." The fact that protein selection levels were also >40% with whey protein and casein (which differ considerably in terms of their organoleptic properties, rates of digestion and absorption, and amino acid patterns) confirmed the robustness of this choice. We also verified in Expt. 2 that whole-milk protein was much less preferred than the FC-mix and ruled out the possibility that the high whole-milk protein intake during the DSS study resulted from a taste preference. Thus, the observations that protein intake is often >40% strongly suggests that positive metabolic signals motivate such a choice. Analysis of the feeding patterns with DSS may provide some answers to this question.
When the diet was self-selected, energy intake was markedly limited to the night period (90%) compared with a single diet (75%), and 80% of energy intake during the light period took the form of pure protein meals. One possible interpretation of our data is that rats self-selecting their diet were able to adjust their energy intake and macronutrient balance to favor a cycle of lipolysis during the day and lipogenesis at night, a cycle that plays an important role in the control of body weight, satiety, and sleep (40,41). When meals were initiated during the light phase, rats preferentially selected protein meals, which limited insulin secretion and the reversal of their lipolytic status. In the long term, the establishment of such an equilibrium should lead to reduced energy requirements, and hence decreased energy intake, body weight gain, and adiposity, which was indeed observed in this study and others (42,43). Decreased energy intake and a reduced rate of weight gain also occurred during the P50 period, probably because the high protein content of this composite diet allowed for metabolic adjustment close to that established with DSS. However, daytime energy intake immediately reverted to 25% of the daily energy intake; the reason for this reversal cannot be assessed from the present data. It is interesting to note, however, that this excess daytime energy intake during the P50 period allowed the rats to ingest almost exactly the same amount of protein as they did during the DSS period. In addition, the fact that body weight gain and daily energy intake were not significantly affected when rats were switched from DSS to the P50 diet suggests that the high protein content of the P50 diet probably prevented at least in part the attenuation of the light-dark cycle of lipogenesis/lipolysis. This may explain the apparently favorable long-term consequences on adiposity and insulinemia in rats fed a P50 diet (34). The situation clearly differed when rats consumed the P14 diet. During the light period, P14-fed rats ate nearly 3 times the amount ingested by the DSS rats, and also ate a high-carbohydrate diet. This ingestion of substantial amounts of carbohydrate with the P14 diet during the light period likely elevated plasma insulin levels at a time when they should be low to favor mobilization of the lipids stored at night. Thus, the daytime carbohydrate intake probably reduced the magnitude of daytime lipogenesis, which may have induced the daily sequestration of some excess fat and led to the higher rate of weight gain that was fueled by the increased energy intake.
Another interesting observation was that after 1 or 2 d of DSS, the rats structured their mixed meals so as to ingest protein after ingesting the FC diet. These results agree with the observations of Jean et al. (19), who reported that rats spontaneously selected high levels of both protein (30–48%) and lipids (30–60%). Based on a 30-min interval between 2 meals, they ingested most of their energy in the form of mixed meals; in most cases, these started with carbohydrate bouts and ended with protein bouts. Our results also agree with those of Konkle et al. (20), showing that carbohydrate meals were eaten first by rats selecting equal proportions (45% each) of carbohydrate and protein. In contrast, Miller et al. (44) reported that rats choosing macronutrients selected a higher level of fat intake (52%) and a lower level of protein intake (19%) than those we studied and, based on an intermeal interval of 7.9 min, ate most meals from a single food cup. Although it is difficult to account for the many differences in dietary selection that occur during this type of study, the high fat intake and consequently, the high number of high energy, fat meals, may have favored ingestion from a single food cup. Miller et al. (44) did not specifically analyze protein intake, but in agreement with our results, indicated that the carbohydrate tended to be favored as the first nutrient ingested. The conclusions on the prevalence of mixed vs. single meals may therefore vary as a function of the macronutrient intake and intermeal interval. However, the feeding sequence that consists in ingesting carbohydrates, then protein, may be quite common, and is likely reinforced by positive postingestive signals. One possible positive postingestive effect may be a reduced amplitude and/or duration of insulin release and/or the establishment of a more favorable insulin to glucagon ratio, thus improving the immediate utilization of ingested nutrients and limiting lipid storage. It is interesting to note that in a study by Jean et al. (19) in which protein ingestion was also reported to be at the end of meals, the body weight and body adiposity of self-selecting rats was not increased, despite a relatively high lipid intake (30% in males, up to 60% in females), levels that induce obesity in rats (even in the absence of increased energy intake) when given in a single composite diet (45). Another mechanism that could motivate the carbohydrate then protein sequence is the control of blood tryptophan and thus brain serotonin because it was proposed that the ratio of dietary protein to carbohydrate selected by rats might be adjusted so as to not change brain serotonin (23,46). In line with the possible specific metabolic consequences of ingesting protein after carbohydrates, brain serotonin levels may be optimal in rats consuming a high level of protein when a protein-free diet or a diet with a very high protein content can be ingested separately and after carbohydrates or, as during our study, after a fat-carbohydrate mix.
In conclusion, when taken together, the results of the present study show that with DSS, rats exhibited a well-structured and reproducible organization of their meal patterns, selected a high level of protein, decreased their energy intake, and reduced their internal fat depots. These observations suggest that although only 14% protein in the diet is sufficient to conserve nitrogen and promote weight gain, it is not the best proportion for optimizing the processes involved in controlling energy metabolism and promoting lean rather than fat body mass. Thus, the metabolic effects of dietary amino acid intake certainly go beyond their strict role of renewing body protein. In this context, amino acids must be considered as energy sources in the same way as carbohydrates and lipids. Indeed, they participate in energy production in several ways, i.e., they can be used efficiently by the liver to generate glucose, and they can be oxidized directly during the Krebs cycle in which they also play an important anaplerotic function that favors oxidative metabolism and thus improves lipid oxidation. For these reasons, the fact that rats self-selecting their diets often ingest a large proportion of their daily energy in the form of protein (particularly when it is available separately as a pure source), may be motivated by improved opportunities to regulate their energy intake and ensure protein ingestion when it is most required as well as reduced meal-induced insulin secretion. This latter phenomenon has the potential to diminish the amplitude of glycogen and lipid synthesis/degradation cycles and in the long-term, may favor lower blood insulin levels and improve insulin sensitivity. Finally, because protein is digested more slowly than carbohydrates, selecting a high-protein diet may provide the advantage of a gradual supply of amino acids from the digestive tract to fuel the regular production of glucose, which is less dependent upon insulin secretion.
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FOOTNOTES |
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Manuscript received 1 October 2003. Initial review completed 1 November 2003. Revision accepted 10 December 2003.
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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