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Weight, Protein, Fat, and Timing of Preloads Affect Food Intake
Physiology & Behavior, Vol. 62, No. 3, pp. 563–570, 1997 Copyright q 1997 Elsevier Science Inc. Printed in the USA. All rights reserved 0031-9384/97 $17.00 / .00
PII S0031-9384(97)00162-5
Weight, Protein, Fat, and Timing of Preloads Affect Food Intake M. PORRINI,* 1 A. SANTANGELO,* R. CROVETTI,* P. RISO,* G. TESTOLIN* AND J. E. BLUNDELL† *Department of Food Science and Technology, Division of Human Nutrition, University of Milan, Via Celoria 2, 20133 Milan, Italy and †Department of Psychology, University of Leeds, Leeds LS2 9JT UK Received 25 March 1996; Accepted 13 February 1997 PORRINI, M., A. SANTANGELO, R. CROVETTI, P. RISO, G. TESTOLIN AND J. E. BLUNDELL. Weight, protein, fat, and timing of preloads affect food intake. PHYSIOL BEHAV 62(3) 563–570, 1997.—Two foods, one rich in protein (HP) and one rich in fat (HF), were employed to evaluate the effect of macronutrients on food intake and to underline the differences that occurred when the foods were served as uniform meal, as first course of a varied meal, and as a snack 2 h before a varied meal. Our results showed that HP food always exerted a higher effect on both intrameal satiation and postingestive satiety than HF food. When a uniform meal was consumed, satiation for the specific food was reached before fullness; in this condition, sensory characteristics of foods played an important role in controlling food intake and made the uniform meal more satiating than the varied one. The consumption of a snack far from a meal did not contribute to satiety; consequently, gastric filling seems to be an important factor determining the amount consumed in a varied meal. q 1997 Elsevier Science Inc. Timing of preload
Weight
Water
Protein
Fat
THERE are many reasons why and how a specific food contributes to the satiety process and there have been extensive studies; as yet, however, no real conclusions have been reached. It is clear that certain nutrients are more satiating than others. Concordant results have been obtained for protein; some authors (2,10,22) demonstrated that there is a stronger action of protein on appetite than of fat or carbohydrate, but little is known about the mechanism that determines such an effect. The role of fat in appetite control is sometimes thought to be problematic. Dietary fat is associated with hyperphagia and the development of obesity, probably because it is palatable and has a high energy density (3,21). On the other hand, studies with human volunteers have suggested that the interaction of fat with gastrointestinal receptors may suppress hunger, induce satiety, reduce subsequent food intake, and delay gastric emptying (12,20,27,29). This issue has been called the ‘‘fat paradox (5). Weight and volume of food may play another important role, because filling and emptying of the stomach are important elements of satiety. The most familiar inhibitory signal to food ingestion is gastric distension. Geliebter et al. (8) demonstrated that, in man, food intake was reduced by inserting into the stomach a 400–600-ml intragastric balloon. Recently, Gustafsson et al. (9) found that, by increasing the dietary fiber content and the weight of the meal (by intrinsically bound water in food), satiety was higher. If volume and weight are key factors in controlling food intake, the contribution of water during a meal should be particularly considered, as we have suggested previously (17). In a recent study, Lappalainen (15) found that drinking 2 glasses of water affects subjective feelings of hunger and satiety during 1
Food intake
the meal due to gastric distension, but this effect is not maintained after the meal. Furthermore, it has been suggested that physiological variables may be influenced by different meal patterning (26). Although the consumption of a breakfast controls hunger and prevents subsequent overeating later in the day (30), discordant results are reported in the literature about the effect of food consumed 90 min before a test meal. Rolls et al. (23) found that there was no difference in food intake 90 min after eating a snack rich in fat or carbohydrates, whereas Blundell et al. (4) found that only the carbohydrate-supplemented breakfast suppressed meal intake 90 min later. The aim of this investigation was to determine the intrameal satiation and the postingestive satiety for a high protein food (HP) and a high fat food (HF) when served on their own (uniform meal), as a first course (preload) of a varied meal, and 2 h before (snack) a varied meal. The results obtained could both highlight the effect of macronutrients on appetite control and underline differences of behaviour due to different timing of preload consumption. SUBJECTS AND METHODS
Subjects Fourteen men between the ages of 20 and 27 were selected from the students of the University of Milan. They were healthy, normal weight for height (BMI Å 22.4 { 1.9 Kg/m 2 ), nonsmokers, not restrained eaters, and were not on any medication
To whom requests for reprints should be addressed.
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or taking any drugs. The study was approved by the Faculty of Agriculture ethical committee. The first phase of recruitment was conducted using a Data Base Programme where the data of about 200 students had been stored. These data came from a questionnaire on subjective eating habits and food preferences. Twenty-five potential subjects having a normal liking for all the foods included in the study were recruited. Then, a further selection was carried out by means of a preliminary trial of the test meal ad lib consumption (no load condition) and a preference test for the 2 types of omelettes to be used in the study. Subjects rated the palatability of the foods during the consumption of a small portion of both the omelettes using a 100-mm visual analogue scale anchored at either end with ‘‘very palatable’’ and ‘‘not at all palatable’’ (11). Subjects with a test meal energy intake more than twice the mean standard deviation and those who experienced a great difference in the pleasantness of the 2 omelettes were excluded. The average palatability ratings for the HP and the HF foods expressed by the 14 men selected (79 { 8 mm and 88 { 8 mm, respectively) were not significantly different. All the subjects selected took part in the whole study; however, only the data of the subjects who completed each experiment are reported. Foods A standard breakfast, consisting of a cup of milk and coffee or white coffee with a maximum of 2 teaspoonsful of sugar and a brioche with jam or 5 biscuits like ‘‘frollini,’’ was offered on the basis of the eating habits of the 14 men selected. Two omelettes as similar as possible for all the orosensory, physical, and chemical characteristics, and differing only in the protein and fat content were used in this study. Nutrient content was varied by adding very low-fat ham to the HP omelette and cream to the HF omelette. Characteristics and chemical composition of the foods determined by means of official chemical analysis (1) are shown in Table 1. The test meal offered in all the experiments consisted of a buffet-style self selection meal that allowed ad lib consumption of a variety of 13 different foods and 2 different drinks. The foods were chosen for their energy density (high- and low-energy dense foods), their nutrient composition (different content of fat, protein, and carbohydrate) and their firmness (solid and liquid foods). They are all well known and typical in Italian cookery. The macronutrient content and energy density of the test-meal foods, determined by means of official chemical analysis (1) are reported in Table 2. Main Procedure A within-ssubjects design was conducted. The subjects, who had no knowledge of the aim of the study, were instructed to fast TABLE 1 NUTRIENT COMPOSITION AND ENERGY VALUE FOR 100 GRAMS OF THE 2 OMELETTES High-Protein Omelette
High-Fat Omelette
155.4 7.8 (45.2%) 0.5 (1.3%) 20.8 (53.5%) 68.4
189.5 16.7 (79.3%) 2.8 (5.9%) 7.0 (14.8%) 70.5
Energy (Kcal) Fat (g) Carbohydrate (g) Protein (g) Water (g) % percentage of energy.
TABLE 2 FOODS AND DRINKS IN THE SELF-SELECTION MEAL
Foods and drinks
Amount Served (g)
Baked lasagna 500 Ham 80 Salami 80 Cream cheese 60 White bread 100 Fried chips 200 Green salad / olive oil 125 / 15 Apple 125 Banana 125 Strawberry yogurt 250 Chocolate cream 125 Chocolate snack 43 Apricot jam-tart 84 Apricot juice 600 ml Water 1500 ml
Energy Density (Kcal/100 g)
Fat
CHO (g/100 g)
PRO
141.6 231.4 341.7 303.5 277.2 256.1 80.2 47.9 84.3 99.9 116.6 554.3 434.5 46.1 –
6.8 13.4 26.9 28.7 0.4 10.9 7.4 0.3 0.3 4.0 3.0 35.9 16.9 0.1 –
12.8 0.0 0.0 4.2 58.8 35.6 2.4 11.1 19.2 12.1 20.4 48.3 66.0 11.3 –
7.3 27.7 24.9 7.1 9.6 3.9 1.0 0.2 1.2 2.9 2.0 9.5 4.6 0.0 –
overnight and consume the standard breakfast before 0830 h each test day. On arrival at the laboratory at 1245 h, they were seated at well-separated tables in a comfortable room. Subjects were asked to be silent and to stay seated during the consumption of the food. In all the experiments, intake was assessed by weighing foods anddrinks before and after consumptio. Information about desire to eat, fullness, and satiety were obtained from a Satiety Ratings Questionnaire (SRQ). Three questions (‘‘How great is your desire to eat,’’ ‘‘How full do you feel?’’ and ‘‘How sated do you feel?’’), already used in a previous investigation (18), provided useful information in discriminating between the different satiety conditions. Three unbroken isosceles triangles with an area of 22.5 cm2 were used as scale and the ratings were expressed in cm square of area. For the investigations, 3 experiments were scheduled. Statistical Analysis The data from ad lib eating in Experiment 1 (energy intake, weight intake, and variations of desire to eat, fullness, and satiety from before to after the food consumption) were computed by means of 1-way analysis of variance (ANOVA) using type of food (HP or HF) as condition. In Experiment 2, energy and weight intake were computed by means of 1-way ANOVA with type of preload (no load, small HP, large HP, small HF, and large HF) as factor and 2-way ANOVA with type of preload (HP and HF) and preload energy level (larger and smaller) as factors. Variations of desire to eat, fullness, and satiety were analysed separately using a 3-factor ANOVA with time (immediately after preload and immediately after test meal) as further factors. In Experiment 3, energy and weight intake were computed by means of 1-way ANOVA with type of preload (no load, HP, and HF) as condition. Variations of desire to eat, fullness, and satiety were analysed separately using a 2-factor ANOVA with time as further factor (immediately after preload, 45 * and 75 * after preload, before and immediately after test meal). For all the experiments, following a significant main effect in the ANOVA, individual means were compared using the LSD test. Criteria for significance were set at p õ 0.05.
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TABLE 4
Method In the first experiment, we studied the effect of macronutrients on satiation for a specific food. On 2 different sessions, subjects received, in random order, 800 g of HP omelette or the same amount of HF omelette. They were instructed to fill in the SRQ before and after eating each food ad lib until they were comfortably sated. Water consumption was not limited. Thirteen men completed this part of the study.
MEAN (SEM) VARIATION OF DESIRE TO EAT, FULLNESS, AND SATIETY FROM BEFORE TO AFTER THE CONSUMPTION OF THE HP AND THE HF OMELETTE (n Å 13)
Desire to eat (cm2) Fullness (cm2) Satiety (cm2)
RESULTS
High-Protein Omelette
High-Fat Omelette
013.3 (1.7) 12.1 (1.9) 17.9 (1.3)*
014.9 (1.6) 12.8 (2.0) 16.9 (1.6)†
* p Å 0.006; † p Å 0.031 ANOVA compared to Fullness.
Table 3 summarises the mean { SEM of energy intake and weight intake (with or without water) of the 2 foods under study. The mean energy intake of the 2 foods was significantly lower consumption of the HP omelette than the HF omelette [F (1, 12) Å 29.654, p õ 0.001] (mean difference ( { SED Å 302 { 55 Kcal). By analysing the weight ingested without water, the result was the same, significantly less of the HP omelette was eaten to reach satiation [F (1,12) Å 13.854, p Å 0.003] (mean difference { SED Å 111 { 30 g). No significant difference was observed in the water consumption even if subjects drank more during the consumption of the HP omelette (mean difference { SED Å 73 { 37 g). When the water intake was considered, the total weight of intake was not different (mean difference { SED Å 38 { 59 g). Comparing the HP with the HF food, there were no significant differences in the mean variation of desire to eat, fullness, and satiety from before to after consumption, as shown in Table 4. However, it is interesting to underline that, after consumption of both the omelettes, the mean decrease of desire to eat ( 014.1 { 1.2 cm2 ) was not statistically different from the mean increase of the fullness sensation (12.5 { 1.3 cm2 ). On the other hand, this mean increase of fullness sensation was lower compared with the mean increase of satiety sensation (17.4 { 1.0 cm2 ) [ F(1,25) Å 17.019, p õ 0.001].
sumption of the HP omelette, subjects felt thirstier or to the different consistency compared to the HF omelette. The SRQ support intake data and describe clearly the phenomenon of satiation for a specific food. After the ad lib consumption of HP and HF omelettes, subjects had the same level of desire to eat, fullness, and satiety, independently from the energy intake, supporting the hypothesis that satiation had really been reached. The decrease of desire to eat and the increase of fullness were the same, but the increase of satiety was higher. A similar trend was observed in our previous work (17) where subjects consumed ad lib meal consisting of baked macaroni or meat balls or cooked vegetables or fruit salad. This shows that the consumption of a uniform meal increases the sensation of satiety for the specific food consumed, but the sensations of desire to eat and fullness made us realise that the subjects were in a condition of satiation for a specific food. In fact, they didn’t feel completely full and their desire to eat, probably for something different, was still high. Summarising, when a uniform meal is consumed: 1. Subjects stop eating when they feel sated but not completely full; 2. energy intake is lower when subjects eat ad lib a food rich in protein compared to a food rich in fat.
DISCUSSION
Our results show that a food rich in protein consumed with an ad lib amount of water limits its own consumption and induces a higher consumption of water compared to a food rich in fat. It could be hypothesised that the water plays a role in the onset of satiation. In fact, by considering the omelette plus water, satiation was reached for both foods with a similar total weight intake. Because the intake of the HP was low and more water was consumed, there was a lower energy intake. It is not possible to determine if this result was due to the fact that, during the conTABLE 3 ENERGY AND WEIGHT INTAKE (WITH OR WITHOUT WATER) OF THE 2 OMELETTES High-Protein Omelette
Energy intake (Kcal) Weight intake (g) Water consumption (g) Total weight intake (g)
411 265 448 713
(42)* (27)† (48) (56)
High-Fat Omelette
713 376 375 751
(67) (35) (48) (71)
* p õ 0.001; † p Å 0.003 ANOVA compared to HF omelette.
EXPERIMENT 2 Method The objective of this experiment was to explore the different satiating properties of the foods used in the previous experiment when consumed as a first course of a complete meal (satiation for varied foods). The preloading paradigm strategy was used, but with no time interval between preload and test meal (13); the differences in intakes of a test meal were assessed after the HP preload or the HF preload, each at 2 different energy levels, had been consumed. The 2 energy levels were chosen on the basis of the results obtained from the first experiment, one corresponding to the satiation for the specific food (large preload) and the other exactly half the satiating energy level (small preload). The 4 preloads were consumed in random order and water consumption was not limited. Subjects were instructed to eat the preload in full, then a test meal was immediately served. Subjects were told to eat and drink as much as they wanted until they were comfortably sated. Desire to eat, fullness and satiety were rated just before (t Å 0) and immediately after the preload (a.p.) and after the test meal (a.t.m.). A scheme of this procedure is reported in Fig. 1. Ten of the 14 men selected completed this experiment, 4 withdrew.
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FIG. 1. Scheme of the procedure followed in the second and third experiments. RESULTS
Table 5 summarises the mean { SEM of energy intake and weight intake (with or without water) in the 4 different conditions plus the no-load condition. The mean total energy intake (preload / test meal) for both the large and small HP omelettes was significantly lower than both the HF omelettes and the noload condition [F (4,36) Å 6.284, p õ 0.001]. Considering only the test-meal energy intake, we observed a significant difference between all the omelette conditions and the no-load condition [F (4,36) Å 15.537, p õ 0.001]. As expected, there was a higher intake after the consumption of both the small HP and HF omelettes than after both the large omelettes [F (1,9) Å 7.194, p Å 0.025]. The total and the test-meal energy intake were, respectively, 280 Kcal { 102 SED and 324 Kcal { 102 SED less after the large HP than the small HF, LSD Test showed a significant difference between the 2 conditions (p Å 0.009 and p Å 0.004, respectively). The mean total weight intake (omelette / test meal / water) was the same in the 4 conditions, but significantly lower compared to the no-load condition [F (4,36) Å 3.264, p Å 0.022]. Analysing only the test-meal weight intake, we found the same results [F (4,36) Å 13,393, p õ 0.001]. Water consumption was similar in all the conditions.
The satiety ratings, expressed in the 4 different conditions plus the no-load condition are presented in Table 6. Variations, from before to after the consumption of the preload, of desire to eat [F (1,9) Å 32.214, p õ 0.001] and fullness [ F(1,9) Å 29.210, p õ 0.001] were significantly different after the consumption of both the large HP and HF omelettes compared to both the small omelettes. After the large preloads, the desire to eat diminished greatly and the sensation of fullness also increased more. We also observed a higher increase of satiety after the consumption of both the large HP and HF omelettes compared to both the small omelettes, but this difference was not significant. After the ad lib consumption of the test meal, there were no differences in desire to eat, fullness, or satiety among all the conditions. DISCUSSION
When the foods rich in protein or in fat were consumed as a first course in a real meal, the total weight intake, including water, was similar and twice as big as the total weight intake registered in the uniform meal (1453 g in the 2nd experiment compared to 732 g in the 1st experiment). The enhancement of intake is probably due to the variety of food presented with the test meal, as suggested by Rolls et al. (24,25). Anyway, subjects did not reach the weight intake registered in the no-load condition (1686 g).
TABLE 5 ENERGY AND WEIGHT INTAKE IN THE 4 DIFFERENT CONDITIONS OF THE SECOND EXPERIMENT PLUS THE NO-LOAD CONDITION High-Protein Omelette
Preload energy intake (Kcal) Test meal energy intake (Kcal) Total energy intake (Kcal) Preload weight intake (g) Test meal weight intake (g) Water consumption (g) Total weight intake (g)
High-Fat Omelette
No-Load
Large
Small
Large
Small
0 1803 (61)† 1803 (61) 0 1236 (67)† 450 (65) 1686 (60)†
404 1006 (140) 1410 (140)* 260 755 (99) 460 (54) 1475 (88)
202 1218 (101) 1420 (101)* 130 844 (67) 445 (71) 1420 (110)
720 1089 (80) 1809 (80) 380 731 (54) 323 (38) 1434 (72)
360 1330 (119) 1690 (119) 190 914 (73) 381 (47) 1485 (87)
Results expressed as mean (SEM) (n Å 10). * p õ 0.001 ANOVA compared to NO LOAD and HF conditions. † p õ 0.05 ANOVA compared to HP and HF conditions.
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MEAN (SEM) VARIATION OF DESIRE TO EAT, FULLNESS, AND SATIETY IN THE 4 DIFFERENT CONDITIONS OF THE SECOND EXPERIMENT PLUS THE NO-LOAD CONDITION, AFTER SUBTRACTION OF THE FASTING VALUES (n Å 10) High-Protein Omelette
Desire to eat (cm2) tÅ0 a.p. a.t.m. Fullness (cm2) tÅ0 a.p. a.t.m. Satiety (cm2) tÅ0 a.p. a.t.m.
High-Fat Omelette
No load
Large
Small
Large
Small
0.0 – 018.6 (1.0)
0.0 010.0 (2.0)* 018.1 (1.2)
0.0 03.0 (1.7) 017.2 (1.4)
0.0 09.7 (2.1)* 019.5 (1.0)
0.0 02.8 (1.3) 018.0 (1.3)
0.0 – 17.1 (1.3)
0.0 4.3 (1.0)* 18.7 (1.1)
0.0 1.5 (0.5) 17.8 (1.2)
0.0 6.4 (1.5)* 18.7 (1.4)
0.0 1.2 (0.4) 19.2 (1.0)
0.0 – 18.2 (1.1)
0.0 4.8 (1.0) 17.6 (1.2)
0.0 2.3 (0.7) 16.5 (1.4)
0.0 3.5 (0.6) 17.5 (1.0)
0.0 2.4 (1.2) 17.6 (1.4)
* p õ 0.001 ANOVA compared to small omelettes; a.p., after preload; a.t.m., after test meal.
No specific macronutrient selection was observed in all the conditions (data omitted). Subjects continued eating different foods and drinking water until the physiological sensation of fullness reached a high value and their desire to eat dropped to zero. In fact, although the increase of satiety (17.5 cm2 ) was the same as in the previous experiment (17.4 cm2 ), the variations of fullness (18.3 vs. 12.5 cm2 ) and of desire to eat ( 018.2 vs. 014.1 cm2 ) were bigger, confirming that subjects were in a condition of general satiation (satiation for varied foods). Satiation was reached with a lower total energy intake (preload plus test meal) when the preloads were HP omelettes. It is interesting to observe the eating behaviour after the consumption of an isocaloric amount of preload (400 Kcal from HP omelette vs. 360 Kcal from HF omelette). Both the test meal and the total energy were significantly lower after consumption of the large HP omelette with respect to the small HF omelette. The information obtained from the SRQ clearly showed that subjects experienced a greater decrease of desire to eat and a larger increase of fullness and satiety after the large HP preload. These differences are too big to presume that the satiating power of the HP omelette is only due to the extra content of 40 kcal of this preload. Summarising, in a varied meal: 1. Subjects stop eating when they feel sated and completely full; 2. energy intake is lower when subjects eat the preload rich in protein as a first course, compared with the preload rich in fat.
h and 1300 h, subjects left the department, but they were not allowed to eat or drink anything else. Two questionnaires were also completed at 1200 h (45 *a.p.) and 1230 h (75 *a.p.). The test meal was served in the department at 0100 h, subjects were told to eat and drink as much as they wanted until they were comfortably sated. Desire to eat, fullness, and satiety were rated just before the test meal (b.t.m.) and immediately after (a.t.m.). A scheme of this procedure is reported in Fig. 1. All 14 men completed this last part of the study. RESULT
Table 7 summarises the mean { SEM of energy intake and weight intake (with or without water) after the 2 different conditions (HP and HF preloads consumed as snack at 1100 h) plus the no-load condition. The mean total energy intake (preload / test meal) for both the omelettes was similar to that of the noload condition. Considering only the test meal energy intake, we observed a significant difference between the preloads and the no-load condition [F (2,26) Å 9.845, p õ 0.001]. The mean total weight intake (omelette / test meal / water) was the same in all the conditions and, once again, analysing only the test-meal TABLE 7 ENERGY AND WEIGHT INTAKE IN THE 2 DIFFERENT CONDITIONS OF THE THIRD EXPERIMENT PLUS THE NO-LOAD CONDITION
No-Load
HighProtein Preload
High-Fat Preload
0 1861 (50)* 1861 (50) 0 1240 (51)* 462 (55) 1702 (48)
274 1385 (127) 1659 (127) 176 939 (102) 446 (69) 1561 (109)
284 1596 (98) 1881 (98) 150 1065 (71) 407 (70) 1622 (91)
EXPERIMENT 3 Method The objective of this experiment was to analyse the satiating capacity of the 2 omelettes when consumed as a snack 2 h before a meal (postingestive satiety). The preloading paradigm strategy was also used in this experiment with the following procedure: subjects came to the department at 1100 h on 2 occasions 1 week apart from the other. They received, in random order, a portion of HP omelette (176 g, 273.5 Kcal) or a portion of HF omelette (150 g, 284.3 Kcal) and a glass of water (150 ml). They were instructed to eat the preload in full, drink all the water, and fill in the SRQ before (t Å 0) and after eating (a.p.). Between 1115
Preload energy intake (Kcal) Test-meal energy intake (Kcal) Total energy intake (Kcal) Preload weight intake (g) Test-meal weight intake (g) Water consumption (g) Total weight intake (g)
Results expressed as mean (SEM) (n Å 14). * p õ 0.05 ANOVA compared to HP and HF conditions.
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weight intake, we found a significantly higher intake in the noload condition [F (2,26) Å 8.195, p Å 0.002]. Water consumption was similar in all the conditions. The satiety ratings expressed during the 2 meals are shown in Fig. 2. Variations, from before to after the preload consumption, of desire to eat [F (1,13) Å 4.555, p Å 0.052], fullness [ F (1,13) Å 16.946, p Å 0.001], and satiety [F(1,13) Å 21.414, p õ 0.001] depended on the type of preload eaten. After eating the HP preload at 1100 h, the desire to eat decreased and the feeling of fullness and satiety increased more than after the HF omelette. The ratings profiles were almost the same during the rest of the morning and after the ad lib consumption of the test meal. As expected, there was a significant effect of time on all the sensations (p õ 0.001), showing that the subjects were responsive to the consumption of the preloads and the test meal. DISCUSSION
Total weight intake was similar for both HP and HF conditions and for the no-load condition, suggesting that the mass of the snack eaten 2 h before did not provide any contribution to the weight reduction of the following intake. Probably the preloads had already left the stomach at the end of the 2-h interval. Comparing the amount of food ingested in the 2nd and 3rd experiments, the weight consumed on one single occasion (lunch time) was comparable (2nd experiment 1475 and 1420 g for HP omelette and 1434 and 1485 g for HF omelette, in the large and small condition, respectively; 3rd experiment 1385 (1561 0 176) and 1472 (1622 0 150) g for HP an HF omelette, respectively). The total energy intake was lower for the HP omelette than the HF and the no-load conditions but this difference was not significant. This seems to demonstrate that consuming a snack is not the best way to reduce energy intake. Maybe the amount we served at 1100 h was not enough to exert a strong effect 2 h later; however, we wanted to offer a correct amount of preload that could easily be consumed as a snack. Summarising: 1. A snack consumed 2 h before does not reduce energy intake at the test meal. GENERAL DISCUSSION In general, what emerges from this study is the primary role of weight intake, including water, and the role of protein in modulating the food intake in the different meal patterns examined. Researchers have usually concentrated their interests on energy intake and the influence of weight and volume has been studied very little, with differing conclusions (14,17,22), especially when considering caloric or noncaloric fluid intake. The present study shows that, in a uniform meal, subjects stop eating when a specific weight of food and water was ingested, reaching a higher satiety sensation compared to fullness sensation. Moreover, this intake is lower compared to the intake registered in a varied meal where subjects reach fullness and satiety at the same time. Water may play a role in the onset of satiety, in addition to contributing its own weight to gastric distention, liquefies the material in the stomach as reported by some authors (7). In this way, intestinal receptors, which are sensitive to nutrients, may be reached more quickly. As suggested by Kissileff (14), it is possible that the receptors respond best to nutrients that are most physically dispersed per unit of nutrient. In particular, protein seems to exert a stronger effect on satiation both in a uniform and in a varied meal, resulting in a lower total energy intake when the HP omelette was eaten on its own or as a preload immediately before a test meal. Another important fact to consider is that according to Sunkin and Garrow (28) and Pudel and Oetting (19), the eating behav-
FIG. 2. Mean (SEM) variation of desire to eat, fullness, and satiety in the 2 different conditions of the third experiment after subtraction of the fasting values (n Å 14). * mean significantly different (p Å 0.052) compared to HF omelette; 7 mean significantly different ( p Å 0.001) compared to HF omelette; § mean significantly different (p õ 0.001) compared to HF omelette.
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iour of people is greatly influenced by what they have eaten and what they think they have eaten. First of all, asking the subjects to consume a preload just before the test meal reduces the subsequent and the total weight intake compared to a no-load condition. Generally subjects think that the onset of hunger is delayed for a longer time after a high protein food (for example, a steak, which is considered particularly nutritious and satisfying). Consequently, we hid the protein and fat in a food, egg, which is generally considered both high in protein and fat and what we found was a similar consumption in weight intake. Finally, another aim of this work was to explore the effect of different meal timing on eating behaviour. In a recent study, Schlundt et al. (26) demonstrated that physiological variables may be influenced by meal pattern, eating one’s daily allotment of food in a few large meals may be physiologically and metabolically different from eating the same amount of calories in several smaller meals. For example, eating breakfast provides some advantages over eating only 2 meals a day; in particular, breakfast eaters show a lower fat intake and a higher carbohydrate intake. In the present study, the consumption of a snack 2 h before the meal did not reduce subsequent food intake and the total weight intake was similar to the no-load condition. This behaviour seems to indicate that the snack was metabolised and its effect on the food-intake control system was dissipated. The snack-meal relationship can be compared with the results reported by de Castro (6), who found a significant and positive correlation between the duration of the interval between meals and the size of the meal. As we have already discussed, probably our 2 snacks were not big enough to modulate subsequent intake
or, alternatively, our subjects were not used to consuming snacks. In fact, Louis-Sylvestre et al. (16) demonstrated that calorie compensation for a snack served 60 min before a dinner appeared only after subjects had received repeated experiences, but not the first time. Better results could be obtained by getting the subjects used to dividing up their daily intake into a breakfast, 2 main meals, and 1 or 2 ad hoc snacks. Overall, sensory characteristics of foods play an important role in controlling food intake and make a uniform meal more satiating that a varied meal. Weight and volume of food are important factors determining the amount consumed in a varied meal; consequently, the consumption of a snack far from a meal does not contribute to satiety. In each meal pattern adopted, protein always exerted a higher effect on satiety than fat. In conclusion, the weight and protein content of food are 2 important factors that must be considered when studying how to reduce food intake. Because it is inadvisable to have a high protein intake, we would suggest that further research should be made on the influence of weight on the control of food intake. From the results of our work, it seems that drinking water during a meal could contribute to increase the weight and volume of intake, inducing people to stop eating earlier. ACKNOWLEDGEMENTS
This research was supported by grant No. 94.00635.PF41 from the National Research Council, Targeted Project ‘‘Prevention and Control Disease Factors’’, Subproject ‘‘Nutrition.’’ The authors thank Silvia Tasca for her help in carrying out the study.
REFERENCES 1. AOAC. Official methods of analysis. Washington, DC: Association of Official Analytical Chemists; 1984. 2. Barkeling, B.; Rossner, S.; Bjorvell, H. Effects of a high-protein meal (meat) and a high-carbohydrate meal (vegetarian) on satiety measured by automated computerized monitoring of subsequent food intake, motivation to eat and food preferences. Int. J. Obes. 14:743–751; 1990. 3. Blundell, J. E.; Burley, V. J. Evaluation of the satiating power of dietary fat in man. In: Oomura, Y.; Baba, S.; Shimazu, T., eds. Progress in obesity research 1990. London: John Libbey & Company Ltd. 1991:453–457. 4. Blundell, J. E.; Burley, V. J.; Cotton, J. R.; Lawton, C. L. Dietary fat and the control of energy intake: evaluating the effects of fat on meal size and postmeal satiety. Am. J. Clin. Nutr. 57:772s–778s; 1993. 5. Blundell, J. E.; Cotton, J. R.; Delargy, H. J.; Green, S.; Greenough, A.; King, N. A.; Lawton, C. L. The fat paradox: fat-induced satiety signals vs. high fat overconsumption. Int. J. Obes. 19:832–835; 1995. 6. de Castro, J. M. Physiological, environmental, and subjective determinants of food intake in humans: a meal pattern analysis. Physiol. Behav. 44:651–659; 1988. 7. Deutsch, J. A. The role of the stomach in eating. Am. J. Clin. Nutr. 42:1040–1043; 1985. 8. Geliebter, A.; Westreich, S.; Gage, D. Gastric distension by balloon and test-meal intake in obese and lean subjects. Am. J. Clin. Nutr. 48:592–594; 1988. 9. Gustafsson, K.; Asp, N. G.; Hagander, B.; Nyman, M. Satiety effects of spinach in mixed meals: comparison with other vegetables. Int. J. Food Sci. Nutr. Res. 46:327–334; 1995. 10. Hill, A. J.; Blundell, J. E. Comparison of the action of macronutrients on the expression of appetite in lean and obese human subjects. Ann. NY Acad. Sci. 575:529–531; 1989. 11. Hill, A. J.; Magson, L. D.; Blundell, J. E. Hunger and palatability:tracking ratings of subjective experience before, during and after the consumption of preferred and less preferred food. Appetite 5:361–371; 1984.
12. Houghton, L. A.; Mangnall, Y. F.; Read, N. W. Effect of incorporating fat into a liquid test meal on the relation between intragastric distribution and gastric emptying in human volunteers. Gut 31:1226–1229; 1990. 13. Kissileff, H. R. Satiating efficiency and a strategy for conducting food loading experiments. Neurosci. Biobehav. Rev. 8:129–135; 1984. 14. Kissileff, H. R.; Gruss, L. P.; Thornton, J.; Jordan, H. A. The satiating efficiency of foods. Physiol. Behav. 32:319 – 332; 1984. 15. Lappalainen, R.; Mennen, L.; van Weert, L.; Mykkanen, H. Drinking water with a meal: a simple method of coping with feelings of hunger, satiety and desire to eat. Eur. J. Clin. Nutr. 47:815 – 819; 1993. 16. Louis-Sylvestre, J.; Tournier, A.; Verger, P.; Chabert, M.; Delorme, B.; Hossenlopp, J. Learned caloric adjustment of human intake. Appetite 12:95–103; 1989. 17. Porrini, M.; Crovetti, R.; Riso, P.; Santangelo, A.; Testolin, G. Effects of physical and chemical characteristics of food on specific and general satiety. Physiol. Behav. 57:461–468; 1995. 18. Porrini, M.; Crovetti, R.; Testolin, G.; Silva, S. Evaluation of satiety sensations and food intake after different preloads. Appetite 25:17– 30; 1995. 19. Pudel, V.; Oetting, M. Eating in the laboratory: behavioural aspects of the positive energy balance. Int. J. Obes. 1:369–386; 1977. 20. Read, N. W.; French, S.; Cunningham, K. The role of the gut in regulating food intake in man. Nutr. Rev. 52:1–10; 1994. 21. Rogers, P. J. Dietary fat, satiety and obesity. Food Qual. Pref. 2:103– 110; 1990. 22. Rolls, B. J.; Hetherington, M.; Burley, V. J. The specificity of satiety: the influence of foods of different macronutrient content on the development of satiety. Physiol. Behav. 43:145–153; 1988. 23. Rolls, B. J.; Kim, S.; McNelis, A. L.; Fishman, M. W.; Foltin, R. W.; Moran, T. H. Time course of effects of preloads high in fat or carbohydrate on food intake and hunger ratings in humans. Am. J. Physiol. 260:R756–R763; 1991.
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24. Rolls, B. J.; Rowe, E. A.; Kingston, B.; Megson, A.; Gunary, R. Variety in a meal enhances food intake in man. Physiol. Behav. 26:215–221; 1981. 25. Rolls, B. J.; van Duijvenvoorde, P. M.; Rolls, E. T. Pleasantness changes and food intake in a varied four-course meal. Appetite 5:337–348; 1984. 26. Schlundt, D. G.; Hill, J. O.; Sbrocco, T.; Pope-Cordle, J.; Sharp, T. The role of breakfast in the treatment of obesity: a randomized clinical trial. Am. J. Clin. Nutr. 55:645–651; 1992.
27. Sepple, C. P.; Read, N. W. Effect of prefeeding lipid on food intake and satiety in man. Gut 31:158–161; 1990. 28. Sunkin, S.; Garrow, J. S. The satiety value of protein. Human Nutr. Appl. Nutr. 36A:197–201; 1982. 29. Welch, I. M.; Sepple, C. P.; Read, N. W. Comparisons of the effects on satiety and eating behaviour of infusion of lipid into the different regions of the small intestine. Gut 29:306–311; 1988. 30. Zabik, M. E. Impact of ready-to-eat cereal consumption on nutrient intake. Cereal F. W. 32:234–239; 1987.
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Weight, Protein, Fat, and Timing of Preloads Affect Food Intake M. PORRINI,* 1 A. SANTANGELO,* R. CROVETTI,* P. RISO,* G. TESTOLIN* AND J. E. BLUNDELL† *Department of Food Science and Technology, Division of Human Nutrition, University of Milan, Via Celoria 2, 20133 Milan, Italy and †Department of Psychology, University of Leeds, Leeds LS2 9JT UK Received 25 March 1996; Accepted 13 February 1997 PORRINI, M., A. SANTANGELO, R. CROVETTI, P. RISO, G. TESTOLIN AND J. E. BLUNDELL. Weight, protein, fat, and timing of preloads affect food intake. PHYSIOL BEHAV 62(3) 563–570, 1997.—Two foods, one rich in protein (HP) and one rich in fat (HF), were employed to evaluate the effect of macronutrients on food intake and to underline the differences that occurred when the foods were served as uniform meal, as first course of a varied meal, and as a snack 2 h before a varied meal. Our results showed that HP food always exerted a higher effect on both intrameal satiation and postingestive satiety than HF food. When a uniform meal was consumed, satiation for the specific food was reached before fullness; in this condition, sensory characteristics of foods played an important role in controlling food intake and made the uniform meal more satiating than the varied one. The consumption of a snack far from a meal did not contribute to satiety; consequently, gastric filling seems to be an important factor determining the amount consumed in a varied meal. q 1997 Elsevier Science Inc. Timing of preload
Weight
Water
Protein
Fat
THERE are many reasons why and how a specific food contributes to the satiety process and there have been extensive studies; as yet, however, no real conclusions have been reached. It is clear that certain nutrients are more satiating than others. Concordant results have been obtained for protein; some authors (2,10,22) demonstrated that there is a stronger action of protein on appetite than of fat or carbohydrate, but little is known about the mechanism that determines such an effect. The role of fat in appetite control is sometimes thought to be problematic. Dietary fat is associated with hyperphagia and the development of obesity, probably because it is palatable and has a high energy density (3,21). On the other hand, studies with human volunteers have suggested that the interaction of fat with gastrointestinal receptors may suppress hunger, induce satiety, reduce subsequent food intake, and delay gastric emptying (12,20,27,29). This issue has been called the ‘‘fat paradox (5). Weight and volume of food may play another important role, because filling and emptying of the stomach are important elements of satiety. The most familiar inhibitory signal to food ingestion is gastric distension. Geliebter et al. (8) demonstrated that, in man, food intake was reduced by inserting into the stomach a 400–600-ml intragastric balloon. Recently, Gustafsson et al. (9) found that, by increasing the dietary fiber content and the weight of the meal (by intrinsically bound water in food), satiety was higher. If volume and weight are key factors in controlling food intake, the contribution of water during a meal should be particularly considered, as we have suggested previously (17). In a recent study, Lappalainen (15) found that drinking 2 glasses of water affects subjective feelings of hunger and satiety during 1
Food intake
the meal due to gastric distension, but this effect is not maintained after the meal. Furthermore, it has been suggested that physiological variables may be influenced by different meal patterning (26). Although the consumption of a breakfast controls hunger and prevents subsequent overeating later in the day (30), discordant results are reported in the literature about the effect of food consumed 90 min before a test meal. Rolls et al. (23) found that there was no difference in food intake 90 min after eating a snack rich in fat or carbohydrates, whereas Blundell et al. (4) found that only the carbohydrate-supplemented breakfast suppressed meal intake 90 min later. The aim of this investigation was to determine the intrameal satiation and the postingestive satiety for a high protein food (HP) and a high fat food (HF) when served on their own (uniform meal), as a first course (preload) of a varied meal, and 2 h before (snack) a varied meal. The results obtained could both highlight the effect of macronutrients on appetite control and underline differences of behaviour due to different timing of preload consumption. SUBJECTS AND METHODS
Subjects Fourteen men between the ages of 20 and 27 were selected from the students of the University of Milan. They were healthy, normal weight for height (BMI Å 22.4 { 1.9 Kg/m 2 ), nonsmokers, not restrained eaters, and were not on any medication
To whom requests for reprints should be addressed.
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or taking any drugs. The study was approved by the Faculty of Agriculture ethical committee. The first phase of recruitment was conducted using a Data Base Programme where the data of about 200 students had been stored. These data came from a questionnaire on subjective eating habits and food preferences. Twenty-five potential subjects having a normal liking for all the foods included in the study were recruited. Then, a further selection was carried out by means of a preliminary trial of the test meal ad lib consumption (no load condition) and a preference test for the 2 types of omelettes to be used in the study. Subjects rated the palatability of the foods during the consumption of a small portion of both the omelettes using a 100-mm visual analogue scale anchored at either end with ‘‘very palatable’’ and ‘‘not at all palatable’’ (11). Subjects with a test meal energy intake more than twice the mean standard deviation and those who experienced a great difference in the pleasantness of the 2 omelettes were excluded. The average palatability ratings for the HP and the HF foods expressed by the 14 men selected (79 { 8 mm and 88 { 8 mm, respectively) were not significantly different. All the subjects selected took part in the whole study; however, only the data of the subjects who completed each experiment are reported. Foods A standard breakfast, consisting of a cup of milk and coffee or white coffee with a maximum of 2 teaspoonsful of sugar and a brioche with jam or 5 biscuits like ‘‘frollini,’’ was offered on the basis of the eating habits of the 14 men selected. Two omelettes as similar as possible for all the orosensory, physical, and chemical characteristics, and differing only in the protein and fat content were used in this study. Nutrient content was varied by adding very low-fat ham to the HP omelette and cream to the HF omelette. Characteristics and chemical composition of the foods determined by means of official chemical analysis (1) are shown in Table 1. The test meal offered in all the experiments consisted of a buffet-style self selection meal that allowed ad lib consumption of a variety of 13 different foods and 2 different drinks. The foods were chosen for their energy density (high- and low-energy dense foods), their nutrient composition (different content of fat, protein, and carbohydrate) and their firmness (solid and liquid foods). They are all well known and typical in Italian cookery. The macronutrient content and energy density of the test-meal foods, determined by means of official chemical analysis (1) are reported in Table 2. Main Procedure A within-ssubjects design was conducted. The subjects, who had no knowledge of the aim of the study, were instructed to fast TABLE 1 NUTRIENT COMPOSITION AND ENERGY VALUE FOR 100 GRAMS OF THE 2 OMELETTES High-Protein Omelette
High-Fat Omelette
155.4 7.8 (45.2%) 0.5 (1.3%) 20.8 (53.5%) 68.4
189.5 16.7 (79.3%) 2.8 (5.9%) 7.0 (14.8%) 70.5
Energy (Kcal) Fat (g) Carbohydrate (g) Protein (g) Water (g) % percentage of energy.
TABLE 2 FOODS AND DRINKS IN THE SELF-SELECTION MEAL
Foods and drinks
Amount Served (g)
Baked lasagna 500 Ham 80 Salami 80 Cream cheese 60 White bread 100 Fried chips 200 Green salad / olive oil 125 / 15 Apple 125 Banana 125 Strawberry yogurt 250 Chocolate cream 125 Chocolate snack 43 Apricot jam-tart 84 Apricot juice 600 ml Water 1500 ml
Energy Density (Kcal/100 g)
Fat
CHO (g/100 g)
PRO
141.6 231.4 341.7 303.5 277.2 256.1 80.2 47.9 84.3 99.9 116.6 554.3 434.5 46.1 –
6.8 13.4 26.9 28.7 0.4 10.9 7.4 0.3 0.3 4.0 3.0 35.9 16.9 0.1 –
12.8 0.0 0.0 4.2 58.8 35.6 2.4 11.1 19.2 12.1 20.4 48.3 66.0 11.3 –
7.3 27.7 24.9 7.1 9.6 3.9 1.0 0.2 1.2 2.9 2.0 9.5 4.6 0.0 –
overnight and consume the standard breakfast before 0830 h each test day. On arrival at the laboratory at 1245 h, they were seated at well-separated tables in a comfortable room. Subjects were asked to be silent and to stay seated during the consumption of the food. In all the experiments, intake was assessed by weighing foods anddrinks before and after consumptio. Information about desire to eat, fullness, and satiety were obtained from a Satiety Ratings Questionnaire (SRQ). Three questions (‘‘How great is your desire to eat,’’ ‘‘How full do you feel?’’ and ‘‘How sated do you feel?’’), already used in a previous investigation (18), provided useful information in discriminating between the different satiety conditions. Three unbroken isosceles triangles with an area of 22.5 cm2 were used as scale and the ratings were expressed in cm square of area. For the investigations, 3 experiments were scheduled. Statistical Analysis The data from ad lib eating in Experiment 1 (energy intake, weight intake, and variations of desire to eat, fullness, and satiety from before to after the food consumption) were computed by means of 1-way analysis of variance (ANOVA) using type of food (HP or HF) as condition. In Experiment 2, energy and weight intake were computed by means of 1-way ANOVA with type of preload (no load, small HP, large HP, small HF, and large HF) as factor and 2-way ANOVA with type of preload (HP and HF) and preload energy level (larger and smaller) as factors. Variations of desire to eat, fullness, and satiety were analysed separately using a 3-factor ANOVA with time (immediately after preload and immediately after test meal) as further factors. In Experiment 3, energy and weight intake were computed by means of 1-way ANOVA with type of preload (no load, HP, and HF) as condition. Variations of desire to eat, fullness, and satiety were analysed separately using a 2-factor ANOVA with time as further factor (immediately after preload, 45 * and 75 * after preload, before and immediately after test meal). For all the experiments, following a significant main effect in the ANOVA, individual means were compared using the LSD test. Criteria for significance were set at p õ 0.05.
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TABLE 4
Method In the first experiment, we studied the effect of macronutrients on satiation for a specific food. On 2 different sessions, subjects received, in random order, 800 g of HP omelette or the same amount of HF omelette. They were instructed to fill in the SRQ before and after eating each food ad lib until they were comfortably sated. Water consumption was not limited. Thirteen men completed this part of the study.
MEAN (SEM) VARIATION OF DESIRE TO EAT, FULLNESS, AND SATIETY FROM BEFORE TO AFTER THE CONSUMPTION OF THE HP AND THE HF OMELETTE (n Å 13)
Desire to eat (cm2) Fullness (cm2) Satiety (cm2)
RESULTS
High-Protein Omelette
High-Fat Omelette
013.3 (1.7) 12.1 (1.9) 17.9 (1.3)*
014.9 (1.6) 12.8 (2.0) 16.9 (1.6)†
* p Å 0.006; † p Å 0.031 ANOVA compared to Fullness.
Table 3 summarises the mean { SEM of energy intake and weight intake (with or without water) of the 2 foods under study. The mean energy intake of the 2 foods was significantly lower consumption of the HP omelette than the HF omelette [F (1, 12) Å 29.654, p õ 0.001] (mean difference ( { SED Å 302 { 55 Kcal). By analysing the weight ingested without water, the result was the same, significantly less of the HP omelette was eaten to reach satiation [F (1,12) Å 13.854, p Å 0.003] (mean difference { SED Å 111 { 30 g). No significant difference was observed in the water consumption even if subjects drank more during the consumption of the HP omelette (mean difference { SED Å 73 { 37 g). When the water intake was considered, the total weight of intake was not different (mean difference { SED Å 38 { 59 g). Comparing the HP with the HF food, there were no significant differences in the mean variation of desire to eat, fullness, and satiety from before to after consumption, as shown in Table 4. However, it is interesting to underline that, after consumption of both the omelettes, the mean decrease of desire to eat ( 014.1 { 1.2 cm2 ) was not statistically different from the mean increase of the fullness sensation (12.5 { 1.3 cm2 ). On the other hand, this mean increase of fullness sensation was lower compared with the mean increase of satiety sensation (17.4 { 1.0 cm2 ) [ F(1,25) Å 17.019, p õ 0.001].
sumption of the HP omelette, subjects felt thirstier or to the different consistency compared to the HF omelette. The SRQ support intake data and describe clearly the phenomenon of satiation for a specific food. After the ad lib consumption of HP and HF omelettes, subjects had the same level of desire to eat, fullness, and satiety, independently from the energy intake, supporting the hypothesis that satiation had really been reached. The decrease of desire to eat and the increase of fullness were the same, but the increase of satiety was higher. A similar trend was observed in our previous work (17) where subjects consumed ad lib meal consisting of baked macaroni or meat balls or cooked vegetables or fruit salad. This shows that the consumption of a uniform meal increases the sensation of satiety for the specific food consumed, but the sensations of desire to eat and fullness made us realise that the subjects were in a condition of satiation for a specific food. In fact, they didn’t feel completely full and their desire to eat, probably for something different, was still high. Summarising, when a uniform meal is consumed: 1. Subjects stop eating when they feel sated but not completely full; 2. energy intake is lower when subjects eat ad lib a food rich in protein compared to a food rich in fat.
DISCUSSION
Our results show that a food rich in protein consumed with an ad lib amount of water limits its own consumption and induces a higher consumption of water compared to a food rich in fat. It could be hypothesised that the water plays a role in the onset of satiation. In fact, by considering the omelette plus water, satiation was reached for both foods with a similar total weight intake. Because the intake of the HP was low and more water was consumed, there was a lower energy intake. It is not possible to determine if this result was due to the fact that, during the conTABLE 3 ENERGY AND WEIGHT INTAKE (WITH OR WITHOUT WATER) OF THE 2 OMELETTES High-Protein Omelette
Energy intake (Kcal) Weight intake (g) Water consumption (g) Total weight intake (g)
411 265 448 713
(42)* (27)† (48) (56)
High-Fat Omelette
713 376 375 751
(67) (35) (48) (71)
* p õ 0.001; † p Å 0.003 ANOVA compared to HF omelette.
EXPERIMENT 2 Method The objective of this experiment was to explore the different satiating properties of the foods used in the previous experiment when consumed as a first course of a complete meal (satiation for varied foods). The preloading paradigm strategy was used, but with no time interval between preload and test meal (13); the differences in intakes of a test meal were assessed after the HP preload or the HF preload, each at 2 different energy levels, had been consumed. The 2 energy levels were chosen on the basis of the results obtained from the first experiment, one corresponding to the satiation for the specific food (large preload) and the other exactly half the satiating energy level (small preload). The 4 preloads were consumed in random order and water consumption was not limited. Subjects were instructed to eat the preload in full, then a test meal was immediately served. Subjects were told to eat and drink as much as they wanted until they were comfortably sated. Desire to eat, fullness and satiety were rated just before (t Å 0) and immediately after the preload (a.p.) and after the test meal (a.t.m.). A scheme of this procedure is reported in Fig. 1. Ten of the 14 men selected completed this experiment, 4 withdrew.
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FIG. 1. Scheme of the procedure followed in the second and third experiments. RESULTS
Table 5 summarises the mean { SEM of energy intake and weight intake (with or without water) in the 4 different conditions plus the no-load condition. The mean total energy intake (preload / test meal) for both the large and small HP omelettes was significantly lower than both the HF omelettes and the noload condition [F (4,36) Å 6.284, p õ 0.001]. Considering only the test-meal energy intake, we observed a significant difference between all the omelette conditions and the no-load condition [F (4,36) Å 15.537, p õ 0.001]. As expected, there was a higher intake after the consumption of both the small HP and HF omelettes than after both the large omelettes [F (1,9) Å 7.194, p Å 0.025]. The total and the test-meal energy intake were, respectively, 280 Kcal { 102 SED and 324 Kcal { 102 SED less after the large HP than the small HF, LSD Test showed a significant difference between the 2 conditions (p Å 0.009 and p Å 0.004, respectively). The mean total weight intake (omelette / test meal / water) was the same in the 4 conditions, but significantly lower compared to the no-load condition [F (4,36) Å 3.264, p Å 0.022]. Analysing only the test-meal weight intake, we found the same results [F (4,36) Å 13,393, p õ 0.001]. Water consumption was similar in all the conditions.
The satiety ratings, expressed in the 4 different conditions plus the no-load condition are presented in Table 6. Variations, from before to after the consumption of the preload, of desire to eat [F (1,9) Å 32.214, p õ 0.001] and fullness [ F(1,9) Å 29.210, p õ 0.001] were significantly different after the consumption of both the large HP and HF omelettes compared to both the small omelettes. After the large preloads, the desire to eat diminished greatly and the sensation of fullness also increased more. We also observed a higher increase of satiety after the consumption of both the large HP and HF omelettes compared to both the small omelettes, but this difference was not significant. After the ad lib consumption of the test meal, there were no differences in desire to eat, fullness, or satiety among all the conditions. DISCUSSION
When the foods rich in protein or in fat were consumed as a first course in a real meal, the total weight intake, including water, was similar and twice as big as the total weight intake registered in the uniform meal (1453 g in the 2nd experiment compared to 732 g in the 1st experiment). The enhancement of intake is probably due to the variety of food presented with the test meal, as suggested by Rolls et al. (24,25). Anyway, subjects did not reach the weight intake registered in the no-load condition (1686 g).
TABLE 5 ENERGY AND WEIGHT INTAKE IN THE 4 DIFFERENT CONDITIONS OF THE SECOND EXPERIMENT PLUS THE NO-LOAD CONDITION High-Protein Omelette
Preload energy intake (Kcal) Test meal energy intake (Kcal) Total energy intake (Kcal) Preload weight intake (g) Test meal weight intake (g) Water consumption (g) Total weight intake (g)
High-Fat Omelette
No-Load
Large
Small
Large
Small
0 1803 (61)† 1803 (61) 0 1236 (67)† 450 (65) 1686 (60)†
404 1006 (140) 1410 (140)* 260 755 (99) 460 (54) 1475 (88)
202 1218 (101) 1420 (101)* 130 844 (67) 445 (71) 1420 (110)
720 1089 (80) 1809 (80) 380 731 (54) 323 (38) 1434 (72)
360 1330 (119) 1690 (119) 190 914 (73) 381 (47) 1485 (87)
Results expressed as mean (SEM) (n Å 10). * p õ 0.001 ANOVA compared to NO LOAD and HF conditions. † p õ 0.05 ANOVA compared to HP and HF conditions.
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MEAN (SEM) VARIATION OF DESIRE TO EAT, FULLNESS, AND SATIETY IN THE 4 DIFFERENT CONDITIONS OF THE SECOND EXPERIMENT PLUS THE NO-LOAD CONDITION, AFTER SUBTRACTION OF THE FASTING VALUES (n Å 10) High-Protein Omelette
Desire to eat (cm2) tÅ0 a.p. a.t.m. Fullness (cm2) tÅ0 a.p. a.t.m. Satiety (cm2) tÅ0 a.p. a.t.m.
High-Fat Omelette
No load
Large
Small
Large
Small
0.0 – 018.6 (1.0)
0.0 010.0 (2.0)* 018.1 (1.2)
0.0 03.0 (1.7) 017.2 (1.4)
0.0 09.7 (2.1)* 019.5 (1.0)
0.0 02.8 (1.3) 018.0 (1.3)
0.0 – 17.1 (1.3)
0.0 4.3 (1.0)* 18.7 (1.1)
0.0 1.5 (0.5) 17.8 (1.2)
0.0 6.4 (1.5)* 18.7 (1.4)
0.0 1.2 (0.4) 19.2 (1.0)
0.0 – 18.2 (1.1)
0.0 4.8 (1.0) 17.6 (1.2)
0.0 2.3 (0.7) 16.5 (1.4)
0.0 3.5 (0.6) 17.5 (1.0)
0.0 2.4 (1.2) 17.6 (1.4)
* p õ 0.001 ANOVA compared to small omelettes; a.p., after preload; a.t.m., after test meal.
No specific macronutrient selection was observed in all the conditions (data omitted). Subjects continued eating different foods and drinking water until the physiological sensation of fullness reached a high value and their desire to eat dropped to zero. In fact, although the increase of satiety (17.5 cm2 ) was the same as in the previous experiment (17.4 cm2 ), the variations of fullness (18.3 vs. 12.5 cm2 ) and of desire to eat ( 018.2 vs. 014.1 cm2 ) were bigger, confirming that subjects were in a condition of general satiation (satiation for varied foods). Satiation was reached with a lower total energy intake (preload plus test meal) when the preloads were HP omelettes. It is interesting to observe the eating behaviour after the consumption of an isocaloric amount of preload (400 Kcal from HP omelette vs. 360 Kcal from HF omelette). Both the test meal and the total energy were significantly lower after consumption of the large HP omelette with respect to the small HF omelette. The information obtained from the SRQ clearly showed that subjects experienced a greater decrease of desire to eat and a larger increase of fullness and satiety after the large HP preload. These differences are too big to presume that the satiating power of the HP omelette is only due to the extra content of 40 kcal of this preload. Summarising, in a varied meal: 1. Subjects stop eating when they feel sated and completely full; 2. energy intake is lower when subjects eat the preload rich in protein as a first course, compared with the preload rich in fat.
h and 1300 h, subjects left the department, but they were not allowed to eat or drink anything else. Two questionnaires were also completed at 1200 h (45 *a.p.) and 1230 h (75 *a.p.). The test meal was served in the department at 0100 h, subjects were told to eat and drink as much as they wanted until they were comfortably sated. Desire to eat, fullness, and satiety were rated just before the test meal (b.t.m.) and immediately after (a.t.m.). A scheme of this procedure is reported in Fig. 1. All 14 men completed this last part of the study. RESULT
Table 7 summarises the mean { SEM of energy intake and weight intake (with or without water) after the 2 different conditions (HP and HF preloads consumed as snack at 1100 h) plus the no-load condition. The mean total energy intake (preload / test meal) for both the omelettes was similar to that of the noload condition. Considering only the test meal energy intake, we observed a significant difference between the preloads and the no-load condition [F (2,26) Å 9.845, p õ 0.001]. The mean total weight intake (omelette / test meal / water) was the same in all the conditions and, once again, analysing only the test-meal TABLE 7 ENERGY AND WEIGHT INTAKE IN THE 2 DIFFERENT CONDITIONS OF THE THIRD EXPERIMENT PLUS THE NO-LOAD CONDITION
No-Load
HighProtein Preload
High-Fat Preload
0 1861 (50)* 1861 (50) 0 1240 (51)* 462 (55) 1702 (48)
274 1385 (127) 1659 (127) 176 939 (102) 446 (69) 1561 (109)
284 1596 (98) 1881 (98) 150 1065 (71) 407 (70) 1622 (91)
EXPERIMENT 3 Method The objective of this experiment was to analyse the satiating capacity of the 2 omelettes when consumed as a snack 2 h before a meal (postingestive satiety). The preloading paradigm strategy was also used in this experiment with the following procedure: subjects came to the department at 1100 h on 2 occasions 1 week apart from the other. They received, in random order, a portion of HP omelette (176 g, 273.5 Kcal) or a portion of HF omelette (150 g, 284.3 Kcal) and a glass of water (150 ml). They were instructed to eat the preload in full, drink all the water, and fill in the SRQ before (t Å 0) and after eating (a.p.). Between 1115
Preload energy intake (Kcal) Test-meal energy intake (Kcal) Total energy intake (Kcal) Preload weight intake (g) Test-meal weight intake (g) Water consumption (g) Total weight intake (g)
Results expressed as mean (SEM) (n Å 14). * p õ 0.05 ANOVA compared to HP and HF conditions.
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weight intake, we found a significantly higher intake in the noload condition [F (2,26) Å 8.195, p Å 0.002]. Water consumption was similar in all the conditions. The satiety ratings expressed during the 2 meals are shown in Fig. 2. Variations, from before to after the preload consumption, of desire to eat [F (1,13) Å 4.555, p Å 0.052], fullness [ F (1,13) Å 16.946, p Å 0.001], and satiety [F(1,13) Å 21.414, p õ 0.001] depended on the type of preload eaten. After eating the HP preload at 1100 h, the desire to eat decreased and the feeling of fullness and satiety increased more than after the HF omelette. The ratings profiles were almost the same during the rest of the morning and after the ad lib consumption of the test meal. As expected, there was a significant effect of time on all the sensations (p õ 0.001), showing that the subjects were responsive to the consumption of the preloads and the test meal. DISCUSSION
Total weight intake was similar for both HP and HF conditions and for the no-load condition, suggesting that the mass of the snack eaten 2 h before did not provide any contribution to the weight reduction of the following intake. Probably the preloads had already left the stomach at the end of the 2-h interval. Comparing the amount of food ingested in the 2nd and 3rd experiments, the weight consumed on one single occasion (lunch time) was comparable (2nd experiment 1475 and 1420 g for HP omelette and 1434 and 1485 g for HF omelette, in the large and small condition, respectively; 3rd experiment 1385 (1561 0 176) and 1472 (1622 0 150) g for HP an HF omelette, respectively). The total energy intake was lower for the HP omelette than the HF and the no-load conditions but this difference was not significant. This seems to demonstrate that consuming a snack is not the best way to reduce energy intake. Maybe the amount we served at 1100 h was not enough to exert a strong effect 2 h later; however, we wanted to offer a correct amount of preload that could easily be consumed as a snack. Summarising: 1. A snack consumed 2 h before does not reduce energy intake at the test meal. GENERAL DISCUSSION In general, what emerges from this study is the primary role of weight intake, including water, and the role of protein in modulating the food intake in the different meal patterns examined. Researchers have usually concentrated their interests on energy intake and the influence of weight and volume has been studied very little, with differing conclusions (14,17,22), especially when considering caloric or noncaloric fluid intake. The present study shows that, in a uniform meal, subjects stop eating when a specific weight of food and water was ingested, reaching a higher satiety sensation compared to fullness sensation. Moreover, this intake is lower compared to the intake registered in a varied meal where subjects reach fullness and satiety at the same time. Water may play a role in the onset of satiety, in addition to contributing its own weight to gastric distention, liquefies the material in the stomach as reported by some authors (7). In this way, intestinal receptors, which are sensitive to nutrients, may be reached more quickly. As suggested by Kissileff (14), it is possible that the receptors respond best to nutrients that are most physically dispersed per unit of nutrient. In particular, protein seems to exert a stronger effect on satiation both in a uniform and in a varied meal, resulting in a lower total energy intake when the HP omelette was eaten on its own or as a preload immediately before a test meal. Another important fact to consider is that according to Sunkin and Garrow (28) and Pudel and Oetting (19), the eating behav-
FIG. 2. Mean (SEM) variation of desire to eat, fullness, and satiety in the 2 different conditions of the third experiment after subtraction of the fasting values (n Å 14). * mean significantly different (p Å 0.052) compared to HF omelette; 7 mean significantly different ( p Å 0.001) compared to HF omelette; § mean significantly different (p õ 0.001) compared to HF omelette.
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iour of people is greatly influenced by what they have eaten and what they think they have eaten. First of all, asking the subjects to consume a preload just before the test meal reduces the subsequent and the total weight intake compared to a no-load condition. Generally subjects think that the onset of hunger is delayed for a longer time after a high protein food (for example, a steak, which is considered particularly nutritious and satisfying). Consequently, we hid the protein and fat in a food, egg, which is generally considered both high in protein and fat and what we found was a similar consumption in weight intake. Finally, another aim of this work was to explore the effect of different meal timing on eating behaviour. In a recent study, Schlundt et al. (26) demonstrated that physiological variables may be influenced by meal pattern, eating one’s daily allotment of food in a few large meals may be physiologically and metabolically different from eating the same amount of calories in several smaller meals. For example, eating breakfast provides some advantages over eating only 2 meals a day; in particular, breakfast eaters show a lower fat intake and a higher carbohydrate intake. In the present study, the consumption of a snack 2 h before the meal did not reduce subsequent food intake and the total weight intake was similar to the no-load condition. This behaviour seems to indicate that the snack was metabolised and its effect on the food-intake control system was dissipated. The snack-meal relationship can be compared with the results reported by de Castro (6), who found a significant and positive correlation between the duration of the interval between meals and the size of the meal. As we have already discussed, probably our 2 snacks were not big enough to modulate subsequent intake
or, alternatively, our subjects were not used to consuming snacks. In fact, Louis-Sylvestre et al. (16) demonstrated that calorie compensation for a snack served 60 min before a dinner appeared only after subjects had received repeated experiences, but not the first time. Better results could be obtained by getting the subjects used to dividing up their daily intake into a breakfast, 2 main meals, and 1 or 2 ad hoc snacks. Overall, sensory characteristics of foods play an important role in controlling food intake and make a uniform meal more satiating that a varied meal. Weight and volume of food are important factors determining the amount consumed in a varied meal; consequently, the consumption of a snack far from a meal does not contribute to satiety. In each meal pattern adopted, protein always exerted a higher effect on satiety than fat. In conclusion, the weight and protein content of food are 2 important factors that must be considered when studying how to reduce food intake. Because it is inadvisable to have a high protein intake, we would suggest that further research should be made on the influence of weight on the control of food intake. From the results of our work, it seems that drinking water during a meal could contribute to increase the weight and volume of intake, inducing people to stop eating earlier. ACKNOWLEDGEMENTS
This research was supported by grant No. 94.00635.PF41 from the National Research Council, Targeted Project ‘‘Prevention and Control Disease Factors’’, Subproject ‘‘Nutrition.’’ The authors thank Silvia Tasca for her help in carrying out the study.
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