OBJECTIVE: To explore the relative importance of a food's macronutrient composition, energy value, energy density, fiber content, weight, volume, sensory properties and rheology on hunger and food intake.
DESIGN: Preloads of peanuts, peanut butter (rheology control), almonds (tree nut), chestnuts (macronutrient control), chocolate (sensory control), rice cakes (volume control), pickles (weight control) and no load (time control) were consumed by subjects in random order at weekly intervals and hunger was assessed over the subsequent 180 min. Free-feeding energy and macronutrient intake were monitored 24 h before and following preload ingestion.
SUBJECTS: Twelve male and 12 female healthy, normal weight (12–28% body fat), adults (mean (s.d.) age 22±2.5 y) with low dietary restraint.
RESULTS: Hunger ratings following consumption of the 2092 kJ (500 kcal) preloads of peanuts, peanut butter, almonds, chestnuts and chocolate were significantly lower than the low energy preloads or no preload condition, but with the exception of peanut butter, did not vary from each other. The rate of hunger recovery was consistent across all preloads so the overall impact of each food on hunger was determined by the initial drop it evoked. Total energy, but not macronutrient, compensation was observed with all preloads. Consequently, the fatty acid profile of the total diet reflected the composition of the preloads.
CONCLUSIONS: Energy content may be the primary determinant of a food's impact on hunger. Because macronutrient compensation is weak, a dietary supplement or substitute may influence the daily dietary nutrient profile.
A major obstacle to weight loss and the reduction of obesity is the feeling of hunger associated with negative energy balance. Suppression of hunger through behavioral, dietary and pharmacological means has been a cornerstone of therapy. When achieved, dietary compliance is improved. However, the low long-term success rate of weight reduction regimens is evidence of the difficulty in achieving a sustained suppression of hunger. In part, the failure to therapeutically manage hunger stems from a lack of understanding of food properties that modify the sensation. Among the potentially relevant attributes cited in the literature are macronutrient composition, energy value, energy density, fiber content, weight, volume, sensory properties and rheology. However, the relative efficacy of each remains controversial. The present study sought to clarify this issue by contrasting hunger responses following preloads of foods typifying each of these attributes.
Inconsistent findings have been obtained from studies exploring differences in the suppressive effects of the macronutrients on hunger. While there is support for the view that the ordering is protein>carbo-hydrate>fat1 other data indicate they are equivalent.2,3,4,5 The passive over-consumption noted with high-fat foods implies a weak effect of this macronutrient, but this has recently been attributed to a related property, its high energy density.6,7,8
Meals high in total energy generally reduce hunger to a greater degree than those of lower energy content.9,10,11,12 However, similar hunger ratings have also been reported after consumption of preloads with different energy values.13,14 At least upon initial exposures, belief about the energy value of a meal may have a greater effect than actual energy content.12 High fiber foods are often recommended to modulate hunger and there is evidence for such an effect.15,16,17,18,19 Others have failed to note decreased feelings of hunger.20 Inconsistencies may be due, in part, to differences in the types of fiber consumed.
Commonly, studies involving covert manipulation of the energy content of a food or meal reveal that individuals consume a consistent weight of food. This has prompted the hypothesis that physical weight exerts an important influence on appetitive signals.21,22,23,24 Indeed, several recent studies indicate hunger ratings are better explained by the weight of food ingested than energy density8,21 or macronutrient composition.21 However, others report no relationship between the weight of food consumed and satiety or dietary compensation.25,26 High-fat foods may be heavy or light and still promote passive over-consumption. This is also true for carbohydrate. We have recently obtained hunger ratings from individuals after consumption of equal energy loads of soda or jelly beans.49 The weights of the loads differed markedly (259 g for jelly beans and 978 g for soda), but hunger ratings over the 3 h post-meal interval were nearly identical.
Distention of the stomach with a balloon suppresses hunger, indicating that volume of a food or meal exerts a modulatory effect.13 Studies involving administration of water27 or varying portions of preloads matched on macronutrient and energy content as well as palatability provide additional evidence supporting such a view.24,28 However, because the loads covaried in volume and weight, a conclusion isolating a volume effect is not possible. Whether the cognitive impression or physical dimension of a food's volume may be most important has not been evaluated.
Sensory properties of foods have been reported to influence hunger, although the direction of effects is inconsistent. For example, sweetness has been shown to enhance,29,30,31 suppress32 or have no influence33 on hunger. Such discrepancies may be due to confounding with palatability, although even palatability does not elicit a reliable effect. High palatability has been shown to enhance34 and suppress hunger.35 The desire for sensory stimulation in general may also contribute to the variance.36,37
A meta-analysis revealed compensatory dietary responses to preloads of varying rheology were weakest for fluids, intermediate for semi-solids and strongest for solids.38 This is suggestive of an influence of food form, but the assumption that dietary compensation reflects an influence of appetitive signals such as hunger has yet to be verified.
Undoubtedly, methodological issues such as timing of food presentation and hunger rating response format and subject expectations account for some of these noted discrepancies.36,39 To reduce the influence of such potential confounding factors on hunger ratings, the present study used a within-subject design. This work was undertaken as part of an international investigation of the satiety effect of peanuts. Because peanuts are high in protein and fiber, energy dense and solid, we hypothesized that peanuts would have a strong suppressive effect on hunger. Consistent with this view, epidemiological data indicate nut (including peanut) consumption is associated with reduced body mass index.40
Eight preloads were administered to participants in random order at approximately weekly intervals. Participants reported to the laboratory 3.5 h prior to their customary midday meal time after having fasted from 11:00 pm the previous evening. Baseline questionnaires eliciting information about hunger, fullness, desire to eat and prospective consumption were completed and saliva samples were collected by the method of Christensen and Navazesh.41 The purpose of the latter was to distract participants from the true purpose of the study. The participants were then allotted 15 min to consume the preload and 150 ml of deionized water. Immediately after ingesting the load, participants again completed the questionnaires (time 0) and fasted for 3 h. They were provided with timers and printed sets of questions and completed the questionnaires at 15, 30, 60, 90, 120, 150 and 180 min. They kept free-feeding dietary records during the prior and ensuing 24 h. The study protocol was approved by the Human Subjects Committee of Purdue University.
Twenty-four healthy adults (12 male and 12 female), mean (s.d.) age 22±2.5 y were recruited through the use of printed advertisements. Eligibility criteria included: 12–28% body fat as measured by bioelectrical impedance analysis (BIA); not on prescription medications, except for birth control; not pregnant or lactating; not on any specific diet or health program; no recent history of weight loss or gain; reported regular consumption of breakfast and lunch during the morning to early afternoon hours; and low dietary restraint.42,43
The eight preloads included: (1) unsalted cocktail peanuts (Planters, Nabisco Foods, Planters Division, Winston-Salem, NC); (2) low sodium peanut butter (Peter Pan, Hunt Wesson Inc., Fullerton, CA); (3) almonds (bulk, raw); (4) chestnuts (whole chestnuts in water, Clement Faugier, Privas, France); (5) milk chocolate (Hershey Foods, Hershey Chocolate USA, Hershey, PA); (6) dill pickles (kosher dill spears, Vlasic Foods Inc., Camden, NJ; (7) salt-free and fat-free rice cakes (Quaker Oats Co., Chicago, IL), and (8) a no-load condition. The subjects also consumed 150 ml of deionized water at each session. All preloads, except chestnuts, were given as prepared by the manufacturer. The chestnuts were rinsed and baked at 155°C for 30 min.
Preload selection was based on the properties of peanuts. Peanut butter provided a rheology control. Over 85% of the energy in chestnuts is derived from carbohydrate so they served as a macronutrient control. Chocolate is a sweet snack and provided a sensory control. Almonds were included because of a planned comparison with peanuts on post-prandial lipid concentration (not reported here). Each of the above was provided as a 2092 kJ (500 kcal) portion (Table 1). The pickles were matched to the peanuts on weight, each provided approximately 90 g. The approximate preingestive volume of the rice cake and peanut preloads was 37.5 cm3 (the post-ingestive effects on gastric distention were not measured). The no load condition was used as the time control.
Hunger and desire to eat assessments
Hunger was recorded on a 13 point category scale with end anchors of ‘not at all hungry’ and ‘extremely hungry’. Ratings were also obtained for questions about fullness, desire to eat and how much participants thought they could eat (data not included). In addition, participants indicated the strength of their desire to consume foods from a list of 39 items comprising the preload foods and others representing various nutrient content and sensory properties.
Participants were trained to keep free-feeding dietary records prior to beginning the study. Training included estimation of food portions using plastic food models. A standard form with columns for amounts and descriptions of the foods and beverages consumed was used throughout the study. Participants' selection of food was uncontrolled but recorded for the 24 h periods prior to and following preload consumption. Each dietary record was reviewed with the participant to ensure its accuracy and completeness. All dietary records were analyzed with the Nutritionist IV nutrient database (First Databank, San Bruno, CA). Analyses were conducted by a single individual to standardize coding.
Due to the within-subject design, hunger ratings and dietary intake were analyzed by repeated measures analysis of variance (ANOVA). Where appropriate, Duncan's multiple range test (Duncan's means test) was used for post-hoc analyses. Power analysis44 indicated that a sample of 24 would permit detection of a treatment effect that accounted for 10% of the within-subject variance in energy intake with 85% power at the 5% level of probability.
The time course of preload effects on hunger was evaluated by the following indices: (1) initial change from baseline to time 0 (onset); (2) change between baseline and 180 min post-loading (rebound); (3) slope of the regression line from time 0 to 180 min post-loading (recovery); and (4) area under the curve from time 0 to 180 min post-loading (AUC). Associations between these measures were assessed by Pearson correlation coefficients.
Dietary compensation for the 2092 kJ preloads was calculated as: (energy intake from the self-selected diet+energy from the preload (this sum equals total daily energy intake assuming there is no adjustment in the self-selected diet)) minus (actual energy intake from the self-selected diet+energy from the preload (this sum equals total daily intake accounting for any adjustment in self-selected diet)) divided by the energy value of the preload. The result of this calculation is the proportion of energy provided by the preload that was offset by an adjustment in the self-selected diet. Thus, for an individual who normally consumed 10,000 kJ per day, the first term in the numerator would equal 12,092 kJ (10,000 kJ+ 2092 kJ). However, if the individual reduced energy intake from their self-selected diet to 8954, their daily intake including the preload would be 11,046 kJ (the second term in the numerator). Dividing the difference by the preload energy consumed ((12,092− 11,046)/2092) results in a compensation score of 0.5 or 50%. Paired t-tests were performed to compare the macronutrient and percentage of saturated, monounsaturated and polyunsaturated fat intakes on the preload day and prior no-load day. Intake was monitored in addition to hunger ratings on the basis that it reflects, in part, a response to internal hunger cues.
Hunger rating data are presented in Figure 1. Baseline hunger ratings were not significantly different across treatments. Immediately following preload ingestion (onset), significant differences were observed between treatments (F=10.59, P<0.001). Relative to the no-load condition, all preloads except the rice cakes and pickles led to a suppression of hunger. All loads containing 2092 kJ reduced hunger to a greater degree than the rice cakes and pickles. The decline after peanut butter ingestion was significantly less than that reported after peanuts or chocolate.
Rebound (the difference between baseline and 180 min post-loading) differed significantly across treatments (F=5.55, P<0.001). The higher energy loads (peanuts, peanut butter, almonds, chocolate and chestnuts) produced lower values than the no-load, rice cake and pickles. Rebound was greater for the chestnuts and peanut butter compared to the peanuts, almonds and chocolate. Values for the latter three did not differ.
Recovery (slope of the regression line from time 0 to 180 min post-loading) did not differ across treatments (Figure 2).
Significant treatment effects were observed for AUC values (area under the curve from time 0 to 180 min post-loading, F=12.44, P<0.001). The high energy loads all led to lower values compared to the no-load, rice cake and pickles treatments. Responses to the high energy loads did not differ from each other.
Comparisons of energy intake during the day preceding preload consumption and the day of preload consumption were comparable for each treatment (Figure 3). The percentage of energy derived from carbohydrate and protein were also similar during these times. The percentage of energy from fat on days of peanut, peanut butter and almond loading was significantly greater than each of the respective prior control days (F=8.22, P<0.001; Figure 4). Saturated fat, as a percentage of total daily energy intake, was significantly higher on the chocolate preload day relative to its preceding day (F=8.59, P<0.001), but this was not observed with any other treatment (Figure 4). The percentage of energy from monounsaturated fats was higher on days that peanuts, peanut butter and almonds were consumed compared to their control days (F=14.71, P<0.001). The percentage of energy from polyunsaturated fats was higher on days that peanut butter and almonds were consumed compared to their control days (F=11.90, P<0.002).
Mean (s.e.) dietary compensation scores for the energy matched preloads were: peanuts, 104±24%; peanut butter, 151±33%; almonds, 57±25%; chestnuts, 57±40%; chocolate, 89±37%. ANOVA indicated these values were not significantly different. The percentage of participants showing partial compensation (a reduction in free-feeding energy intake that partially offset the energy contributed by the preload), over compensation (a reduction in free-feeding energy intake that more than offset the energy contributed by the preload) and no compensation (no reduction or an increase in free-feeding energy intake) are shown in Figure 5. The proportion of participants with no compensatory response was significantly higher (P<0.05) following the chestnuts compared to the peanut, peanut butter, almond and chocolate loads.
Following consumption of the peanut and chocolate preloads, the desire to consume additional peanuts and chocolate was significantly reduced (all P<0.006, Bonferroni correction applied because of multiple comparisons) for the subsequent 180 min. Peanut butter led to a reduced desire to consume additional peanut butter from 90 to 180 min post-loading. No other load led to a significant reduction in desire to consume that specific food. Similar results were obtained for the desire to consume foods high in fat and protein except the peanut butter led to a reduction of desire for high protein foods over the full 180 min assessment period. Only peanut butter and chestnuts led to a consistent reduction of desire to consume the high carbohydrate foods. The chocolate load reduced the desire for salty snacks and peanut butter did so at 90, 120 and 180 min. Desire to consume sweet snacks was reduced by peanut butter only at the 150 and 180 min time points and by chocolate only at 90 min.
No significant correlations were observed between the various computed hunger indices and total daily energy intake or ingestion of energy from total fat, saturated fat, monounsaturated fat, polyunsaturated fat, carbohydrate or the weight of food.
The effect of any food or meal on hunger will reflect the combined influence of multiple food attributes. Nevertheless an understanding of the relative importance of different attributes should aid in basic studies of feeding and therapeutic dietary manipulations. Although the foods used in this trial were not perfect controls for each of the attributes under study and were all familiar to participants, the clarity of the findings underscores the predominant influence exerted by the energy content of a food. All of the foods presented in 2092 kJ (500 kcal) portions led to similar suppressions of reported hunger and reductions that differed significantly from foods containing less energy. Using peanuts as a standard, the similarity in hunger responses to chocolate, a high-fat but sweet snack, suggests that taste properties were overridden by energy content. A subordinate role for sensory properties, in general, is supported by the similarity of responses to all of the high energy loads, which differed markedly in odor, texture and appearance. The similarity in response between chestnuts, which represented an isoenergetic carbohydrate load and the higher fat peanuts indicates macronutrient content was not the key determinant of hunger. This finding has recently received increasing support.6,8 The degree of fatty acid saturation was also of lesser importance since the peanuts and almonds are high in mono- and polyunsaturated fatty acids whereas chocolate is higher in saturated fats. Peanut butter did offer the ideal rheological control for the effect of peanuts on hunger. It elicited a significantly smaller initial drop in hunger and a significantly greater recovery. This underscores an important role for rheological properties consistent with a meta-analysis indicating the compensatory dietary response to foods of varying energy content is greater for solids than semi-solids or fluids.38 The pickle and rice cake preloads led to significantly smaller reductions of hunger than the peanut load despite being matched for weight and volume, respectively. This calls into question the importance of these attributes in regulating hunger. Indeed, the portions of the preloads, which were equal or greater than customary serving sizes, did not lead to responses that differed markedly from the no-load treatment. The lack of a greater impact on hunger by the chestnuts relative to the other higher energy loads, despite their markedly greater mass, offers additional evidence for the weak effect of volume or weight under the test conditions. Previous work has yielded mixed findings on the importance of these attributes.8,21,22,23,24,25,26 It may be that weight and volume are closely, but not invariably, linked with culturally defined portion sizes and that the latter is the stronger determinant of appetitive responses. Given that culturally defined portion sizes reflect a host of non-biological influences (eg cost, marketing) as well as dietary experience and that food processing practices are increasingly uncoupling weight, energy density or energy content from portion size, high appetitive response variability would be expected. Recent evidence indicates the influence of culture on portion size is apparent by 5 y of age45 and under certain conditions, cognitive factors exert a stronger influence on reported hunger than physiological cues.12
While differential responses to the preloads were noted on most hunger indices, no effects were observed for rebound. The rate of growth of hunger following the initial post-load drop was constant across foods. This is apparent in many preload studies and has been documented previously.17 Thus, the degree to which a food or meal will suppress hunger appears to be primarily determined by the initial drop it elicits.
Although individual variability was high, the participants exhibited accurate compensatory dietary energy responses to the preloads. Free-feeding energy intake was reduced on days the high energy preloads were consumed so that total daily energy intake was comparable both across treatments and between treatment and control days. An adjustment was observed in 70–80% of participants. If these findings, based on acute loading, hold for chronic use of the test foods, they indicate the foods do not pose a risk for positive energy balance. Indeed, while nut consumers may differ from non-users in other respects, evidence indicates they are not heavier.40
The dietary adjustment following ingestion of the peanuts, peanut butter, almonds and chocolate, involved small reductions of protein and carbohydrate intake. Fat consumption was significantly elevated on days these high-fat loads were presented. Thus, as has been reported previously,46,47,48 there was energy, but not macronutrient compensation. Similarly, the high carbohydrate chestnut load led to a significant increase of carbohydrate intake. The lack of adjustment of fat intake resulted in a dietary fatty acid mixture that reflected the composition of the loads. Thus, when the peanuts, peanut butter and almonds were ingested, the daily dietary fatty acid profile was significantly elevated in mono- and polyunsaturated fats. When the load was chocolate, there was an elevated total and proportional intake of saturated fatty acids.
The preload foods had differential effects on the reported desire to consume an array of similar and dissimilar foods. After consuming the peanuts and chocolate, participants expressed a significantly reduced desire to consume more of the same food as well as other high-fat and high-protein items. Peanut butter had a similar, but less consistent effect. Both peanuts and chestnuts were associated with reduced desirability for high carbohydrate foods. The chocolate load did not reduce the desire of other sweet snacks and the peanuts did not lessen the desire for salty snacks. The other preloads did not markedly alter participant ratings for the same or different foods. None of the loads led to an overall reduction in desirability of foods. These observations argue against a sensory or nutrient-specific effect of ingestion of a single food on affective ratings of foods generally. The energy density and energy content of the preloads also did not lead to predictable shifts in food desirability.
Several points that bear on the interpretation and extrapolation of these observations warrant mention. First, there were different constraints imposed on control and preload days that could have influenced responses. On preload days, participants were required to eat a load and fast for 3 h. We do not feel this poses a substantive threat to interpretation since all participants ate breakfast on control days (recruitment was based, in part, on this behavior) and eating during the following 3 h was minimal. Second, the percentage of energy derived from fat on control days was low relative to population statistics. We believe this reflects the highly educated, health conscious sample recruited. Given the within-subject design and fact that subjects were not restrained eaters, who may be more inclined to exhibit a disinhibition response to the high-energy, high-fat preloads, we do not think this behavior undermines the findings.
In summary, the present findings indicate that the energy content of a preload exerts a stronger influence on hunger over the 3 h post-ingestive period than the food's macronutrient composition, energy density, fiber content, weight, volume, sensory properties or rheology. The rate of hunger recovery after food ingestion is also unaffected by these attributes. Finally, while ingestion of foods varying along these dimensions did result in shifts of subsequent diet composition and affective responses to foods, total energy balance was maintained.
Within the limits of the foods and attributes tested, this study has not revealed unique characteristics of foods that exert suppressive effects on hunger that are disproportionate to the energy content of the food. At the same time, the data indicate exclusion of specific foods with any of the assessed features to achieve weight reduction may not be warranted.
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This work was supported by a grant from the United States Agency for International Development (no. RD309-022/4092094).
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Kirkmeyer, S., Mattes, R. Effects of food attributes on hunger and food intake. Int J Obes 24, 1167–1175 (2000). https://doi.org/10.1038/sj.ijo.0801360
- food intake
- energy density
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