To investigate the independent effect of food form on appetite and energy intake in lean and obese adults using high carbohydrate, fat or protein food stimuli.
Crossover dietary challenge with matched beverage and solid food forms: high carbohydrate (watermelon and watermelon juice); high protein (cheese and milk); high fat (coconut meat and coconut milk).
A total of 120 lean (18–23 kg/m2; N=60) and obese (30–35 kg/m2; N=60) adults (18–50 years old) with stable body weight. Forty different participants (N=20 lean and 20 obese) were tested with each of the food systems.
Appetitive sensations, food palatability and dietary intake.
Regardless of the predominant energy source, the beverage food form elicited a weaker compensatory dietary response than the matched solid food form. Thus, total daily energy intake was significantly higher by 12.4, 19 and 15% on days the beverage forms of the high-carbohydrate, -fat and -protein foods were ingested, respectively. This was due more to a weak effect on satiety than satiation. The obese participants had higher energy intake at the lunch, including the beverage high-protein load, but overall differences between lean and obese participants were small and not systematic.
Food rheology exerts an independent effect on energy intake. Dietary compensation for beverages is weaker than for solid food forms of comparable nutrient content. Thus, they pose a greater risk for promoting positive energy balance.
Accumulating evidence indicates that energy-yielding beverages evoke weaker appetitive and compensatory dietary responses than energy-matched food challenges in solid form.1, 2, 3, 4, 5, 6, 7 Further, there is increasing documentation of a positive association between beverage consumption and body weight or body mass index (BMI).4, 8, 9, 10, 11, 12, 13 The mechanisms by which beverages and solid food forms elicit differential appetitive and dietary responses are not known.
Studies comparing responses to different beverage and solid foods (for example, fruit juice vs cheese and crackers,14 or soda vs cookies15) have yielded mixed findings. To isolate the independent effect of food rheology on appetitive and dietary responses, it is essential to hold other attributes constant. One study applied this approach to contrast responses to a solid casserole and soup,16 but responses to soups and beverages differ markedly – soup has higher satiety value.17, 18 An aim of this study was to contrast appetitive and acute compensatory dietary responses to solid foods and beverages closely matched on all but rheological properties.
Macronutrient-specific effects on satiety and satiation are well documented.19, 20, 21 Most, although not all, studies of these effects employed solid food vehicles. Less is known about the existence or magnitude of differential influences in beverages. Some findings suggest that they may not hold.22, 23 While there may be differences in nutrient composition and energy density among beverages that mitigate viewing all beverages similarly, from an energy balance perspective, distinctions may not be valid. The principal source of energy from beverages in the US diet over the past two decades has derived from carbohydrate,24 but there is increasing popularity of beverages with different primary energy sources (for example, specialty coffees with high fat content and performance enhancing beverages containing high protein concentrations). Whether, and to what extent, these items pose a particular challenge to energy balance requires assessment. A second aim of this study was to compare solid and beverage forms of foods comprised primarily of carbohydrate, fat or protein. The intent was to document the independent effect of food form in foods with different dominant macronutrient sources, not to contrast the relative magnitude of responses across the foods. Isolation of macronutrient effects would have required matching the items on all other relevant attributes (for example, energy density, osmolality) and this was not possible in the present context.
The obese may be at particular risk for positive energy balance due to beverage consumption. Reduction of beverage intake leads to a more robust loss of body weight in this group.25 However, the role of responsiveness to a beverage medium has not been explored as a mechanism. Responses of lean and obese people to comparable beverage and solid foods were contrasted in this trial.
Participants were instructed to fast for 10 h overnight, eat their typical breakfast (consisting of the same meal for each of the 3 test days) and fast again for at least 3 h before reporting to the lunch appointment. A finger stick glucose measurement was taken to verify the pre-test fast was maintained (values <110 mg/dl). Visits were scheduled during their customary lunchtime. On arrival at the laboratory, participants completed a motor skills test and an appetite questionnaire on a personal digital assistant (PDA). Participants were then provided a meal, consisting of chicken sandwiches and water for the control session or the sandwiches and a solid food or beverage sample on the other 2 test days. Meals were consumed in their entirety in individual booths within 20 min. Participants were provided two sandwich sections to begin the trial and were permitted to reach behind a partition to obtain as many additional sandwich sections as they desired to reach a comfortable level of fullness. They were unaware of how many sandwich sections were behind the partition.26 Minimizing the risk of participants passing a level of comfortable fullness, the test food was divided into thirds. On the days that samples were provided, participants were instructed to eat the first two-thirds of the test foods, to evaluate their level of fullness, and then to decide if eating the sandwiches would interfere with finishing the sample and going beyond a comfortable level of fullness. Samples were rated for palatability. After finishing their lunch, participants again completed the motor skills test and the appetite questionnaire. Before leaving the lab, participants were instructed to keep a food record of each eating or drinking occasion until going to sleep for the night. At the initial session, they were instructed in portion size estimation using NASCO food models (Fort Atkinson, WI, USA) and true-size pictures with a PowerPoint presentation. Additionally, the participants were requested to complete the appetite questionnaire on the PDA each hour and draw a single geometric form in the PDA every other hour until going to sleep for the night. Participants were informed of the researcher's interest in the association between appetite and fine motor control as a means to de-emphasize the focus on ingestive behavior and thereby minimize atypical feeding behavior or biased dietary reporting. All participants completed and signed an informed consent form approved by the Purdue University Institutional Review Board and received monetary compensation.
Study eligibility was established through completion of a screening questionnaire eliciting health and demographic information as well as anthropometric measurements. Participants meeting eligibility criteria, consisting of a BMI between 18–23 or 30–35 kg/m2, 18–50 years of age, stable body weight (3 kg change within the past 3 months), not taking medication known to influence appetite, self-reported regular consumer of breakfast and lunch, non-restrained eater (score <14 on the three factor eating questionnaire27), and nonsmoker were recruited by public advertisement. They were divided into two groups, lean and obese, for three dietary interventions based on preloads of foods providing energy primarily as protein (N=40, 20 lean and 20 obese), carbohydrate (N=40, 20 lean and 20 obese) and fat (N=40, 20 lean and 20 obese). Characteristics of these groups are presented in Table 1.
The participants were presented a meal consisting of chicken sandwiches that were provided in excess and were ingested ad libitum. However, only two sandwich sections were visible at any time.
The test food samples consisted of solid and beverage forms with one predominant macronutrient (Table 2). For the protein samples, a fat-free, low carbohydrate milk (Carb Countdown Fat Free Dairy Beverage, Hood, Chelsea, MA, USA) and cheese fortified with whey to a concentration comparable to the milk were consumed (fat free Mozzarella, Kraft Foods North America Inc., Rye Brook, NY, USA). For the carbohydrate samples watermelon fruit and watermelon juice were consumed. The fat sample consisted of coconut milk (A Taste of Thai Andre Prost Inc, Old Saybrook, CT, USA) and coconut meat (fresh). Water (1:1) and a sweetener (1 tsp of Equal® Sweetener, Chicago, IL, Merisant Co.) were added to the coconut milk to match the sweetness of the meat (this formulation was developed and pilot tested before the study). To match the beverage and solid sample volumes, participants were required to drink additional water when consuming the samples of coconut meat and cheese. Participants in the BMI range of 18–23 kg/m2 received a 125 kcal load and those between 30–35 kg/m2 received a 225 kcal load. These energy levels were selected to provide the two groups roughly comparable metabolic challenges (that is, 5–10% of estimated energy requirement) and volumes.
BMI was assessed by measurement of height and weight. Height was measured (±0.1 cm) on a wall-mounted stadiometer. Body weight was measured (±0.1 kg) using calibrated scales with participants wearing no shoes and a light gown. Participants were categorized as normal weight (BMI=18–23 kg/m2) or obese (BMI=30–35 kg/m2).
Dietary analyses and appetite/sensory assessments
Food records were kept each testing day to permit determination of energy intake and dietary compensation. They were analyzed using version 7.6 of the Food Processor nutrient database (ESHA, Research, Salem, OR). Satiation was estimated according to the discretionary energy consumed at lunch. Satiety was estimated in two ways; by energy consumed at the first meal after lunch, and by time (minutes between completion of lunch and onset of next eating or drinking occasion greater than or equal to 150 kcal). Percentage dietary energy compensation was calculated as [((energy intake in the absence of a preload)−(actual intake on test days−experimental load)/energy intake in the absence of a preload) × 100)]. The baseline energy values were for the midday meal or daily intake depending on the time frame of interest. Appetite ratings were recorded by participants on visual analog scales on PDA's, before and after consuming lunch, and each hour after leaving the lab. Questions included ‘How hungry do you feel right now? How full are you right now? How strong is your desire to eat right now? How strong is your feeling of thirst right now? How strong is your desire to eat something salty right now? How strong is your desire to eat something sweet right now? How strong is your desire to eat something fatty right now? ‘The scales were anchored with ‘not at all…/very weak’ and ‘as …I’ve ever felt/very strong’. The validity of this approach has been established.28, 29 Food sample palatability was rated on a visual analog scale with end anchors of ‘dislike extremely’ and ‘like extremely’ after sampling each item.
Repeated measures analyses of variance with one within-subject factor (meal form – beverage and solid) and one between-subject factor (lean vs obese) were used to assess responses to the intervention foods in each macronutrient pair. The study was not powered for comparisons between food products, nor would they reveal effects unequivocally attributable to the dominant macronutrient, because the foods varied on numerous additional attributes. The criterion for statistical significance was P<0.05, two-tailed. The dependent variables were discretionary energy consumed at lunch, energy consumed after lunch and the sum of these estimates, referred to as post-breakfast energy intake, satiety (that is, energy content of the first post-lunch meal and interval between lunch and first eating occasion of >150 kcal) and each appetitive index. Power calculations indicated a sample size of 20 participants per group (lean vs obese), would permit detection of between-group treatment effects equal to a standardized difference of 1 with 80% power. The Statistical Package for the Social Science (SPSS) version 12.0 was used for all analyses.
Appetite and hedonic ratings
With the exception of an isolated marginal effect of the beverage protein load being associated with elevated desire to eat something salty relative to the solid load, no significant effects of any test food form (Table 3) or BMI were observed for the mean daily appetitive ratings.
Mean hedonic ratings of the samples are presented in Table 4. All samples were rated as neutral or better (that is, >3.0); however, the solid high CHO (P<0.01) and fat (P<0.05) foods were rated higher than their beverage forms. There was no significant difference between the cheese and milk.
Post-breakfast energy intake and grams of fat consumed after lunch were higher with the beverage load compared to the solid (Table 5). Dietary compensation was significantly higher with the solid load compared to the beverage version for the post-breakfast energy intake (Table 5). The score was negative for the beverage load indicating slight reverse compensation (that is, failing to compensate for any portion of the beverage energy and actually eating more of the customary diet than baseline). The score was over 100% for the solid load, indicating the reduction of energy intake over the day exceeded the energy content of the load itself. There was a significant treatment by BMI interaction for energy consumed at lunch (Table 5). Obese participants consumed more energy at lunch than the lean (577 vs 436 kcal) with the beverage load (P=0.011), but their consumption did not differ from the lean participants with the solid load (470 vs 408 kcal). The obese ate more with the beverage load compared to the solid (577 vs 471 kcal) (P<0.0001). The latter was not true for the lean participants (436 vs 408 kcal) (P=0.318). Energy consumed after lunch and the intermeal interval (IMI; an index of satiety) were not significantly different between food loads or between the lean and obese groups.
Post-breakfast energy intake and energy consumed after lunch were significantly higher with the beverage load compared to the solid (Table 6). Dietary compensation over the day was also higher with the solid load. It reflected a small reverse daily compensation with the beverage load and overcompensation with the solid load. There was a significant treatment by BMI interaction for percentage dietary energy compensation at lunch. Obese participants compensated more (P=0.016) with the beverage load (46 vs 6%) compared to lean, but this did not hold for the solid treatment (P=0.284). The lean participants compensated more completely with the solid load (P=0.001) compared to the beverage load (24 vs 6%). There was a significant treatment by BMI interaction for energy consumed at lunch. The lean participants consumed more energy at lunch with the beverage load, compared with solid (519 vs 460 kcal) (P=0.008), but this did not hold for the obese participants (P=0.643). The obese and lean participants did not differ in energy consumed at lunch with the beverage (P=0.321) or solid (P=0.794) loads. No difference in post-lunch eating interval was detected.
Significantly, more energy was consumed after lunch (P=0.026) and post-breakfast (P=0.016) with the beverage load compared to the solid (Table 7). There was no difference of energy consumed at lunch between treatments. Post-lunch carbohydrate energy consumed was higher after the beverage load compared to solid, but there were no differences for protein and fat consumption. Dietary compensation was significantly higher with solid load compared to the beverage load over the day (P=0.016). The beverage load led to marked reverse compensation, while the solid load resulted in partial compensation. No difference of compensation was observed at lunch. The intermeal interval was not significantly different between loads or between the lean and obese groups.
A strong body of evidence indicates that energy-yielding beverages are contributing to the positive energy balance and increasing incidence and prevalence of overweight/obesity.7 This has prompted recommendations to moderate their level of ingestion.30, 31 Some have targeted these recommendations to particular beverages, but from an energy balance perspective, the rationale for this approach has not been substantiated. Others have challenged the data specifically linking beverage ingestion to BMI, primarily on the grounds that there is a lack of a plausible biological basis for such an association.32 There is a need to identify and characterize the properties of beverages that may contribute to the reported differential responses they elicit relative to solid foods to substantiate this view and to develop appropriate guidelines for beverage consumption. To this end, the primary hypothesis addressed in this work was that energy-yielding beverages exert weaker appetitive and compensatory dietary responses than the same foods ingested in solid form. Further, these effects were explored in foods varying in the predominant energy source to determine the relative importance of the energy source and medium in these outcomes. Finally, the responses of lean and obese individuals to challenges with beverages and solid foods were contrasted to gain insights on whether the obese are at greater risk for positive energy balance due to beverage consumption. The key feature of this work was the isolation of the rheological property of the test foods as the independent variable.
No evidence was obtained that the beverage and solid forms of the same foods elicited different appetitive responses. This is consistent with findings from several trials,15, 33 but that work used foods with different nutritional composition, thereby hampering conclusions about the role of rheology. Others have noted weaker appetitive responses for fruit juices relative the whole fruit,34, 35 but here again, there are compositional differences, such as higher fiber in the solid forms. Even a small addition of fiber to a beverage that increases its viscosity augments reported hunger reduction.6 Some work indicates soups, a beverage food form, are actually more satiating than solids, but this appears to be a unique property of this food (likely the cognitive expectations it elicits36), so of limited relevance to a consideration of beverage effects.18 Clearly, there is some structural difference between beverages and solid foods. The present results suggest that disruption of that structure (for example, by blending), without changing composition, does not exert a marked effect on appetite, as measured by questionnaire.
Although it is commonly assumed that appetitive sensations serve to link energy need with energy intake, this is not reliably observed.17 The present data are a case in point because, despite the lack of a differential appetitive response to the beverage and solid food forms, there was a strong and consistent difference in the compensatory dietary response they elicited. This finding is not surprising given the multitude of factors that independently influence appetite and feeding.
With all three foods, daily energy intake was significantly greater when the beverage form was ingested compared to the solid. Indeed, the compensation scores were negative for all three beverages, indicating they resulted in reverse compensation. That is, daily energy intake was actually greater than baseline by an amount that exceeded the energy contributed by the beverage. In contrast, the compensation scores for the solid forms were all positive. They varied from partial to over compensation (that is, intake lower than baseline). The compensation score for the high-fat food was the lowest, consistent with other reports;37 however, given that only three foods were tested, the generality of this observation is uncertain. The energy intake differences and compensation scores at lunch were less consistent and smaller in magnitude. This suggests the effects of rheology are more pronounced on satiety than satiation. This was not reflected in the interval between lunch and the next eating occasion, as this was not different for the beverage and solid food forms. Thus, the difference may lie in the energy content of subsequent eating events. Only small and inconsistent differences in post-lunch macronutrient intake were noted between the two food forms, suggesting the compensation was attributable to altered intake of the general diet. Others have also reported a lack of macronutrient compensation.38
Differential macronutrient effects on appetite and dietary compensation have been reported such that protein>carbohydrate>fat.39 Generally, this stems from trials involving solid foods. There are suggestions that these discrepancies are less reliable in beverages. In particular, the reported high-satiety value of protein and its suppressive effect on energy intake often is not observed when delivered in beverage form.22, 23 The three foods tested here derived most of their energy from a different macronutrient and they were not closely matched on other nutrients. Thus, contrasting responses across foods would be of limited value. However, in the beverages, none of the macronutrients prompted any offsetting adjustment in subsequent energy intake. Post-breakfast energy intake was significantly higher than baseline in each case. This raises questions about the likely benefit of substituting one form of beverage for another (for example, 100% fruit juice or milk for soda) with respect to energy balance. There may be some differences in nutrient density between beverages that are nutritionally relevant when making public health recommendations, but if the focus is on energy balance, it is not clear that distinctions are appropriate.
There is a long history of research on potential differences in behavioral40 and metabolic41 responses to foods in the lean and obese that may account for their phenotypes. Evidence that the increasing incidence of obesity stems from a disproportionate increase in BMI by heavier individuals than the lean42 suggests that there may be BMI-related differences in responses to food cues. This study provides new data on the appetitive and dietary responses of lean and obese individuals to energy provided in different rheological forms. The loads differed in energy content so that comparable metabolic challenges were present to the two groups. No BMI differences were observed for appetitive ratings. Differences in intake were small and inconsistent. The obese consumed more energy at the lunch that included the beverage high-protein load, while there was no difference with the solid load. However, there was no difference in energy consumed at lunch between the BMI groups when the high-carbohydrate or high-fat loads were presented. Others43 have also reported little BMI-related difference in dietary responses to beverage and solid loads, although the stimuli used previously (flavored milk and an angel food cake with jam) differed on many dimensions. Thus, these data do not support a view that beverage consumption is more likely to lead to positive energy balance in the obese.
The present findings should not be over-interpreted. This study involved acute testing of a relatively small sample of participants. The sample size limits extrapolation of the findings, but not the study power, because significant effects were clearly documented. Data are presented at a meal and over a single day. The latter observations are emphasized as they provide greater opportunity for compensatory responses to manifest, but even daily intake is highly variable and additional compensation may occur over days and weeks.44 However, there are data indicating a reduction of energy from beverages results in weight loss45, 10, 25 and addition of energy-yielding beverages leads to weight gain.8, 46, 12 Both of these sets of observations are consistent with the present acute, but more tightly controlled tests. Another limitation is that only three foods were tested. They were selected on the basis of their primary energy source and potential for modification of form. They do not represent the universe of foods and many facets of products, ranging from the cognitive impression they impart17 to the bioaccessibility of the energy they contain,47 may modulate the responses to and consequences of ingesting foods of varying rheology. Still, accumulating evidence indicates this food attribute holds nutritional consequence. While efforts were made to equate the foods on palatability, this was not accomplished. The solid forms of the high-carbohydrate and high-fat foods were rated higher than their beverage version. This was probably attributable to the novelty of these beverage forms; the solid and beverage forms of the high-protein food are commonly consumed. As palatability is generally assumed to be directly related to intake,48, 49 it would be predicted that these solid forms would lead to greater intake than the beverage versions. However, the opposite was observed. Thus, it would not appear that this discrepancy accounts for the study findings.
With documentation of this effect of food form, the question turns to possible mechanisms. Feeding is guided by environmental and physiological (for example, cognitive, orosensory, digestive, metabolic, endocrine, neural) influences. Differential responses to beverages and solid food forms may be posited at each level. Environmentally, portion sizes of beverages have increased markedly,50, 51 they are among the least expensive sources of energy and are a meal component that is provided in unlimited quantity in most commercial restaurants. Beverages have lower expected satiety value, lower demand for oral processing, shorter gastrointestinal transit times and the energy they contain has greater bioaccessibility and bioavailability. Each of these attributes has been associated with weaker effects on appetite and dietary compensation.52, 53, 54, 55, 56, 57, 58, 59 The absolute and relative importance of these properties, and others, has not been established, but warrant exploration.
In summary, the present trial supports an independent effect of food rheology on energy intake. The inclusion of a caloric beverage in a lunch meal led to greater daily energy intake compared to customary intake or days, where a solid version of the same food was ingested. This occurred regardless of the primary energy source. There was no clear indication that the lean and obese differ in this regard. Efforts to moderate energy intake should consider the contribution of beverages of all types.
This work was supported by PHS grant no. 1 R01 DK 063185 and CNPq, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasília/Brazil.