Clinical Studies and Practice

Effects of fruit and vegetable, consumed in solid vs beverage forms, on acute and chronic appetitive responses in lean and obese adults

Abstract

Background:

The effects of fruits and vegetables in solid vs beverage forms on human appetite and food intake, acutely and chronically, are unclear.

Methods:

This 21-week, randomized, crossover study assessed appetitive ratings following the inclusion of fruits and vegetables, in solid and beverage form, into the habitual diet of healthy lean (n=15) and overweight/obese (n=19) adults with low customary consumption. The primary acute outcomes were satiation (amount of challenge meal consumed), satiety (latency of subsequent eating event) and dietary compensation after a 400 kcal fruit preload. Ratings of appetite were also obtained before and after 8 weeks of required increased fruit and vegetable consumption (20% estimated energy requirement).

Results:

Acutely, overweight/obese participants reported smaller reductions of hunger after consuming the fruit preload in beverage compared with solid form (preload × form × body mass index effects, P=0.03). Participants also consumed significantly less of a challenge meal (in both gram and energy) after the ingestion of the solid fruit preload (P<0.005). However, the subsequent meal latency was not significantly different between the solid and the beverage fruit preloads. Total daily energy intake was significantly higher when the obese participants consumed the beverage fruit preload compared with the solid (P<0.001). Daily energy intake was markedly, but not significantly, higher among the lean with the beverage vs solid food form. Hunger and fullness ratings remained stable when participants consumed fruits and vegetables in solid or beverage form for 8 weeks each.

Conclusion:

Acute post-ingestive appetitive responses were weaker following consumption of fruits in beverage vs solid food forms. Consumption of beverage or solid fruit and vegetable food loads for 8 weeks did not chronically alter appetitive responses.

Introduction

Decreasing the energy density of the diet through increased consumption of fruits and vegetables has been suggested as a method to decrease or maintain body weight.1, 2, 3, 4 The purported mechanism is based on energy displacement where foods of higher volume and lower energy density lead to decreased hunger, increased fullness and decreased total energy intake.5, 6, 7, 8 Short-term preload and some long-term weight-loss trials provide experimental evidence to support this hypothesis,3, 7, 9, 10 but long-term, more ecologically valid data derived from trials with non-covert energy density manipulations,8, 11 using common foods such as fruits and vegetables in populations encompassing both sexes, a range of body mass index (BMI) categories and minimal counseling intervention (representing the general population), are needed to verify this effect. Although the Dietary Guidelines for Americans12 suggest there is strong evidence to support a relationship between low energy density and weight loss/weight-loss maintenance among adults, a deeper examination of the literature suggests alternate interpretations are viable and recommendations should proceed with caution.

Well-established data incongruous with the energy displacement hypothesis pose a challenge to its veracity. First, reduced food intake noted with gastric distention13, 14, 15 may be short-lived.16 Over a period longer than several hours, other factors (for example, the absolute energy content of the meal) also contribute to satiety, particularly when low energy dense foods are included as part of the typical diet.11, 17, 18, 19, 20 Second, foods at the extremes of the energy density continuum do not support energy density as the primary control of energy intake. Owing to their high water content, sweetened beverages have very low energy densities (for example, cola: 0.4 kcal g−1 (ref. 21)) so they should aid weight management. However, the evidence is strong, albeit not uniform,22 that sweetened beverages elicit weak dietary compensation23, 24, 25, 26, 27 and may promote weight gain.23, 28 In contrast, nuts have high energy density (for example, dry peanuts: 5.8 kcal g−1 (ref. 21)) and should theoretically promote weight gain. To the contrary, acute feeding studies consistently demonstrate nuts are satiating29, 30, 31 and do not contribute to weight gain.32, 33, 34, 35, 36 Third, disagreement in the literature of how to report energy density may lead to energy density associations that are of questionable practical significance. For instance, many studies reporting an association between energy density of the diet and total energy intake exclude beverages from the analysis and the relationship is not present or markedly diminished when they are included.37, 38, 39, 40, 41 It has been suggested that beverages should be removed from analyses because they add variance to data and reduce statistical power.3, 37, 42, 43, 44 A physiological rationale for this argument is lacking and is required given that energy-containing beverages now contribute 18% of dietary energy.45 Fourth, if energy density is a primary factor affecting energy intake, there should be evidence that dietary energy density has changed over the past three decades coincident with the increased obesity incidence. Again, these data are not clear. Between the years 1971–2000, there was a decrease in the proportion of fat in the American diet, an increase in carbohydrate, and maintenance of protein and fiber.46, 47, 48 Since 2000, trends of fat and carbohydrate consumption have reversed49 while fiber intake has remained unchanged without the change of predicted BMI.50 Data on total water consumption are sparse, but there is no evidence that water consumption has decreased over time.51, 52, 53 Combined, the three main contributing factors to energy density (water, fat and fiber) are unchanged or shifting in the direction opposite to the expected increasing energy density in the American diet. Overall, these observations raise questions about the long-term effects of energy displacement through consuming low energy dense foods on appetite and energy intake. As there was a strong emphasis on energy density for weight management in the most recent Dietary Guidelines for Americans,2 it is critical to continue to review the applicability of this diet strategy for Americans.

Foods in beverage form are consumed faster,54 producing shorter oral exposure time,55 and they are emptied faster from the stomach than the solid forms.56 For these reasons, short-term trials demonstrated that energy compensation for beverage forms of fruits and vegetables57, 58, 59 is weak in comparison with solid forms of these foods. However, long-term appetite data are needed to confirm this observation and establish its nutritional implications. Using data from a previously published study,60 the primary aim of this paper was to assess acute and chronic changes in appetite with prescribed inclusion of fruits and vegetables in solid vs beverage form in the diet. A second aim of this paper was to contrast appetitive effects between lean and overweight/obese groups, as there is evidence of weaker dietary compensation and propensity towards weight gain in individuals with higher BMI.60, 61, 62, 63

Materials and methods

Experimental protocol

This protocol was a 21-week, randomized, crossover intervention with a 1-week pre-intervention period (first baseline, week 1), an 8-week intervention (weeks 2–9), followed by a 3-week washout (weeks 10–12), a second 1-week pre-intervention (second baseline, week 13) and second 8-week intervention (weeks 14–21). Each participant consumed their usual, unrestricted diet during the two pre-intervention weeks and the 3-week washout. They were provided portioned quantities of fruits and vegetables to consume daily along with their otherwise usual, unrestricted diet during the 8-week intervention periods. Approximately half of the participants were randomly assigned to consume isoenergetic portions of fruits and vegetables in solid (raw) form during the first intervention and in beverage form during the second intervention, while the remaining subjects completed the beverage intervention first and the solid intervention second. Selected outcomes (energy intake and body weight changes) of this study were previously published.60 In the current paper, we examine the acute and 8-week appetite responses during the original study. This study was conducted according to the guidelines laid down in the Declaration of Helsinki, and all procedures involving human participants were approved by the Purdue University Institutional Review Board. Written informed consent was obtained from all participants. This trial was registered at clinicaltrials.gov as NCT00260130.

Participants

Participants (n=34, 18 females/16 males) were 18–38 years of age (mean 23±0.8 years), normal (n=15, mean BMI: 20.9±0.3 kg m−2) or overweight/obese (n=19, mean BMI: 29.9±0.4 kg m−2), weight stable during the previous 3 months, able to maintain a consistent activity pattern throughout the study, low fruit/vegetable consumption (able to comfortably double their baseline intake), not taking medications known to significantly influence appetite, non-restrained eater (<14 on restraint scale of the Three Factor Eating Questionnaire64) and willing to consume the required study foods. The original study required at least 27 participants to detect a difference of 1.5 kg in weight change between study groups at 80% power. Thirty-one participants completed the full protocol, while two participants completed only the beverage treatment and one completed only the solid treatment. All 34 of these participants were included in analyses by using group means in place of their missing values.

Measures

Acute appetite and dietary compensation

During the first and second pre-intervention baseline periods, each participant completed 2 days, one was without a preload and the other included a fruit preload. Both entailed monitoring of short-term appetite and ingestive behavior. The day without preload acted as baseline of each food-form intervention. On each testing day, participants arrived at the facility at around noon, 3 h after their usual breakfast meal. Appetite ratings before fruit preload were recorded, and this was immediately followed by consumption of an ad libitum test meal. The preloads were in solid or liquid form, and the form given during the pre-intervention corresponded to the form the participants would consume during the 8-week intervention period, determined randomly.

The solid and beverage fruit preloads contained 400 kcal (Table 1). The solid preload included a medium Gala apple, red seedless grapes, dried apples, raisins and 470 g of water to match the volume of the beverage preload. Forty percent of the energy was from the Gala apple and red grapes, and 60% of the energy was from the dried fruit (similar to the long-term intervention). The beverage preload contained apple juice and grape juice (200 kcal of each), and 150 g of water. Soluble fiber was added to the grape juice in an amount equal to that of the solid preload.

Table 1 Approximate energy and macronutrient content of preload

The challenge meal was macaroni and cheese (M&C) (Easy Mac, Kraft Foods Inc., Glenview, IL, USA) (150 kcal 100 g−1, 15% energy as fat, 12% energy as protein and 73% energy as carbohydrate). On the fruit preload testing days, the participants were asked to consume the entire preload, immediately followed by as much M&C as they desired to reach a comfortable level of fullness (3 on a 9-point scale of arbitrary units: 1: extremely full and 9: not full at all). On the testing days without a fruit preload, the participant was asked to consume only the M&C until the same fullness level was reached. Participants were asked to pace themselves to reach a fullness sensation of ‘3’ within 20 min, and all participants remained seated at the dining table for the entire 20 min. After completing the meal, appetite ratings were completed. Subsequently, participants recorded their appetitive responses hourly and the quantity and timing of all foods and beverages consumed for the remainder of the day away from the laboratory.

Acute appetite responses were measured as (1) hunger, (2) fullness, (3) satiation, quantified by the amount of M&C challenge meal consumed to the nearest tenth of a gram, (4) satiety, as indicated by the latency of the subsequent meal (>100 kcal) in minutes after the M&C test meal and (5) dietary compensation (equation shown in Data Analysis). Both hunger and fullness ratings were recorded on visual analog scales (VAS) electronically on a Palm Pilot device (Palm Inc., Sunnyvale, CA, USA).

Chronic appetite and energy intake

During the 8-week solid and liquid fruit and vegetable exposures, appetite ratings65 were completed on a Palm Pilot (Palm Inc). Hunger and fullness ratings were recorded every waking hour for 24 h during 2 days that included a weekday and a weekend day at the baseline, the middle and the final week of each food-form intervention period. Pre-programmed timers reminded participants to make the hourly recordings. Most data were recorded between 0010 to 2200 hours and were included in the data analyses. Energy intake was assessed by self-administered 24-h diet records on three consecutive days, which included two weekdays and a weekend day at baseline, and week 8 of each intervention period. The diet records were subsequently checked for accuracy by trained personnel. Compliance to dietary interventions (solid and beverage fruits and vegetables) was assessed through the measurements of plasma ascorbic acid and carotenoid.60

During the two 8-week intervention periods, each participant was provided pre-portioned quantities of fruits and vegetables equal to 20% of their estimated energy need (calculated using the sex-specific Harris–Benedict equation of resting energy expenditure multiplied by an activity factor of 1.55) rounded to the nearest 50 kcal (between 400–550 kcal per day) on a daily basis. They were provided on a weekly basis. Participants were asked to consume their daily pre-portioned fruits and vegetables only and avoid these foods from other sources.

For the solid food intervention, 10% of energy from the prescribed fruits and vegetables was provided as raw broccoli, carrots and cauliflower, which was equivalent to 1.3–2.8 servings of vegetables per day based on the USDA National Nutrient Database for Standard Reference.66 The remaining energy was provided as fruits (40% as fresh fruit and 60% as dried fruit), which included fresh apples, grapefruit, grapes, oranges and a variety of dried fruit (Sun-Maid, Kingsburg, CA, USA): apples, apricots, cranberries, mixed dried fruit, peaches and raisins. Dried fruits, which have a higher energy density than fresh fruits, were used to help achieve the energy prescription while keeping the volume to consume reasonable. Together, the fruits and vegetables provided to the participants during the solid intervention equaled 6–8 servings per day. Participants were allowed to select fruits and vegetables according to preference with the exception of apples and carrots (these were consumed daily by all participants, unless substituting broccoli or cauliflower for carrots).

For the beverage intervention, fruit and vegetable juices were isoenergetic to the solid food forms. All juices were commercially available products and included: V8 Splash (The Campbell Soup Company, Camden, NJ, USA), Juicy Juice (Nestlé, Glendale, CA, USA), Minute Maid apple (The Coca-Cola Company, Atlanta, GA, USA), Minute Maid orange (The Coca-Cola Company), grapefruit (The Kroger Co., Cincinnati, OH, USA), Dole grape (PepsiCo Inc., Purchase, NY, USA), Ocean Spray cranberry (Ocean Spray Cranberries Inc., Lakeville-Middleboro, MA, USA) and Dole pineapple (PepsiCo Inc). Soluble fiber (Nutriose FB 06 (Wheat Dextrin), Roquette America Inc., Keokuk, IA, USA), in an amount matching the corresponding fresh and dried fruits and vegetables, was added to the juice. Participants were required to consume apple juice and V8 Splash at least 4 days per week, but were allowed to vary other juices according to preferences.

Data analysis

During the acute appetite test days, dietary compensation for the lunch visits was calculated as: 100%—(((test meal total energy intake (kcal) on day with preload—test meal total energy intake (kcal) on day without preload)/(preload energy: 400 kcal)) × 100%). Dietary intake data were collected by 24-h diet records and energy intake was analyzed using the University of Minnesota Nutrition Data System for Research 2005 and 2006.

Hunger and fullness ratings were collected with visual analog scales and converted to percentage of VAS line on a Palm Pilot by asking participants to answer ‘How strong is your feeling of hunger?’ and ‘How strong is your feeling of fullness?’. For longer-term appetite assessment, these questions were answered every hour, on the hour, for a weekday and weekend day at the baseline (week 1), middle (week 6) and end (week 9) of each intervention period. In addition, the area under the curve (AUC, determined using the trapezoidal rule) of hunger and fullness ratings reported by participants during the 8-week food-form intervention periods was also calculated for each of the two recording days, and the average AUC (weekday and weekend day) for hunger and fullness was taken for a better representation of daily appetite at the three stages (at baseline, middle and final) of the intervention periods.

Statistical analyses were conducted with the Statistical Package for the Social Sciences (SPSS Inc., Chicago, IL, USA), version 16.0. The criterion for statistical significance was set at P<0.05, two-tailed. Repeated-measures analysis of variance, with post-hoc comparisons (Bonferroni correction) when appropriate, was conducted to assess appetite and energy consumption. T-tests were used to compare satiety between treatments. Data are reported as means±s.e.

Results

Acute appetite responses

Hunger and fullness ratings

Hunger ratings were significantly different following challenge meals with vs without preload, for solid vs beverage preloads as well as between lean and overweight/obese participants (repeated-measures analysis of variance; preload × form × BMI interaction effects, P=0.030). As shown in Figure 1, overweight/obese participants reported significantly greater hunger on the beverage fruit preload visit compared with the solid preload visit. No significant difference was noted in lean participants. A trend for a similar interaction was noted for fullness ratings (P=0.055) (results not shown).

Figure 1
figure1

Acute hunger ratings measured as the percentage of 100 mm VAS used. Lunch intervention × treatment × BMI group interaction (P=0.030, n=34). Acute hunger ratings were presented as the mean percentage of VAS scale before and after fruit preloads and hourly subsequently until 2200 hours on lunch visit days.

Satiation and dietary compensation

There were significant preload (F(1,64)=158.738, P<0.001) effects, as well as food-form × preload (F(1,64)=7.524, P=0.008), and food-form × preload × BMI (F(1,64)=5.638, P=0.021) interactions for the amount of M&C challenge meal consumed (Table 2). Without a fruit preload, the participants consumed 535±40 and 542±32 g of the challenge meal on the testing days corresponding with the solid and beverage intervention periods, respectively. Consumption of the 400 kcal fruit preload in either form significantly decreased the amount of M&C consumed when compared with days when participants consumed only M&C without any preload, but intake suppression was greater when the preload was a solid (350±41 g or 57% less than without preload) vs beverage (216±20 g or 41% less than without preload) (P=0.005). Consumption of the challenge meal was higher after the beverage compared with the solid preload, especially in overweight/obese participants (188±44 g) but less so in lean participants (80±50 g) (P=0.114, not significant). In the full sample, dietary compensation for the solid preload was 136±13%, but only 73±7% with the beverage reload.

Table 2 Acute consumption data during beverage and solid preloads

Satiety or latency of subsequent meal

The time to the next eating occasion was not significantly different between days with and without preloads (P=0.484), between BMI groups (P=0.722), food-form of preload (P=.765) or an interaction effect among these factors (preload × BMI × food-form: F(1,64)=0.004, P=0.948). With preload in beverage form, meal latency was 270±28 min in lean and 306±37 min in overweight/obese adults (t-test, P=0.750). In contrast, the solid fruit preload led to a longer between-meal interval in lean (291±25 min), but shorter interval in overweight/obese (255±34 min) participants but this was not significant. All data combined, meal latency was 271±22 min for the solid and 290±24 min for the beverage preload (latency × BMI × food-form: F(1,64)=0.004, P=0.948).

Daily energy intakes and dietary compensation

There was a significant preload effect (F(1,64)=75.429, P<0.001), as well as food form × preload (F(1,64)=55.001, P<0.001) interaction, for energy intake from the challenge meal, but this interaction was not affected by the BMI status of participants (F(1,64)=0.008, P=0.929) (Table 2). Total daily energy consumed was higher, but not significantly, during the beverage preload visit (2729±280 kcal per day) compared with the solid preload visit (2328±123 kcal per day) (one-way analysis of variance, P=0.194). Overweight/obese participants consumed 547±462 kcal per day more when given the beverage than the solid preload, while lean individuals consumed only 218±280 kcal per day more, but this difference was not statistically significant (P=0.572). The total daily energy consumed was not significantly different between days with vs no preloads, or the food forms of preloads, although the total daily energy intake tended to be higher on days with the beverage preload. Total daily energy intake compensation was 36±59% on the beverage preload day and 133±33% on the solid preload day. There were no BMI group differences in total energy intake.

Longer-term appetitive responses

There were no significant time × food-form or time × food form × BMI interaction effects for the hunger and fullness ratings as mean percentage of VAS line or AUC (Figure 2). However, strong and significant correlations were observed between the AUC for hunger and fullness ratings at baseline, middle and the final week of solid and beverage exposure (fullness: baseline vs middle, r=0.811, P<0.001; baseline vs final, r=0.750, P<0.001; hunger: baseline vs middle, r=0.598, P<0.001; baseline vs final, r=0.522, P<0.001).

Figure 2
figure2

Longer-term hunger and fullness ratings, measured as the percentage of 100-mm VAS used, at week 1, 6 and 9 of intervention period. (a) Hunger and (b) Fullness ratings at baseline, week 6 and at final week 9. No treatment or group effects were found. Hunger was measured for 34 human participants in a randomized, crossover trial (8-weeks for each study arm). The lean (n=15) and overweight/obese (n=19) groups were purposefully recruited and were compared for testing our primary hypothesis. Data collected between 0010 and 2200 hours were used for analysis.

Discussion

Short-term and some longer-term studies indicate that low energy dense foods, such as fruits and vegetables, lead to increased fullness and satiety.3, 7, 9, 10, 67 These observations have been extrapolated to long-term diet recommendations for weight loss or weight maintenance,68 with minimal data showing long-term effects on appetite and intake in representative American populations. Indeed, there is evidence that adding fruits and vegetables to the diet leads to weight loss,69, 70, 71 weight gain72 and weight maintenance.73, 74, 75, 76

Our data revealed lower satiation (greater M&C consumed) when fruit beverages were consumed at a lunch visit compared with when solid fruits were consumed under comparable conditions, especially for the overweight/obese participants. Satiety, as indicated by time until the next eating occasion, was not different between treatments (with or without a fruit preload). This is consistent with some other short-term data.24, 25, 77 Only beverages were associated with greater energy intake at the subsequent M&C challenge meal. The overweight/obese participants experienced smaller reductions of hunger on the beverage preload day and had higher intake of a challenge meal and markedly (about 550 kcal) higher total daily energy intake (albeit not statistically significant). The lack of statistical significance for the latter observation may reflect true lack of food-form effects. Alternatively, it may be attributable to limited statistical power as daily energy intake is highly variable and the power calculation for this study was based on body weight changes. Nonetheless, this increase is potentially clinically important as it suggests imprecise dietary compensation and this may translate into weight gain over time. Indeed, significant weight gain was observed in both the lean (+1.61±0.44 kg, P=0.003) and especially in overweight/obese (+2.22±0.47 kg, P<0.001) participants during the 8-week beverage fruit and vegetable consumption period, as reported previously.60 Weight gain was due to the failure to compensate for the additional fruits and vegetables provided to the participants.

Appetitive responses remained unchanged after 8 weeks of fruit and vegetable consumption in both solid and beverage forms. Thus, reports that fruits and vegetables increase fullness and decrease hunger sensations68, 78 may be mediated by acute post-ingestion appetitive signals, rather than longer-term adjustments. Furthermore, this study demonstrated that the satiating effects of fruits and vegetables diminished when they were in an isoenergetic beverage form. Although fiber was added to beverages, it might be argued that the fiber choice did not represent fiber commonly found in fruit (that is, pectin). However, evidence suggests that fiber added to beverages does not have an effect on satiety.79 In this study, being exposed to beverage forms of fruits and vegetables significantly increased the energy intake and body weight of lean and overweight/obese individuals after the 8-week exposure periods.60 Solid exposure increased the intake and body weight of overweight/obese, but not in lean adults. This suggests that fruits and vegetables, despite being low in energy density, did not prevent weight gain in adults who were already overweight or obese. Our findings call for careful implementation of recommendations through counseling and/or follow-up intervention to increase fruit and vegetable consumption to ensure these foods do not promote positive energy balance and weight gain.

The long-term stability of hunger and fullness ratings in this study are consistent with observations from another study of similar study length that manipulated dietary fat intake (a high energy dense dietary manipulation).80 However, it should be noted that there is large inter-individual variability in appetite ratings with some individuals reporting low daily mean hunger (for example, 15–20% on a 100 mm scale) and others with strong daily means (for example, 55–60% of scale).81 It is also notable that despite the consistency of appetitive responses over time, energy intake and body weight increased significantly in lean and especially overweight/obese adults after an 8-week exposure to beverage forms of fruits and vegetables.60 Together, these observations suggest that greater energy intake during this beverage intervention period was sought to maintain pre-exposure appetitive responses. This observation is also consistent with previous findings that liquids are less satiating and elicit weaker dietary compensation than solid food forms.82

It is acknowledged that the current intervention did not faithfully follow the Dietary Guidelines for Americans for the variety of fruits and vegetables and recommended number of servings of fruits vs vegetables. The overall purpose of the study was to compare beverage vs solid food forms.60 Another limitation of the present study was that participants were provided with both fruits and vegetables daily during the 8-week intervention periods to test for chronic dietary effects on appetitive responses whereas only fruits were used in the acute preload study sessions. Further, pre-study testing lead to inclusion of dried fruit, to achieve portions of fruits deemed achievable long-term in low-fruit and -vegetable consumers. Additional testing of long-term appetitive effects upon addition of fruits and vegetables, completely consistent with Dietary Guidelines for Americans, is an area of future research. Interventions should include both men and women, all BMI categories and populations who are not involved in weight-loss trials with significant dietary counseling.

Conclusion

In summary, our data confirm weaker acute satiation and satiety effects of beverage compared with solid food forms of fruits as measured by appetitive responses and energy intake, especially among the overweight/obese. Over 8 weeks, there was no altered chronic appetitive response upon addition of fruits and vegetables (beverage or solid) to the diet. These data suggest that implementing energy displacement strategies for weight management requires careful consideration of total energy intake.

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Acknowledgements

This study was funded by the National Institutes of Health (Grant #R01—DK63185).

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Houchins, J., Tan, S., Campbell, W. et al. Effects of fruit and vegetable, consumed in solid vs beverage forms, on acute and chronic appetitive responses in lean and obese adults. Int J Obes 37, 1109–1115 (2013). https://doi.org/10.1038/ijo.2012.183

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Keywords

  • solid
  • beverages
  • fruits
  • vegetables
  • appetite

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