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ORIGINAL RESEARCH COMMUNICATION |
1 From the Nutritional Sciences Program, School of Public Health and Community Medicine (PM, MMP, and AD), and the Department of Dental Public Health Sciences, School of Dentistry (PM), University of Washington, Seattle, WA
2 Supported by a grant from the American Beverage Association, by the Corn Refiners Association, and by fellowship T32 DE07132 from the National Institute of Dental and Craniofacial Research (to PM). 3 Reprints not available. Address correspondence to A Drewnowski, 305 Raitt Hall, Box 353410, University of Washington, Seattle, WA 98195. E-mail: adamdrew{at}u.washington.edu.
| ABSTRACT |
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Objective: The objective of the study was to compare the relative effect of commercial beverages containing sucrose or HFCS on hunger, satiety, and energy intakes at the next meal with the use of a within-subject design.
Design: Thirty-seven volunteers (19 men, 18 women) aged 2029 y consumed isocaloric cola beverages (215 kcal) sweetened with sucrose, HFCS 42, or HFCS 55. HFCS 42 contains 42% fructose, and HFCS 55 contains 55% fructose. Diet cola (2 kcal), 1%-fat milk (215 kcal), and no beverage were the control conditions. The 5 beverages were consumed at 1010 (2 h after a standard breakfast). Participants rated hunger, thirst, and satiety at baseline and at 20-min intervals after ingestion. A tray lunch (1708 kcal) was served at 1230, and energy intakes were measured. The free sugars content of sucrose-sweetened cola was assayed at the time of the study.
Results: We found no differences between sucrose- and HFCS-sweetened colas in perceived sweetness, hunger and satiety profiles, or energy intakes at lunch. The 4 caloric beverages tended to partially suppress energy intakes at lunch, whereas the no-beverage and diet beverage conditions did not; the effect was significant (P < 0.05) only for 1%-fat milk. Energy intakes in the diet cola and the no-beverage conditions did not differ significantly.
Conclusion: There was no evidence that commercial cola beverages sweetened with either sucrose or HFCS have significantly different effects on hunger, satiety, or short-term energy intakes.
Key Words: Beverages sucrose fructose high-fructose corn syrup HFCS sweetness hunger fullness satiety energy intakes
| INTRODUCTION |
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One of the criteria for establishing causality in evidence-based medicine is a biologically plausible mechanism. Attempts to establish a causal link between soft drink consumption and rising obesity rates have therefore relied on the notion that caloric beverages in general (6), and HFCS-sweetened beverages in particular (2, 7), lack satiating power. Research reports have suggested that liquids were less satiating than were solids (8); that sugars were less satiating than was either protein or fat (9); and that HFCS blunted the satiety response more than did other sweeteners (2, 10, 11). The metabolic and endocrinologic processes associated with the ingestion of free fructose have featured prominently in arguments that HFCS-sweetened beverages are the principal culprit in the obesity epidemic (2, 6, 7).
However, satiety-related arguments based on the ingestion of pure fructose or fructose-rich stimuli (12, 13) may not apply to sweetened beverages, given that the 2 most common forms of HFCSHFCS 55 and HFCS 42contain 55% and 42% free fructose, respectively, and the remainder is free glucose. Furthermore, the sharp distinctions made between HFCS-sweetened and sucrose-sweetened beverages (2, 14) may be incorrect. The low pH of carbonated soft drinks favors the breakdown of sucrose into free glucose and free fructose before consumption (15), and the rate of hydrolysis is dependent on storage variables, temperature, and time (16). Perhaps most important, the short-term satiating power of foods and beverages may have little to do with the long-term regulation of body weight (13, 17).
The present study was a direct test of the hypothesis that HFCS-sweetened carbonated soft drinks differ significantly from sucrose-sweetened soft drinks and from low-fat milk in their effect on satiety. Aiming to approximate naturalistic conditions of soft drink use, we compared the effect of commercially available cola beverages, sweetened with sucrose or with 2 types of HFCS (HFCS 42 and HFCS 55), on hunger, satiety, and energy intakes (EIs) at the test meal. Because so much has been made of the metabolic differences between free fructose and fructose bound within disaccharide sucrose molecules (2, 14), we sent samples of the sucrose-sweetened beverage to be analyzed for free sugars content at the time of the experiment.
| SUBJECTS AND METHODS |
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2 of the foods or beverages in the study; those taking prescription medications that were likely to affect taste, smell, or appetite; athletes in training; pregnant or lactating women; and persons reporting recent weight loss or weight cycling were excluded. Potential candidates were invited to report to the laboratory for a brief session, during which their weight and height were measured. The Eating Disorder Inventory (18) and the cognitive restraint subscale of the Eating Inventory (19) were administered as screening instruments to exclude persons with indications of eating disorders or restrained eating patterns. Persons who met all eligibility criteria were invited to participate and were given a reminder card stating the dates and times for the study sessions. To minimize variability, each participant was asked to report to the laboratory on the same day of the week throughout the study, to keep evening meals and activity levels on the day before each test as similar as possible, to refrain from drinking alcohol the day before each test, and to have a standardized breakfast at
0800 on the mornings when they were scheduled to have a test. The participants standardized breakfasts were consumed at home and were composed of specified servings of hot or cold cereals with milk along with a medium-sized apple, orange, or banana or a specified serving of low-fat yogurt along with a medium-sized fruit. All participants provided written informed consent. The study protocol was approved by the Institutional Review Board at the University of Washington. All 37 subjects completed the study and were compensated for their time.
Study design
The study followed a repeated-measures within-subject design, in which each participant returned for 6 separate test sessions. The sessions lasted from 0930 to 1310 and were spaced at least a week apart. The order of presentation of the 5 preloads and the no-beverage condition was counterbalanced. The same lunch foods were offered on all 6 testing occasions. The magnitude of the energy manipulation (0 or 215 kcal) was based on a review of previous studies in this area (20). Power analysis indicated that, with a power of 80% and an alpha of 0.05, a sample of 35 subjects was sufficient to detect a minimum difference of 150 kcal in compensation (21).
Beverage stimuli
The 5 beverages were cola sweetened with HFCS 42 (Sam's Choice Cola; Cott Beverages, Toronto, Canada), cola sweetened with HFCS 55 (Coca-Cola Classic; Coca-Cola Co, Atlanta, GA), cola sweetened with sucrose (Coca-Cola Classic), cola sweetened with aspartame (Diet Coke; Coca-Cola Co), and 1%-fat milk (Darigold; Wesfarm Foods, Seattle, WA). All preload beverages with the exception of the diet cola (2 kcal) were isoenergetic (894 kJ or 215 kcal) and of comparable sweetness, but they differed in sugar composition. To keep both sweetness and energy constant, the preload volume was allowed to vary within narrow limits (from 475 to 525 mL.). The composition and energy density of the 5 beverage preloads are shown in Table 1
. All beverages were coded and were served chilled, without ice, in opaque containers with a lid and a straw. Participants were asked to consume the entire amount within 15 min.
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Motivational ratings and hedonic evaluations
Participants used computerized, semi-anchored visual analogue scales (VASs) to rate their hunger, fullness, thirst, nausea, and desire to eat. The VAS software was custom-written by using the LABVIEW graphic programming software (version 6.1; National Instruments, Austin, TX) that was running on 10 identical Macintosh G3 computers (Apple Computers, Cupertino, CA). Motivational scales were presented one at a time (ie, one scale per screen) on the computer monitor. Each participant used a mouse to position a cursor along the 100-mm bar displayed on a flat-panel LCD computer monitor. The VAS bars were anchored at each extreme with the labels "not at all ..." and "extremely ..." (22). A semi-anchored VAS was also used for quantifying several sensory and hedonic attributes of each beverage. Each sensory attribute scale also was anchored with the labels "not at all..." and "extremely ...". Hedonic ratings and ratings along 11 sensory attribute scales were obtained for each beverage.
Test meal
A lunch meal served on a tray was provided at 1230. Identical meals were provided on each occasion. The set meal was 7120 kJ (1708 kcal) and included a variety of foods, both savory and sweet. Each lunch consisted of a selection of 2 grains, 2 types of fruit, 2 vegetables, 2 cheeses, 2 meats, 2 candies, 1 yogurt, 1 ice cream cup, hummus, chips, and water. A large cup containing 591 mL (20 fl oz) still water was provided with the test lunch. Participants were told that they could have as much or as little as they would like of any food or water and that they could request unlimited additional portions. All foods and water were weighed at the time of serving. Plate waste was collected and weighed by the experimenters. Food energy and nutrient values were calculated with FOOD PROCESSOR software (version 8.1; ESHA Research, Salem, OR) and from the manufacturer's food labels. The nutrient composition of the meal is shown in Table 2
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Data analyses and statistical tests
We used SPSS for WINDOWS software [version 11.1 (23)] for all analyses. Normality was determined by the Kolmogorov-Smirnov test (normal if P > 0.05). Analyses of motivational ratings used a nested repeated-measures analysis of variance (ANOVA) with beverage type and time after ingestion (times 28) as the within-subjects factors and sex as the between-subjects factor. Analyses were conducted for all 6 conditions together and separately for the 3 sweetener conditions (sucrose, 42% HFCS, and 55% HFCS) and the 3 comparison conditions (aspartame, 1%-fat milk, and no beverage). Univariate tests of within-subject effects were subject to Huynh-Feldt correction when the sphericity assumption was violated. Bonferroni-adjusted pairwise comparisons were made when ANOVAs were significant. Because there were no significant main effects or sex-related interactions (P > 0.05 for all tests), the data were combined by sex for each beverage condition. Analyses of EIs and the weight of foods and water consumed at lunch used a repeated-measures ANOVA with beverage type as the within-subject factor and sex as the between-subjects factor. The strength of the association between prelunch (time 8) appetite ratings and energy or water intakes at lunch was tested by using Pearson's correlation coefficients. Prelunch appetite ratings were computed by averaging 3 proxies for appetite according to a method similar to that of Anderson et al (11): hunger, desire to eat, and the inverse of fullness (ie, 100 fullness). Sweetness intensity and hedonic ratings were analyzed by repeated-measures ANOVA.
| RESULTS |
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Analysis of sweetness ratings for the 4 cola beverages found a significant (F3, 99 = 11.1, P < 0.001) main effect of beverage type. However, that was entirely due to the aspartame-sweetened cola, which was perceived as significantly less sweet than the 3 sugar-sweetened colas (P < 0.01 for all 3 comparisons). Cola beverages sweetened with sucrose, HFCS 55, and HFCS 42 did not differ significantly in perceived sweetness ratings. Milk (1% fat) was not perceived as sweet. All 5 beverages (including milk) were rated as equally palatable by the participants. The analysis of hedonic preference ratings showed no significant main beverage effect (F41, 32 = 2.5).
Motivational ratings
All 5 beverages (caloric and not) led to lower hunger ratings during the initial 20 min after ingestion than were seen in the no-beverage condition. Repeated-measures ANOVA showed significant main effects of both beverage type and time and a significant beverage x time interaction (P < 0.001 for all). Separate analyses were then conducted for the 3 colas and the 3 comparison conditions.
The time course of energy and volume effects on short-term hunger is shown in Figure 1
(left). In the first 60 min after their ingestion, equal volumes of 1%-fat milk and noncaloric diet cola had comparable effects on perceived hunger. However, hunger ratings rose more rapidly in the diet cola condition than in the milk condition, and a separation in hunger ratings was visible before lunch. ANOVA found a significant (P < 0.001) main effect of beverage type and a significant (P < 0.005) beverage x time interaction.
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ANOVA of fullness ratings found significant main effects of beverage type and time (P < 0.001 for both) and a significant beverage x time interaction (P < 0.005). As shown in Figure 2
(left), milk and diet cola had different effects on fullness ratings, depending on the time after ingestion. The beverage effect and the beverage x time interaction were significant (P < 0.01 for both). In contrast, the sucrose- and the HFCS-sweetened colas differed significantly (P < 0.001) from the no-beverage condition but not from each other. The beverage x time interaction was not significant (Figure 2
, right).
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The combined energy content of the preload and the lunch also showed significant main effects of beverage type (P < 0.001). Pairwise comparisons showed that the 3 sugar conditions did not differ significantly from each other or from milk. However, all 4 caloric beverages differed significantly from both the diet cola and the no-beverage conditions.
Beverage type significantly affected the weight of food and the amount of water consumed at lunch (P < 0.001 for both). Participants in the no-beverage condition consumed significantly more water at lunch than did subjects in all of the other preload conditions except for the diet cola condition. The nutrients consumed in association with each beverage condition are shown in Table 4
. Beverage type did not significantly affect the nutrient composition of the lunch meal. Overall, the meals selected and consumed by the participants provided 51.2% of energy as carbohydrate, 17.2% of energy as protein, and 32.8% of energy as fat. The nutrient composition of lunch did not differ significantly by sex.
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Free sugar content of sucrose-sweetened beverage
The progressive hydrolysis of sucrose in cola beverages over the course of the study is shown in Figure 5
. Each point is based on the analysis of 3 samples. As sucrose hydrolyzed, its concentration declined from 36% of total sugars on June 30 to just above 10% on August 24, or
3 mo after the beverages were manufactured (May 25). Free fructose increased from 32% to
44%. Free glucose (not shown) followed the same course as fructose. During the time of the satiety study (period indicated by the shaded bar), the principal sugars in the sucrose-sweetened cola were free fructose and glucose. Dashed reference lines at 50.6% and 6.4% indicate concentrations of sucrose present in samples from a separate lot of sucrose-sweetened cola measured 10 d and 1 y after manufacture.
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| DISCUSSION |
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As the present study shows, the 3 cola beverages, which were sweetened with sucrose, HFCS 55, or HFCS 42, were perceived as equally sweet and significantly sweeter than diet cola. All 3 beverages showed identical temporal profiles of motivational ratings, which were different from the no-beverage condition. There were no differences between the reported temporal profiles for hunger, satiety, and the desire to eat obtained after the ingestion of HFCS- or sucrose-sweetened colas. Compared with the EIs under the no-beverage condition, the 3 colas and 1%-fat milk weakly suppressed EIs at lunch, whereas the diet cola did not. However, the effect was significant only for 1%-fat milk.
The present study used the conventional preload paradigm (25-27) and commercially available colas and 1%-fat milk. The statistical power was similar to that used in past research (9, 25). The study design was thus able to separate the effects of preload energy and preload volume. As had been noted in previous reports, diet cola suppressed hunger immediately after ingestion, but hunger ratings recovered sooner than did those after ingestion of caloric 1%-fat milk. Preload volume alone had no effect on EIs 120 min later. The amount of food consumed at lunch in the diet cola condition did not differ significantly from that in the no-beverage condition.
The notion that HFCS-sweetened beverages differ substantially from sucrose-sweetened beverages (2, 14) seems to have been based on the incorrect assumption that sucrose in solution remains stable. As documented by multiple laboratory assays conducted over the course of the present study, the sucrose content of the cola beverage dropped from 35% to 10%, whereas the free fructose content rose from 32% to 44% of total sugars. Other hydrolysis data indicate that 50% of the sucrose in carbonated beverages is hydrolyzed within 10 d of manufacture and that
90% is hydrolyzed within 3 mo. Given the time lag between production and consumption, it is likely that most sugars in sucrose-sweetened beverages are already in the form of free fructose and glucose by the time the beverages are consumed (16).
Previous laboratory studies of sugars and satiety in humans, most often conducted with aqueous solutions of pure sugars (11, 12), produced inconsistent results. One early study did not find differences between glucose and fructose in hunger ratings or EIs (12). A study in 16 women showed that 50 g fructose in 500 mL water significantly reduced lunch intakes as compared with a water control (28). A study of different glucose-fructose mixtures showed that high-glucose (80%) stimuli elevated blood glucose concentrations more than did high-fructose stimuli (80%), but that the 2 mixtures had similar effects on appetite (T Akhavan and GH Anderson, unpublished observations, 2005). The same study showed that high-fructose stimuli (65% and 80%) were associated with lower short-term food intake than was sucrose.
The putative effect of HFCS on satiety hormones awaits further research. In a recent study, 30 lean women consumed cola beverages at lunch served at 1300 h, and blood samples were drawn before the meal and 30 min and 60 min afterward (29). There were no significant differences between plasma glucose, insulin, leptin, or ghrelin after the ingestion of HFCS- or sucrose-sweetened cola. It is possible that the responses to sucrose- and HFCS-sweetened cola beverages were similar because the sugar content of the stimuli was, in fact, much the same. Studies of the human response to sweetened liquids should assess the stimulus sugar composition at the time of testing.
The present study does not resolve the underlying question of whether liquids differ from solids in their satiating power. Past studies found no difference in satiating power between liquid cola and solid fat-free cookies (30) or between a drinkable liquid yogurt and the same yogurt that was eaten with a spoon (9). A review (20) showed that, whereas some studies found that liquids were less satiating than solids, other studies showed the opposite. Most recently, a study showing that apple juice had higher satiating power when it was called a "soup" attributed the difference to cognitive rather than physiologic factors (31).
In the present study, conducted with liquids only, a slightly but significantly different degree of compensation as compared with the no-beverage condition was obtained for 1%-fat milk only. This finding is of interest because 2 previous studies observed no differences in EIs among regular cola, orange juice, or 1%-fat milk, no matter whether the beverages were consumed 135 min before lunch (32) or with lunch (27). On the other hand, yogurts were associated with higher fullness ratings than were either dairy- or fruit-based drinks (9), possibly because of their higher protein content.
Although laboratory studies conducted with pure sugar solutions provide valuable data on fructose metabolism (12, 13), not all observations can be extrapolated to the human food supply. The hydrolysis of sucrose in soft drinks before consumption suggests that the substitution of HFCS for sucrose did not have the dramatic effects that had been claimed (2). The emerging view voiced in the scientific literature (33) and in the news media (34) is that any potential contribution of sugars to obesity is unlikely to be mediated by metabolic effects that are unique to HFCS.
| ACKNOWLEDGMENTS |
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The authors responsibilities were as followsPM, MMP, and AD: study design and writing of the manuscript; PM and MMP: study implementation and data collection; PM, MMP, and AD: statistical analysis and revision of the dietary data. None of the authors had a personal or financial conflict of interest.
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