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Original Research Communication |
1 From the Research Department of Human Nutrition, Centre for Advanced Food Studies, The Royal Veterinary and Agricultural University, Frederiksberg, Denmark.
2 Supported by the Danish Research and Development Programme for Food Technology 19901994 and Danisco Sugar. Coca Cola (Nordic and Eurasia Divisions) generously provided soft drinks for the study. 3 Address reprint requests to A Raben, Research Department of Human Nutrition, Centre for Advanced Food Studies, The Royal Veterinary & Agricultural University, 30 Rolighedsvej, DK-1958 Frederiksberg C, Denmark. E-mail: ar{at}kvl.dk.
| ABSTRACT |
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Objective: We investigated the effect of long-term supplementation with drinks and foods containing either sucrose or artificial sweeteners on ad libitum food intake and body weight in overweight subjects.
Design: For 10 wk, overweight men and women consumed daily supplements of either sucrose [n = 21, body mass index (BMI; in kg/m2) = 28.0] or artificial sweeteners (n = 20, BMI = 27.6). On average, sucrose supplements provided 3.4 MJ and 152 g sucrose/d and sweetener supplements provided 1.0 MJ and 0 g sucrose/d.
Results: After 10 wk, the sucrose group had increases in total energy (by 1.6 MJ/d), sucrose (to 28% of energy), and carbohydrate intakes and decreases in fat and protein intakes. The sweetener group had small but significant decreases in sucrose intake and energy density. Body weight and fat mass increased in the sucrose group (by 1.6 and 1.3 kg, respectively) and decreased in the sweetener group (by 1.0 and 0.3 kg, respectively); the between-group differences were significant at P < 0.001 (body weight) and P < 0.01 (fat mass). Systolic and diastolic blood pressure increased in the sucrose group (by 3.8 and 4.1 mm Hg, respectively) and decreased in the sweetener group (by 3.1 and 1.2 mm Hg, respectively).
Conclusions: Overweight subjects who consumed fairly large amounts of sucrose (28% of energy), mostly as beverages, had increased energy intake, body weight, fat mass, and blood pressure after 10 wk. These effects were not observed in a similar group of subjects who consumed artificial sweeteners.
Key Words: Aspartame acesulfame-K cyclamate saccharin obesity fat-free mass fat mass appetite bone mineral content artificial sweeteners sugar sucrose weight control weight management weight reduction
| INTRODUCTION |
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Therefore, epidemiologic studies or studies lasting for weeks or months are of greater interest. Long-term intervention studies without energy restriction are scarce, and those that have been done did not last for > 3 wk (1820). These studies suggested that increased intake of artificial sweeteners either has no effect or decreases energy intake and body weight compared with sucrose consumption. Epidemiologic studies, on the other hand, found an inverse relation between the intake of sucrose and body weight in adults (21) and children (22,23), suggesting that sucrose may help prevent overweight. These epidemiologic data were recently supported by the long-term, multi-center trial CARMEN, in which a diet low in fat and high in simple sugars, consumed ad libitum for 6 mo, reduced body weight and fat mass in overweight subjects (6). Furthermore, normal-weight to moderately overweight Scottish men lost more body weight and fat mass with a fat-reduced diet than with a fat- and sucrose-reduced diet (24).
Regarding artificial sweeteners, a long-term epidemiologic study reported a positive relation between saccharin intake and weight change in adults (25) and a positive relation between intake of carbonated soft drinks and body mass index (BMI; in kg/m2) in 1216-y-old children (26). This may suggest that artificial sweeteners do not prevent weight gain, although cause and effect cannot be determined from these studies. In contrast, long-term intervention studies with energy restriction have shown that the inclusion of artificial sweeteners can increase compliance, improve quality of life, and help maintain weight loss (27). Persons who are concerned about their weight but are not following a diet typically use artificial sweeteners because they wish to reduce their daily energy intake without changing the rest of their diet; with this approach, they hope to maintain or reduce their body weight. Whether this actually happens or not has not been adequately investigated yet. Therefore, the purpose of the present study was to monitor changes in ad libitum energy and macronutrient intakes, body weight, and body composition during 10 wk of supplementation with either sucrose or artificial sweeteners.
| SUBJECTS AND METHODS |
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Several measurements were performed before, during, and at the end of the 10-wk intervention period. At weeks 0, 2, 4, 6, 8, and 10, we measured body weight, fat mass, and fat-free mass. At weeks 0, 5, and 10, subjects completed 7-d dietary records, 7-d diaries (for monitoring hunger, fullness, palatability of the food, and well being), 24-h urine collections, and diurnal appetite scores. At weeks 0 and 10, dual-energy X-ray absorptiometry (DXA) scans were performed and the waist-to-hip ratio, sagittal height (height of abdomen when lying in a supine position), and blood pressure were measured. In addition, subjects completed a 3-factor questionnaire about eating behavior (28) and a questionnaire about habitual physical activity. After the intervention, subjects also completed a questionnaire about the experimental diet. Once each week throughout the intervention, subjects came to the research department to collect their drinks and foods and to deliver their diaries, questionnaires, urine samples, and other materials.
Subjects
Subjects for the study were recruited with posters and with advertisements in newspapers and magazines. The inclusion criteria were: 2050 y old, overweight [BMI of 2530 or > 10% overweight according to weight-and-height tables (29)], healthy, not dieting, and not pregnant or lactating. We received
300 telephone calls from interested potential subjects and we provided written and oral information about the study to 100 of them. Forty-two subjects enrolled in the study and 41 of them (35 women and 6 men; n = 21 for the sucrose group and n = 20 for the sweetener group) completed the study. The subjects were randomly assigned to the 2 intervention groups, which were matched for sex, age, weight, height, BMI, fat mass, fat-free mass and usual amount of physical activity (Table 1
). The study was approved by the Municipal Ethical Committee of Copenhagen and Frederiksberg as being in accordance with the Helsinki II Declaration. All subjects gave their written consent after the experimental procedure had been explained to them orally and in writing.
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70% of the sucrose came from drinks and
30% came from solid foods. About 80% by wt of the supplements were beverages and
20% by wt were solid foods. This distribution corresponds to the populations intake of artificially sweetened foods (31,32). The beverages consisted of several soft drinks (Coca Cola, Fanta, and Sprite, all from Coca-Cola Tapperierne A/S, Fredericia, Denmark) and flavored fruit juices (orange, raspberry, "sport," and mixed). The caps on all the soft drinks were changed and all labels were removed for our study, because the pilot study showed that subjects could guess which drinks were "light" from the color of the caps. The solid foods consisted of yogurt (strawberry, Peach Alexander, and cherry for the sucrose group or strawberry-rhubarb, Peach Melba, and forest berries for the sweetener group), marmalade (orange, raspberry, or black currant), ice cream (strawberry, pistachio, or vanilla), and stewed fruits (apricots, prunes, or apples). Great efforts were made before the intervention to find the most palatable artificially sweetened food products on the market for which a matching sucrose-containing product existed. Subjects were invited to taste all the products in their respective diet group before the intervention started, so that they could select the ones they wanted to consume during the intervention. To keep the fat intake from the provided foods as similar as possible for the 2 groups, subjects in the sweetener group were given additional butter or corn oil every week. This was necessary because some of the artificially sweetened products were fat-reduced.
The amounts of supplemental drinks and foods to be consumed were calculated on the basis of a sucrose intake of
2 g/kg body wt daily. This corresponded to 23% of energy for an 80-kg person with an energy intake of 12 MJ/d (ie, it was a rather high sucrose intake). To ensure that each subject received the correct sucrose intake, subjects were assigned to 3 different intake levels according to their initial body weight, as follows: level 1, 6075 kg; level 2, 7590 kg; and level 3, > 90 kg. Subjects on levels 1, 2, and 3 received drinks and foods containing a total of 125, 150, or 175 g sucrose/d, respectively. This corresponded to a total energy intake from the sucrose supplements of 2738, 3285, or 3833 kJ/d, respectively. The sweetener group received an equivalent amount (by weight) of drinks and foods, resulting in an average intake of artificial sweeteners of 0.48, 0.57, or 0.67 g/d and an average energy intake of 694, 832, or 971 kJ/d on levels 1, 2, and 3, respectively. The percentage contributions of the different artificial sweeteners were 54% from aspartame, 22% from acesulfame K, 23% from cyclamate, and 1% from saccharin. The average daily intakes of the different sweeteners in the sweetener group were far below the acceptable daily intakes.
In addition to the experimental diet, subjects were free to consume their own diet ad libitum until they felt pleasantly satisfied. To monitor any changes in food intake, subjects completed 7-d weighed dietary records, along with 24-h urine collections, during weeks 0, 5, and 10. Digital food scales with an accuracy of 1 g were used (Soehnle 8020 and 8009; Soehnle-Waagen GmbH & Co, Murrhardt, Germany). A 7-d dietary record was also completed 12 mo before the intervention to get the subjects accustomed to the method. The computer database of foods from the National Food Agency of Denmark (Dankost 2.0) was used to calculate the energy and nutrient intakes (33).
Measurements
Anthropometry
All measurements except the DXA scans were done in the morning after the subjects had fasted from 2200 the previous night. For all measurements, the same device was used every time. Body weight was measured to the nearest 0.1 kg with a digital scale (Seca model 708; Seca Mess und Wiegetechnik, Vogel & Halke GmbH & Co, Hamburg, Germany) after the subject voided. Body composition was subsequently estimated with the bioelectrical impedance method by using an Animeter (HTS-Engineering Inc, Odense, Denmark). Fat mass (FM) and fat-free mass (FFM) were calculated as described previously (33). Height was measured to the nearest 0.5 cm at the screening visit by using a wall-monitored stadiometer. Waist and hip circumferences were measured with a tape measure. Sagittal height was measured in the supine position to the nearest 0.5 cm. Blood pressure was also measured in the supine position after 10 min of rest with an automatically inflating cuff (UA-743, A&D Company Ltd, Tokyo).
Whole-body DXA scans were performed with a Hologic 1000 W DXA scanner (Hologic Inc, Waltham MA) at Rigshospitalet in Copenhagen. The scanner uses an X-ray source with 2 photon-energy levels (45 and 105 keV), and the difference in energy makes it possible to determine the calcium content of the bones. The X-ray dose received from a whole-body scan is a maximum of 0.01 mSv (34). Each scan took 1020 min. During the scan, bone mineral content, bone area, and bone mineral density were determined. Because the scans were performed when subjects were not fasting and at different times during the day, DXA data on body composition were not used.
Urine samples
Subjects collected 24-h urine samples during the sixth day and night of every dietary record period (weeks 0, 5, and 10) to validate the dietary records. During these 24-h periods, subjects ingested a paraaminobenzoic acid (PABA) pill with the 3 main meals (a total of 240 mg PABA/d) to serve as an indicator of complete urine collection (35). Urine samples containing < 85% recovered PABA were excluded from further analyses. The volume and density of each 24-h urine collection were determined and a 2-mL sample was frozen at -20 °C until further analyses. The nitrogen content was determined in 30 µL urine on a nitrogen analyzer (NA 1500 Carlo Erba; Fisons Instruments, Milano, Italy). PABA was determined spectrophotometrically (Bodenseewek Perkin-Elmer & Co GmbH, Überlingen, Germany).
The analyzed urinary nitrogen was converted to protein equivalents by multiplying by 6.25. It is estimated that 81% of ingested protein is excreted in urine (36). Urinary protein was therefore converted to ingested protein with the formula:
![]() | (1) |
Dietary protein recovery was subsequently calculated as the index:
![]() | (2) |
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Questionnaires
To monitor each subjects well-being during the intervention period, 7-d diaries and week diaries were used. The 7-d diaries were completed every day during each of the 7-d dietary record periods. They contained a visual analogue scale for monitoring each of the following: hunger, fullness, palatability of the food, and well being. The scales consisted of 10-cm, unmarked, unipolar, horizontal lines with words anchored at each end, expressing the most positive (ie, good or pleasant) or the most negative (ie, bad or unpleasant) ratings (37). The week diaries were used in the weeks without 7-d dietary records and were only used for recording comments about events such as illness, menstruation, altered diet, medication, or altered physical activity pattern.
Subjective appetite sensations (hunger, satiety, prospective consumption, fullness, and desire to eat something sweet, salty, fat-rich, or savory) were registered under free-living conditions by using a visual analogue scale. Subjects were instructed to complete the visual analogue scale just before and 1, 2, and 4 h after each main meal on day 4 of each 7-d dietary record period. The data were subsequently analyzed by using a mean value for the day, because subjects recorded the scores at different time points during the day as a result of different meal patterns.
A Three-factor Eating Questionnaire on dietary habits and eating behavior (translated from Stunkard and Messick, 28) was completed by the subjects before and after the intervention period. On the basis of the subjects answers to 51 questions on dietary habits, eating behavior and patterns, slimming diets, and thoughts on food, they received scores for 3 categories of eating behavior: FI, cognitive control of eating behavior; FII, disinhibition of control; and FIII, susceptibility to hunger. If the individual has normal attitudes about foods and body weight, a low score is obtained for all 3 categories.
Before and after the intervention period, subjects recorded information about their physical activity, namely the amount (hours of activity/wk) and intensity (rated 15, for low to high). The information was used to match the 2 study groups before the intervention and to monitor any changes after the 10-wk intervention.
A questionnaire regarding the supplements was completed by the subjects after the intervention to investigate whether all subjects believed that they had been consuming artificial sweeteners. The subjects answered questions indicating how much of each of the following substances was in the supplements, in their opinion: salt, sucrose, protein, vitamin C, artificial sweetener, carbohydrate, fat, or other. They chose from the following possible responses: nothing (0), a little (1), medium (2), much (3), or do not know. Only the results on sucrose and artificial sweetener are reported here.
Statistical analyses
All results are given as means ± SEM. Initial group differences were tested by using an unpaired t test (Table 1
). Other differences between groups and times were tested by using parametric analysis of variance with the general linear model procedure in SAS. The factors were diet, time, and diet x time with subject (group) as an error term for group effects. When the interaction of diet and time was significant, Tukeys post hoc tests were applied. Linear and stepwise regression analyses were performed. The significance level was set at P < 0.05. STATGRAPHICS software version 4.2 (Graphic Software Systems Inc, Rockville, MD) and SAS version 6.12 (SAS Institute, Cary, NC) were used in the statistical calculations.
| RESULTS |
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1285 g/d. This was determined by multiplying the total average weight of foods and drinks consumed (1600 g/d) by the percentage of this total weight that was contributed by drinks (80%).
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Body weight and composition
Body weight and FM increased in the sucrose group and decreased in the sweetener group during the 10-wk intervention (diet x time interactions for body wt and FM, P < 0.0001 and P < 0.05, respectively) (Figure 2
). For the sucrose group, the total weight gain at week 10 averaged 1.6 kg, of which 1.3 kg was a gain in fat mass (Table 4
). For the sweetener group, the total weight loss at week 10 averaged 1.0 kg, of which 0.7 kg was FFM and 0.3 kg was FM.
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Blood pressure
After 10 wk of supplementation, systolic and diastolic blood pressure had increased in the sucrose group but decreased in the sweetener group, resulting in significant between-group differences of 6.9 and 5.3 mm Hg, respectively (Table 4
). The changes in systolic blood pressure were positively correlated with the changes in body weight (r = 0.41, P < 0.01), FM (r = 0.39, P < 0.05), sucrose intake in g and percent of energy (r = 0.43 and 0.40, P < 0.01 for both), and total energy (r = 0.33, P < 0.05). Changes in diastolic blood pressure were positively correlated with sucrose intake in g and percent of energy (r = 0.39 and 0.38, P < 0.05) and total energy intake (r = 0.34, P < 0.05). Stepwise multiple regression analyses including these variables showed that only changes in FM and sucrose intake in g remained significant predictors of changes in systolic blood pressure. For changes in diastolic blood pressure, only the change in sucrose intake in g was retained in the regression model.
Diaries and questionnaires
The 7-d food diaries completed 3 times during the intervention showed no significant differences between the 2 groups ratings of hunger, fullness, palatability of the food, and general well-being (data not shown). Furthermore, mean scores for postprandial appetite sensations on day 4 of each dietary record showed no significant differences between the 2 groups during the intervention (data not shown). There were also no significant between-group differences in the changes in the amount of physical activity or level of physical activity, as recorded by the subjects, after the 10-wk intervention (Table 4
).
The Three-factor Eating Questionnaire showed that about half of the subjects in each group had controlled eating behavior before the intervention (FI). For all 3 factors, the number of positive subjects (those with values above the mean score) had decreased in the sucrose group (by 23 subjects) and increased in the sweetener group (by 13 subjects) after the intervention (Table 5
). There were no significant differences between the 2 groups in the average scores of the positive subjects before or after the intervention.
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| DISCUSSION |
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One likely reason for the increases in energy intake and body weight in the sucrose group is the fact that
70% of the sucrose came from fluids. Energy obtained from fluids was shown to be less satisfying than energy from solid foods (40). Thus, energy from liquids may not be fully compensated for, making it is easier to overconsume energy when drinking liquids than when eating solids (40). This is in agreement with a recent prospective study in children that reported that the intake of sugar-sweetened drinks increased the risk of becoming overweight (41). These findings and the current results are not in agreement with data from the CARMEN intervention study (6), but we believe that a difference in the amount of sugars from fluids as compared with solids may explain the different outcomes of these studies.
A second possible reason for overconsumption of energy during sucrose supplementation may be that overweight subjects are less sensitive to dietary manipulations and cannot adjust their energy intake to match their energy needs as effectively as can lean subjects (42). Thus, a similar study performed in lean subjects might not have produced the same results. A third possible reason for the current results is that subjects consumed rather large amounts of sucrose per day (28% of energy), with an average intake of sweetened drinks of
1285 g/d. Smaller amounts may not have produced the effects we observed here. Finally, after the intervention, the number of subjects with controlled eating behavior decreased in the sucrose group and increased in the sweetener group. This may also have caused the higher energy intake in the sucrose group compared with the sweetener group, although we cannot determine what is cause and effect here.
The increase in total energy intake compared with habitual energy intake in the sucrose group was 1.5 MJ/d. The supplemental drinks and foods supplied 3.4 MJ/d, and subjects in the sucrose group reduced their energy intake from their own foods (ie, all foods other than supplemental foods) by 1.9 MJ/d, (ie, 56% of the supplemental amount). This implies that the large amount of sucrose consumed by the sucrose group (28% of energy) did satisfy the subjects appetites to some degree, but not to the extent that subjects reduced their energy intake from their own foods by an equal amount and thereby maintained body weight. We found no differences in appetite sensations between the 2 study groups. This result could be explained by either similar sensations of hunger and satiety in the 2 groups, a lack of sufficient sensitivity of the method (43), or lack of appetite control in overweight subjects, as discussed above (42).
In the sucrose group, subjects reduced their intakes of sucrose and total carbohydrate from their own foods, which compensated partially for the supplemental sucrose. Thus, from week 0 to week 10, sucrose intake from the subjects own foods decreased by 46 g [72 g (from own food in week 0) + 151 g (from sucrose supplement in week 10) - 177 g (total intake in week 10)] or 64%, and total carbohydrate intake from their own foods decreased by 83 g (288 g + 176 g - 381 g) or 29%. Interestingly, sucrose and total carbohydrate intakes from the subjects own foods also decreased in the sweetener group. Thus, from week 0 to week 10, intake of sucrose from the subjects own foods decreased by 15 g (39 g - 24 g) or 38%, and total carbohydrate decreased by 43 g (241 g + 31 g - 229 g) or 18%. Therefore, this diet did not stimulate either sucrose or carbohydrate intake as was suggested previously (7,10) but instead had the opposite effect.
An increase in energy intake of 1.5 MJ/d for 70 d (= 105 MJ in total) would result in a weight gain of 3.1 kg, if one assumes that an average of 34 MJ is required to make 1 kg body tissue (containing a combination of FM and FFM) (44), if all other factors are held constant. We only observed half that amount of weight gain (ie, 1.6 kg or 52% of the predicted weight gain). Thus, 48% of the extra energy intake in the sucrose group must have been used for other energy-demanding processes in the body (eg, facultative thermogenesis or de novo lipogenesis). This value corresponds to the estimated 49% of energy that was used for thermogenesis after 3 wk of carbohydrate overfeeding in lean young men (45).
It was suggested from short-term studies that artificial, nonenergetic sweeteners can increase appetite through cephalic stimulation (eg, the taste, smell, and sight of food) and that aspartame in particular may have a paradoxical stimulating effect on appetite (7,9,10). We were not able to confirm such an effect in this long-term study, and our findings were therefore in agreement with several previous short-term studies (8,1117). Body weight actually decreased by 1.0 kg in the sweetener group, and although 70% of this resulted from a loss of FFM (probably glycogen and water), 0.3 kg of FM was also lost. This weight loss may have been caused by the low-energy sweetener supplements replacing higher-energy foods and drinks, leading to a lower overall energy density in the subjects diets. The decrease in energy intake in the sweetener group (439 kJ/d) was not significant. However, 439 kJ/d (= 30.7 MJ) over 70 d would give rise to a weight loss of 0.9 kg (assuming 34 MJ/kg weight loss). This calculated weight loss is very close to the observed weight loss of 1.0 kg.
Systolic and diastolic blood pressure increased in the sucrose group but decreased in the sweetener group. This was related to changes in FM and sucrose intake. The correlation with sucrose intake could indicate an effect of sucrose per se on the sympathetic nervous system, as suggested previously (38,46).
All subjects were told that they received supplements containing artificial sweeteners. At the end of the study, the questionnaire on supplements revealed that subjects in the sweetener group believed this, but subjects in the sucrose group had guessed to some extent the true contents of their supplements. In theory, this could have influenced the subjects eating behavior so that subjects in the sucrose group would have eaten less of their own foods and subjects in the sweetener group would have eaten more of their own foods. However, the data show that this was apparently not the case, perhaps because of a lack of control over eating behavior.
In conclusion, predominantly female overweight subjects who were given supplemental drinks and foods containing sucrose for 10 wk experienced increases in total energy intake, body weight, FM, and blood pressure. This was not observed in a similar group of subjects given similar drinks and foods containing artificial sweeteners. The most likely reason for these differences between the groups was the use of large amounts of beverages, giving rise to overconsumption of energy on the high-sucrose diet. Therefore, overweight individuals may want to consider choosing beverages containing artificial sweeteners rather than sucrose to prevent weight gain.
| ACKNOWLEDGMENTS |
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