Sucrose compared with artiﬁcial sweeteners: a clinical intervention
study of effects on energy intake, appetite, and energy expenditure
after 10 wk of supplementation in overweight subjects1–3
Lone B Sørensen, Tatjana H Vasilaras, Arne Astrup, and Anne Raben
ABSTRACT
Background: There is a lack of appetite studies in free-living subjects
supplying the habitual diet with either sucrose or artiﬁcially
sweetened beverages and foods. Furthermore, the focus of artiﬁcial
sweeteners has only been on the energy intake (EI) side of the energybalance
equation. The data are from a subgroup from a 10-wk study,
which was previously published.
Objective: The objective was to investigate changes in EI and
energy expenditure (EE) as possible reasons for the changes in body
weight during 10 wk of supplementation of either sucrose or artiﬁcial
sweeteners in overweight subjects.
Design: Supplements of sucrose-sweetened beverages and foods
(2 g/kg body weight; n = 12) or similar amounts containing artiﬁcial
sweeteners (n = 10) were given single-blind in a 10-wk parallel
design. Beverages accounted for 80% and solid foods for 20% by
weight of the supplements. The rest of the diet was free choice.
Indirect 24-h whole-body calorimetry was performed at weeks
0 and 10. At week 0 the diet was a weight-maintaining standardized
diet. At week 10 the diet consisted of the supplements and ad
libitum choice of foods. Visual analog scales were used to record
appetite.
Results: Body weight increased in the sucrose group and decreased
in the sweetener group during the intervention. The sucrose group
had a 3.3-MJ higher EI but felt less full and had higher ratings of
prospective food consumption than did the sweetener group at week
10. Basal metabolic rate was increased in the sucrose group,
whereas 24-h EE was increased in both groups at week 10. Energy
balance in the sucrose group was more positive than in the sweetener
group at the stay at week 10.
Conclusion: The changes in body weight in the 2 groups during the
10-wk intervention seem to be attributable to changes in EI rather than
to changes in EE. Am J Clin Nutr 2014;100:36–45.
INTRODUCTION
Overweight and obesity are inﬂuenced by genetic and environmental
factors, including insecurity, stress, lack of sleep, and
epigenetics (1, 2). The cause of the worldwide increase in the
prevalence of obesity is not known but is most probably a result of
2 major lifestyle factors: an increasingly sedentary lifestyle and
the energy content of the modern diet (3). An inappropriate
macronutrient composition of the diet can increase energy intake
(EI)4
(4). Both cohort studies and randomized controlled studies
have found positive associations between consumption of sugars
and body weight, especially when the sugar was added to beverages
(5–8). Whether this is the result of an effect by sugar per
se or an effect explained by the additional energy from the sugar
or of the effects of food forms is controversial. However, it may
be relevant to reduce the consumption of sugar as part of
a strategy to lose weight or maintain a normal body weight.
Intuitively, using artiﬁcial sweeteners as a substitute for sugar
could be a way to reduce sugar consumption and thus EI. Whereas
some earlier short-term studies have indicated a stimulating effect
of artiﬁcial sweeteners on appetite, more recent studies have not
shown this effect (9). However, these studies have mainly been
preload studies (10, 11). There is a lack of appetite studies in freeliving
subjects supplying the habitual diet with either sugar or
artiﬁcially sweetened beverages and foods for a longer period of
time. Furthermore, until now the focus of artiﬁcial sweeteners has
only been on the EI side of the energy-balance equation. No studies
have compared the effect of sugar and artiﬁcial sweeteners on
energy expenditure (EE). Diet-induced thermogenesis (DIT) after
a meal is proportional to the energy and macronutrient contents
of the meal (12). In addition, earlier studies have suggested that
both the amount and type of carbohydrate has an inﬂuence on EE
(13–15); results have shown that consumption of mono- and disaccharides
lead to a higher DIT than do polysaccharides, presumably
because of an increased sympathetic nervous system
activity (13). Because DIT accounts for 10% to 15% of total daily
EE, it could be expected that daily EE would be lower with
consumption of artiﬁcial sweeteners than with consumption of
sugars, all else being equal (12).
The current study is a substudy that investigated the effect on
energy balance of supplementation of sucrose and artiﬁcial
sweeteners for 10 wk. Results from the main study showed that
during 10 wk, the sucrose group had an increase in body weight of
1
From the Department of Nutrition, Exercise and Sports, Faculty of Science,
University of Copenhagen, Copenhagen, Denmark.
2
Supported by The Danish Research Councils, FØTEK (Development
Programme for Food Technology), Danisco Sugar (unrestricted grant), and
Coca Cola (Nordic and Eurasia Divisions) (unrestricted grant).
3
Address correspondence to LB Sørensen, Department of Nutrition, Exercise
and Sports, Faculty of Science, University of Copenhagen, Rolighedsvej
26, DK-1958 Frederiksberg C, Denmark. E-mail: lbs@life.ku.dk.
4
Abbreviations used: BMR, basal metabolic rate; DIT, diet-induced thermogenesis;
EE, energy expenditure; EI, energy intake; GLP-1, glucagon-like
peptide-1; SPA, spontaneous physical activity; VAS, visual analog scale.
ReceivedDecember 17, 2013. Accepted for publication April 1, 2014.
First published online April 30, 2014; doi: 10.3945/ajcn.113.081554.
36 Am J Clin Nutr 2014;100:36–45. Printed in USA. Ó 2014 American Society for Nutrition
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1.6 kg, and the sweetener group had a decrease in body weight of
1.0 kg (16). Considering these results, it could be expected that
the sucrose group would be in positive energy balance and the
sweetener group in negative energy balance on the test day at
week 10. Thus, the objective of the current study was to compare
the effects of sucrose and artiﬁcial sweeteners on EI, subjective
appetite sensations, and EE for 24 h in a respiration chamber.
SUBJECTS AND METHODS
The main part of the study, conducted in 42 subjects, was
described in detail elsewhere (16).
Study design
The main study had a single-blind, parallel design with 2 intervention
groups. For 10 wk, one group received supplemental drinks
and foods containing sucrose and the other group received similar
drinks and foods containing artiﬁcial sweeteners. In the current
substudy, the subjects were tested in respiratory chambers on 2
different test days; the ﬁrst test day was before the intervention (week
0) and the second test day was the last day of the 10-wk intervention.
Subjects
A total of 24 healthy, overweight subjects were included in this
substudy; subjects from the main study volunteered to participate
in the substudy. None of the subjects were dieting, and none of the
women were pregnant or lactating. Approval was obtained from
the Ethical Committee of Copenhagen and Frederiksberg, and the
study was performed in accordance with the Helsinki II Declaration.
Each subject signed an informed-consent document
before the start of the study. The study was conducted in 1995.
Diets
The diet during the 10-wk intervention
During the 10-wk intervention, the subjects were supplemented
with a speciﬁc minimum amount of either sucrose-sweetened or
artiﬁcially sweetened foods and drinks daily. The subjects were
assigned to 3 different levels of supplements according to their
initial body weight: level 1, 2, or 3 corresponding to 60–75, 75–90,
and .90 kg, respectively. The minimum intake of the experimental
diet was regulated by the sucrose intake and corresponded
to a sucrose intake of 125 g/d (level 1), 150 g/d (level 2), and
175 g/d (level 3). This corresponded to a total EI from sucrose
supplements of 2.74, 3.29, and 3.83 MJ/d, respectively. The
sweetener group received an equivalent amount (by weight) of
foods and drinks, which resulted in an average EI of 694, 832, or
971 kJ/d at levels 1, 2, and 3, respectively. The artiﬁcial sweetener
content of the intervention diet was 54% aspartame, 23% cyclamate,
22% acesulfame K, and 1% saccharin.
In the sucrose group, w70% of the sucrose came from drinks
(average: ~1.3 L/d), and w30% came from solids foods. About
80% by weight of the supplements were beverages, and w20%
by weight were solid foods. The beverages consisted of several
soft drinks and fruit juices, and the solid foods consisted of
yogurt, marmalade, ice cream, and stewed fruit. Some of the
artiﬁcially sweetened products were low fat, so the subjects in
the sweetener group were given additional butter or corn oil to
keep the fat intake in the 2 intervention diets as similar as
possible.
The subjects were supplied with all the drink and food supplements
at the Department of Nutrition, Exercise, and Sports.
The content of sucrose and artiﬁcial sweeteners in the supplemented
products was unknown to the subjects. The subjects were
all told that they would receive supplements containing artiﬁcial
sweeteners, and they were not informed about the real purpose of
the study. In addition to consuming the food and drink supplements,
the subjects were free to consume their habitual diet ad
libitum.
The diets during the chamber stays
During the chamber stay in week 0, the diet was a weightmaintaining
standardized diet estimated to meet each subject’s
individual energy requirement, adjusted to the nearest 0.5 MJ.
The subjects’ energy requirements were estimated by using the
results from the measurements of electrical impedance (17),
corresponding to a mean EI of 9.69 MJ in both groups. Carbohydrate
provided 50.2% of energy, fat 36.8% of energy, and
protein 13.9 % of energy.
During the chamber stay in week 10, the diet consisted of the
supplement assigned to each individual; the supplements consisted
of the same kind of beverages and foods provided to the
subjects during the 10 wk. In addition, the subjects were offered
an ad libitum choice of foods served at breakfast, lunch, and
dinner. The breakfast buffet contained different types of bread,
butter, cheese, fruit juice, cereals, and milk. The lunch buffet
consisted of different types of bread, butter, cheese, vegetables,
sandwich spread with meat and ﬁsh, eggs, and milk. The lasagna
served for dinner was made of pasta, minced meat, onion, garlic,
oil, carrots, milk, squash, and red pepper. The subjects were
allowed to consume all of the meals ad libitum, and the amounts
consumed were recorded. The solid supplemental foods were
consumed at breakfast and the supplemental beverages were served
at all 3 meals. The amount of water, coffee, and tea consumed
during the ﬁrst chamber stay were recorded and reproduced during
the second chamber stay.
Measurements during the 10-wk intervention
Body weight, fat mass, and lean body mass were measured at
weeks 0, 2, 4, 6, 8, and 10. Subjects completed 7-d weighed
dietary records and 24-h urine collections (to validate the protein
intake records) at weeks 0, 5, and 10. Waist and hip circumferences,
sagittal height, and blood pressure were measured, and
blood samples were collected at weeks 0 and 10. After the intervention,
subjects also completed a questionnaire about the
experimental diet. The questionnaire included questions indicating
how much of each of the following substances was in the
supplements, in the subjects’ opinion: salt, sucrose, protein,
vitamin C, artiﬁcial sweetener, carbohydrate, fat, or other. The
questions were part of a smokescreen to investigate whether all
subjects believed that they had been consuming artiﬁcial
sweeteners. Protocols for carrying out the 7-d weighed dietary
records, the collection of urine samples, and the conversion of
urinary protein to ingested protein and calculation of dietary
protein recovery were reported elsewhere (16). The same applied
to the results concerning the effects of the diets on body
SUCROSE, ARTIFICIAL SWEETENER, AND ENERGY BALANCE 37
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weight, sagittal height and blood pressure (16), and blood
samples (18, 19).
Experimental protocol for the chamber study
The subjects had been instructed to maintain the same level of
physical activity on the day before the test days (weeks 0 and 10)
to ensure equally ﬁlled glycogen stores (20). On the evening
before the test days, the subjects arrived at the respiratory
chamber at 2200. Bedtime was set at 2300, but reading was
allowed until 2400. The following morning at 0800, body weight
was measured after the subjects voided, and body composition
was measured after the subjects rested for 10 min in a supine
position. The chamber was closed and assessments started at
0900. Urine was subsequently collected throughout the 24-h
measurement. Appetite sensations were recorded every hour from
0900 onward. Breakfast was served at 0900, lunch at 1300, dinner
at 1800, and coffee or tea at 2000. Palatability ratings were
assessed immediately after consumption of the test meals.
Bedtime was at 2315; however, reading was allowed until 2400.
During the day, physical activity was scheduled; at 0930 and 1430
there were sessions of walking back and forth 25 times in the
chamber, and at 1100 and 1600 there was 15 min of cycling on an
ergometer bicycle (Monark 814E; Monark AB) (75 W). On the
following day, the subjects were wakened at 0730. While the
subjects were resting in a supine position, the basal metabolic rate
(BMR) was measured from 0800 to 0900; the subjects were
awake but lying relaxed in bed.
Appetite ratings
Appetite ratings were recorded on 10-cm visual analog scales
(VASs) with words anchored at each end describing the extremes
of a unipolar question (eg, for hunger: “I am not hungry at all”
and ”I have never been more hungry”). VASs were used to assess
hunger, satiety, fullness, prospective food consumption,
desires for special foods, and palatability of the test meal (taste,
smell, visual appeal, aftertaste, and overall palatability) (21).
Measurements in the respiratory chamber
The 24-h EE, BMR, and substrate oxidation rates were measured
in 2 open-circuit respiratory chambers that were described in detail
previously (22). The gas exchange of the subjects was calculated
from measurements of oxygen and carbon dioxide concentrations
at the outlet of the chamber and from measured air ﬂow through the
chambers. Protein oxidation was calculated from urea nitrogen
content in the 24-h urine collection. The oxygen and carbon dioxide
exchanges, including urinary nitrogen measurements, were used to
calculate EE, and utilization rates of lipid and carbohydrate were
calculated as described by Elia and Livesey (23). The whole unit
was regularly calibrated by comparing a known volume of carbon
dioxide entering the chamber with the volume of carbon dioxide
measured by the unit (22). The within-subject variation for 24-h EE
measured in the chambers is 2.3% (22).
DIT was calculated as the incremental area under the curve for
EE for 4 h after the dinner meal (1800–2200), with BMR as the
baseline measure, and 24-h energy balance was calculated (energy
balance = EI 2 EE). Body weight was measured to the
nearest 0.1 kg on a digital scale (Seca model 708; Seca Mess
und Wiegetechnik). Body composition was estimated by using
bioelectric impedance (Animeter; HTS-Engineering Inc). Fat
mass and lean body mass were calculated as described previously
(24).
Statistical analyses
On the basis of a previous study (25), power analysis showed
that 10 subjects in each group were sufﬁcient to detect a difference
of 145 kJ in 24-h EE; 24 subjects were originally recruited in
order to allow for dropouts.
Repeated-measures ANOVAwas used to test for differences in
dietary intake during the 10-wk intervention and during the test
day in week 10 and differences in VAS scores between diet
groups and time. The MIXED procedure in the SAS software
package (version 9.3) was used (SAS Institute). Subjects were
included as random factors.
To investigate the effect of diet on EE, carbohydrate and fat
oxidation, and spontaneous physical activity (SPA), repeated-measures
ANOVA was used to test for interaction between diet groups,
week, and time. EE was additionally adjusted for sex, age, 24-h
SPA, EI, fat mass, and lean body mass. To investigate the effect of
diet on protein oxidation, ANOVA was used to test interactions
between diet and week. The effect of diet on body weight, BMI,
fat and lean body mass, BMR, DIT, and energy balance was tested
with ANCOVA, with week 10 values as response and week 0 values
as covariates. BMR was additionally adjusted for sex, age, SPA
recorded during the period when BMR was measured, and changes
in fat mass and lean body mass at week 10 and EI in the chamber at
week 10. Energy balance was additionally adjusted for sex, age,
24-h SPA, fat mass, and lean body mass at week 10. DIT was
additionally adjusted for sex, age, SPA recorded during the 4-h
measurement, fat mass, and lean body mass at week 10. Tukey’s
adjustments for multiple testing were applied.
RESULTS
A total of 24 subjects participated, and 22 subjects completed
the study; one subject dropped out after the randomization but
before the intervention had started, and another subject did not
complete the second chamber stay and was excluded. Thus, 12
subjects from the sucrose group and 10 subjects from the
sweetener group were included in the data analyses (Table 1). No
differences were found at baseline (week 0) in food intake,
anthropometric characteristics, subjective appetite sensations,
TABLE 1
Characteristics of the subjects at baseline
Sucrose group
(n = 12)
Sweetener group
(n = 10)
Age (y) 35.3 6 9.81
35.2 6 12.4
Sex (M/F) 2/10 2/8
Body weight (kg) 84.5 6 8.4 80.5 6 10.1
Height (m) 1.72 6 0.69 1.72 6 0.63
BMI (kg/m2
) 28.7 6 2.3 27.3 6 2.5
Fat mass (kg) 31.2 6 3.9 27.3 6 4.92
Lean body mass (kg) 53.3 6 5.8 53.2 6 8.0
24-h SPA3
(%) 7.2 6 0.4 8.7 6 0.72
1
Mean 6 SD (all such values).
2
Signiﬁcantly different from the sucrose group, P , 0.05 (unpaired t test).
3
SPA, spontaneous physical activity.
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and respiratory measurements between the 2 groups, except for
a higher fat mass and a lower 24-h SPA in the sucrose group than
in the sweetener group.
Results from the 10-wk intervention
Dietary intake
The 7-d dietary food records showed that there was a higher
intake of carbohydrate and sucrose in the sucrose group compared
with the sweetener group during the 10-wk intervention.
The intake of energy was higher in the sucrose group than in the
sweetener group; the average difference in total EI between the 2
groups was 2.29 MJ (95% CI: 0.56, 4.01 MJ) during the 10 wk.
Validation of the protein intake showed no differences between
urinary protein and self-reported dietary protein, either between
groups or times. Urinary protein correlated with dietary protein at
all 3 time points (16).
Body weight
In the sucrose group, mean (6SEM) body weight (1.4 6 0.6 kg)
and fat mass (1.2 6 0.6 kg) increased and in the sweetener group
body weight (21.2 6 0.6 kg) and fat mass (20.9 6 0.6 kg) decreased
during the 10-wk intervention, which resulted in betweengroup
differences amounting to 2.7 kg body weight (95% CI: 0.8,
4.6 kg body weight; P = 0.007) and 2.0 kg body fat (95% CI: 0.2,
3.8 kg body fat; P = 0.007). No changes in lean body mass was
found in the 2 groups during the intervention.
Results from the chamber study
Dietary intake
During the test day in week 10, the sucrose group had a higher
total EI than did the sweetener group, which resulted in a between-group
difference of 3.26 MJ (95% CI: 0.28, 6.58 MJ)
(Table 2). The mean (6SEM) energy from the supplements was
TABLE 2
Average intake, including the supplements, of energy and macronutrients in the sucrose (n = 12) and sweetener (n = 10)
groups at breakfast, lunch, and dinner on the test day during the chamber stay in week 101
Breakfast Lunch Dinner P for main diet effect2
Energy (MJ)
Sucrose 4.26 6 0.42 4.53 6 0.58 5.77 6 0.46 0.04
Sweetener 2.91 6 0.47 3.60 6 0.45 4.78 6 0.47
Carbohydrate (g)
Sucrose 184 6 20 126 6 21 197 6 14 0.003
Sweetener 110 6 24 83 6 8 162 6 22
Carbohydrate (% of energy)
Sucrose 73 6 3 47 6 3 58 6 3 0.05
Sweetener 61 6 4 41 6 2 56 6 3
Sucrose (g)
Sucrose 91 6 133
49 6 143
28 6 7 ,0.00014
Sweetener 11 6 8 0.2 6 0.1 7 6 4
Sucrose (% of energy)
Sucrose 35 6 33
18 6 33
12 6 35
,0.00016
Sweetener 3.6 6 2.6 0.1 6 0.0 2.2 6 1.4
Fat (g)
Sucrose 21 6 4 44 6 6 42 6 5 0.3
Sweetener 16 6 3 39 6 8 34 6 4
Fat (% of energy)
Sucrose 18 6 2 37 6 3 27 6 2 0.6
Sweetener 21 6 3 39 6 3 28 6 2
Protein (g)
Sucrose 31 6 3 38 6 6 53 6 7 0.7
Sweetener 28 6 3 36 6 4 46 6 3
Protein (% of energy)
Sucrose 13 6 1 14 6 1 15 6 1 0.003
Sweetener 19 6 2 17 6 1 17 6 1
Dietary ﬁber (g)
Sucrose 7 6 1 13 6 1 12 6 1 0.7
Sweetener 8 6 1 14 6 1 11 6 1
Energy density (kJ/g)
Sucrose 3.5 6 0.2 3.6 6 0.2 4.5 6 0.3 0.02
Sweetener 2.7 6 0.2 3.5 6 0.4 3.9 6 0.3
Weight of food (g)
Sucrose 1315 6 174 1296 6 180 1309 6 87 0.4
Sweetener 1167 6 211 1077 6 89 1267 6 111
1
All values are means 6 SEMs.
2
P values were derived by repeated-measures ANOVA of the interaction between diet groups and meals. Subjects were
included as random factors.
3,5
Signiﬁcant difference between the sucrose and sweetener groups (Tukey’s post hoc tests): 3
P , 0.0001, 5
P , 0.05.
4,6
Signiﬁcant group 3 time interaction: 4
P = 0.002, 6
P = 0.007.
SUCROSE, ARTIFICIAL SWEETENER, AND ENERGY BALANCE 39
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3.46 6 0.09 MJ in the sucrose group and 0.93 6 0.05 MJ in the
sweetener group. No difference in ad libitum EI was found
between the groups, which amounted to 11.10 6 1.13 MJ in the
sucrose group and 10.37 6 1.16 MJ in the sweetener group
(P = 0.7).
No group 3 meal interactions were found for any of the
variables, except for sucrose (Table 2). The intake of carbohydrate
and sucrose and the percentage of energy from protein
and the energy density were higher in the sucrose group than in
the sweetener group during the test day in week 10 (Table 2).
The palatability of the test meals was rated similarly in the 2
groups.
Subjective appetite sensations
On the test day in week 10, a group 3 time interaction was
found in the feeling of fullness (P = 0.005) and prospective
consumption (P = 0.003), and post hoc tests showed that the
subjects in the sucrose group felt less full in the periods after
lunch and dinner and had higher ratings of prospective food
consumption in the period after lunch and dinner, compared with
the sweetener group (Figure 1). No group 3 time interactions
were found with respect to sensations of satiety and hunger
(Figure 1). No differences in the subjective desires for sweet,
salty, or fatty foods were found between the 2 groups.
Respiratory measurements
BMR increased in the sucrose group (7.6%) after the 10-wk
intervention (between-group mean difference: 24 kJ/h; 95% CI:
0.3, 47.5 kJ/h; P = 0.02) (Table 3). However, the difference
between the 2 groups disappeared after adjustments for sex, age,
and SPA recorded during the period when BMR was measured,
changes in fat mass and lean body mass, and the energy consumed
in the chamber (Table 3). The signiﬁcant covariates were
sex (P = 0.001), SPA (P = 0.01), and the energy consumed
during the chamber stay (P = 0.008). No difference in DIT was
found between the 2 groups either before or after adjustments
for sex, age, SPA recorded during the 4-h measurement, fat
mass, and lean body mass.
FIGURE 1. Mean (6SEM) appetite scores (hunger, satiety, fullness, and prospective food consumption) recorded during the chamber stay at week 10 in
the sucrose group (n = 12) and in the sweetener group (n = 10). The visual analog scale equal to 10 cm corresponds to “I cannot eat another bite” (satiety), “I
have never been more hungry” (hunger), “I am totally full” (fullness), and “I can eat a lot” (prospective food consumption). Repeated-measures ANOVA was
used to test differences between appetite scores in the 2 groups. The group 3 time interactions were signiﬁcant for the appetite variables: fullness: P = 0.005;
prospective food consumption: P = 0.003. Tukey’s post hoc tests: *P , 0.05, **P , 0.01, ***P , 0.001.
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There was a group 3 week 3 time interaction for EE (P =
0.03); however, after Tukey’s adjustments for multiple tests, the
post hoc tests showed no relevant differences. After adjustment for
sex, age, 24-h SPA, fat mass, lean body mass, and EI, the interaction
remained and post hoc tests showed a difference between
the groups at week 10; EE was higher at 1100 in the sucrose group
than in the sweetener group, P = 0.008) (Figure 2). A group 3
week interaction for EE (P = 0.0003) was also found. Post hoc
tests showed that 24-h EE increased in the sucrose group by
686 kJ/d (95% CI: 514, 859 kJ/d; P , 0.0001) and in the
sweetener group by 329 kJ/d (95% CI: 142, 518 kJ/d; P , 0.0001)
after 10 wk (Figure 2). However, after adjustment for sex, age, 24-h
SPA, fat mass, lean body mass, and EI, this interaction disappeared
(group 3 week: P = 0.3). The signiﬁcant covariates were 24-h SPA
(P , 0.001), EI (P , 0.001), and lean body mass (P , 0.001).
No difference in SPAwas found between the sucrose (7.7%; 95%
CI: 7.0, 8.4%) and sweetener (8.4%; 95% CI: 7.7, 9.2%) groups
during the chamber stay in week 10. A group 3 week interaction
was found for carbohydrate oxidation (P , 0.0001); post hoc tests
showed that carbohydrate oxidation was 44% higher in the sucrose
group than in the sweetener group during the chamber stay in
week 10 (P , 0.0001) (Figure 3). A group 3 week interaction
was also found for fat oxidation (P , 0.0001). Post hoc tests
showed that fat oxidation was 37% lower in the sucrose group than
TABLE 3
BMR, DIT, and 24-h energy expenditure before (day 0) and after (day 70) the intervention in the sucrose (n = 12) and
sweetener (n = 10) groups1
Day 02
Day 702
LS means3
P3
LS means (adjusted) P
BMR (kJ/h)
Sucrose 314 6 8 338 6 16 332 (319, 348) 0.02 332 (323, 341)4
0.074
Sweetener 310 6 14 309 6 18 308 (294, 323) 318 (308, 327)
DIT (kJ/4 h)
Sucrose 344 6 28 377 6 34 374 (317, 431) 0.4 429 (354, 504)5
0.25
Sweetener 332 6 37 409 6 28 412 (350, 475) 347 (261, 432)
24-h EE (kJ/d)
Sucrose 9611 6 225 10,298 6 395
Sweetener 9402 6 357 9732 6 385
1
There were no signiﬁcant differences in baseline values between the 2 groups (unpaired t test). BMR, basal metabolic
rate; DIT, diet-induced thermogenesis; EE, energy expenditure; LS, least squares.
2
Values are means 6 SEMs.
3
Derived by ANCOVA with diet (sucrose and sweetener) as factor and baseline values as covariates. Values in
parentheses are 95% CIs (all such values).
4
P values were derived by ANCOVA with diet as factor and baseline values, age, sex, spontaneous physical activity
during measurement of BMR, changes in fat mass and lean body mass, and energy intake during the chamber stay in week
10 as covariates.
5
P values were derived by ANCOVA with diet as factor and baseline values, age, sex, spontaneous physical activity
during the 4-h measurement of DIT, lean body mass, and fat mass at week 10 as covariates.
FIGURE 2. Mean (6SEM) energy expenditure during 24 h measured at week 0 (A) and after 10 wk of intervention (B) in the sucrose group (n = 12) and in
the sweetener group (n = 10). Breakfast was consumed at 0900, lunch at 1300, and dinner at 1800. Physical activity was scheduled: walking back and forth 25
times in the chamber at 0930 and 1430 and 15 min of cycling on an ergometer bicycle at 1100 and 1600. Repeated-measures ANOVA was used to test for
differences between energy expenditure in the 2 groups. The group 3 week 3 time interaction was signiﬁcant (P = 0.03). Tukey’s post hoc tests after
adjustment for sex, age, 24-h spontaneous physical activity, fat mass and lean body mass, and energy intake during the chamber stay: **P,0.01.
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in the sweetener group during the chamber stay in week 10 (P ,
0.0001) (Figure 3). No difference in 24-h protein oxidation was
found between the 2 groups during the chamber stay in week 10.
The 24-h respiratory quotient was higher in the sucrose group
(0.87; 95% CI: 0.85, 0.88) than in the sweetener group (0.92; 95%
CI: 0.90, 0.94; P , 0.0001) during the chamber stay at week 10.
Energy balance
Mean (6SEM) energy balance was more positive in the sucrose
group (4264 6 889 kJ) than in the sweetener group (1565 6 997 kJ);
the mean difference was 3321 kJ (95% CI: 997, 5645 kJ; P = 0.008).
After adjustments for sex, age, 24-h SPA, fat mass, and lean body
mass, the difference disappeared (P = 0.2). The energy balance
correlated with 24-h respiratory quotient at the chamber stay in week
10 (r = 0.64, P=0.001).
DISCUSSION
The main ﬁndings of the current study were that the sucrose
group had a higher EI during the chamber stay in week 10 than did
the sweetener group. Despite this, there was a strong trend for the
subjects in the sucrose group to have a higher appetite between
lunch and dinner and after dinner compared with the sweetener
group. BMR increased in the sucrose group, whereas no difference
in DITor 24-h EE was found between the 2 groups after the 10-wk
intervention. Both groups were in positive energy balance during
the chamber stay in week 10, although energy balance in the
sucrose group was more positive than that in the sweetener group.
Nearly 3.5 MJ of the higher EI in the sucrose group was from
the supplements; 70% of the sucrose in the supplements came
from sucrose-sweetened beverages. Already in the 1990s, it was
hypothesized that liquid calories fail to trigger appetite regulation
(26, 27); at present, several studies support this. Recently, Maersk
et al (11) conducted a test meal crossover study that served
a sucrose-sweetened soft drink, semiskim milk, an artiﬁcially
sweetened soft drink, or water. An ad libitum meal was served
after 4 h. Total EI was higher after the energy-containing beverages
than after the artiﬁcial sweetened beverage and water, as
were insulin and glucagon-like peptide-1 (GLP-1) concentrations
(11). In a crossover design, Anton et al (28) served preloads
FIGURE 3. Mean (6SEM) carbohydrate oxidation and fat oxidation during 24 h measured at week 0 and after 10 wk of intervention in the sucrose group
(n = 12) and in the sweetener group (n = 10). Breakfast was consumed at 0900, lunch at 1300, and dinner at 1800. Physical activity was scheduled: walking
back and forth 25 times in the chamber at 0930 and 1430 and 15 min of cycling on an ergometer bicycle at 1100 and 1600. Repeated-measures ANOVA was
used to test for differences between carbohydrate oxidation and fat oxidation in the 2 groups. The group 3 week interaction was signiﬁcant for both
carbohydrate and fat oxidation (P , 0.0001). Tukey’s post hoc tests: difference between weeks 0 and 10 for the sucrose group (P , 0.0001) and difference
between the sucrose and the sweetener groups for substrate oxidation (P , 0.0001).
42 SØRENSEN ET AL
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containing stevia (290 kcal), aspartame (290 kcal), or sucrose
(493 kcal) before an ad libitum lunch and an ad libitum dinner.
Despite differences in energy in the preloads and a difference in
glucose and insulin concentrations, no differences in ad libitum
food intake and hunger or satiety scores were observed (28). This
phenomenon could be a result of insufﬁcient sensory signaling
(29) because liquids are easier to consume and therefore can be
consumed more rapidly (30).
In connection with the current study, another substudy was
conducted to measure, among others, fasting and postprandial
glucose, insulin, leptin, and GLP-1 concentrations (18). Blood
sampling was started after the subjects had ended the stay in the
chambers. Breakfast and lunch were precise reproductions of the
meals on the day before in the chamber. Analyses showed that
fasting insulin and leptin concentrations and postprandial glucose,
insulin, GLP-1, and leptin concentrations were higher in the
sucrose group than in the sweetener group. Regardless of this, the
sucrose group consumed 3 MJ more than did the sweetener group.
Furthermore, the sucrose group reported a periodically higher
appetite. So, it seems that the physiological satiety mechanisms
were being put out of action in the current study. This was also the
case with the studies mentioned above by Maersk et al (11) and
Anton et al (28). Karl et al (31) also showed that higher-energydensity
meals were associated with higher concentrations of
insulin, peptide YY, and GLP-1; however, there was no energy
compensation at the following meal. The authors suggest that an
explanation for the lack of energy compensation observed in their
study may be that the effects of gut hormones on appetite are
masked by the numerous environmental, sensory, and cognitive
cues that can affect appetite and EI (31). The current study
provides possible support for this suggestion. Results from the
main study showed that the subjects in the sucrose group were
partly unaware of the caloric manipulation (16). Consequently,
they did not acknowledge the need to compensate for the extra
energy. The sweetener group, on the other hand, thought that they
received no sucrose and medium to much artiﬁcial sweetener. In
another study conducted by Maersk et al (32), participants
consumed 1 L/d of sugar-sweetened cola, diet cola, semiskim
milk, or water for 6 mo. That study was not blind, which gave the
participants the opportunity to acknowledge the additional energy
they consumed. After the 6-mo intervention, there were only
small numerical differences in body weight between the 4 groups.
The sugar-sweetened beverage group had managed to compensate
for most of the extra energy during the 6 mo (32).
The sweetener group in the current study had a reduced EI
during the 10-wk intervention. However, in the chamber, the
subjects increased the ad libitum EI equivalent to that in the
sucrose group. The unexpected higher ad libitum intake in both
groups could partly be a result of boredom or because of the
awareness of the time before they had access to food again. In
a preload-test meal design, De Graaf et al (33) showed that
subjects who had 90 min between an ad libitum soup and an ad
libitum meal consumed more soup than when they only had
15 min between the 2 meals. Giving the subjects in the current
study access to 1 or 2 more meals and also instructing the subjects
to eat only until comfortably satisﬁed could probably have
avoided some of the overeating.
BMR increased in the sucrose group by 7.6% after 10 wk and
body weight increased by 1.7%. Most of the weight gain in the
sucrose group consisted of fat mass, and neither fat mass nor lean
body mass was associated with changes in BMR. So, the increase
in BMR can probably not be explained by the increase in body
weight. It is likely that the increase is related to the “overfeeding
situation.” Dauncey et al (34) measured resting metabolic rate
after just 1 d of overfeeding and found that resting metabolic
rate remained elevated by 12% 14 h after the last meal. Both
Diaz et al (35) and Ravussin et al (36) observed increases in
BMR after long-term overfeeding. However, both research
groups stated that the length of time from the last meal to the
measurement of BMR was possibly inadequate to ensure that
the thermic effect of the evening meal had completely disappeared.
Diaz et al performed the measurements after 12.5 h
and Ravussin et al after 14 h. Harris et al (37) recorded weekly
changes in BMR during 8 wk of overfeeding. BMR increased
over the ﬁrst 2 wk, decreased in the third week, and increased
and reached a plateau after 5 wk (37). In that study, BMR was
measured ,10 h from the last meal. When the current study was
planned, it was not predicted that the sucrose group would
overeat in that way. Therefore, the 12.5 h between the last meal
and the measurements of BMR may have been inadequate. This
makes it difﬁcult to distinguish between the short-term effect of
the diet and the long-term effect of the intervention. Statistical
adjustments including the EI during the chamber stay made the
difference between groups disappear, which indicates that most
of the increase in BMR was a result of overeating during the
chamber stay.
The lack of difference in DIT between the groups was unexpected
because the difference in EI at the dinner meal was
almost 1 MJ. A study by Weststrate (38) showed that meal size
differences of ,1 MJ result in differences in DIT. An explanation
could be that the measured BMR in the sucrose group
was high because it was inﬂuenced by the last meal. This would
lead to a lower estimated DIT in the sucrose group and mask the
difference between the groups.
DITwas only estimated after the dinner meal. It is possible that
if DIT had been estimated after every meal, a difference between
groups and/or between weeks 0 and 10 would have been shown,
especially because of the breakfast meal, which was 1.35 MJ
larger in the sucrose group. In addition, the sucrose intake was
higher in the sucrose group than in the sweetener group during
breakfast and lunch. The design of the test day made it impossible,
however, to estimate DIT for the breakfast and lunch meals
because of physical activity during the day.
The objective of the current substudy was to investigate the
effect of the sweetener supplements on energy balance, including
some of the components of total EE. To detect small effects
requires a high accuracy of measurements and control of day-today
variation in physical activity to ensure any effects to be
detected. Therefore, the respiratory chamber was chosen because
that was the only way to measure all of the variables of interest.
With the use of doubly labeled water, only 24-h EE would be
measured and the ventilated-hood system could measure some of
the components but not total EE. The effect of the sweetener
supplements on 24-h EE and components of total EE could have
been measured in the chamber by serving the subjects meals with
ﬁxed energy instead of ad libitum meals. This could, however, not
have been done within the 10-wk intervention period.
In conclusion, body weight increased in the sucrose group and
decreased in the artiﬁcial-sweetener group during the 10-wk
intervention. BMR increased in the sucrose group, but no
SUCROSE, ARTIFICIAL SWEETENER, AND ENERGY BALANCE 43
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difference in 24-h EE was found between the 2 groups in week
10. The increase in BMR was probably caused by the very high EI
in the sucrose group during the chamber stay in week 10. Thus,
the changes in body weight in the 2 groups during the 10-wk
intervention seemed to be a result of changes in EI rather than of
changes in EE.
We thank Bente Kramer Møller for helping prepare the data for the
statistical analyses and John Lind and the rest of the technical staff at the
Department of Nutrition, Exercise and Sports, University of Copenhagen, for
expert assistance. We gratefully acknowledge the participation of all persons
involved in the study.
The authors’ responsibilities were as follows—AR and AA: designed the
research; THV and AR: conducted the research; and LBS: performed the statistical
analyses, interpreted the data, and wrote the manuscript. All authors
read and approved the ﬁnal manuscript and had primary responsibility for
the ﬁnal content. THV declared no conﬂicts of interest. LBS, AA, and AR
reported that their department, the Department of Nutrition, Exercise and
Sports at the University of Copenhagen, has received research support from
more than 100 food companies for studies. AA reports having served or serving
as an executive board member of Almond Board of California European
Almond Bureau Advisory Board (2004–2009) & European Steering Committee
2008; Amgen Inc, USA; Endocrinology Advisory Board (2005–2006); Arla
Foods, DK, Nutrition Advisory Board (2002–2007); Aventis Sanoﬁ, DK,
Rimonbant Advisory Board (2004–2007); Bell Institute of Health and Nutrition,
General Mills Operations LLC, USA (2012); Bristol-Myers Squibb,
USA; SGLT2 Advisory Board (2006); Choices International Foundation,
European Scientiﬁc Committee (2007–2012); Danone A/S Scandinavia, SE
(2010–2011); ILSI Europe Expert Group “Best Common Practice Guidelines
for Human Intervention Studies to Scientiﬁcally Substantiate Claims on Foods”
(2007–2009); Johnson & Johnson, USA; Topiramate Obesity Advisory Board
(2001–2007); Kraft Foods, USA; Worldwide Health & Wellness Advisory
Council (2010–2012), Merck Sharp and Dome, USA (2006–2009); Novo
Nordisk, DK; Liraglutide Obesity Advisory Board (2006–2009); Nutri
Pharma, UK; External Scientiﬁc Council (1999–2005); Pﬁzer, USA; Global
Research & Development, Obesity Disease Management Program Expert
Panel (2004–2008); Unilever, NL (2007–2008); Vivus Inc, USA (2008–
2010); BioCare Copenhagen, DK (2012–); Dutch Beer Knowledge Institute,
NL (2008–); Global Dairy Platform, USA; Communications and Scientiﬁc
Advisory Board (2006–); Jenny Craig, USA (2009–); McDonald’s, USA,
Global Advisory Board (2012–); Pathway Genomics Corporation, USA
(2010–); Vivus Inc, USA; and OB-401 Study Executive Committee
(2012–). Furthermore, AA has consulted or consults for 7TM Pharma,
DK (2004–2011); Cadbury Ltd, UK (2008–2009); GlaxoSmithKline,
USA (2006–2011); ISIS Pharmaceuticals Inc, USA (2006–2007);
Johnson & Johnson Pharmaceutical Research & Development LLC, USA
(2009); European Food Information Council, Media Guide Expert (2003–
2004); Merck Sharp and Dome, USA (2006–2008); Metabolife International
Inc, USA (1996–1998); NeuroSearch, DK (2006–2011); Nordic Biotech, DK
(2004–2007); Novartis Pharmaceuticals Corporation, Switzerland (2007);
Reuters Insight, USA (2008–2009); Roche Pharmaceuticals, DK (2007–
2008); Schering-Plough, USA (2004–2007); Takeda Global Research &
Development Center Inc, USA (2010); Weight Watchers, USA (2001–2010);
Arena Pharmaceuticals Inc, USA (2009–); Basic Research, USA (2007–);
Boehringer Ingelheim Pharma GmbH & Co KG, Germany (2013); Gelesis,
USA (2012–); Novo Nordisk, DK (2001–2009, 2011–); Orexigen Therapeutics
Inc USA (2009–); Psyadon Pharmaceuticals Inc, USA (2012–); Rhythm
Pharmaceuticals, USA (2010–); S-Biotek, DK (2008–); and Twinlab, USA
(2011–).
REFERENCES
1. St-Onge MP. The role of sleep duration in the regulation of energy
balance: effects on energy intakes and expenditure. J Clin Sleep Med
2013;9:73–80.
2. Casazza K, Fontaine KR, Astrup A, Birch LL, Brown AW, Bohan Brown
MM, Durant N, Dutton G, Foster EM, Heymsﬁeld SB, et al. Myths,
presumptions, and facts about obesity. N Engl J Med 2013;368:446–54.
3. Speakman JR, Levitsky DA, Allison DB, Bray MS, de Castro JM,
Clegg DJ, Clapham JC, Dulloo AG, Gruer L, Haw S, et al. Set points,
settling points and some alternative models: theoretical options to
understand how genes and environments combine to regulate body
adiposity. Dis Model Mech 2011;4:733–45.
4. Larsen TM, Dalskov SM, van Baak M, Jebb SA, Papadaki A, Pfeiffer
AF, Martinez JA, Handjieva-Darlenska T, Kunesova´ M, Pihlsga˚rd M,
et al. Diets with high or low protein content and glycemic index for
weight-loss maintenance. N Engl J Med 2010;363:2102–13.
5. Mattes RD, Shikany JM, Kaiser KA, Allison DB. Nutritively sweetened
beverage consumption and body weight: a systematic review and
meta-analysis of randomized experiments. Obes Rev 2011;12:346–65.
6. Te Morenga L, Simonette M, Jim M. Dietary sugars and body weight:
systematic review and meta-analyses of randomised controlled trials
and cohort studies. BMJ 2013;346:e7492.
7. Mozaffarian D, Hao T, Rimm EB, Willett WC, Hu FB. Changes in diet
and lifestyle and long-term weight gain in women and men. N Engl J
Med 2011;364:2392–404.
8. Malik VS, Pan A, Willett WC, Hu FB. Sugar-sweetened beverages and
weight gain in children and adults: a systematic review and metaanalysis.
Am J Clin Nutr 2013;98:1084–102.
9. Mattes RD, Popkin BM. Nonnutritive sweetener consumption in humans:
effects on appetite and food intake and their putative mechanisms.
Am J Clin Nutr 2009;89:1–14.
10. Sørensen LB, Moller P, Flint A, Martens M, Raben A. Effect of sensory
perception of foods on appetite and food intake: a review of studies on
humans. Int J Obes Relat Metab Disord 2003;27:1152–66.
11. Maersk M, Belza A, Holst JJ, Fenger-Grøn M, Pedersen SB, Astrup A,
Richelsen B. Satiety scores and satiety hormone response after sucrosesweetened
soft drink compared with isocaloric semi-skimmed milk and
with non-caloric soft drink: a controlled trial. Eur J Clin Nutr 2012;97:
523–9.
12. Donahoo WT, Levine JA, Melanson EL. Variability in energy expenditure
and its components. Curr Opin Clin Nutr Metab Care 2004;7:
599–605.
13. Raben A, Kiens B, Richter EA. Differences in glycaemia, hormonal
response and energy expenditure after a meal rich in mono- and disaccharides
compared to a meal rich in polysaccharides in physically ﬁt
and sedentary subjects. Clin Physiol 1994;14:267–80.
14. Raben A, Astrup A. Manipulating carbohydrate content and sources in
obesity prone subjects: effect on energy expenditure and macronutrient
balance. Int J Obes Relat Metab Disord 1996;20(suppl 2):S24–30.
15. Horton TJ, Drougas H, Brachey A, Reed GW, Peters JC, Hill JO. Fat
and carbohydrate overfeeding in humans: different effects on energy
storage. Am J Clin Nutr 1995;62:19–29.
16. Raben A, Vasilaras TH, Moller AC, Astrup A. Sucrose compared with
artiﬁcial sweeteners: different effects on ad libitum food intake and
body weight after 10 wk of supplementation in overweight subjects.
Am J Clin Nutr 2002;76:721–9.
17. Toubro S, Sorensen TI, Ronn B, Christensen NJ, Astrup A. Twentyfour-hour
energy expenditure: the role of body composition, thyroid
status, sympathetic activity, and family membership. J Clin Endocrinol
Metab 1996;81:2670–4.
18. Raben A, Moller BK, Flint A, Vasilaris TH, Christina Møller A, Juul
Holst J, Astrup A.. Increased postprandial glycaemia, insulinemia, and
lipidemia after 10 weeks’ sucrose-rich diet compared to an artiﬁcially
sweetened diet: a randomised controlled trial. Food Nutr Res (Epub
ahead of print 20 July 2011).
19. Sørrensen LB, Raben A, Stender S, Astrup A. Effect of sucrose on
inﬂammatory markers in overweight humans. Am J Clin Nutr 2005;82:
421–7.
20. Costill DL. Carbohydrates for exercise: dietary demands for optimal
performance. Int J Sports Med 1988;9:1–18.
21. Raben A, Tagliabue A, Astrup A. The reproducibility of subjective
appetite scores. Br J Nutr 1995;73:517–30.
22. Astrup A, Thorbek G, Lind J, Isaksson B. Prediction of 24-h energy
expenditure and its components from physical characteristics and body
composition in normal-weight humans. Am J Clin Nutr 1990;52:777–83.
23. Elia M, Livesey G. Energy expenditure and fuel selection in biological
systems: the theory and practice of calculations based on indirect
calorimetry and tracer methods. World Rev Nutr Diet 1992;70:68–131.
24. Heitmann BL. Prediction of body water and fat in adult Danes from
measurement of electrical impedance. A validation study. Int J Obes
1990;14:789–802.
44 SØRENSEN ET AL
atEBSCOhostonJune24,2014ajcn.nutrition.orgDownloadedfrom
25. Astrup A, Buemann B, Christensen NJ, Madsen J. 24-hour energy
expenditure and sympathetic activity in postobese women consuming
a high-carbohydrate diet. Am J Physiol 1992;262:E282–8.
26. De Castro JM. The effects of the spontaneous ingestion of particular
foods or beverages on the meal pattern and overall nutrient intake of
humans. Physiol Behav 1993;53:1133–44.
27. Mattes RD. Dietary compensation by humans for supplemental energy
provided as ethanol or carbohydrate in ﬂuids. Physiol Behav 1996;59:
179–87.
28. Anton SD, Martin CK, Han H, Coulon S, Cefalu WT, Geiselman P,
Williamson DA.. Effects of stevia, aspartame, and sucrose on food
intake, satiety, and postprandial glucose and insulin levels. Appetite
2010;55:37–43.
29. de Graaf C. Why liquid energy results in overconsumption. Proc Nutr
Soc 2011;70:162–70.
30. Viskaal-van Dongen M, Kok FJ, de Graaf C. Eating rate of commonly
consumed foods promotes food and energy intake. Appetite 2011;56:25–31.
31. Karl JP, Young AJ, Rood JC, Montain SJ. Independent and combined
effects of eating rate and energy density on energy intake, appetite, and
gut hormones. Obesity (Silver Spring) 2013;21:E244–52.
32. Maersk M, Belza A, Stødkilde-Jørgensen H, Ringgaard S, Chabanova
E, Thomsen H, Pedersen SB, Astrup A, Richelsen B. Sucrose-sweetened
beverages increase fat storage in the liver, muscle, and visceral fat
depot: a 6-mo randomized intervention study. Am J Clin Nutr 2012;95:
283–9.
33. De Graaf C, De Jong LS, Lambers AC. Palatability affects satiation but
not satiety. Physiol Behav 1999;66:681–8.
34. Dauncey MJ. Metabolic effects of altering the 24 h energy intake in
man, using direct and indirect calorimetry. Br J Nutr 1980;43:257–69.
35. Diaz EO, Prentice AM, Goldberg GR, Murgatroyd PR, Coward WA.
Metabolic response to experimental overfeeding in lean and overweight
healthy volunteers. Am J Clin Nutr 1992;56:641–55.
36. Ravussin E, Schutz Y, Acheson KJ, Dusmet M, Bourquin L, Jequier E.
Short-term, mixed-diet overfeeding in man: no evidence for "luxuskonsumption.
Am J Physiol Endocrinol Metab 1985;249:E470–7.
37. Harris AM, Jensen MD, Levine JA. Weekly changes in basal metabolic
rate with eight weeks of overfeeding. Obesity (Silver Spring) 2006;14:
690–5.
38. Weststrate JA. Resting metabolic rate and diet-induced thermogenesis:
a methodological reappraisal. Am J Clin Nutr 1993;58:592–601.
SUCROSE, ARTIFICIAL SWEETENER, AND ENERGY BALANCE 45
atEBSCOhostonJune24,2014ajcn.nutrition.orgDownloadedfrom
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