Effects of sugar intake on body weight: a review

obesity reviews
Effectsof sugar intakeon body weight:a review
S. H. F.Vermunt.W. J. Pasman,G. Schaafsmaand A. F. M. Kardinaal
TNO Nutritionand FoodResearch,Department
of NutritionalPhysiology,Zeist,the Netherlands
Beceived26 December 2N2; revised28
February 2O03; accepted 3 March 2003
Address reprintrequeststo: SHFVermunt,TNO
Nutritionand Food Research,Departmentof
Nutritional Physiology,PO Box 360, 3700 AJ
Zeist, the Netherlands.
nl
E-mail: [email protected].
Summary
rUreight reduction prograÍnmes are mainly focused on reducing intake of fat and
sugar. In this review we have evaluated whether the replacement of dietary (added)
sugar by low-energy sweeteners or complex carbohydrates contributes to weight
reduction. In rwo experimental studies, no short-term differences in weight loss
were observed after use of aspartame as compared to sugar in obese subiects
following a controlled energy-restricteddiet. However, consumption of aspartame
was associated with improved weight maintenance after a yeaÍ.In two short-terrn
studies in which energy intake was not restricted, substitution of sucrose by
artificial sweeteners, investigated mostly in beverages, resulted in lower energy
intake and lower body weight. Similarly, r'wo short-term studies, comparing the
effect of sucrose and starch on weight loss in obese subjects did not find differences
when the total energy intake was equal and reduced. An ad libitutn diet with
complex carbohydrates resulted in lower energy intake compared to high-sugar
diets. In rwo out of three studies, this was reflected in lower body weight in
subjects consuming the complex carbohydrate diet. In conclusion, a limited number of relatively short-term studies suggest that replacing (added) sugar by lowenergy sweeteners or by complex carbohydrates in an ad libitum diet might result
in lower energy intake and reduced body weight. In the long term, this might be
beneficial for weight maintenance. Howevet the number of studies is small and
overall conclusions, in particular for the long term' cannot be drawn.
Keywords: Body weight, carbohydrates, sugarobesity
reviews (2003) 4, 91-99
lntroduction
The prevalence of obesity is increasing around the world
and it is a significant public health problem in many countries (1). An accurate energy balance (energy intake equals
energy expenditure) is essential to maintain a stable body
weight. In weight reduction programmes, dietary recommendations have been mainly focused on reducing intake
of. fat and sugar In this review, we will not discuss fat, but
carbohydrate intake. It is not quite clear whether the
replacement of (added) sugar (meaning all simple carbohydrates [SCHOs]) by low-energy sweeteners or by complex
carbohydrates (CCHOs), introduced as a tool to lower
energy intake, truly contributes to weight reduction.
Replacing sugar by low-energy sweeteners may affect
subjects' energy balance. Theoretically, energy intake will
be lowered, while sweetnessremains. However, the energy
content of carbohydrates, fat and proteins, may have an
impact on appetite and sadery as well (2). Therefore, consumption of products with sweeteneÍs may lead to the
adaptation of eating habits that compensate for the reduced
energy intake. So, it may be possible that in the end the
energy intake does not change when low-energy sweeteners
are used.
In this review, published data from Medline (National
Library of Medicine, Bethesda, MD), dated from 1980
onwards, on the role of sugars, CCHOs and sweetenersin
human body-weight maintenance are evaluated [search
words: simple or complex carbohydrate, sugar or sucrose,
body weight, BMI (body mass index), sweeteners,obesiry
energy intake and starch]. Only articles written in English
were included, with a limitation up to 35 publications.
@ 2OO3The lnternationalAssociation Íor the Study oÍ Obesity. obesity reviews 4, 91-99
92 Sugar intakeand body weight S. H. E Vermuntet al
Studies were categorized into investigations reporting
effects of dietary sugar relative to low-energy sweeteners,
CCHOs and fat, on body weight. The regulation of food
intake with respect to appetite, satiety and energy intake
as well as adaptation of eating habits is briefly discussed.
Sugar vs. low-energysweeteners
Few studies, which are summarized in Table 1, have investigated the effects of sugar replacement by sweeteners on
body weight. Kanders et al. studied 59 obese men and
women following an energy-restricted diet (4.2 MJ fl for
rryomen and 5 MJ dt for men) during a L2-week weight
loss programme with l-year follow-up (3,4). Subjects were
either required to use aspartame-sweetened products or
prohibited from using aspaÍtame-sweetened products.
'Women
who used aspartame-sweetened products lost more
weight than non-users (7.5 kg vs. 5.8 kg), although differences were not statistically significant. The weight loss seen
in the experimental group, after the active weight loss
phase, compared to the control group might indicate that
compliance of reduced energy intake was facilitated for
subjects allowed to use low-energy sweetened products.
In a later study by the same group of investigators with
obese women only, 163 subjects received aÍr energyrestricted diet (4.2 MJ d-t) during a 19-week weight loss
programme (5). The women were again assigned to either
consume or abstain from aspartame-containing products.
After 19 weeks, the aspartame intake increased in the
aspartame group and decreased in the non-aspartame
group. Energy intake did not differ between the aspartame
and non-aspartame groups. In both groups, women lost
about 10% (9.9 kg) of body weight in the active weight
loss phase, which was nor different between the groups. In
\ /omen who used the aspartame-sweetened products,
intake of aspartame \ryaspositively correlated with loss of
body weight during active weight loss. After l-year weight
maintenance, women who used aspartame-sweetened
foods and beverages besides rhe 6.2MI weight maintenance diet regained significantly less weight (2.6 kg) than
the non-aspartame users (5.4 kg) (P < 0.05). Afrer the 2year follow-up, the aspartame users srill had a mean weight
loss of 5.1 kg, whereas the non-aspartame users had
regained all their weight lost. Both studies suggest thar,
although no short-term effects of aspartame consumption
on body weight could be demonsrrated, this high-intensiry
sweetener may be useful to maintain a reduced body weight
during a weight control prograÍnme in the long term (3-S).
Compliance to a weight maintenance prograÍnme seems to
be facilitated with the use of low-energy sweeteners.
Becauseof the growing intake of soft drinks in our diet
and the accompanying rise in obesity especially seen in
children (6), the question arises whether there is a causal
relationship. Recently, this discussion gor a lot of attention
obesity reviews
and in the USA, can machines were even removed frorn
school buildings. The evidence comes from differenr studies. In a 10-week supplementation study, subjects (on average 35 years) were supplemented with sucrose [3.4 MJ;
L52g sucroseper day=28 energy percent (en%)J or artificial sweeteners (1.1 MJ; 0 g sucrose per day; aspartarne,
acesulfame K, cyclamate and saccharine), mostly as beverages in a further ad libitum diet (7). After 10 weeks, a
decrease in body weight was seen in those consuming the
artificially sweetenedsupplements (1 kg), in contrast ro the
increase in those supplemented with sucrose (1.6 kg)
(P < 0.001). The main explanation for this difference in
body weight was found to be the difference in energy intake
coming from experimenral fluids. DiMeglio and Maftes
have already reported that compensarion of energy intake
is less accurate with energy intake from liquids vs. solid
foods (8). Carbohydrate intake from liquids therefore promotes a positive energy balance, whereas carbohydrate
intake from solid foods will be compensated for (8).
In a cross-over study, Tordoff and Alleva compared
3 weeks consumption of 1.150g soda sweetened with
aspartame (3kcal=17.6kJ) per day with 1150g highfructose corn syrup (530 kcal =2.2 MJ) per da5 and with
no soda (control) in 30 men and women with a healthy
body weight (9). After 3 weeks consumption of highfructose corn syrup, body weight \Mas significantly
increased as compared to consumption of aspartamesweetened soda and no soda. In both groups consuming
experimental drinks, energy intake Írom the diet was lowered as compared to control [7.5 MJ for diet with the
aspartame-sweetened soda; 7.3 MI for diet with the highfructose corn syrup (excludng 2.2MJ from the soda);
8.5 MJ per day for the control diet]. When energy contenr
of the high-fructose corn syrup was included, energy intake
in this group was higher than that in the group using the
aspartame-sweetened soda and the control group. The only
difference in energy intake between the diets with the
experimental drinks was the amount of energy from the
high-fructose corn syrup l2.2}iíD, which may explain the
difference in body weight berween these groups. In both
treatment groups, sugar intake from the diet was reduced
as compared to the control group, probably becausecommonly used energy-containing drinks were replaced by
experimental drinks (9). From this short-term studS it may
be concluded that reducing total sugar intake by replacing
consumption of large volumes of high-fructose-containing
soda by aspartame-sweetened drinks may be favourable for
body-weight control. This would only be favourable when
there is no compensation for the reduced energ-y intake
from other food products.
In a long-term observational study (19 months), Ludwig
and colleagues reported a positive relation between intake
of sugar-sweetened drinks and prevalence of childhood obesity (6). The beverage intake (of 57% of the participating
@ 2003 The International Association for the Study oÍ obesity. obesity reviews 4, 91-gg
obesity reviews
Sugar intake and body weight S. H. F. Vermuntet al. 93
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@ 2OO3The InternationalAssociation for the Study oí Obesity. obesity reviews 4, 91 -99
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obesity reviews
94 Sugar intake and body weight S. H. F. VermunteI al.
children) as well as BMI had increased during the j.9-month
observation period. Although the study was observational
in nature and causality is not proven, the results are consistent with the above-mentioned mechanism that consumption of sugar-sweeteneddrinks could lead to obesity because
of imprecise and incomplete compensation for energy consumed in liquid form (6). Overweight individuals, who wanr
to prevent weight gain, may want to choose beverages
containing low-energy sweetenersrather than sucrose (7).
Few epidemiological studies have investigated the relationship between use of sweerenersand BMI. In a Spanish
cross-sectionalstudy with 2450 men and women, intake of
cyclamate, an artificial sweetener,was negatively correlated
with BMI (10). Previous prospective studies with women
showed a positive association between use of artificial
s\ /eeteners (saccharine and./or cyclamate) and BMI at start
of the snrdy (71,12). After !-year follow-up, weight gain
was higher in the group of users than in the group of nonusers. From these studies, it may be concluded that longterm usage of sweeteners (1 year) does not result in
reduction of body weight. However, the lamer study was
designed to study cancer incidence and not obesity. Body
weight was not measured but recalled, which was not
checked at all, although body weight is known to be
affected, especially for cancer. But the fact that affected the
data the most is that women who changed their eating
habits, including use of srveeteners,were excluded from the
analysis. This could be the reason for the lack of weight
loss. Moreover, the authors had already mentioned that
sweetener use might have prevenred weight gain (12). In
another prospective cohort study a positive association
was found between use of saccharine and body-weight
changes both at the start of the study and after 4-year
follow-up (13). However, these epidemiological studies are
based on observations, therefore, no causal relations can
be made. It might be possible rhat subjects who are concerned about their weight were already using low-energy
sïyeeteners to prevent weight gain.
Thus, results of experimental and epidemiological studies on the relationship between use of sweetenersand BMI
are not univocal. At present, use of low-energy sweeteners
does not seem to result in weight loss per se, but might be
useful for weight maintenance in healthy-weight subjects.
Sugar vs. complex carbohydrates
Several intervention studies investigating the effects of
dietary sugar relative ro CCHOs on body weight are
described (Table 2).
Energy-restricteddiets
In a recent study by Vest and de LooS 68 obese subjects
(34 men and 34 women) received a low-fat (33 enT"|,
energy-restricted low-sucrose diet (S en"Á sucrose) or an
energy-restricted sucrose-containing diet (10 enoÁ sucrose)
(14). The deficit in energy of 2.51MJ ft resulted in a
reported energy intake of 5.6 + 1.5 MJ for the low-sucrose
diet and 5.9!1,.6MJd-1 for rhe sucrose-containingdiet
(14). Diets only differed in source of carbohydrates
(sucrosevs. starch). After a period of 8 weeks, body weight
had declined in both groups: 3.0 kg in the group with a
sugar-containing diet and 2.2kg in the group with a lowsugar diet, which was significantly different from baseline
but not significantly different berween both groups (14).
Based on the low reported intakes and the known energy
deficit, it was calculated that the gÍoups should have lost
about 6.9 kg in 8 weeks. This means that most probably
under-reporting took place, and t}rat the subiects did not
fully comply with the reduced energy diet. ln another study
by Surwit et al., 42 obese women followed an energyrestricted low-fat diet (11 enoÁ fat, 'J,9enY" protein and
77 en"/" carbohydrates) of 4.6 MI d-1. Within the diet, rwo
variations of carbohydrate were made: one diet with
43 en"/" sucrose (sugar-containing diet) and anorher with
4 en"Á sucrose (low-sugar diet) (15). As before, the diets
differed only in rhe source of carbohydrates (sugar vs.
starch). After 6 weeks, body weight decreasedby 7.0 kg for
the sugar-containing diet and by 7.4 kg for the low-sugar
diet, which was not significantly different between both
groups as well. Both srudies illustrate that weight loss is a
consequence of the energy deficit, regardless of the type of
macronutrient, let alone within the fype of macronutrient
(SCHO vs. CCHO).
Ad libitum diets
The CARMEN study, a European multicentre study, investigated differences berween an ad libitum low-fat highSCHO diet and a low-fat high-CCHO diet vs. a control
diet in relation to body weight in 316 obese adults (16).
After 6 months, body weight was lowered by 1..7kg in the
SCHO group and by 2.6kg in the CCHO group as compared to the control group. Differences in body-weight
changes between the treatment groups did not reach significance, despite the significantly higher energy intake in the
SCHO group (10.4 MJ d-t) as compared to the CCHO
group (9.3 MJ d-1). Compared to the control group, the
changes in body weight between the treatment groups were
significantly different.
As a part of the CARMEN snrdy, Poppin and co-workers
investigated the same design and diet as well in another
subgroup of 39 overweight subjects (1,2 men and 27
women) with symptoms of the metabolic syndrome (17).
Six-month ad libitum diet intervention resulted in decreases
in body weight in both the SCHO group (-1.3 kg) and the
CCHO group (-5.3 kg) as compared to the control group.
In this low-fat diet with a difference in carbohydrate
o 2003 The InternationalAssociation Íor the study of obesity. obesity reviews 4, 91-99
obesity reviews
Sugar intakeand body weight S. H. F. Vermunteï al. 95
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obesity reviews
96 Sugar intakeand body weight S. H. F. Vermuntet al.
source, but not limited in energy intake, weight gain was
prevented in overweight subjects with characteristics of the
metabolic syndrome. Most of the weight loss was found
when fat was replaced by CCHOs. As \À/as seen in the
CARMEN trial, both studies showed that a diet high in
CCHO is favourable for weight loss.
In a cross-over trial of a group of 40 women with a
healthy body weight, body weight decreasedby 0.7 kg after
14 d of a high-starch diet with an ad libitum energy intake
(18). This weight loss differed significantly from the stable
body weight after a high-sucrose diet (increase of 0.2 kg)
(P < 0.05). The difference may result from a higher energy
intake in the high-sucrose group (on average 10.3 MJ dt)
as compared to the high-starch group (9.1 MJ trl). This
spontaneous reduction in energy intake of a diet rich in
starch and dietary fibre is consistent with other studies, in
which the type of diet is suggested to facilitate compliance
to lower energy intake.
Glycaemicindex
The variation in SCHO and CCHO present in a diet or
meal, with respect to type of carbohydrate as well as
amount, will affect the blood glucose response caused by
the time necessaryfor digestion and absorption. Glycaemic
index (GI) is defined as the incrementalareaunder the blood
glucose response curve after consumption of carbohydrates.
In general, high-Gl foods have a high-SCHO content and
are rapidly digested. Products have a higher GI when they
have (1) a higher refined carbohydrare conrent, (2) a high
glucose and/or starch content relative to lactose, sucrose
and fructose, or (3) a low soluble fibre content, and (4)
when their texture is soft, overcooked, highly processed or
over-ripened (19). The GI of a carbohydrate-rich diet not
only affects glucose, insulin and lipid response of food (20),
but also affects appetite, energy intake and body weight.
Consumption of low-Gl food increasessatiety and reduces
hunger as compared to products with high GI (19). Summarizing data from six cross-over studies suggested that
consumption of high-Gl carbohydrates promotes a shorttime increase in energy intake as compared to lower-Gl
carbohydrates (21). However, others have found a lower
energy intake and a higher weight loss after a carbohydraterich diet with high GI for 2 weeks, as compared to a lowGI diet (22). Recently, the pros and cons of GI on appetite,
food intake, energy expenditure and body weight was thoroughly reviewed by Raben (23). Numerous srudies showed
conflicting results for the items mentioned, and therefore
Raben concluded that at present there was no evidence to
state that low-Gl foods were superior to high-Gl foods with
regard to long-term weight mainrenance (231. So, although
a low-Gl diet is generally recommended, no definite conclusions on the effects of the GI on appetite and bodyweight maintenance can be drawn.
Based on the studies described above, it was concluded
that when energy intake was restricted, the source of carbohydrate does not seem to be importanr for body weight.
Results of ad libiturn energy intake studies revealed that,
for both obese subiects and subjects with a healthy body
weight, there were differences in weight loss for highSCHO vs. high-CCHO diets. The decreasedbody weights
in both SCHO- and CCHO-rich diets as compared to the
control group may be explained by differences in energy
intake, which are easier kept reduced in a high-CCHO diet.
Sugar vs. fat
To examine the effect of exchange of sugar vs. fat on body
weight, a limited number of studies \Mere reviewed
(Table3).
In a parallel intervention trial by Gatenby et aI., 49
healthy-weight women received instructions for a lowsugar diet, a low-fat diet or a control diet during 10 weeks
(2a). Subjects in the low-sugar and low-fat groups were
instructed to reduce intake of sugar or fat by replacing fullsugar or full-fat items with low-sugar and low-fat products,
respectively. At the start of the study, energy intake did not
differ between the groups. After 10 weeks, the energy
intake was lowered in all groups as compared to baseline
(-1.37 ML -1,.22 MJ and -1.15 MJ, for the low-sugar,
low-fat and control groups, respectively, nor significantly
different between groups). A decrease which appeared to
be a reflection of repeated record keeping was seen- In the
reduced-fat group, the reported fat intake decreased from
37 to 33 en"/" (P: 0.017). A reduction of reported sucrose
intake (but not total carbohydrate intake) was seen in the
reduced-sugar group (a reduction of about 2.5 enY"l. None
of the three groups showed changes in body weight because
of these differences in macronutrient composition (241.
Raben et al. also found no differences in changes of body
weight after 14 d on a high-sucrose diet or a high-fat diet
in their cross-over study of 20 healthy-weight women using
an ad libitum food intake (18). The energy intake was
10.2 MJ d-l in the high-fat diet and 10.3 MJ 4-t in the
high-sucrose diet, which did not differ significantly.
In a multicentre trial, the effect of consumprion of fullfat or reduced-fat products was investigated in247 healthyweight subjects, known as the MSFAT study (25). In an
open, randomized controlled trial, subjects consumed food
products containing either a full-fat or a reduced-fat composition for 6 months. About 3040% of the total daily
energy intake was covered by the products provided. A
significant increase in body weight of 1.1 kg was seen in
the group consuming a full-fat diet, compared with a relatively stable weight in the reduced-fat group (+0.a kS)
(P = 0-023). The investigators concluded that a switch from
full-fat to reduced-fat in an ad libitum diet could prevent
body-weight gain. The reduced-fat products will help in a
@ 2003 The lnternational Association Íor the Study oÍ obesity. obesity reviews 4, 91-99
obesity reviews
Sugar intake and body weight S. H. F. Vermuntet al. W
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In the studies described, energy intake and body weight
did not differ between a low-fat and low-sugar diet (24,25),
or a high-fat and high-sucrose diet (18). The macronutrient
composition (fat or carbohydrates) does not affect body
weight, but the total amount of the fat and carbohydrates
eaten (amount of energy intake) does affect body weight.
Epidemiological studies indicate a possible inverse relationship between intake of total and extrinsic or added
sugar and BMI in adults (28). In these studies, high-fat,
high-sugar food products (snacks) were investigated. The
negative relationship between sugaÍ intake and BMI was
observed in different studies (28-30). No negative association was found between the intake of intrinsic sugar or
lactose and BMI, suggesting that the extrinsic sugar source
may specifically play a role in body-weight maintenance.
Besides the absolute sugar intake, the ratio between intake
of. Íat and sugar may be important in body-weight regulation (28-3L). Subiectswith a higher dietary fat to extrinsic
sugar ratio had a higher BMI (28). The indication that
high-sugar intake is negatively correlated with BMI, especially in men as was found in two studies (29,301, is inter-
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in an increased fat intake. Furthermore, dietary sugar may
increase acceptance of a low-fat diet, which may increase
long-term compliance. In a recent study, compliance in a
high-carbohydrate low-fat diet may be increased by sugar
intake, which is preferable in reducing body weight (27).
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Food intake is regulated for an important part by rwo
processes:satiation and satiery Satiation is related to meal
termination after inhibition of hunger and appetite within
meals, while satiery refers to inhibition of feelings of hunger
and appetite following food consumption in the postprandial phase. Both short-term and long-term studies have
investigated effects of sugar on satiation, satiety and energy
intake.
Pre-load studies, which are often used to investigate
short-term effects of sugar on feelings of hunger, satiefy and
energy intake on additional food intake, showed contradictory results. Several studies found that sweeteners (e.g.
aspartame alone or combined with acesulfame-K, sucralose) as compared to sucrose did not have any effect on
O 2003 The International Association Íor the Study oÍ Obesity. obesity reviews 4, 91-99
obesity reviews
98 Sugar intakeand body weight S. H. F. Vermuntet al,
feelings of hunger (32-35). Some studies found increases
of appetite after a pre-load of sweetenersrelative to sucrose
(36), while others did not (37). Therefore, it may be concluded that replacing sugar with low-energy sweeteners,
like aspartame, may hardly affect short-term satiety aher a
pre-load.
A pre-load with low-calorie sweetenersmay lead to an
increased energy intake afterwards as compared to an
energy-containing pre-load (35,36,3840 ), however, orhers
did not find any such effects (32,33,37). Two experimental
studies showed decreasesin energy intake when sucrose
was used as pre-load as compared to fat or control (41,,42').
These conflicting results from short-term studies may be
because of differences in designs, study populations and
study parameters. In addition, differenr carbohydrates and
various kinds of sweeteners may also have other effects on
appetite, satiety and food intake. Sucrose consists of fructose and glucose,while starch consists of a chain of glucose
units only. Therefore, effects of sucrose on appetite, satiefy
and energy intake may differ from that of starch, and starch
may act differently from single glucose units.
Only a few clinical and epidemiological studies have
investigated long-term effects of sweetenersuse on appetite,
satiety and energy intake (a3). Epidemiological studies
have shown that a high-sucrose intake is associated with a
lower BMI and reduction of energy intake and body
weight, while starch had neutral effects (28). As described
earlier, no causal relations were examined in the epidemiological studies. The observation that obese subjects are
more inclined to avoid sugar intake and replace them with
no-calorie sweetenerscould also be explained as an individual strategy to prevenr further weight gain. The positive
relation found betrveen low-calorie sweeteners consumption and BMI needs further study. Long-term intervention
studies have not confirmed the negative association
between sugar intake and body weight. From several studies, it has been observed that a low intake of low-sugar
products seemsto have minor effects on total energy intake
or body weight (24).
In healthy-weight subjects, ad libitum energy intake was
reduced for a diet rich in starch and fibre, but no changes
were observedfor a diet rich in fat and sucrose (18). Results
suggest that a diet rich in starch and fibre is more efficient
in reducing energy intake and body weight than a sucroserich diet.
Adaptationof eating habits
As described earlier, sweeteners may affect appetite and
satiety. It is not quite clear whether the consumption of
products with sweeteners also leads to the adaptation of
eating habits that compensate for the reduced energy
intake. Porikos et al. investigated the change in energy
intake when sucrose-containing products were replaced,by
comparable products sweetened with aspartame in six
healthy-weight men (44). During the first 3 d, no change in
food intake was observed, but after 4-6 d, about 40% of
the missed sucrose calories in the aspartame diet was compensated. Another study showed compensation of ^
reduced fat intake by higher intake of full sugar (271.
Compensation of a low-energy diet by high-sucrose snacks
seems to result in a lower total daily energy intake as
compared to compensation by high-far snacks (42). So
compensation of the missed calories is often found, and
depending upon the type of product present (low/high fat
or lodhigh carbohydrate), compensation in energy intake
is more or less complete.
Conclusion
In conclusion, a limited number of relatively short-term
studies suggestthat replacing (added) sugar by low-energy
sweetenersor by CCHOs ín an ad libitum diet might result
in lower energy intake and reduced body weight. In the
long term, this might be beneficial for weight maintenance.
However, the number of studies is small and overall conclusions, in particular for the long term, cannot be drawn.
Acknowledgements
A grant from'Suikerstichting Nederland' (the Netherlands)
for writing this article is gratefully acknowledged.
References
1.. International Obesiry TaskForce- About obesity: lncidence,
prevalence (y co-morbidity. 20A2. NfVlf
documentJ. URL
http ://www. íotf. orgl
2. Holt SHA, Brand Miller JC, Petocz P, Farmakalidis E. A satiety
index of common foods. Eur J Clin Nutr 1995;49: 675-690.
3. Kanders BS, Lavin PT, Kowalchuk
MB, Greenberg I,
Blackburn GL. An evaluation of the effect of aspartame on weight
loss. Appetite 1988t 11 (Suppl-): 73-84.
4. Kanders BS, Lavin PT, Kowalchuk M, Blackburn GL. Do
aspartame (AMP-) sweetened foods and beverages aid in long-term
control of body weight? Am J Clin Nutr L990;51: 515 (Abstract).
5. Blackburn GL, Kanders BS, Lavin PT, Keller SD,'!íhatley J.
The effect of aspartame as parr of a multidisciplinary weightcontrol program on short- and long-term conrrol of body weight.
Am J Clin Nutr 1997;65:409478.
6. Ludwig DS, Peterson KE, Gortmaker SL. Relation berween
consumption of sugar-sweetened drinks and childhood obesiry: a
prospective, observational analysis. Lanczt 2001; 35 7: 505-508.
7. Raben A, Vasilaras TH, Msller AC, Astrup A. Sucrose compared with artificial sweeteners: different effects on ad libiturn
food intake and body weight after 10 wk of supplementation in
overweight subjects. Am J Clin Nutr 2002;762 721-729.
8. DiMeglio DP, Mattes RD. Liquid versus solid carbohydrate:
effects on food intake and body weight. lnt J Obes 2000;24:794800.
@ 2003 Fhe InternationalAssociation Íor the Study oÍ Obesity. obesity reviews 4, 91 -99
obesity reviews
9. Tordoff MG, Alleva AM. Effect of drinking soda sweetened
with aspartame or high-fructose corn syrup on food intake and
body weight. Am J CIin Nutr 1990;51:963-969.
10. Serra-Majem L, Ribas L, Ingles C, Fuentes M, Lloveras G,
Salleras L. Cyclamate consumption in Catalonia, Spain (1.992):
relationship with the body mass index. Food Addit Contam 1996;
13:695-703.
11. Stellman SD, Garfinkel L. Arti6cial sweetener use and oneyear weight change among ïvomen. Preu Med 1986; 15: l9S-202.
12. Stellman SD, Garfinkel L. Patterns of artificial sweetener use
and weight change in an American Cancer Society prospective
study. Appetite 1988; 11: 85-91.
13. Parker DR, Gonzalez S, Derby CA, Gans KM, Lasater TM,
Carleton RA. Dietary factors in relation to weight change among
men and women from two southeastern New England communities. Int J Obes I997i 2l: 103-109.
'West
14.
JA, de Looy AE. Iíeight loss in overweight subjects
following low-sucrose or sucrose-containing diets. lnt J Obes
2001; 8:11.22-1128.
15. Surwit RS, Feinglos MN, McCaskill CC, Clay SL, Babyak
MA, Brownlow BS, Plaisted CS, Lin PH. Metabolic and behavioral
effects of a high-sucrose diet during weight loss. Áz J CIin Nutr
7997;65t 908-915.
16. Saris WFIM, Astrup A, Prentice AM, Zunft HJF, Formiguera
X, Verboeket-van de Venne\VPHG, Raben A, Poppin AD, Seppelt
B, Johnston S, Vasilaras TH, Keogh GF. Randomized controlled
trial of changes in dietary carbohydrateVfat ratio and simple vs
complex carbohydrates on body weight and blood lipids: the
CARMEN study. Int J Obes 2000; 24: 1310-731817. Poppitt SD, Keogh GF, Prentice AM, Williams DEM,
Sonnemans HMW, Valk EEJ, Robinson E,'Wareham NJ' Longterm effects of ad libitum low-fat, high-carbohydrate diets on body
weight and serum lipids in overweight subjects with metabolic
syndrome. Am J CIin Nut 2002;75: 17-2018. Raben A, Macdonald I, Astrup A. Replacement of dietary fat
by sucrose or starch: effects on 14 d ad libitum energy intake,
energy expenditure and body weight in formerly obese and neverobese subjects. Int J Obes 1997;21: 846-859.
19. Roberts SB. High-glycemic index foods, hunger, and obesity:
is there a connection? Nutr Reu 2000;58:.163-76920. Jenkins DJ,'!íolever TM, Taylor RH, Barker H, Fielden H,
Baldwin JM, Bowling AC, Newman HC, Jenkins AL, Goff DV.
Glycemic index of foods: a physiological basis for carbohydrate
exchange. Am J Clin Nutr 7987;34:362-36621. Roberts SB, McCrory MA, Saltzman E. The influence of
dietary composition on energy intake and body weight. J Am Coll
Nutr 2002; 21: 1405-1455.
22. Jenkins DJA,'Wolever TMS, Buckley G, Lam KY, Giodici S,
Kalmusky J, Jenkins AL, Patten RL, Bird J,'Wong GS, Josse RG.
Low-glycemic index starchy foods in the diabetic diet. Am J Clin
Nutr 1,988; 48: 248-254.
23. Raben A. Should obese patients be counselled to follow a lowglycaemic index diet?. Obes Reu 2002;3:245-25624. Gatenby SJ, Aaron JI, Jack VA, Mela DJ. Extended use of
foods modified in fat and sugar content: nutritional implications
in a free-living female population. Am J ClinNutr 1997;65:.78671873.
25. Veststrate JA, van het
I?ierik EJM, de Graaf C,
'Westerterp-Plantenga
MS,
comparison of the effect of
their full fat equivalents on
Hof KH, van den Berg H, Velthuis-te
Zimmermanns NJH, \Èíesterterp KR,
Verboeket-van de Venne IIPHG- A
free access to reduced fat products or
food intake, body weight, blood lipids
Sugar intakeand body weight S. H. F. VermunteI al. 99
and fat-soluble antioxidants levels and haemostasis variables. Eur
I CIin Nutr t998; 52:389-395.
26. Kirk TR. Role of dietary carbohydrate and frequent eating in
body-weight control. Proc Nutr Soc 2000; 59: 349-358.
27. Drummond S, Kirk T. Assessment of advice to reduce dietary
fat and non-milk extrinsic sugar in a freeJiving male population.
"1.999;2:
1'87-1,97.
Public Heabh Nutr
28. Bolton-Smith C,'Woodward M. Dietary composition and fat
to sugar ratios in relation to obesity. Int J Obes Relat Meub
D isord'1.994; 12: 820-828.
29. Gibson SA. Are high-fat, high-sugar foods and diets conducive
to obesity?Int J Food Sci Nutr 1,996;47:405-415.
30. Macdiarmid JI, Vail A, Cade JE, Blundell JE. The sugar-fat
relationship revisited: differences in consumption between men
and women of varying BMI. lnt J Obes Relat Metab Dkord'1,9981'
22:1,053-7061.
31. Lewis CJ, Park YK, Dexter PB, Yetley EA. Nutrient intakes
and body weights of persons consuming high and moderate levels
of added sugaÍs.J Am Diet Assoc t992;92:708-713.
32. Drewnowski A, Massien C, Louis-Sylvestre J, Fricker J,
Chapelot D, Apfelbaum M. Comparing the effects of aspartame
and sucrose on motivational ratings, taste preferences, and energy
intakes in humans. Am J CIin Nutr 7994; 59: 338-34533. Drewnowski A, Massien C, Louis-Sylvestre J, Fricker J,
Chapelot D, Apfelbaum M. The effects of aspartame versus
sucrose on motivational ratings, taste preferences, and energy
intakes in obese and lean women. lnt J Obes 1994; 18l. 570-578.
34. Rolls BJ, Hetherington M, Laster LJ. Comparison of the
effects of aspartame and sucrose on appetite and food intake.
Appetite 1988; 11: 62-67.
35. King NA, Appleton K, Rogers PJ, Blundell JE. Effects of
sweetness and energy in drinks on food intake following exercise.
Physiol Behau 1999; 66: 37 5-379.
36- Voodend DM, Anderson GH. Effect of sucrose and saf0ower
oil preloads on short term appetite and food intake of young men.
Appetite 2001; 37: 185-195.
37. Holt SH, Sandona N, Brand-Miller JC. The effects of sugarfree vs sugar-rich beverages on feelings of fullness and subsequent
food intake. lnt J Food Sci Nutr 2000; 5L: 59-7'l'38. Lavin JH, French SJ, Read NW. The effect of sucrose- and
aspartame-sweetened drinks on energy intake, hunger and food
choice of female, moderately restrained eaters. Int J Obes 7997;
27:3742.
39. Reid M, Hammersley R. The effects of sucrose on everyday
eating in normal weight men and women. Appetite 1'994;22:227-
23r.
40. Reid M, Hammersley R. The effects of sucrose and maize oil
"l'999
on subsequent food intake and mood. Br J Nutr
; 82: 447 4 5 5 .
41. Green SM, Burley VJ, Blundell JE. Effect of fat and sucrosecontaining foods on the size of eating episodes and energy intake
in lean males: Potential for causing overconsumption. Eur J Clin
Nutr'1,994; 48: 547-5 5 5.
42. Green SM, Blundell JE. Effect of fat- and sucrose-containing
foods on the size of eating episodes and energy intake in lean
dietary restrained and unrestrained females: Potential for causing
overconsnmption. Eur J Clin Nutr 1996; 50: 625-635.
43. Drewnowski A. Intense sweeteners and energy density of
foods: implications for weight control (review). Eur J CIin Nutr
7999; 53:757-763.
44. Porikos KP, Hesser MF, van Itallie TB. Caloric regulation in
normal-weight men maintained on a palatable diet of conventional
foods. Physiol Behau 1982; 29: 293-300 -
@ 2003 The InternationalAssociation for the Study of Obesity. obesity reviews 4, 91 -99