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 t^',b 9 se ! Ëo Ë Ë s E -? $c\t I 9Ë- ï FË _99I f; 6 = ï ; , a Ë ËËg. s E P i _c h 'o = D (D =a= g, q) o.o*9 EÉ G-Q6 =.àHÈ _Ë+È + óË-*- È : Fe ! ;Ë : : 5qï :": Ë r ï r8e 3 ; Ë q E ? . . - z Ír : : = z r _ - @ U) a ! o & Ë3ÈÈÈË= s 3 Ë { { Ë Ë ËË { * ï ï Ë i = = . . - @ b : = = í ) s 5 - q ) - * € E : E Ë E È € E P J g = g P E J I - o = - í ) = 6 í c H E 7 ' à = o :EE E ÉË Ë =_ È 8 g p = S , r Ë Aà; >-=; 3; >= : ' ( o ïEFE3à ) : = = à q . I ! : E E E o , * - - o )K = E F o ; E e Ë FP Ë ËUs á gËE Ë Égs - ë g È E á :* _c ' c') o i Ë i * Ë Ë Ë ÉËËËgËË a q (tt 3 oo E o -o o 6 c -i= GJ E .c (tt q) c o o q) = (t) O) 0) E q) ox LU EËeËËe;egË ï a: ;e; cq ËËt Ë;ËrËEi EË Ëg ,E;E tË Ë s ËE s ó= h =Ë s se Ë:Ë:;EËEË;iEËËgÏ o .9' (t q) o ea o) o E (tr 3 2 v O h d (d o_ o at (D È (U E E + > o í (l) o) :l U) o (r> o Q) c :. - Ë È ' d u (t f< ]C o o o_ -- o o E E E o * U L m ( D à = = N o c) 9 .ó cx g 968 = ot c) c (5 o, U) o -c (, .9 S o(o+ ; $ . n E U) (D f a E Ë 9v. Ë \_,, \ ^ = .9 t1 ! g : ásr^ =.Ho* 9 n i; Bs U' *v s \- cr) (o r o - * ; x cí) í E o 3 '- a -:< O o ' Y J ( 9 _ í 9.É.o' O O o f c D ( U 6 (6 q * o H -E q) x uJ g Íl _6 f.r c : E b à o ; \u o E o) Q) o E ! 5o a E \ l R (D = * e E $ È 6 ! q " l *o @ 2OO3The InternationalAssociation for the Study oí Obesity. obesity reviews 4, 91 -99 Ea ; ó Ë Po 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 g c? = = a U' 0) E oQ EE V gF 8 3 R p E u v 8 9 " " I ó " - Z ó = = - Z E p . v ^ = p ó r c ó = : i = = u ) a = : = = ( D a E o q g È o ^ b 9o . óc ^ à s È ( , o : 9 + = o o Y O s 9 5 a o =: so Ë ó Q < à Ë 3 a (L À ( o' x^ x > = 9 l J o o 6 ; ó Q 3 j 2 i U) () .,o 3 s: i s :ËË : 3j s 3 * ËÈí;:Ë ss3 gËss s r :ï : 3 : Ëa Ë3 si ËeeaEï i ËaEs Ëe E q) E 't o 6 9^ Eq É EÉ Ë i i g : = S i = E i o) '6 o rn Ë ce gE E 6 Ëo Eq F -1 .,8 H . 9 r ::Ë ; 6 Q < àt : i n - x ( o + ë c l a 3 5 n O - - ( r EI D 1 ó r9. E ' ó o- ; r g ! P E = J Ë e * .9 (I) 3 c. ' à - - : 5 .9 fr 6x . | :íid o)à o 3 = P H =: ^ : " , ^ ; o -o o (u $ g 4 | ! .; à i è E - c; Ë = -E c .o o (l) h óa v - U' o o o) 6 o E o o x ul R*!E*.ï*E5;=; = ? ^--) è €_ó 3 =3 ; Y q : P g= E 6 5 o F =Ë - .P ,E = d E c Ë 4 l Z :ePP fs Ë e : È t r \ ( g ) È . Èà ' X è.È'- 5 Q€ gsÈËee.gËËÈce c g) 'o o) 6 E o o- t o- o 6 (tt (L cn CI' E i U' -c o .o o) o_ o ó = c o E c (E r @ s . . . . v r ^ + ^ E o = o B A x : ; ; 3 E Ë Ë S Ë Ë Ë;: *F à9P ë e Ë g Ë s E g E Ë Ë Ë Ë s á ia ? ; 9 a ? È F F s - Cí) -(1)O ):.tr ; ' 8 ï È E QË € -- \ 5 srEe Èrl -o (I' o o U) g, x q) o_ E o o o r E u o- ( q ) E c (D (E o C' o, att (t) l o ó = é @ @ ( 0 at) Ch O) e^ 8or- o o) .F o O) (t, o) -c U' -q) - v ó p o o o -o' l U) 8G -3a F E 'ó'Í ( 3 EË 3r^' o - 5 n :-i E fr 3 Ë -, I , -ó s cY) .J o N o o X (o - ,^ro Y p E^ o 9or 5 P * Ë €r*t a 3 a , , Y 'oo ), 5 3 =à c O g : È l e F Ë b H& Ë È t s g -c ' €) u lr uEr c s: - \ t -ác 3 U' 6 c a o '-E o o_ x UJ (! _g ! 6 F_ à o J (D o o o) o CE 8 r C < o È c : . 6^ d -o).+ ' N c\l Q) \ g - o 8 F- o) N < $ l < $ i Q) ' = ^: 6 .a =lo Ë O 2003 The lnternational Association Íor the Study oÍ Obesity. obesity reviews 4, 91 -99 -= o;i (U o q) F.- o_ .:- ó ^ È = ; i o 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 -^ ., á2 _c .9' o = E o I = a (t (D (r È Ë - \ ] Ë ;E[ ë Ég Ë * Ë Ë : Ê Fs a É Ë { - e ' s gË E9E* " Ë so o3 p = 9 x o o-ïÉ (I'o C'r(|) à g = è ó v oO ( , ;t >,o = b € 9 x Y o - Y E E ; o o i9 €- $È X ó '===u l o E 4 o_ : . € . . : l ' Y ' - . - v H'o ! Íq ,r -y L o . o= F L :. Eo - o f = à : = .Y .. (D 3 i=3 sË: - 6 0 5 E a 3 o g a h 5 > f 9 E q) E -o o X IJ ïl:ËÍË E u i J l o; - Ë c -P - P f o Y . t ' À - Q @ * l E Q = = ËgsÈÈr : = _É. (tt c "9 (t) q) (U E (U Ë : o ! ë Íl 6 .'ï E = E < l (u esting for further study. E z. È - 9 ' o t = \ o- D U' o (D o_ É o o J o) 9 i E ( o o o E I 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- . . .9 (! q) .E Ë Ë ! E E S - - r + Y X ( U o_Yo L - - - C D ^ .s, = sity. On the contrary, a reduction of sugar intake may result 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). d o - ol o o) G c o) E o Several observational studies found an inverse relationship between energy intake from fat and from sugar, but not between fat and starch intake (26). Thus, sugat intake may reduce intake of. Íat simultaneously and subsequently reduce the energy intake, because of the lower-energy den- Ë á: : : Ë á Ë E È I Ë Ë I a population strategy aimed at Preventing overweight and obesiry (25). E $ A u = > È <{ . . . J g U' Control of Íood intake E Appetite,satiety and energy intake u, o o q) (D o, .F o o) U' o .; .o) o .9, q = ) = (t, o -o f r c l c o Q o o ) ! t - c E U) + = n O o O < = E .9 t\ o ) v = È;G E Í 2 4 ë 8 : o .9 ! Lr) N l an @ E O) o .E < o o X LIl (D ID g (l) o lt G (D q) (r 6'c c c\j :' c \ l í ) C ' 0) (D (0 (t U' o = 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. 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