Appetite 51 (2008) 291295

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Appetite
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Research report

A low-energy-dense diet adding fruit reduces weight and energy intake in women
o de Oliveira *, Rosely Sichieri, Renzo Venturim Mozzer Maria Conceic a
de Coletiva, Faculdade de Medicina-FM, Universidade Federal do Amazonas - UFAM, Rua Dr. Martins Santana, Departamento de Sau polis, CEP 69073-270, Manaus-AM, Brazil 1053, Adriano

A R T I C L E I N F O

A B S T R A C T

Article history: Received 8 June 2007 Received in revised form 24 February 2008 Accepted 3 March 2008 Keywords: Energy density Diets Fruit Oats Randomized Clinical trial

This study evaluated the effect of adding fruit or oats to the diet of free-living women on energy consumption and body weight. Fruit and oat cookies had the same amount of ber and total calories ($200 kcal), but differed in energy density. We analyzed data from a clinical trial conducted in a primary care unit in Rio de Janeiro, Brazil. Fortynine women, ages ranging from 30 to 50 years, with body mass index (BMI) > 25 kg/m2, were randomly chosen to add three apples (0.63 kcal/g energy density) or three pears (0.64 kcal/g energy density) or three oat cookies (3.7 kcal/g energy density) to their usual diet for 10 weeks. Fiber composition was similar ($6 g). Statistical analysis of the repeated measures of dietary composition and body weight were analyzed using mixed model procedures. Results showed a signicant decrease in the energy density during the follow-up (1.23 kcal/g, p < 0.04, and 1.29 kcal/g, p < 0.05) for apples and pears, respectively, compared to the oat group. The energy intake also decreased signicantly (25.05 and 19.66 kcal/day) for the apple and pear group, respectively, but showed a small increase (+0.93) for the oat group. Apples and pears were also associated ( p < 0.001) with weight reduction (0.93 kg for the apple and 0.84 for the pear group), whereas weight was unchanged (+0.21; p = 0.35) in the oat group. Results suggest that energy densities of fruits, independent of their ber amount can reduce energy consumption and body weight over time. 2008 Elsevier Ltd. All rights reserved.

Introduction The energy density of various foods is considered a key determinant of energy intake because a greater intake of a lowenergy-dense diet, such as fruits, makes excessive energy intake more difcult (Oliveira, Sichieri, & Moura, 2003). This is not a new idea (Rolls, 2000), but few studies have been conducted on weight management associated with energy density (Rolls, Ello-Martin, & Tohill, 2004; Rolls, Roe, & Meengs, 2004). Energy density refers to the amount of energy in a given weight of food (kcal/g). For the same amount of energy, a greater weight of food can be consumed when the food is low in energy density than when its energy density is high (Rolls, Drewnowski, & Ledikwe, 2005). Moreover, dietary energy density reductions are associated with energy intake reductions, but little is known about inuences on body weight (Ledikwe et al., 2007). Although research has not directly addressed the effects of fruit on energy density, Oliveira et al. (2003) showed, using a randomized intervention, that body weight was reduced by adding

fruit to a diet where energy intake and frequency of meals was controlled (Oliveira & Sichieri, 2004). Fruits add weight to meals without increasing calories, consequently decreasing energy density, energy intake and reducing body weight. Additionally, low-energy-dense diets often are recommended for weight control (Drewnowski, Monsivais, Maillot, & Darmon, 2007), however, weight status has not been clearly shown in free-living men (Ledikwe et al., 2006) or in women. We conducted a randomized one-blind clinical trial with three arms to evaluate the effect of adding three apples or three pears or three oat cookies to the daily intake of overweight middle-aged women to assess the effect of caloric density on body weight, body mass index (BMI) and arm circumference. The amount of ber was similar in the apples, pears or oat cookies, but the cookies had greater energy density compared to the fruits. Subjects and methods Subjects This is a secondary analysis of a clinical trial by Oliveira et al. (2003). Non-smoking women between 30 and 50 years with

* Corresponding author. E-mail address: olivmc@ufam.edu.br (M.C. de Oliveira). 0195-6663/$ see front matter 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.appet.2008.03.001

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M.C. de Oliveira et al. / Appetite 51 (2008) 291295 Table 1 Nutrient composition of supplements Nutrient intakea Fuji apple (300 g)b Energy (kcal) Carbohydrate (g) Protein (g) Total ber (g)* Energy density
a b *

BMI > 25 kg/m2 and minimal hard alcohol consumption, less than three drinks per week, and low physical activity were invited to participate. Women who had a diagnosis of diabetes (fasting glycemia was above 140 mg/dL) or a regular intake of medicine or substances that might alter the metabolism and weight or who disliked apples, pears or cookies were excluded. Women receiving clinical or nutritional advice for weight loss were also excluded. The eligible participants who expressed an interest in participating in this dietary study were asked to attend an orientation session during which conditions, procedures, and interventions were explained. Of 411 eligible women, 49 were randomly assigned to the three treatment groups. A written consent form was obtained from each subject prior to beginning the study. The Ethical Committee of Rio de Janeiro State UniversityUERJ, Brazil, approved the protocol. Diets During a 2-week run-in period, the participants were instructed by a dietician to eat a standardized hypocaloric diet, (55% energy from carbohydrates, 15% from protein, and 30% from fat), aiming at minor weight reduction of approximately 500 g corresponding to an energy restriction of 250 kcal/day according to baseline energy intakes and estimated expenditure (WHO, 1985). Diets were adjusted every 2 weeks according to changes in body weight in three groups, and the differences in energy composition of supplements were compensated by a reduction of rice and beans for energy adjustment. The subjects consumed approximately 2401 389 kcal/day, 2459 464 kcal/day or 2383 31 kcal/day for the apple, pear or oat group, respectively. The energy intake was evaluated by an energy density table (food composition table assembled from USDA, 2001). For each food, the energy density was calculated (kcal/g). Participants were instructed to consume a diet including breakfast, lunch, dinner and three snacks per day for 10 weeks. Those women who attended after the run-in phase were randomly allocated to receive the supplements twice a month in an amount sufcient for their families, and the women were encouraged to eat: three apples (300 g) or three pears (300 g) or three oat cookies (60 g) per day during the follow-up. Each 2 weeks, the participants were instructed to ll out dietary records for 3 consecutive days, including 1 weekend day to evaluate compliance. Weight, height and mid-arm circumference were measured every 2 weeks, according to a standard protocol. The supplements were given every 2 weeks, and participants were instructed to eat them as snacks between the three meals. The oat cookies were equal to the average amount of ber, protein and carbohydrate in the fruits, according to the amount of ber in Brazilian food composition (Mendez, Derivi, Rodrigues, & Fernades, 1995), with different energy density (0.63 for apple, 0.64 for pear and 3.7 for oat cookies). The total energy was adjusted, but the energy density and food volume were not. The diet composition is presented in Table 1.
Table 2 Characteristics of participants at the baseline and energy density of diet

Williams pear (300 g)b 191.6 45.3 1.32 7.32 0.64

Oat cookies (60 g)b 221.1 40.9 1.8 6.46 3.7

188.5 45.7 0.63 6.42 0.63

USDA Nutrient Database for Standard Reference. Amount per day divided into three meals. Fiber by Mendez et al. (1995).

With the addition of supplements, the diet was recalculated by reducing rice and bean for energy adjustment, since they constitute staple foods in Brazil. Registered dietitians evaluated dietary compliance via patient interviews every 2 weeks. Participants received bus tickets to commute to the clinic every 2 weeks to receive the fruits or oat cookies. Statistical analysis The target sample size was 49 women or 16 women per each treatment group. The data was adjusted by 30% for possible participant losses, and analyses were performed on an intentionto-treat basis, considering a 0.95 power to detect an effect on the apple intervention, with a = 0.01 (Pocock, 1988). Fifty-one women were enrolled to adjust for losses, and 49 nished the run-in period. The characteristics and metabolic prole of participants were compared at the baseline, and one-way analysis of variance was used. Mixed models for repeated measures were applied, performed with the statistical software program SAS1 (Statistical Analysis System v.8.2, 2000) to account for repeated measurements. Models included an interaction variable between the 3-class treatment and time of follow-up. The magnitude of change and treatment in this modeling is given by the b coefcient associated with the interaction term. Baseline weight, height, BMI, energy intake and caloric density value were obtained by averaging the rst fasting measurement with the post run-in measurement. Results Of 411 of the women screened, 51 (12%) started the run-in phase and 49 were further randomly assigned to treatment. Fifteen participants discontinued the study for personal reasons and job commitments. The demographic health status at the baseline, such as body weight, BMI, mid-arm circumference and energy intake of participants showed no differences. However, among the apple group, participants were younger, and as expected the oat group

Apple (n = 16) Mean Age (years) BMI (kg/m2) Body weight (kg) Mid-arm circumference (cm) Energy intake (kcal) Energy density of supplement plus other fruits in the diet (kcal/g) 41.6 32.0 77.3 35.45 2,401 1.67a
a

Pear (n = 16) S.D. 6.4 4.9 10.8 3.52 389 1.14 Mean 44.2 31.7 79.7 35.46 2,459 1.72a
b

Oat cookie (n = 17) S.D. 5.1 4.2 12.9 3.15 464 1.25 Mean 46.2 31.9 78.7 35.08 2,380 2.2b
b

S.D. 4.6 3.3 8.5 2.46 31 1.31

Superscript letters (a and b) denote one-way analysis of variance (ANOVA) for baseline values with different letters, p < 0.05.

M.C. de Oliveira et al. / Appetite 51 (2008) 291295 Table 3 Means and standard deviation (S.D.) of weight change in kg and mean change of caloric density during follow-up of the diets adding apple, pear or oat Weekends 0 Sample size Apple (ED = 0.63) Pear (ED = 0.64) Oat (ED = 3.70) Energy densitya,b Apple Pear Oat Weighta,c Apple Pear Oat
a b c

293

15 16 17

15 14 13

15 14 12

14 13 11

14 14 9

13 13 7

1.67 (1.14) 1.72 (1.25) 2.12 (1.31)

1.93 (1.20) 1.62 (1.51) 2.99 (1.89)

1.49 (1.15) 0.99 (0.85) 1.72 (1.00)

0.81 (0.38) 1.17 (0.93) 2.20 (1.67)

1.23 (0.87) 0.91 (0.38) 1.94 (1.30)

1.52 (1.20) a 1.45 (1.15) a 3.12 (2.02) b

77.25 (10.75) 79.41 (12.89) 78.74 (8.4)

75.62 (10.18) 77.63 (10.9) 79.45 (9.23)

75.41 (10.22) 77.62 (10.9) 78.73 (9.95)

75.77 (10.92) 77.72 (10.85) 78.58 (9.73)

76.06 (10.93) 77.53 (11.54) 78.30 (8.56)

75.93 (11.35) a 77.24 (11.47) a 78.01 (9.15) a

Repeated measurement analysis (proc mixed in SAS1) adjusted for baseline age and treatment. One-way ANOVA comparing the three diets at the end of the study (diet time); alpha = 0.05; F = 3.86; Pr > F = 0.032; R2 = 0.20 or 20% (variance explain). One-way ANOVA comparing the three diets at the end of the study (diet time); alpha = 0.05; F = 0.000; Pr > F = 0.99; R2 = 0.0002.

showed a higher energy density of diet when compared with fruit groups (Table 2). A one-way ANOVA statement was made to evaluate body weight and energy density differences among groups at post timing (week = 7). The results showed signicant differences for energy density ( p > 0.05) in women receiving fruits compared to oat cookies. The R2 (variance explained) was 0.20 or 20% of explication power. However, any differences were shown for body weight at post time among groups conrmed by R2 of 0.0002 or 0.02% (Table 3). The energy density of meals signicantly reduced daily energy intake and body weight for participants consuming fruits using linear test. Thus, post treatment period, the energy intake decreased signicantly for apples (25.05 kcal, p < 0.001) and pears (19.66 kcal, p < 0.01). Also, the energy density showed signicant decreases during the follow-up (1.23 kcal/g, p = 0.04, and 1.29 kcal/g, p = 0.05) for apples and pears, respectively (Table 4). Conversely, the oat cookies were ineffective in reducing energy intakes (Fig. 1) and body weight (Fig. 2). A greater decrease in energy density (kcal/g of food) and total energy intake (kcal) was observed for the rst 2 months of follow-up in the fruit groups. Nonetheless, those consuming them as snacks between the three meals a normal diet with added fruits decreased their body weight (0.92 kg of body weight, p = 0.0001 for apple and 0.84 kg of body weight, p = 0.0004 for pear group) after 10 weeks, compared to the group with oat cookies added to the diet, when

adjusted means by age and type of treatment, while the oat group suggested a non statistically signicant increase in body weight (+0.21 kg of body weight, p = 0.35). The mid-arm circumference not showed effect for the apple group (0.22 cm p = 0.20) however showed statistically signicant differences (0.49 cm, p = 0.01) for the pear group (Table 4). The BMI, after adjusted for age and type of treatment showed signicant differences for fruit groups (0.39, p = 0.0001 for apple and 0.34, p = 0.0006 for apple); however, the oat cookie group seems to increase (+0.005, p = 0.40 for oat) but these changes were not statistically signicant (Table 4). Our data clearly showed the body weight difference between before and after fruit treatment: 77.25 10.875.93 11.35 kg/three apple per day (1.70%); 79.41 12.8977.24 11.35 kg/three pear per day (2.73%) and 78.74 8.478.01 9.10 kg/three oat per day (0.93%), adjusted by age and type of treatment (Table 3 and Fig. 2). Then, after 10 weeks, the body weight decreased by approximately 1.32 kg; 2.17 kg and 0.73 kg for apple, pear and oat cookie groups, respectively. These differences were statistically signicant for apple and pear when compared with the oat group. Discussion This analysis showed that caloric density affects calorie intake, and consequently the body weight when fruits are added to diet. The same serving weight of apple (300 g) and pear (300 g) per day added to the diet decreased the energy density. In contrast, when

Table 4 Mean change in anthropometric measures, energy intake, and estimated energy density during 7-week of addition of apple (300 g) or oat cookies (60 g) to three daily meals Apple Pear p Oat cookies p

b
Treatment effect in follow-up Energy density (kcal/g)
a

b
1.19 0.068 19.66 0.84 0.49 0.34

b
0

1.23 0.028 25.05 0.92 0.22 0.39

0.04

0.05

Pos timing treatment groups Energy density (kcal/g) Energy intake (kcal/day) Body weight (kg) Mid-arm circumference (cm) BMI (kg/m2)

0.92 0.001 0.0001 0.20 0.0001

0.03 0.01 0.0004 0.01 0.0006

0.14 +0.69 +0.21 +0.007 +0.005

0.66 0.92 0.35 0.96 0.40

Mixed models linear procedure adjusted by age and type of supplement. a Linear test. Low-energy-density effects. b Linear test. Post time fruits group treatments.

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M.C. de Oliveira et al. / Appetite 51 (2008) 291295

Fig. 1. Caloric density and energy intake changes during the follow-up by addition of apples and pears. Mixed model (adjusted by age, type of supplement). Linear test. Post time fruits group treatments using procedures SAS1. (*) Caloric density kcal/ g, (lines), p < 0.02 apples plus fruits and p < 0.04 pears plus fruits. (**) Energy intake kcal, (bars), p < 0.001 and p < 0.01 apple and pear groups, respectively.

Fig. 2. Caloric density and body weight changes during the follow-up by addition of apples and pears. Mixed model (adjusted by age, type of supplement) procedure SAS1. Linear test. Post time fruits group treatments. (*) Caloric density kcal/g, (lines), p < 0.02 apples plus fruits and p < 0.04 pears plus fruits. (**) Body weight kg, (bars), p < 0.0001 and p < 0.0004 apple and pear group, respectively.

oat, with an equivalent amount of ber is added, high caloric density is achieved. Fruits are composed of a high percentage of water. Consequently, as water is an important component of lowenergy-density meals and among macro and micronutrients, fruits have a higher impact on energy density (Rolls & Bell, 2000). In the present study, it was possible to change energy intake and body weight through fruits compared with oat cookies, which are very low in water. Fruits are lower in energy density compared with oat, but the macronutrient quantities were xed. Ledikwe et al. (2007) examined how 6-month energy density changes reduced body weight following 658 prehypertensive and hypertensive persons randomly assigned to three groups with differences in energy density. Furthermore, Bell, Castellanos, Pelkman, Thorwart, and Rolls (1998) evaluated average-weight women provided with meals for 2 days. During lunch, dinner, and an evening snack, subjects were given free access to a main entree varying in energy density (low, medium, or high). The researchers concluded that the energy

density affects energy intake independent of macronutrient content or palatability, suggesting that the overconsumption of high-fat foods may be due to their high energy density rather than to their fat content. Further, Rolls, Bell, and Thorwart (1999) showed that adding water to the ingredients with high caloric density was associated with reduced intake in lean women, and the addition of water affect the energy density of the preloads and the volume of food consumption. In addition, Yao and Roberts (2001) reviewed and summarized published studies, suggesting that the energy density is an important determinant of energy intake and regulation. Energy density could have a signicant inuence on the energy intake, even when individuals are informed about the energy density of their meals, as cited by Kral, Roe, and Rolls (2002). Therefore, lowdensity diets promote moderate weight loss in long-term studies (Cox et al., 2007; Yao & Roberts, 2001) but more long-term studies will be required to make clear recommendations regarding dietary composition to aid in decreasing energy intake or body weight. Although oat has a signicant amount of soluble ber or total ber, it was not effective in reducing the energy density and total energy intake, nor was it effective in decreasing body weight in this study. Saltzman et al. (2001) also concluded that use of a cereal rich in soluble ber in a closely monitored hypocaloric regimen does not improve body weight loss. In the present study, weight loss and reduced BMI was not different within the fruit groups, but was statistically different compared with the oat group in the follow-up. The apple group reduced 0.93 kg of body weight, and the pear group reduced 0.84 kg suggesting that fruits could affect hunger and satiety (Leathwood & Pollet, 1988). However, satiety was not accessed in our study. Therefore, a large portion of a low-energy-density food at the start of a meal may be an effective strategy for weight management (Rolls, Ello-Martin, et al., 2004; Rolls, Roe, et al., 2004). Furthermore, Barclay (2007) followed 97 obese women, who were randomized to groups counseled either to reduce fat intake (reduced in Fat group) or to reduce fat intake and increase intake of water-rich foods, particularly fruit and vegetables (reduced in Fat + Fruits and Vegetable group). Patients in the reduced in Fat + Fruits and Vegetable group, lost a third more weight in 6 months compared to those who only decreased their fat intake. Our results provide sound evidence to raise the currently recommended amount of fruit in the daily diet. These ndings could be important for nutritional counselors advising patients on weight management through a diet containing additional lower energy density fruits, such as apples and pears, since the lower energy density contributes to overall lower energy intake and, therefore, higher weight loss. However, further follow-up studies will be needed to conrm these results as well as to elaborate on their implications. Acknowledgements Sponsorship: Brazilian manufacturer Association of Apple ABPM; Policlinica Piquet Carneiro; Institute of Social Medicine IMS, Rio de Janeiro State UniversityUERJ; Federal University of o de AperAmazon; Pedro Ernesto Hospital; Coordenac a vel SuperiorCAPES. feic oamento de Pessoal de N

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