http://informahealthcare.com/ijf ISSN: 0963-7486 (print), 1465-3478 (electronic) Int J Food Sci Nutr, 2014; 65(7): 899–902 ! 2014 Informa UK Ltd. DOI: 10.3109/09637486.2014.931359
STUDIES IN HUMANS
A Mediterranean-like breakfast affects energy intake and appetite-related feelings Mary Yannakoulia, Dora Aggelopoulou, Katerina Skenderi, Stella Koinaki, and Nikolaos Yiannakouris Department of Nutrition and Dietetics, Harokopio University, Athens, Greece
Abstract
Keywords
Energy intake and appetite feelings after the consumption of two different types of breakfast, a high-fiber, traditional, Mediterranean-type breakfast and a low-fiber, Western-type breakfast were compared. Sixteen non-obese young men received the two treatments on separate days: the Mediterranean- and the Western-type breakfasts were isocaloric, similar in volume and macronutrient content, but different in fiber content. Following a 4-hour fast, subjects offered an ad libitum lunch. Food consumed and subjective feelings of hunger, fullness, and desire to eat were evaluated. Energy intake in the ad libitum lunch was significantly lower after the Mediterranean-type, compared to the Western-type breakfast, adjusting for previous day’s energy intake (1488 ± 468 versus 1674 ± 416 kcal, respectively), whereas no energy compensation was made throughout the day. Furthermore, those who had the Mediterranean-type breakfast reported lower values in the desire to eat during study’s course. These findings propose a fulfilling effect of a traditional, Mediterranean, high in fiber breakfast.
Appetite control, energy balance, fiber, Mediterranean diet, obesity
Introduction Satiety and food intake in humans are influenced by a number of factors related to the individual, the food or the environment. Among others, the macronutrient content of the food has received great attention so far. A hierarchy has been established for the satiating efficacies of proteins, carbohydrates and lipids, with proteins being considered more satiating than carbohydrates and carbohydrates more satiating than lipids (Anderson & Woodend, 2003; Soenen & Westerterp-Plantenga, 2008). The effect of fiber has also been extensively explored. In general, fiber or fibercontaining foods are considered as promoting satiety, operating through several physiologic mechanisms, and thus may suppress energy intake and reduce the risk of obesity (Burton-Freeman, 2000). However, there is also evidence of no effect or an opposite effect on energy intake (Clark & Slavin, 2013). The fact that the results of the studies are variable and, partly inconsistent may be due to use of the different types of fiber (soluble versus insoluble) and/or of a variety of food sources of fiber (different types of cereals, fruits and vegetables), or to the modulating effect of other food or non food-related factors (Burley et al., 1987; Delargy et al., 1997; Porikos & Hagamen, 1986). Current research in nutrition tends to move from nutrients and foods to dietary patterns, i.e. to the combination of foods with complex combinations of nutrients (Hu, 2002). This may also apply to the study of appetite/satiety. The effect of a single nutrient may be too small to detect, but the cumulative effects of several nutrients included in a meal or a dietary pattern may be sufficiently large to be detectable. Intercorrealations and/or Correspondence: Mary Yannakoulia, PhD, Department of Nutrition and Dietetics, Harokopio University, El. Venizelou 70, Athens 17671, Greece. Tel: +30 210 9549175. Fax: + 30 210 9549141. E-mail: [email protected]
History Received 8 January 2014 Revised 20 May 2014 Accepted 2 June 2014 Published online 10 July 2014
interactions between nutrients in different foods should also be taken into account and the collinearity of nutrients and/or foods be used as an advantage. Under the perspective of dietary patterns, Mediterranean diet has been investigated in relation its health effects, including obesity and energy balance. Cross-sectional and longitudinal studies have revealed a protective role in overweight and obesity (Mendez et al., 2006; Panagiotakos et al., 2006; Schroder et al., 2004) or no effect (Rossi et al., 2008; SanchezVillegas et al., 2006; Trichopoulou et al., 2005; Yannakoulia et al., 2009). Buckland et al. (2008) in their review concluded that although the results so far have been inconsistent, the evidence points towards a possible role of the Mediterranean diet in preventing overweight. The main physiological mechanisms proposed for this protective role are the increased satiety and satiation that this pattern induces, due to its fiber content, the prolonged mastication, the increased gastric detention and the enhanced release of cholecystokinin, as well as its low glycemic load and low-energy density (Buckland et al., 2008; Schroder, 2007). However, no investigation has been undertaken to evaluate the effect of a Mediterranean dietary pattern, rich in fiber on satiety indices. In the present study, the effects of a high-fiber, traditional, Mediterranean-type breakfast on energy intake and the feelings of hunger, fullness and desire to eat were compared to one of a low-fiber, common Western-type breakfast.
Methods Study participants Sixteen healthy, non-obese (BMI 530 kg/m2) young men completed the study (Table 1). Smokers, professional athletes, restrained eaters (as this was evaluated using the Dutch Eating Behavior Questionnaire and a total score 42.5 (van Strien et al., 1986)), those who reported slimming or any other dietary regime,
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Int J Food Sci Nutr, 2014; 65(7): 899–902
and/or great body weight fluctuations during the last 2 months (change of 42 kg) were excluded from participation. Also, subjects who were not breakfast-eaters, were on medication that may had an impact on appetite and sensory functioning or who reported a metabolic or endocrine disease, gastrointestinal disorders, or a history of medical or surgical events possibly affecting study outcomes were not included. Potential participants were informed that the purpose of the project was to investigate the impact of dietary composition on blood lipids (sham); the true purpose of the study was not revealed to them to decrease potential reactivity associated with preconceived notions regarding the effect of specific food items or nutrients on appetite. All participants reported usual lifestyle and dietary habits and a stable body weight for at least 3 months before the study. They gave their written informed consent before participating in any aspect of the investigation. Approval for the study was obtained from the Ethics Committee of Harokopio University. The study took place in the Metabolic Unit of the Department of Nutrition and Dietetics, Harokopio University. Study design The experiment had a crossover design. Each subject received 2 treatments on separate days, with a washout period of two weeks between treatments, in a random order. The treatments were the two isocaloric breakfasts (Mediterranean-type and Western-type), which were similar in their volume and macronutrient content, quite similar in the food sources of nutrients, but they were different in the dietary fiber content. The Mediterranean-type breakfast was based on the traditional Cretan diet, as this was revealed in the Seven Countries Study and other studies and it evaluated and analyzed recently (Kafatos et al., 2000). This breakfast provided 14.9 g of dietary fiber and consisted of 30 g (1 slice) Cretan Graviera cheese (a traditional, Gruye`re-type cheese), 60 g (1 big) barley-made, Cretan rusk, 260 g (1 big) fresh peeled orange and 2.5 cups of water; the Western-type breakfast provided 0.7 g of fiber and consisted of 30 g white bread, 5 g (1 teaspoon) butter, 14 g (2 teaspoons) honey, 366 g (1.5 cup) semi-skimmed milk (1.5% fat) and 244 g (1 cup) orange juice. The energy and macronutrient contents of the two breakfasts are presented in Table 1. The participants were instructed to eat and drink the same foods the evening before a test day and to record this dietary intake in a diary, as well as to abstain from excess exercise. After an overnight fast (nothing to eat or drink except for water after 22:00 h), they came to the Metabolic Unit. A member of the research team made all the anthropometric measurements and interviewed the participants for previous day’s dietary intake (24-h recall). Body weight, height and waist circumference were Table 1. Energy and macronutrient composition of the two treatments (breakfasts). Mediterranean-type breakfast Fluid volume, ml Energy, kcal Proteins, g % energy intake Carbohydrates, g % energy intake Lipids, g % energy intake Dietary fiber, g
625 465
Western-type breakfast 625 456
17.5 15.1
16.5 14.5
73.3 63.1
74.2 65.1
11.0 21.8 14.9
10.7 21.1 0.7
measured, and Body Mass Index (BMI) was calculated as weight (in kilograms) divided by height (in meters squared). Then, they had to consume one of the two treatments (breakfasts) in 10 min. They were not allowed to eat or drink anything for 4 hours, and they refrained from doing any physical activity. At the end of this time period, they received a buffet-style ad libitum lunch, consisting of standard Greek food items (pasta, tomato sauce, beef, salad, cheese, yogurt, fruit, chocolate). They were instructed to eat until they were satiated, within 30 min. To prevent habitual intake, foods were provided in excess amounts and participants had to serve themselves the quantities they wanted to eat. Food quantities served were weighted as well as any leftovers, in order to estimate dietary intake in the ad libitum meal. The day after the experiment, participants were asked through a telephone call to recall their food intake during the rest of the experimental day. Nutritional analyses For the analysis of the dietary intake, in terms of energy and macronutrient intake, the Nutritionist Pro, version 2.2 software (Axxya Systems-Nutritionist Pro, Stafford, TX) was used. The software food database was expanded by the analyses of traditional Greek foods and recipes as well as information provided by food companies. For the determination of participants’ usual caffeine intake the caffeine content from the various foods and beverages included in the FFQ was calculated using information from the United States Department of Agriculture National Nutrient Database for Standard Reference (U.S. Department of Agriculture, 2010) as well as the food industry. Appetite feelings assessment Before breakfast consumption, just after that and, then, every 30 min till the ad libitum lunch buffet participants filled out three 10-point Visual Analogue Scales (VAS) for the evaluation of their subjective feelings of hunger, fullness, and desire to eat, respectively (Figure 1). Each VAS scale was 10 cm in length and subjects recorded their respective ratings by marking a point on the scale that best described their feeling at each time point. VAS ratings are a reliable tool for appetite assessment (Flint et al., 2000) and they have been consistently used in the relevant research (Blom et al., 2006; Gavrieli et al., 2011). Statistical analysis Descriptive characteristics of the study participants are presented as means ± standard deviations. Energy intakes between the two treatments were compared using analysis of variance (ANOVA), or analysis of covariance (ANCOVA), adjusting for potential confounders. ANCOVA (subject as the covariate) for repeated measures was used to compare the response curves of VAS scores after the 2 treatments over time.
Results The baseline characteristics of the study participants are shown in Table 2. Previous day’s dietary energy intake was not statistically different between the two treatments and the same was also true for the macronutrient intake. A significant difference between the two treatments during the study’s course was found for the Desire to eat (p ¼ 0.016). The ratings dropped just after breakfast consumption and then they were steadily increasing, with those who had the Mediterraneantype breakfast exhibiting lower values. The analysis by time points revealed that at 150, 180, 210 and 240 min the differences between the two treatments were statistically significant (p50.05). Furthermore, although consumption of the
Breakfast and energy intake
DOI: 10.3109/09637486.2014.931359
901
Table 2. Baseline characteristics of the study participants. Mean ± standard deviation (range) Age, years Weight, kg Body Mass Index, kg/m2 Waist circumference, cm Total score in the Dutch Eating Behavior Questionnaire (0–5)
25 ± 4 78.0 ± 5.6 24.1 ± 1.6 82.0 ± 4.5 2.2 ± .0.3
(19–33) (67.6–88.0) (21.5–27.9) (75.5–91.0) (1.6–2.5)
Table 3. Energy intake of the study participants (mean ± standard deviation) following breakfast consumption. Energy intake, kcal Previous day (before the experiment) Ad libitum meal Rest of the day Total day (excluding breakfast intake)
Mediterranean-type Western-type breakfast breakfast
p
p*
2730 ± 1126
2505 ± 886
0.536
1488 ± 468 1082 ± 490 2524 ± 602
1674 ± 416 1229 ± 514 2903 ± 669
0.246 0.045 0.420 0.296 0.109 0.004
*After adjustment for previous day’s energy intake.
that, when participants had the Mediterranean-type breakfast, compared to the Western-type one, their mean energy intakes were higher, but these differences did not reach statistical significance (p ¼ 0.246, 0.420 and 0.109, respectively). However, when taking into account the previous day’s energy intake, both the ad libitum and the total energy intake between the two treatments became statistically significant (p ¼ 0.045 and 0.004, respectively) (Table 3). In specific, participants consumed 251 kcal less during the ad libitum meal after the Mediterraneantype breakfast and 429 kcal less during the total day. No differences were found between the two treatments in the macronutrient contribution to the energy intake.
Discussion
Figure 1. Changes in appetite ratings [hunger, fullness, and desire to eat Visual Analogue Scales (VAS)], after breakfast consumption. Data are presented as means ± SE. Med-Breakfast: Mediterranean-type breakfast; West-Breakfast: Western-type breakfast.
Mediterranean-type breakfast was followed by lower ratings for the hunger and higher for the fullness scales, compared to the consumption of the Western-type breakfast, the between-subjects effects for both scales did not reach a statistical significance (p ¼ 0.193 and 0.281, respectively). Nutritional analysis of the ad libitum meals, the dietary intakes during the rest of the day and the total day (i.e. the sum of the intake during the ad libitum meal and the rest of the day) revealed
A significantly lower energy intake was found in the ad libitum lunch after the consumption of the Mediterranean-type breakfast, compared to the Western-type breakfast, when previous day’s dietary intake was taken into account. The observed effect was evident in meal following breakfast and no compensation was made throughout the day, as total energy intake was also different between the two treatments. Furthermore and in support to the energy-related findings, the desire to eat ratings (a measure of subjective feelings of appetite) were significantly lower following the consumption of the Mediterranean, compared to the consumption of the Western-type breakfast. Lunch and other conditions were identical for the two experimental days, suggesting that the reported findings were a spontaneous response to the treatment taken, i.e. the breakfast eaten. Participants had not been informed about the purpose of the study or that their food intake during lunchtime was recorded, in order to minimize any participant bias. We speculate that most of this effect comes from the fiber content of the Mediterranean-type breakfast (15 g versus 1 g of fiber in the Western-type breakfast), but we cannot exclude the possibility that other factors may also operate, including intercorrelations between nutrients contained in the specific foods chosen. Foods rich in dietary fiber might promote satiation through prolonged mastication, and this was a common comment, or sometimes complaint, reported from the participants in this study, when they had the Mediterranean-type breakfast. Prolonged
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mastication may suppress appetite (Cassady et al., 2009; Hetherington & Boyland, 2007), though neural activation of central satiety centers, increases in saliva, gastric acid production and, thus, gastric distension, as well as through increase in the release of cholecystokinin or other gastrointestinal satiety peptides (Sakata et al., 2003). Along with the fiber content, it may be the glycemic index of the Mediterranean type breakfast that may contribute to the effect on appetite and food intake. Previous evidence suggests that lunch intake is significantly lower and hunger ratings significantly greater after a low glycemic index breakfast compared to the corresponding values after a high glycemic index breakfast in preadolescents children (Warren et al., 2003). In the present study, the effect of a Mediterranean-like pattern on energy balance was evaluated using an ad libitum test meal. It constitutes a reproducible method for measuring spontaneous energy intake; although its reproducibility is not influenced by prior diet standardization, prior diet standardization may exert a significant effect on the ad libitum energy intake (Gregersen et al., 2008). This was also evident in our analysis. Despite the fact that an effort had been made to instruct subjects to have similar food intake the days preceding the experiments and there was no difference in energy intake between the two experiments in the day before the trial, the trend for significance for the energy intake values in the ad libitum meal became a statistically significant finding after adjusting for previous day’s energy intake. Furthermore, in this study we report the acute effects; evidence will also be needed for a sustained effect with continuous consumption of the meal, in order to examine potential adaptation through compensatory mechanisms (EFSA Panel on Dietetic Products Nutrition and Allergies, 2012). Changes in certain biochemical markers related to appetite would also provide useful insight on the underlying mechanisms. Finally, rating of the two meals for taste, appearance, and volume is important for applying these results into modern lifestyles. In conclusion, a Mediterranean-type breakfast, characterized by high fiber content, through consumption of whole-grain cereals and fruits, was found to have a beneficial effect on energy intake and on the subjective feelings of the desire to eat in young nonobese men. Thus, the results of this clinical trial support epidemiological evidence on the anti-obesogenic effect of the Mediterranean diet and call for further trials in other age and/or sex groups, other populations as well as for replication of these findings in long-term interventional studies.
Acknowledgements The authors would like to thank Ms. Antigone Tsiafitsa for her technical assistance.
Declaration of interest The authors have no conflicts of interest.
References Anderson GH, Woodend D. 2003. Effect of glycemic carbohydrates on short-term satiety and food intake. Nutr Rev 61:S17–S26. Blom WA, Lluch A, Stafleu A, Vinoy S, Holst JJ, Schaafsma G, Hendriks HF. 2006. Effect of a high-protein breakfast on the postprandial ghrelin response. Am J Clin Nutr 83:211–220. Buckland G, Bach A, Serra-Majem L. 2008. Obesity and the Mediterranean diet: a systematic review of observational and intervention studies. Obes Rev 9:582–593. Burley VJ, Leeds AR, Blundell JE. 1987. The effect of high and low-fibre breakfasts on hunger, satiety and food intake in a subsequent meal. Int J Obes 11:87–93. Burton-Freeman B. 2000. Dietary fiber and energy regulation. J Nutr 130: 272S–275S.
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Cassady BA, Hollis JH, Fulford AD, Considine RV, Mattes RD. 2009. Mastication of almonds: effects of lipid bioaccessibility, appetite, and hormone response. Am J Clin Nutr 89:794–800. Clark MJ, Slavin JL. 2013. The effect of fiber on satiety and food intake: a systematic review. J Am Coll Nutr 32:200–211. Delargy HJ, O’sullivan KR, Fletcher RJ, Blundell JE. 1997. Effects of amount and type of dietary fibre (soluble and insoluble) on short-term control of appetite. Int J Food Sci Nutr 48:67–77. EFSA Panel on Dietetic Products Nutrition and Allergies. 2012. Guidance on the scientific requirements for health claims related to appetite ratings, weight management, and blood glucose concentrations. EFSA J 10:2604. Flint A, Raben A, Blundell JE, Astrup A. 2000. Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes Relat Metab Disord 24:38–48. Gavrieli A, Yannakoulia M, Fragopoulou E, Margaritopoulos D, Chamberland JP, Kaisari P, Kavouras SA, Mantzoros CS. 2011. Caffeinated coffee does not acutely affect energy intake, appetite, or inflammation but prevents serum cortisol concentrations from falling in healthy men. J Nutr 141:703–707. Gregersen NT, Flint A, Bitz C, Blundell JE, Raben A, Astrup A. 2008. Reproducibility and power of ad libitum energy intake assessed by repeated single meals. Am J Clin Nutr 87:1277–1281. Hetherington MM, Boyland E. 2007. Short-term effects of chewing gum on snack intake and appetite. Appetite 48:397–401. Hu FB. 2002. Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol 13:3–9. Kafatos A, Verhagen H, Moschandreas J, Apostolaki I, Van Westerop JJ. 2000. Mediterranean diet of Crete: foods and nutrient content. J Am Diet Assoc 100:1487–1493. Mendez MA, Popkin BM, Jakszyn P, Berenguer A, Tormo MJ, Sanchez MJ, Quiros JR, et al. 2006. Adherence to a Mediterranean diet is associated with reduced 3-year incidence of obesity. J Nutr 136: 2934–2938. Panagiotakos DB, Chrysohoou C, Pitsavos C, Stefanadis C. 2006. Association between the prevalence of obesity and adherence to the Mediterranean diet: the ATTICA study. Nutrition 22:449–456. Porikos K, Hagamen S. 1986. Is fiber satiating? Effects of a high fiber preload on subsequent food intake of normal-weight and obese young men. Appetite 7:153–162. Rossi M, Negri E, Bosetti C, Dal Maso L, Talamini R, Giacosa A, Montella M, et al. 2008. Mediterranean diet in relation to body mass index and waist-to-hip ratio. Public Health Nutr 11:214–217. Sakata T, Yoshimatsu H, Masaki T, Tsuda K. 2003. Anti-obesity actions of mastication driven by histamine neurons in rats. Exp Biol Med (Maywood) 228:1106–1110. Sanchez-Villegas A, Bes-Rastrollo M, Martinez-Gonzalez MA, SerraMajem L. 2006. Adherence to a Mediterranean dietary pattern and weight gain in a follow-up study: the SUN cohort. Int J Obes (Lond) 30:350–358. Schroder H. 2007. Protective mechanisms of the Mediterranean diet in obesity and type 2 diabetes. J Nutr Biochem 18:149–160. Schroder H, Marrugat J, Vila J, Covas MI, Elosua R. 2004. Adherence to the traditional mediterranean diet is inversely associated with body mass index and obesity in a spanish population. J Nutr 134: 3355–3361. Soenen S, Westerterp-Plantenga MS. 2008. Proteins and satiety: implications for weight management. Curr Opin Clin Nutr Metab Care 11: 747–751. Trichopoulou A, Naska A, Orfanos P, Trichopoulos D. 2005. Mediterranean diet in relation to body mass index and waist-to-hip ratio: the Greek European Prospective Investigation into Cancer and Nutrition Study. Am J Clin Nutr 82:935–940. U.S. Department of Agriculture, Agricultural Research Service. 2010. USDA National Nutrient Database for Standard Reference, Release 23. Van Strien T, Frijters JER, Bergers GPA, Defares PB. 1986. The DEBQ for assessment of restrained, emotional and external eating behaviour. Int J Eat Disord 5:295–315. Warren JM, Henry CJ, Simonite V. 2003. Low glycemic index breakfasts and reduced food intake in preadolescent children. Pediatrics 112:e414–e419. Yannakoulia M, Panagiotakos D, Pitsavos C, Lentzas Y, Chrysohoou C, Skoumas I, Stefanadis C. 2009. Five-year incidence of obesity and its determinants: the ATTICA study. Public Health Nutr 12:36–43.
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STUDIES IN HUMANS
A Mediterranean-like breakfast affects energy intake and appetite-related feelings Mary Yannakoulia, Dora Aggelopoulou, Katerina Skenderi, Stella Koinaki, and Nikolaos Yiannakouris Department of Nutrition and Dietetics, Harokopio University, Athens, Greece
Abstract
Keywords
Energy intake and appetite feelings after the consumption of two different types of breakfast, a high-fiber, traditional, Mediterranean-type breakfast and a low-fiber, Western-type breakfast were compared. Sixteen non-obese young men received the two treatments on separate days: the Mediterranean- and the Western-type breakfasts were isocaloric, similar in volume and macronutrient content, but different in fiber content. Following a 4-hour fast, subjects offered an ad libitum lunch. Food consumed and subjective feelings of hunger, fullness, and desire to eat were evaluated. Energy intake in the ad libitum lunch was significantly lower after the Mediterranean-type, compared to the Western-type breakfast, adjusting for previous day’s energy intake (1488 ± 468 versus 1674 ± 416 kcal, respectively), whereas no energy compensation was made throughout the day. Furthermore, those who had the Mediterranean-type breakfast reported lower values in the desire to eat during study’s course. These findings propose a fulfilling effect of a traditional, Mediterranean, high in fiber breakfast.
Appetite control, energy balance, fiber, Mediterranean diet, obesity
Introduction Satiety and food intake in humans are influenced by a number of factors related to the individual, the food or the environment. Among others, the macronutrient content of the food has received great attention so far. A hierarchy has been established for the satiating efficacies of proteins, carbohydrates and lipids, with proteins being considered more satiating than carbohydrates and carbohydrates more satiating than lipids (Anderson & Woodend, 2003; Soenen & Westerterp-Plantenga, 2008). The effect of fiber has also been extensively explored. In general, fiber or fibercontaining foods are considered as promoting satiety, operating through several physiologic mechanisms, and thus may suppress energy intake and reduce the risk of obesity (Burton-Freeman, 2000). However, there is also evidence of no effect or an opposite effect on energy intake (Clark & Slavin, 2013). The fact that the results of the studies are variable and, partly inconsistent may be due to use of the different types of fiber (soluble versus insoluble) and/or of a variety of food sources of fiber (different types of cereals, fruits and vegetables), or to the modulating effect of other food or non food-related factors (Burley et al., 1987; Delargy et al., 1997; Porikos & Hagamen, 1986). Current research in nutrition tends to move from nutrients and foods to dietary patterns, i.e. to the combination of foods with complex combinations of nutrients (Hu, 2002). This may also apply to the study of appetite/satiety. The effect of a single nutrient may be too small to detect, but the cumulative effects of several nutrients included in a meal or a dietary pattern may be sufficiently large to be detectable. Intercorrealations and/or Correspondence: Mary Yannakoulia, PhD, Department of Nutrition and Dietetics, Harokopio University, El. Venizelou 70, Athens 17671, Greece. Tel: +30 210 9549175. Fax: + 30 210 9549141. E-mail: [email protected]
History Received 8 January 2014 Revised 20 May 2014 Accepted 2 June 2014 Published online 10 July 2014
interactions between nutrients in different foods should also be taken into account and the collinearity of nutrients and/or foods be used as an advantage. Under the perspective of dietary patterns, Mediterranean diet has been investigated in relation its health effects, including obesity and energy balance. Cross-sectional and longitudinal studies have revealed a protective role in overweight and obesity (Mendez et al., 2006; Panagiotakos et al., 2006; Schroder et al., 2004) or no effect (Rossi et al., 2008; SanchezVillegas et al., 2006; Trichopoulou et al., 2005; Yannakoulia et al., 2009). Buckland et al. (2008) in their review concluded that although the results so far have been inconsistent, the evidence points towards a possible role of the Mediterranean diet in preventing overweight. The main physiological mechanisms proposed for this protective role are the increased satiety and satiation that this pattern induces, due to its fiber content, the prolonged mastication, the increased gastric detention and the enhanced release of cholecystokinin, as well as its low glycemic load and low-energy density (Buckland et al., 2008; Schroder, 2007). However, no investigation has been undertaken to evaluate the effect of a Mediterranean dietary pattern, rich in fiber on satiety indices. In the present study, the effects of a high-fiber, traditional, Mediterranean-type breakfast on energy intake and the feelings of hunger, fullness and desire to eat were compared to one of a low-fiber, common Western-type breakfast.
Methods Study participants Sixteen healthy, non-obese (BMI 530 kg/m2) young men completed the study (Table 1). Smokers, professional athletes, restrained eaters (as this was evaluated using the Dutch Eating Behavior Questionnaire and a total score 42.5 (van Strien et al., 1986)), those who reported slimming or any other dietary regime,
900
M. Yannakoulia et al.
Int J Food Sci Nutr, 2014; 65(7): 899–902
and/or great body weight fluctuations during the last 2 months (change of 42 kg) were excluded from participation. Also, subjects who were not breakfast-eaters, were on medication that may had an impact on appetite and sensory functioning or who reported a metabolic or endocrine disease, gastrointestinal disorders, or a history of medical or surgical events possibly affecting study outcomes were not included. Potential participants were informed that the purpose of the project was to investigate the impact of dietary composition on blood lipids (sham); the true purpose of the study was not revealed to them to decrease potential reactivity associated with preconceived notions regarding the effect of specific food items or nutrients on appetite. All participants reported usual lifestyle and dietary habits and a stable body weight for at least 3 months before the study. They gave their written informed consent before participating in any aspect of the investigation. Approval for the study was obtained from the Ethics Committee of Harokopio University. The study took place in the Metabolic Unit of the Department of Nutrition and Dietetics, Harokopio University. Study design The experiment had a crossover design. Each subject received 2 treatments on separate days, with a washout period of two weeks between treatments, in a random order. The treatments were the two isocaloric breakfasts (Mediterranean-type and Western-type), which were similar in their volume and macronutrient content, quite similar in the food sources of nutrients, but they were different in the dietary fiber content. The Mediterranean-type breakfast was based on the traditional Cretan diet, as this was revealed in the Seven Countries Study and other studies and it evaluated and analyzed recently (Kafatos et al., 2000). This breakfast provided 14.9 g of dietary fiber and consisted of 30 g (1 slice) Cretan Graviera cheese (a traditional, Gruye`re-type cheese), 60 g (1 big) barley-made, Cretan rusk, 260 g (1 big) fresh peeled orange and 2.5 cups of water; the Western-type breakfast provided 0.7 g of fiber and consisted of 30 g white bread, 5 g (1 teaspoon) butter, 14 g (2 teaspoons) honey, 366 g (1.5 cup) semi-skimmed milk (1.5% fat) and 244 g (1 cup) orange juice. The energy and macronutrient contents of the two breakfasts are presented in Table 1. The participants were instructed to eat and drink the same foods the evening before a test day and to record this dietary intake in a diary, as well as to abstain from excess exercise. After an overnight fast (nothing to eat or drink except for water after 22:00 h), they came to the Metabolic Unit. A member of the research team made all the anthropometric measurements and interviewed the participants for previous day’s dietary intake (24-h recall). Body weight, height and waist circumference were Table 1. Energy and macronutrient composition of the two treatments (breakfasts). Mediterranean-type breakfast Fluid volume, ml Energy, kcal Proteins, g % energy intake Carbohydrates, g % energy intake Lipids, g % energy intake Dietary fiber, g
625 465
Western-type breakfast 625 456
17.5 15.1
16.5 14.5
73.3 63.1
74.2 65.1
11.0 21.8 14.9
10.7 21.1 0.7
measured, and Body Mass Index (BMI) was calculated as weight (in kilograms) divided by height (in meters squared). Then, they had to consume one of the two treatments (breakfasts) in 10 min. They were not allowed to eat or drink anything for 4 hours, and they refrained from doing any physical activity. At the end of this time period, they received a buffet-style ad libitum lunch, consisting of standard Greek food items (pasta, tomato sauce, beef, salad, cheese, yogurt, fruit, chocolate). They were instructed to eat until they were satiated, within 30 min. To prevent habitual intake, foods were provided in excess amounts and participants had to serve themselves the quantities they wanted to eat. Food quantities served were weighted as well as any leftovers, in order to estimate dietary intake in the ad libitum meal. The day after the experiment, participants were asked through a telephone call to recall their food intake during the rest of the experimental day. Nutritional analyses For the analysis of the dietary intake, in terms of energy and macronutrient intake, the Nutritionist Pro, version 2.2 software (Axxya Systems-Nutritionist Pro, Stafford, TX) was used. The software food database was expanded by the analyses of traditional Greek foods and recipes as well as information provided by food companies. For the determination of participants’ usual caffeine intake the caffeine content from the various foods and beverages included in the FFQ was calculated using information from the United States Department of Agriculture National Nutrient Database for Standard Reference (U.S. Department of Agriculture, 2010) as well as the food industry. Appetite feelings assessment Before breakfast consumption, just after that and, then, every 30 min till the ad libitum lunch buffet participants filled out three 10-point Visual Analogue Scales (VAS) for the evaluation of their subjective feelings of hunger, fullness, and desire to eat, respectively (Figure 1). Each VAS scale was 10 cm in length and subjects recorded their respective ratings by marking a point on the scale that best described their feeling at each time point. VAS ratings are a reliable tool for appetite assessment (Flint et al., 2000) and they have been consistently used in the relevant research (Blom et al., 2006; Gavrieli et al., 2011). Statistical analysis Descriptive characteristics of the study participants are presented as means ± standard deviations. Energy intakes between the two treatments were compared using analysis of variance (ANOVA), or analysis of covariance (ANCOVA), adjusting for potential confounders. ANCOVA (subject as the covariate) for repeated measures was used to compare the response curves of VAS scores after the 2 treatments over time.
Results The baseline characteristics of the study participants are shown in Table 2. Previous day’s dietary energy intake was not statistically different between the two treatments and the same was also true for the macronutrient intake. A significant difference between the two treatments during the study’s course was found for the Desire to eat (p ¼ 0.016). The ratings dropped just after breakfast consumption and then they were steadily increasing, with those who had the Mediterraneantype breakfast exhibiting lower values. The analysis by time points revealed that at 150, 180, 210 and 240 min the differences between the two treatments were statistically significant (p50.05). Furthermore, although consumption of the
Breakfast and energy intake
DOI: 10.3109/09637486.2014.931359
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Table 2. Baseline characteristics of the study participants. Mean ± standard deviation (range) Age, years Weight, kg Body Mass Index, kg/m2 Waist circumference, cm Total score in the Dutch Eating Behavior Questionnaire (0–5)
25 ± 4 78.0 ± 5.6 24.1 ± 1.6 82.0 ± 4.5 2.2 ± .0.3
(19–33) (67.6–88.0) (21.5–27.9) (75.5–91.0) (1.6–2.5)
Table 3. Energy intake of the study participants (mean ± standard deviation) following breakfast consumption. Energy intake, kcal Previous day (before the experiment) Ad libitum meal Rest of the day Total day (excluding breakfast intake)
Mediterranean-type Western-type breakfast breakfast
p
p*
2730 ± 1126
2505 ± 886
0.536
1488 ± 468 1082 ± 490 2524 ± 602
1674 ± 416 1229 ± 514 2903 ± 669
0.246 0.045 0.420 0.296 0.109 0.004
*After adjustment for previous day’s energy intake.
that, when participants had the Mediterranean-type breakfast, compared to the Western-type one, their mean energy intakes were higher, but these differences did not reach statistical significance (p ¼ 0.246, 0.420 and 0.109, respectively). However, when taking into account the previous day’s energy intake, both the ad libitum and the total energy intake between the two treatments became statistically significant (p ¼ 0.045 and 0.004, respectively) (Table 3). In specific, participants consumed 251 kcal less during the ad libitum meal after the Mediterraneantype breakfast and 429 kcal less during the total day. No differences were found between the two treatments in the macronutrient contribution to the energy intake.
Discussion
Figure 1. Changes in appetite ratings [hunger, fullness, and desire to eat Visual Analogue Scales (VAS)], after breakfast consumption. Data are presented as means ± SE. Med-Breakfast: Mediterranean-type breakfast; West-Breakfast: Western-type breakfast.
Mediterranean-type breakfast was followed by lower ratings for the hunger and higher for the fullness scales, compared to the consumption of the Western-type breakfast, the between-subjects effects for both scales did not reach a statistical significance (p ¼ 0.193 and 0.281, respectively). Nutritional analysis of the ad libitum meals, the dietary intakes during the rest of the day and the total day (i.e. the sum of the intake during the ad libitum meal and the rest of the day) revealed
A significantly lower energy intake was found in the ad libitum lunch after the consumption of the Mediterranean-type breakfast, compared to the Western-type breakfast, when previous day’s dietary intake was taken into account. The observed effect was evident in meal following breakfast and no compensation was made throughout the day, as total energy intake was also different between the two treatments. Furthermore and in support to the energy-related findings, the desire to eat ratings (a measure of subjective feelings of appetite) were significantly lower following the consumption of the Mediterranean, compared to the consumption of the Western-type breakfast. Lunch and other conditions were identical for the two experimental days, suggesting that the reported findings were a spontaneous response to the treatment taken, i.e. the breakfast eaten. Participants had not been informed about the purpose of the study or that their food intake during lunchtime was recorded, in order to minimize any participant bias. We speculate that most of this effect comes from the fiber content of the Mediterranean-type breakfast (15 g versus 1 g of fiber in the Western-type breakfast), but we cannot exclude the possibility that other factors may also operate, including intercorrelations between nutrients contained in the specific foods chosen. Foods rich in dietary fiber might promote satiation through prolonged mastication, and this was a common comment, or sometimes complaint, reported from the participants in this study, when they had the Mediterranean-type breakfast. Prolonged
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mastication may suppress appetite (Cassady et al., 2009; Hetherington & Boyland, 2007), though neural activation of central satiety centers, increases in saliva, gastric acid production and, thus, gastric distension, as well as through increase in the release of cholecystokinin or other gastrointestinal satiety peptides (Sakata et al., 2003). Along with the fiber content, it may be the glycemic index of the Mediterranean type breakfast that may contribute to the effect on appetite and food intake. Previous evidence suggests that lunch intake is significantly lower and hunger ratings significantly greater after a low glycemic index breakfast compared to the corresponding values after a high glycemic index breakfast in preadolescents children (Warren et al., 2003). In the present study, the effect of a Mediterranean-like pattern on energy balance was evaluated using an ad libitum test meal. It constitutes a reproducible method for measuring spontaneous energy intake; although its reproducibility is not influenced by prior diet standardization, prior diet standardization may exert a significant effect on the ad libitum energy intake (Gregersen et al., 2008). This was also evident in our analysis. Despite the fact that an effort had been made to instruct subjects to have similar food intake the days preceding the experiments and there was no difference in energy intake between the two experiments in the day before the trial, the trend for significance for the energy intake values in the ad libitum meal became a statistically significant finding after adjusting for previous day’s energy intake. Furthermore, in this study we report the acute effects; evidence will also be needed for a sustained effect with continuous consumption of the meal, in order to examine potential adaptation through compensatory mechanisms (EFSA Panel on Dietetic Products Nutrition and Allergies, 2012). Changes in certain biochemical markers related to appetite would also provide useful insight on the underlying mechanisms. Finally, rating of the two meals for taste, appearance, and volume is important for applying these results into modern lifestyles. In conclusion, a Mediterranean-type breakfast, characterized by high fiber content, through consumption of whole-grain cereals and fruits, was found to have a beneficial effect on energy intake and on the subjective feelings of the desire to eat in young nonobese men. Thus, the results of this clinical trial support epidemiological evidence on the anti-obesogenic effect of the Mediterranean diet and call for further trials in other age and/or sex groups, other populations as well as for replication of these findings in long-term interventional studies.
Acknowledgements The authors would like to thank Ms. Antigone Tsiafitsa for her technical assistance.
Declaration of interest The authors have no conflicts of interest.
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