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Research report

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Higher proportion of total and fat energy intake during the morning may reduce absolute intake of energy within the day. An observational study in free-living Japanese adults ☆

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Yukako Tani a, Keiko Asakura a,b, Satoshi Sasaki a,*, Naoko Hirota c, Akiko Notsu d, Q3 Hidemi Todoriki e, Ayako Miura f, Mitsuru Fukui g, Chigusa Date h a

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Department of Social and Preventive Epidemiology, School of Public Health, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan Interfaculty Initiative in Information Studies, Graduate School of Interdisciplinary Information Studies, The University of Tokyo, Tokyo, Japan c Graduate School of Health Science, Matsumoto University, Matsumoto, Nagano, Japan d Department of Food Science and Nutrition, Tottori College, Tottori, Japan e Department of Public Health and Hygiene, School of Medicine, University of the Ryukyus, Nakagami-gun, Okinawa, Japan f Department of Health and Nutritional Sciences, Faculty of Health Promotional Sciences, Tokoha University, Hamamatsu, Shizuoka, Japan g Laboratory of Statistics, Osaka City University Graduate School of Medicine, Osaka, Japan h Department of Food Science and Nutrition, School of Human Science and Environment, University of Hyogo, Himeji, Hyogo, Japan b

A R T I C L E

I N F O

Article history: Received 2 July 2014 Received in revised form 17 March 2015 Accepted 26 April 2015 Available online Keywords: Meal pattern Timing Circadian rhythms Energy intake Macronutrients Food choice

A B S T R A C T

Background: Although the distribution of energy intake throughout the day appears to impact overall daily energy intake, little is known about the ad libitum distribution of energy intake. Objective: Our aim was to investigate associations between the distribution of energy intake during the day and subsequent or overall energy intake, and food choice in free-living adults. Design: A total of 119 women and 116 men completed 16-day semi-weighed dietary records. The longitudinal dietary intake data for each participant were analyzed using a mixed model to examine the effect of energy intake at various times of day on subsequent or overall energy intake. Results: Mean proportion of total energy intake in the morning (4:00 a.m.–10:29 a.m.), afternoon (10:30 a.m.–4:59 p.m.) and evening (5:00 p.m.–3:59 a.m.) meal was 22.6%, 33.8% and 43.6% in men, and 24.7%, 36.5%, 38.8% in women, respectively. Proportion of energy intake (%) in the morning meal was significantly and negatively associated with energy intake (kcal) in the subsequent afternoon and evening meals, and consequently in the whole day in both sexes. This significant and negative association was also observed for proportion of energy intake (%) of fat, but not of carbohydrate or protein, in both sexes. Proportion of energy intake (%) in the morning meal was negatively associated with overall energy intake (kcal) from the group of meats, fish, and eggs in both sexes, and from the group of confectioneries and soft drinks in women. Conclusions: More energy in the morning meal may reduce energy intake, especially that from fat, in the subsequent meals, and consequently in the whole day. © 2015 Published by Elsevier Ltd.

52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67

Introduction The prevalence of obesity has increased globally during the last decades (Swinburn et al., 2011). One important step in overcoming obesity is to identify strategies to reduce energy intake from each meal. A primary contributor to obesity is the recent increase in unhealthy eating habits, with emphasis on breakfast skipping. Breakfast

Q1 Q2

☆ Acknowledgements: This study was supported by grants from the Ministry of Health, Labour and Welfare, Japan. The authors are grateful to all participants and to the local staff for their participation in this study. Conflicts of interest: None of the authors has any personal or financial conflict of interest. * Corresponding author. E-mail address: [email protected] (S. Sasaki).

consumption in children, adolescents, and adults has dramatically declined over the last decades in the US (Haines, Guilkey, & Popkin, 1996; Siega-Riz, Popkin, & Carson, 1998). Skipping breakfast or consuming a smaller breakfast is associated with an array of unhealthful outcomes (Keski-Rahkonen, Kaprio, Rissanen, Virkkunen, & Rose, 2003), including body weight gain, overweight and obesity (de Castro, 2004; Purslow et al., 2008; Song, Chun, Obayashi, Cho, & Chung, 2005; van der Heijden, Hu, Rimm, & van Dam, 2007), and obese individuals are more likely to skip breakfast or consume less energy at breakfast (Bellisle, Rolland-Cachera, Deheeger, & Guilloud-Bataille, 1988; Berteus Forslund, Lindroos, Sjostrom, & Lissner, 2002; Ortega et al., 1996). However, the proportion of energy intake in the morning meal that is most effective in reducing overall energy intake is unknown.

http://dx.doi.org/10.1016/j.appet.2015.04.071 0195-6663/© 2015 Published by Elsevier Ltd.

Please cite this article in press as: Yukako Tani, et al., Higher proportion of total and fat energy intake during the morning may reduce absolute intake of energy within the day. An observational study in free-living Japanese adults , Appetite (2015), doi: 10.1016/j.appet.2015.04.071

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The timing of energy intake during the day also appears to impact total energy intake. Normal and underweight persons take in more energy in daytime than those with obesity (Bellisle et al., 1988; Berteus Forslund et al., 2002). Higher proportional consumption of energy and macronutrients in the morning meal is associated with lower overall energy intake whereas higher proportional consumption in the evening meal is associated with higher overall intake (de Castro, 2004). Under a cross-over design, eating restriction at night decreased total energy intake and weight change in healthy young men (LeCheminant, Christenson, Bailey, & Tucker, 2013). Moreover, moderately obese women lost more weight when they consumed 70% of their daily energy intake before noon instead of in the afternoon and evening meals (Keim, Van Loan, Horn, Barbieri, & Mayclin, 1997). These findings suggest that the timing of energy intake during the day might influence total daily energy intake. However, few studies have quantified what proportion of energy intake in the morning meal is necessary to reduce subsequent or overall energy intake. Moreover, these previous studies characterized influences on energy intake simply by the amount of energy, and did not describe the source of energy intake. Macronutrient contents of the diet also may influence energy intake. A high-protein breakfast reduced subsequent energy intake compared with a normal-protein breakfast, high-carbohydrate breakfast, or high-fat breakfast (Fallaize, Wilson, Gray, Morgan, & Griffin, 2013; Leidy & Racki, 2010), and a high-fat and high-protein lunch reduced subsequent energy intake compared with a highcarbohydrate lunch in lean subjects (Brennan et al., 2012). However, other studies were inconsistent with these studies (Blatt, Roe, & Rolls, 2011; Raben, Agerholm-Larsen, Flint, Holst, & Astrup, 2003). Meal timing and macronutrient contents appear to influence its satiating properties. Specifically, protein consumed at the morning meal leads to greater initial and sustained feelings of fullness, increased satiety and reduced levels of ghrelin compared to the afternoon or evening meal (de Castro, 2007; Leidy, Bossingham, Mattes, & Campbell, 2009; Leidy, Mattes, & Campbell, 2007; Leidy & Racki, 2010). It has also been shown that the addition of carbohydrates to protein leads to an additional reduction of hunger and increased satiety (Astbury, Taylor, & Macdonald, 2011; Holt, Delargy, Lawton, & Blundell, 1999; Isaksson et al., 2011). This kind of study requires participants to consume a fixed, artificial amount of food, which may differ from the amount they usually consume or would consume ad libitum. As a consequence, these studies have received little attention. In fact, one ad libitum study in US adults suggested that although a higher proportion of carbohydrate and fat intake in the morning meal reduced overall energy intake, the proportion of protein intake did not affect overall intake (de Castro, 2007). With regard to ad libitum macronutrient intake, its role on overall energy intake is also unknown. Our present study had several objectives. First, we wanted to describe the distribution of ad libitum daily energy and macronutrient intake in Japanese adults. Second, we wanted to investigate associations between the proportion of energy intake in the morning, afternoon, and evening meals and subsequent or overall energy intake in free-living adults. Third, we wanted to assess the intake pattern of macronutrients throughout the day, and the effects of the timing of each macronutrient intake on energy intake. Last, we wanted to investigate associations between the proportion of energy intake in the morning meal and subsequent food choice. Methods Study subjects Details of the study design, participant characteristics, and dietary assessment methods of semi-weighed dietary records (DRs) have been reported elsewhere (Kobayashi et al., 2012; Murakami et al.,

2008). Briefly, the study was conducted in four areas in Japan with large differences in geographic conditions and dietary habits, namely: Nagano (Matsumoto City; rural inland), Osaka (Osaka City; urban), Tottori (Kurayoshi City; rural coastal), and Okinawa (Ginowan City; urban island). In each area, the registered dietitians at the municipal government recruited apparently healthy women aged 30–69 years who had a high possibility of participation with a cohabiting husband. The subjects were volunteers and were asked by local staff (registered dietitians) to participate in the study. Subject recruitment was continued until a sufficient number of participants was obtained. In each of the four areas, each 10-year age band (30– 39, 40–49, 50–59, and 60–69 years) included 8 women; the age of the husband was not considered. Thus, a total of 128 women and 128 men were invited. Dietitians were excluded from the study. None of the subjects had recently received dietary counseling from a doctor or dietitian or had a history of educational hospitalization for diabetes or nutritional education from a dietitian. The study was conducted between November 2002 and September 2003. The study did not undergo ethical approval because it was conducted before ethical guidelines for epidemiologic research were enforced in Japan. However, the study was conducted according to the principles of the Helsinki declaration. Before the start of the study, group orientations were held to explain the study purpose and design and written informed consent was obtained from each subject. Use of data from this study was approved by the Ethics Committee of The University of Tokyo Faculty of Medicine (No. 3421). Diet record Between November 2002 and September 2003, each subject completed four 4-nonconsecutive-day semi-weighed DRs, one in each of the four seasons (total 16 days) at intervals of approximately three months. The four recording days consisted of three randomly selected weekdays (Monday through Friday) and one weekend day (Saturday through Sunday). During the orientation session, local staff (registered dietitians) gave subjects both written and verbal instructions on how to keep the dietary record, using a completed recording sheet as an example. Subjects were also instructed on how to weigh each food item and drink and were asked to record all foods and drinks, and the time they started and finished consumption on each recording day. All collected records were checked by trained registered dietitians in each local center and then again in the data center. The coding of records and conversion of measurements into grams were performed by trained registered dietitians in the survey center in accordance with uniform procedures. A total of 1398 food and beverage items appeared in the dietary records. Dietary data were converted into energy using the Standard Tables of Food Composition in Japan (Science and Technology Agency, 2010). Total intake Q5 of energy, carbohydrate, fat, protein and alcohol were calculated by summing the contributions of the individual items. A total of 119 women aged 30–69 years and 116 men aged 30–76 years who completed the 16 DRs and times of consumption were included in the present analysis. Timing of dietary intake To analyze energy and nutrient intake distribution during the day, the starting time of each meal was considered the time of intake. Energy intake in the three periods of morning (4:00 a.m.–10:29 a.m.), afternoon (10:30 a.m.–4:59 p.m.), and evening (5:00 p.m.–3:59 a.m.) was calculated to investigate the effect of energy intake in each period on that in subsequent meals and overall intake. The morning period was specifically defined to capture most of “breakfast” but not lunch. Similarly, the afternoon period was defined to capture most of “lunch” and afternoon snack, while the evening period was determined to capture most of “dinner” and evening snack (de Castro,

Please cite this article in press as: Yukako Tani, et al., Higher proportion of total and fat energy intake during the morning may reduce absolute intake of energy within the day. An observational study in free-living Japanese adults , Appetite (2015), doi: 10.1016/j.appet.2015.04.071

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2009). The proportions of energy intake in each period were also calculated. Definition of “meal” and “snack” We regarded food intake of at least 50 kcal, or more stringently 100 or 200 kcal, as a meal (de Castro, 2004). Therefore, any energy intake of 50 kcal or over at a single occasion was considered a meal or snack. A main meal was defined as ≥ 200 kcal and a snack as ≥ 50 kcal and < 200 kcal. To examine the relationship between dietary intake timing and food choice, food groups were defined as: 1) cereals such as rice, breads or noodles; 2) vegetables and fruits, including potatoes, mushrooms and seaweeds; 3) meat, fish, shellfish and eggs; and 4) confectioneries, soft drinks and juices. Statistical analysis Energy intake in each subject was calculated as the mean value of the 16 DRs. To examine associations between the timing of energy intake and energy intake in subsequent meals or overall daily energy intake, we used all dietary intake data of subjects obtained throughout the year. All 235 subjects completed the 16-day dietary records, providing 3760 energy intake record sets for analysis. Since the absolute amount of energy intake in a period was highly correlated with total energy intake over the day, we used the proportion of energy intake in each period (morning, afternoon, and evening) for total energy intake in a day. Sex-specific mixed linear models of the repeated measurement were used to investigate associations between the distribution of energy intake and subsequent or overall energy intake. Subject identification code was included as a random effect. Age (years), body mass index (kg/m2), area (residential area of Nagano, Osaka, Tottori or Okinawa), season (season of the survey day; autumn, winter, spring or summer) and day of survey (weekday or weekend) were included in each model. In detail, we tested the following model: energy intake in subsequent meals or overall energy intake (kcal/period or day) = intercept + β1 (proportion of energy consumed in a certain period to total energy intake in a day; %) + β2 (age; years) + β3 (body mass index; kg/m2) + β4 (area; Nagano, Osaka, Tottori or Okinawa) + β5 (season; autumn, winter, spring or summer) + β6 (day of survey; weekday or weekend). To examine the effects of intake timing of each macronutrient on energy intake,

Men

3

we included the percentage of energy intake from carbohydrate, fat and protein within the model (de Castro, 2009). We used the following model: subsequent or overall energy intake (kcal/period or day) = intercept + β1 (carbohydrate; percentage of energy intake from carbohydrate in each period to daily total energy intake from carbohydrate in a day, %) + β2 (fat; percentage of energy intake from fat in each period for daily total energy intake from fat in a day, %) + β3 (protein; percentage of energy intake from protein in each period for daily total energy intake from protein in a day, %) + β4 (age) + β5 (body mass index) + β6 (area) + β7 (season) + β8 (day of survey). To make the results of the mixed linear model clearer, the 16 DRs of each subject were divided into two groups (“low” and “high”) for every time period. For example, the “low” group for the morning was lower than the mean proportion of morning energy intake for that subject. Similarly, the “high” group for the evening was higher than the mean proportion of evening energy intake for that subject. The mean proportion and the mean amount of energy intake in each time period were then calculated for the two groups (“low” and “high”). The difference in energy intake in subsequent meal(s) and daily total between the low and high groups in each subject was tested by the paired t test. For the association between energy distribution and food choice, we used the following model: subsequent energy intake from a food group (kcal/period or day) = intercept + β1 (percentage of total energy intake during each period in a day, %) + β2 (age) + β3 (body mass index) + β4 (area) + β5 (season) + β6 (day of survey). Trend results were noted as an increase (+) or decrease (−). All analyses were performed using Statistical Analysis Systems (SAS) version 9.3 (SAS Institute Inc, Cary, NC, USA). A significance level of P < 0.05 was used.

77 Results Distribution of energy intake during the day The distribution of total energy intake and energy intake from carbohydrate, fat, and protein in 24 hours is shown in Fig. 1 for men and women separately. The starting time of the afternoon meal was tightly distributed between 12:00 p.m. and 1:00 p.m., particularly in men, while that of the morning and evening meal was widely distributed between 6:00 a.m. and 9:00 a.m., and 6:00 p.m. and 9:00

Women

43

44 45

46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76

Fig. 1. Distribution of total energy intake and energy intake from macronutrients during the day among Japanese adults. Abbreviation: SEM = standard error of the mean. *The time of intake was considered to be the starting time of each meal.

Please cite this article in press as: Yukako Tani, et al., Higher proportion of total and fat energy intake during the morning may reduce absolute intake of energy within the day. An observational study in free-living Japanese adults , Appetite (2015), doi: 10.1016/j.appet.2015.04.071

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Table 1 Characteristics of study subjects and meal frequency and energy intake during each period by sex among Japanese adults.

3

Men (n = 116)

4

Total

5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42

Women (n = 119) Time period Morning

Mean Age (years) 52.6 Body height (cm) 167.3 Body weight (kg) 66.4 BMI (kg/m2) 23.6 Frequency (n) Meals (≥200 kcal) 3.21 Snacks (≥50, < 200 kcal) 0.67 Amount of energy intake (kcal) Total 2370 Macronutrient Carbohydrate 1273 Fat 614 Protein 341 Food group Cereals 943 Fruits, vegetables 179 Meats, fish, eggs 436 Confectioneries, soft drinks 144 Proportion of energy intake from each macronutrient throughout a day (%) Total 100 Macronutrient Carbohydrate 100 Fat 100 Protein 100 Proportion of energy intake from each macronutrient and alcohol in one meal (%) Carbohydrate 53.9 Fat 25.9 Protein 14.5 Alcohol 5.6

SD

Mean

a

Total Afternoon

SD

Mean

a

SD

Evening Mean

SD

12.2 6.7 10.5 2.9 0.39 0.54

Mean 49.8 154.7 53.0 22.2

0.93 0.17

0.25 0.22

1.11 0.28

0.16 0.26

Time period

a

1.16 0.22

0.23 0.22

3.19 0.94*

SD

Morninga

Afternoona

Eveninga

Mean

Mean

Mean

SD

SD

SD

11.3 6.2 8.3 3.4 0.32 0.53

0.93 0.22

0.22 0.23

1.18* 0.45*

0.16 0.26

1.08* 0.28*

0.14 0.25

416

533

190

793

153

1044

263

1842*

281

455*

150

671*

123

716*

141

240 145 62

318 138 76

123 60 30

472 203 110

93 58 22

484 273 156

124 89 42

1015* 521* 279*

184 104 46

261* 125 68*

92 51 27

396* 181* 93

82 43 18

358* 215* 118*

74 59 25

231 66 116 125

243 45 68 34

103 35 39 50

378 53 141 58

97 29 50 63

329 82 229 54

105 26 82 67

678* 177 325* 176*

149 62 79 80

183* 44 53* 35

64 31 35 36

269* 60 106* 93*

58 26 36 52

230* 75* 168* 48

62 25 55 41

6.1 3.8 1.6 5.6

22.6

7.1

33.8

5.1

43.6

6.8

100

24.7*

6.6

36.5*

4.6

38.8*

5.5

24.7 23.2 22.4

7.7 8.3 8.0

37.5 33.7 32.7

6.0 7.3 5.4

37.8 43.0 44.9

7.0 8.1 7.5

100 100 100

25.5 25.0 24.5*

6.5 8.1 7.5

39.0* 34.8 33.6

5.3 6.7 4.9

35.4* 40.2* 41.9*

5.2 7.3 6.6

61.1 24.7 14.0 0.18

8.4 7.3 2.6 0.80

60.7 24.5 14.0 0.83

5.0 4.6 1.7 1.8

48.6 25.3 15.4 10.7

9.9 4.4 2.8 10.6

58.5* 26.5 14.8*

7.6 6.8 2.6

60.0 25.8* 13.9

4.7 4.4 1.6

51.9* 28.4* 16.8*

6.6 4.3 2.7

55.0 28.3* 15.2*

4.5 3.7 1.6

Abbreviation: BMI = body mass index; SD = standard deviation. a Morning (4:00 a.m.–10:29 a.m.), afternoon (10:30 a.m.–4:59 p.m.), and evening (5:00 p.m.–3:59 a.m.). Sex differences were analyzed using the unpaired t-test. *P < 0.05.

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p.m., respectively. These results showed that meal interval between morning and afternoon meal was about 4–6 hours, while that between afternoon and evening meal was 6–8 hours. The longer intervals may have induced afternoon snacking, which mainly occurred between 3:00 p.m. and 4:00 p.m. The relative contributions of carbohydrate, fat, and protein to total energy intake varied with time during the day. Table 1 shows the characteristics of subjects and the frequency of meals, amount and proportion of energy intake in each period and daily total by sex. The frequency of main meals during the afternoon was significantly higher in women than men, while that during the evening was significantly higher in men than women. Frequency of snacks was significantly higher in women than men (0.45 times vs 0.28 times). Women consumed a larger proportion of energy in the morning and afternoon meals than men, while men consumed a larger proportion of energy in the evening meal than women. Mean proportion of total energy intake in the morning, afternoon and evening meals was 22.6%, 33.8% and 43.6% in men and 24.7%, 36.5%, 38.8% in women, respectively. Composition of macronutrients in the evening meal was different from that in the morning and afternoon meals in both sexes. The proportion of energy intake from carbohydrate was lower in the evening meal, and this difference was more apparent in men. In addition, the proportion of energy intake from alcohol in the evening meal amounted to 10.7% in men, but only 2.9% in women.

Relationship between energy intake in each period and that in the subsequent meal or daily total Table 2 shows the relationship between the proportion of energy intake in each period and energy intake in the subsequent meal(s) or daily total energy intake after adjustment for the effect of research area using a mixed linear model. The regression coefficients (β) indicated the increase (positive value) or decrease (negative value) in energy intake in the subsequent meal(s) or daily total energy intake for a one percent increase in energy intake proportion in each period. The coefficients for total energy intake indicated that a higher proportion of energy intake in the morning meal was associated with a lower energy intake in the afternoon and evening meals in both sexes. Consequently, a higher proportion of energy intake in the morning meal was also related with lower total daily energy intake. Further, a higher proportion of energy intake in the afternoon meal was associated with lower energy intake in the subsequent evening meal and daily total in men. In women, a higher proportion of energy intake in the afternoon meal was associated with lower energy intake in the evening meal only. The decrease in energy intake was smaller in women than in men in all periods. Next, we assessed the contribution of macronutrients to energy intake. A larger proportion of energy intake from carbohydrate in the morning meal was associated with lower energy intake in the afternoon and evening meal, but was not associated with overall

Please cite this article in press as: Yukako Tani, et al., Higher proportion of total and fat energy intake during the morning may reduce absolute intake of energy within the day. An observational study in free-living Japanese adults , Appetite (2015), doi: 10.1016/j.appet.2015.04.071

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Table 2 Relationship between the proportion of energy intake in each period and that in subsequent meal(s) or daily total among Japanese adults. Sex

Time period

Energy source (%)

5

32 33 34 35 36 37 38 39

Subsequent or overall energy intake from all energy source (kcal) Afternoona

4 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31

5

Men

Morninga Afternoona Eveninga Morninga

Afternoona

Eveninga

Women

Morninga Afternoona Eveninga Morninga

Afternoona

Eveninga

Allb Allb Allb Each macronutrientc Carbohydrate Fat Protein Carbohydrate Fat Protein Carbohydrate Fat Protein Allb Allb Allb Each macronutrientc Carbohydrate Fat Protein Carbohydrate Fat Protein Carbohydrate Fat Protein

Eveninga

Overall

β

SE

β

SE

β

SE

−12.34

0.82*

−15.88 −19.87

1.08* 0.75*

−7.80 −3.97 8.13

1.50* 1.16* 1.12*

−6.84 −4.25 −1.28

0.86* 0.62* 0.99

−4.22 −2.02 −5.58 −6.88 −4.61 −5.28

1.16* 0.83* 1.34* 0.86* 0.58* 0.88*

−11.44

0.63*

−10.16 −11.96

0.68* 0.47*

−0.39 −2.53 −1.82 1.23 −1.12 −2.48 −0.18 2.94 2.81 −6.70 0.30 3.64

1.58 1.13* 1.82 1.28 0.86 1.31 1.20 0.81* 1.14* 1.07* 0.81 0.83*

−7.32 −3.51 −0.47

0.71* 0.49* 0.75

−1.83 −4.29 −2.25 −5.50 −4.09 −1.33

0.76* 0.53* 0.81* 0.53* 0.39* 0.57*

−0.51 −4.65 0.15 1.81 −0.38 −0.22 −1.86 3.16 0.32

1.18 0.81* 1.25 0.90* 0.66 0.95 0.93* 0.61* 0.87

a

Morning (4:00 a.m.–10:29 a.m.), afternoon (10:30 a.m.–4:59 p.m.), and evening (5:00 p.m.–3:59 a.m.). Results of the mixed linear model (PROC MIXED): subsequent or overall energy intake (kcal/period of day) = intercept + β (total energy intake during each period (%)) + β2 (age (years)) + β3 (body mass index (kg/m2)) + β4 (area) + β5 (season) + β6 (day of survey). c Results of the mixed linear model (PROC MIXED): subsequent or overall energy intake (kcal/period of day) = intercept + β (energy intake from carbohydrate during each period (%)) + β2 (energy intake from fat during each periods (%)) + β3 (energy intake from protein during each period (%)) + β4 (age (years)) + β5 (body mass index (kg/ m2)) + β6 (area) + β7 (season) + β8 (day of survey). Coefficient (β) represents the predicted change in total daily energy intake for a 1% increase. * P < 0.05. b

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energy intake in either sex. On the other hand, a larger proportion of energy intake from fat in the morning meal was associated with lower energy intake in all subsequent meals and overall energy intake. The proportion of energy intake from protein in the morning meal was associated with lower energy intake only in the evening meal. A larger proportion of energy intake from carbohydrate, fat and protein in the afternoon meal was associated with lower energy intake in the evening meal, but a non-significant effect on overall intake was observed in men. A larger proportion of energy intake from carbohydrate in the afternoon meal was associated with higher overall intake in women only. Regarding the evening meal, the proportion of energy intake from fat and protein was positively associated with overall energy intake in men, while only the proportion of energy intake from fat was positively associated with overall energy intake in women. We then observed the relationship between the timing of energy intake and energy intake in subsequent meal(s) and overall daily energy intake in a different manner. Results are shown in Table 3. When the proportion of morning energy intake for a participant was lower than the mean for the morning by sex (17.9% and 19.5% for men and women), the participant consumed more energy in the afternoon meal (154 and 151 kcal for men and women) and evening meal (222 and 136 kcal for men and women) than they did on days when their morning energy intake was higher than the mean (28.2% and 30.6% for men and women). Overall energy intake (178 and 123 kcal for men and women) was also significantly higher when morning energy intake was higher than the mean. When the proportion of afternoon energy intake was lower than the mean of afternoon energy intake (27.0% and 29.3% for men and women), the participants consumed significantly more energy in the evening meal

(292 and 187 kcal for men and women). Overall energy intake when the proportion of afternoon energy intake was lower than the mean of afternoon energy intake was significantly lower than that in the higher group. On the other hand, when the proportion of evening energy intake was lower than the mean (36.3% and 31.2% for men and women), the participants consumed significantly less energy over the entire day (114 and 56 kcal for men and women) than they did when they were in the higher group (50.8% and 45.9% for men and women). Relationship between the proportion of energy intake in the morning meal and food choice Because morning energy intake had the largest impact on subsequent and overall energy intake, we next examined the effect of energy intake during the morning on food choice in the subsequent meal(s) and throughout the day. Table 1 shows the amount of energy intake from each food group during each period by sex. Amount of energy intake from the cereal and meat groups was significantly lower in women than men in all periods. Amount of energy intake from the confectionery group was significantly higher in women than men in the afternoon meal. Table 4 shows the association between the proportion of energy intake in the morning meal and amount of energy intake from each food group in the subsequent meal or throughout the day using the mixed linear model. Energy intake from cereals in the afternoon and evening meals was decreased, with a higher proportion of energy intake in the morning meal, while overall daily intake from cereals was not affected by the proportion of energy intake in the morning meal in either sex. On the other hand, taking a larger proportion of energy in the morning

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Table 3 Comparison of energy intake in subsequent meals and daily total between the lower and higher groups. Sex

Time period

Group

Mean proportion of energy intake (%)

Mean energy intake (kcal)

17.9 28.2 27.0 41.0 36.3 50.8 19.5 30.6 29.3 44.4 31.2 45.9

443 642 647 950 843 1241 377 542 539 814 568 855

6 7 8 9 10 11 12 13 14 15 16 17 18

Men (n = 116)

19 20 21 22 23 24

a

Morninga Afternoona Eveninga

Women (n = 119)

Morninga Afternoona Eveninga

Lowb Highc Lowb Highc Lowb Highc Lowb Highc Lowb Highc Lowb Highc

Subsequent or overall energy intake (kcal) Afternoona Mean

SD

866 712

182 162

741 590

146 127

Eveninga Difference −154*

−151*

Mean

SD

1150 927 1183 891

310 243 316 236

779 643 805 618

166 144 161 146

Overall Difference −222* −292*

−136* −187*

Mean

SD

2459 2281 2406 2329 2311 2425 1898 1775 1838 1844 1811 1867

462 401 440 445 432 444 313 286 281 307 294 295

Difference −178* −77* 114* −123* 5 56*

Morning (4:00 a.m.–10:29 a.m.), afternoon (10:30 a.m.–4:59 p.m.), and evening (5:00 p.m.–3:59 a.m.). b Low: Includes energy intake data on days when the proportion of energy intake in a certain period (morning, afternoon, or evening) for a participant was lower than its mean in the corresponding period for that participant. c High: Includes energy intake data on days when proportion of energy intake in a certain period (morning, afternoon, or evening) for a participant was higher than its mean in the corresponding period for that participant. Lower and higher mean days were compared with the paired t test. *P < 0.05.

25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49

meal was associated with significantly lower energy intake from the meats group in the subsequent meal and throughout the day in both sexes. In women, taking a larger proportion of energy in the morning meal was also associated with significantly lower energy intake from the confectioneries group in the subsequent meal and throughout the day. The decrease in energy intake from the meats group in the afternoon meal was larger in men, while that from the confectioneries group was larger in women. Discussion In this study, we found that the timing of energy intake during the day affected subsequent and total energy intake. Energy intake in morning meal was particularly important in changing total energy intake. These results will be useful in the development of weight control programs. This study revealed that the energy intake of Japanese adults was better distributed throughout the day than that of US adults. Energy intake in the morning meal accounted for 22.6% and 24.7% in men and women, respectively, versus a reported rate of only about 18– 20% for US adults (Cutler, Gleser, & Shapiro, 2003; de Castro, 2001). We also found a sex difference in the present study (Table 1): energy intake was distributed more uniformly in women than men, and women tended to consume a higher proportion of energy during

the morning and afternoon meals than men; in contrast, men intensively consume a higher proportion of energy during the evening meal than women. Eating a larger proportion of energy in the morning meal is associated with significantly lower overall energy intake than eating a lower proportion of energy in the morning meal. Eating a larger proportion of energy during the evening meal is associated with significantly higher overall energy intake compared to eating a lower proportion of energy in the evening meal. This association between energy distribution throughout the day and overall energy intake is consistent with data in another study (de Castro, 2004). We also found that a lower proportion of energy intake in the morning meal (17.9% and 19.5% for men and women), which reduced energy intake in the morning meal by 199 and 165 kcal for men and women (mean energy intake in high minus that in low), respectively, increased intake in the afternoon meal by about 150 kcals, compensating for the 77% (154 kcal/199 kcal) and 93% (151 kcal/165 kcal) of energy lost by the lower eating in the morning meal for men and women, respectively (Table 3). Interestingly, the compensation in energy intake for the reduction in energy intake in the morning meal was observed not only in the afternoon meal but also during the evening meal. In studies of the effects of breakfast skipping on energy intake in the afternoon meal and overall intake using a cross-sectional and crossover design, breakfast skipping increased energy intake in the

50 51 52 53

Table 4 Association between the proportion of energy intake during the morning meal and energy intake from each food group in subsequent meals and daily total. Independent variable

Sex

54

Subsequent or overall energy intake from each food group (kcal) Food group (source of energy intake)

55 56 57 58 59 60 61 62 63 64 65 66 67 68

Proportion of energy intake during morninga (%)

Men

Women

Cereals Fruits, vegetables Meats, fish, eggs Confectioneries, soft drinks Cereals Fruits, vegetables Meats, fish, eggs Confectioneries, soft drinks

Afternoona

Eveninga

β

SE

β

SE

β

SE

−3.48 −0.46 −2.77 −1.72 −2.95 −0.62 −1.87 −2.66

0.45* 0.14* 0.31* 0.36* 0.33* 0.16* 0.25* 0.35*

−2.96 −0.92 −4.22 −1.18 −1.66 −0.84 −2.83 −1.33

0.48* 0.18* 0.49* 0.35* 0.31* 0.16* 0.34* 0.26*

0.66 −0.17 −3.66 0.04 −0.04 −0.44 −2.37 −1.71

0.78 0.27 0.61* 0.59 0.53 0.26 0.45* 0.49*

Overall

The mixed linear model (PROC MIXED): subsequent or overall energy intake from each food group (kcal/day) = intercept + β (proportion of energy intake during morning (%)) + β2 (age (years)) + β3 (body mass index (kg/m2)) + β4 (area) + β5 (season) + β6 (day of survey). a Morning (4:00 a.m.–10:29 a.m.), afternoon (10:30 a.m.–4:59 p.m.), and evening (5:00 p.m.–3:59 a.m.). Coefficient (β) represents the predicted change in energy intake from each food group for a 1% increase in morning energy intake proportion. * P < 0.05.

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afternoon meal to some extent, but decreased overall energy intake in adults (Cho, Dietrich, Brown, Clark, & Block, 2003; Deshmukh-Taskar, Radcliffe, Liu, & Nicklas, 2010; Kant, Andon, Angelopoulos, & Rippe, 2008; Levitsky & Pacanowski, 2013; NHANES, 2007). These previous and our present results show that both skipping breakfast and a large morning meal (accounting for about 30% of total daily energy intake; 642 and 542 kcal for men and women (Table 3)) may be effective in reducing overall daily energy intake. However, skipping breakfast has been reported to increase the risk of unhealthful outcomes, possibly leading to weight gain and deleterious changes in risk factors for diabetes and cardiovascular disease and insufficient supply of nutrients (Keski-Rahkonen et al., 2003; Timlin & Pereira, 2007). One of the few studies to examine the effect of energy intake timing on health outcomes reported that higher energy intake in the morning meal was associated with a lower prevalence of hypertension, and that higher energy intake in the evening meal was associated with a higher prevalence of hypertension and greater increase in blood pressure (Almoosawi, Prynne, Hardy, & Stephen, 2013). A possible mechanism to explain why more energy intake in the morning reduces overall energy intake involves physiological response. A large morning meal may lead to suppression of the hungerstimulating hormone ghrelin and induce the satiety-stimulating hormone peptide YY compared to a small morning meal. Another possible mechanism is self-discipline (Junger & van Kampen, 2010; Konttinen, Haukkala, Sarlio-Lahteenkorva, Silventoinen, & Jousilahti, 2009; Will Crescioni et al., 2011). If a person overate during the morning, they would likely intentionally decrease the amount of food consumption during the subsequent meal. Although further research is needed, more energy intake in the morning period may be an effective and healthy way of reducing daily energy intake. We found that fat had a greater effect on overall energy intake than other macronutrients in both sexes (Table 2). This may be a reflection of the difference of mealtimes during morning, afternoon and evening. A fat-rich diet causes overeating during mealtimes, because the content of fat is correlated with palatability. When mealtime is short, i.e. during morning, overeating would be limited, while when mealtime is long, i.e. during dinner, overeating would be promoted. The proportion of protein intake in the evening meal affected overall intake in men, while that of carbohydrate intake in the afternoon and evening meals affected overall intake in women (Table 2). These results are partly inconsistent with a previous study that suggested that the proportion of carbohydrate in the morning meal had a stronger effect on overall energy intake than that of fat, and that the proportion of all macronutrients in the evening meal had no effect on overall energy intake (de Castro, 2007). In the present study, carbohydrate intake in the morning meal did not change overall energy intake. One possible reason for this is that carbohydrate constituted a large proportion (about 55%) of total daily energy intake, and that energy intake from carbohydrate in the morning meal accounted for 14% of total daily energy intake (290 kcal). Therefore, although the high proportion of carbohydrate in the morning meal reduced subsequent (afternoon and evening) energy intake (Table 2), this reduction might have been small and did not significantly exceed the energy intake from carbohydrate in the morning meal. These results suggest that the contribution of each macronutrient to total daily energy intake was not equal. Regarding food choice, a higher proportion of energy intake in the morning meal decreased the amount of energy intake from mainly cereals and meats in the afternoon meal in men. On the other hand, it decreased that from mainly cereals and confectioneries in the afternoon meal in women (Table 4). Regarding energy intake from the meats group, one possible reason is that people may prefer foods with high energy density such as meats to compensate for energy depletion when intake in the morning meal has been in-

7

sufficient. Another reason may be that hungry subjects tend to prefer high-protein foods (Barkeling, Rossner, & Bjorvell, 1990; Hill & Blundell, 1986; Vazquez, Pearson, & Beauchamp, 1982). The increase in energy intake from confectioneries in women might reflect snacking frequency: frequency in our population was significantly higher when the proportion of energy intake in the morning meal was low (data not shown). Previous studies showed that people do not compensate for their energy intake after the consumption of snacks (de Graaf, 2006; Marmonier, Chapelot, Fantino, & Louis-Sylvestre, 2002). Therefore, more frequent consumption of snacks leads to an increase in daily energy intake and the prevalence of obesity (Berteus Forslund, Torgerson, Sjostrom, & Lindroos, 2005). In addition, we speculate that women prefer sweets to meats and that this kind of preference is more important than the balance of macronutrient intake to food choice. Several limitations of this study should be mentioned. First, we were concerned about the under-reporting of energy intake. On average, energy intake estimated by DRs is considered to be underreported by 20% to 25% compared to that estimated using doubly labeled water as standard (Rennie, Coward, & Jebb, 2007). Because underestimation influences the absolute amount of energy intake (de Castro, 2006), we analyzed not only the absolute values but also the proportions of energy intake. Second, the generalizability of our results was hampered by the fact that the subjects were not randomly sampled from the general Japanese population, but were rather volunteers who were possibly health-conscious. In addition, research areas in this study were restricted. Third, we had no information on physical activity, eating-out and the working hours of each research day, and might therefore have failed to adjust for several confounding factors in the mixed models. Fourth, there is no established definition of meals and snacks. The definition of snacks is complex; it may consist of confectionery items or beverages only (Andersson & Rossner, 1996), self-reported criteria (Berteus Forslund et al., 2005; Kim & Kim, 2010), snacking foods like chips, or even light meals (Chamontin, Pretzer, & Booth, 2003; Poulain, 2002). Many studies use self-reported criteria. Here, we distinguished meals from snacks by the amount of energy intake on the basis that people perceive a low amount and a low portion size as a snack (Wansink, Payne, & Shimizu, 2010), albeit that the cut-off points are not clear. Therefore, some foods and beverages which were consumed as snacks might have been better considered a meal. To summarize, we found that greater energy intake in the morning meal may be effective in reducing daily total energy intake, as well as the intake of high fat foods such as meats and confectioneries. These results provide useful information for the development of weight control programs.

67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114

Authorship

115 116 Y.T. performed the statistical analyses and wrote the manu117 script. K.A. assisted in writing and editing the manuscript. S.S. 118 contributed to the concept and design of the study, study proto119 col, and data collection, and assisted in writing and editing the 120 manuscript. H.O. assisted in manuscript preparation. N.H., A.N., H.T., Q6 121 A.M., M.F., and C.D. were involved in the study design, data collec122 tion and data management. 123 124 References Almoosawi, S., Prynne, C. J., Hardy, R., & Stephen, A. M. (2013). Time-of-day of energy intake. Association with hypertension and blood pressure 10 years later in the 1946 British Birth Cohort. Journal of Hypertension, 31(5), 882–892. Andersson, I., & Rossner, S. (1996). Meal patterns in obese and normal weight men. The ‘Gustaf’ study. European Journal of Clinical Nutrition, 50(10), 639–646.

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