European Journal of Nutrition https://doi.org/10.1007/s00394-017-1585-x
ORIGINAL CONTRIBUTION
The association of whole and refined grains consumption with psychological disorders among Iranian adults Omid Sadeghi1,2 · Ammar Hassanzadeh‑Keshteli3 · Hamid Afshar4 · Ahmad Esmaillzadeh2,5,6 · Peyman Adibi7 Received: 29 December 2016 / Accepted: 21 November 2017 © Springer-Verlag GmbH Germany, part of Springer Nature 2017
Abstract Purpose Although several studies have examined the link between different types of carbohydrate consumption and depression and anxiety, limited data are available linking whole and refined grains consumption to psychological disorders. We aimed to investigate the association of whole and refined grains consumption with psychological disorders among Iranian adults. Methods A total of 3172 adult people with age range of 18–55 years were included in this cross-sectional study. Data on grains consumption were collected using a validated dish-based 106-item semi-quantitative food frequency questionnaire. To assess depression and anxiety, Iranian validated version of Hospital Anxiety and Depression Scale (HADS) was applied. Furthermore, psychological distress was examined using General Health Questionnaire (GHQ). Psychological disorders were defined based on standard criteria. Results Mean age of participants was 36.5 ± 7.9 years. Women in the third quartile of whole grains consumption had lower odds for having anxiety (OR 0.62, 95% CI 0.45–0.85) compared with those in the first quartile. This relationship was also seen even after controlling for potential confounders (OR 0.65, 95% CI 0.44–0.96). In contrast, compared with the first quartile, women in the highest quartile of refined grains consumption had greater odds to have depression (OR 1.76, 95% CI 1.00–3.09) and anxiety (OR 2.03, 95% CI 1.00–4.10) after adjusting for covariates. Such relationships were not observed among men. Conclusion Moderate consumption of whole grain foods was inversely associated with anxiety in women, but not in men. Furthermore, we found a significant positive association between refined grains consumption, depression and anxiety in women. Keywords Anxiety · Depression · Diet · Psychological distress · Whole grains
Introduction
Ammar Hassanzadeh-Keshteli: Co-first author. * Ahmad Esmaillzadeh a‑
[email protected] 1
The prevalence of psychological disorders has been growing in both developed and developing countries [1, 2]. As the common psychological disorders, depression and anxiety are associated with a high economic burden, disability, 5
Obesity and Eating Habits Research Center, Endocrinology and Metabolism Molecular, Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran
Students’ Scientific Center, Tehran University of Medical Sciences, Tehran, Iran
6
Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, P.O. Box 14155‑6117, Iran
Department of Community Nutrition, School of Nutrition and Food Science, Isfahan University of Medical Sciences, Isfahan, Iran
7
Integrative Functional Gastroenterology Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
2
3
Department of Medicine, University of Alberta, Edmonton, AB, Canada
4
Psychosomatic Research Center, Isfahan University of Medical Sciences, Isfahan, Iran
13
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chronic disorders and even mortality [3, 4]. It has been estimated that 4.7 and 7.3% of adults, around the world, suffer from depressive and anxiety disorders [5, 6]. In Iran, the prevalence of depression and anxiety in adult population has been reported to be 20 and 20.8%, respectively, which is considered to be high [7]. Therefore, appropriate strategies are required to prevent these conditions. It seems that genetic, psychological and environmental factors, including diet, are involved in the etiology of depression and anxiety [8]. Among dietary intakes, consumption of n-3 PUFAs, folate, sweetened beverages and processed foods including sweetened desserts, fried foods, processed meats, and high-fat dairy products might contribute to psychological disorders [9–13]. In addition, the association between carbohydrate consumption and psychological disorders has received great attention in recent studies [14–16]. For instance, consumption of lactose, fiber, fruit, and vegetables was significantly associated with lower odds of incident depression, while dietary intake of refined grains and high glycemic-index (GI) foods were associated with increased odds of depression [17]. However, little emphasis has been laid down on whole-grain foods in this regard. Whole grains contain high amounts of bioactive compounds including fiber, vitamins B, E, magnesium, antioxidants, and phytoestrogens [18, 19]; some have been shown to protectively affect the risk of psychological disorders [20–22]. B-vitamins including B 1, B3, B6, B9 and B 12 are essential for neuronal function; their deficiencies have been associated with increased risk of depressive symptoms [23, 24]. Furthermore, beneficial effects of vitamins B supplementation as well as antioxidant intake on depression have been demonstrated [25, 26]. However, consumption of foods containing these nutrients, including whole grains, in relation to depression and anxiety has been given less attention. Earlier studies have mostly focused on the association of refined grains and high-GI foods in relation to depression and anxiety [27, 28]. We are aware of only one prospective cohort study that examined the association of whole grains consumption with depression. In a study on 69,954 adults in US, Gangwisch et al., found a non-significant inverse association between consumption of whole grain foods and risk of depression [17]. Investigating the association of whole grains consumption and psychological disorders is particularly relevant for Middle Eastern population, where the psychological disorders are highly prevalent and people are habitually consuming high carbohydrate diets. Given the limited evidence, we aimed to investigate the association of whole and refined grains consumption with depression and anxiety among a large group of Iranian adults.
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Subjects and methods Participants The current cross-sectional study was carried out within the framework of the Study on the Epidemiology of Psychological-Alimentary Health and Nutrition (SEPAHAN) that was performed in a large population of Iranian general adults working in 50 different health centers affiliated to Isfahan University of Medical Sciences (IUMS). Details about the study design, participants and data collection method were described elsewhere [29]. Briefly, we collected data at two separate main phases between April 2010 and May 2010 to increase the accuracy of the data and response rates. At first phase, we distributed 10,087 pretested self-administered questionnaires to collect data on demographic variables along with dietary intakes, and 8691 completed questionnaires were returned (response rate: 86.16%). At the second phase, data on psychological health were collected. After merging data from these two phases, complete information was available for 4763 people. In the current analysis, we excluded participants who had total caloric intakes outside the range of 800–4200 kcal/day, as under-reporters and over-reporters of energy intake (n = 1271). Furthermore, women with pregnancy and lactation (n = 190) and also participants with missing data on anthropometric information as well as dietary intakes were excluded (n = 130). These exclusions resulted in a dataset of 3172 participants including 1398 men and 1774 women (Fig. 1). All participants provided signed informed written consent forms. The Bioethics Committee of Isfahan University of Medical Sciences, Isfahan, Iran approved the study [29].
Dietary assessment Data on usual dietary intakes was collected using a validated Willett-format [30] Dish-based 106-item Semi-quantitative Food Frequency Questionnaire (DS-FFQ), which was designed specifically for Iranian adults. Detailed information about design, foods included as well as the validity of this questionnaire has been reported elsewhere [31]. Briefly, to develop the questionnaire, first we constructed a comprehensive list of foods and dishes commonly consumed by Iranian adults. Then, we selected those which were nutrient-rich, consumed reasonably often, or contributed to between-persons variations from this list. Food items which were consumed at least once a week were considered as common foods. This process led to the remaining of the 106 food items in five different categories in the questionnaire: (1) mixed dishes (cooked
European Journal of Nutrition Fig. 1 Flowchart of study
or canned, 29 items); (2) carbohydrate-based foods (different types of bread, cakes, biscuits and potato, 10 items); (3) dairy products (dairies, butter and cream, 9 items); (4) fruits and vegetables (22 items); and (5) miscellaneous food items and beverages (including sweets, fast foods, nuts, desserts and beverages, 36 items). Participants were asked to report their dietary intakes of foods and mixed dishes based on nine multiple choice frequency response categories varying from “never or less than once a month” to “12 or more times per day.” The frequency response categories for the food list varied from 6 to 9 choices. For foods consumed infrequently, we omitted the high-frequency categories, while for common foods with a high consumption, the number of multiple choice categories increased. For instance, the frequency response for tuna consumption included 6 categories, as follows: never or less than once/month, 1–3 times/month, 1 time per week, 2–4 times/week, 5–6 times/week and 1–2 times/day, and for tea consumption, the frequency response included 9 categories, as follows: never or less than 1 cup/month, 1–3 cups/month, 1–3 cups/week, 4–6 cups/week, 1 cup/day, 2–4 cups/day, 5–7 cups/day, 8–11 cups/day and ≥ 12 cups/day. Finally, daily intakes of all foods and dishes were computed and converted to grams per day using household measures [32]. Furthermore, daily nutrient intakes for each participant were calculated by summing up the nutrient contents of all foods and dishes. To obtain nutrient contents of foods and
dishes, we used the US Department of Agriculture’s (USDA) national nutrient databank [33]. In the current study, wholegrain foods were defined as wheat seed (used for cooking), diet bread (cooked by whole flour) and dark breads including Iranian breads of Sangak and Barbari. In Iranian food culture, whole flour without any refined sugar is used for cooking dark bread. Refined grains were defined as the sum of white breads (eg, the Iranian bread Lavash and Boguette), rice, pasta, noodles, white flour, and biscuits. A validation study was conducted to assess the validity and reliability of DS-FFQ [31, 34]. In mentioned study, a total of 200 randomly selected participants of SEPAHAN project were included. All participants completed the DSFFQ at study baseline and 6 months later. In addition, three detailed dietary records, used as gold standard, were collected from the participants during the validation study. Findings from this study showed that the DS-FFQ could provide reasonably valid and reliable measures of long-term dietary intakes in Iranian population; for instance, the correlation coefficient for dietary carbohydrate intake between DS-FFQ and the average of three dietary records was 0.81.
Assessment of psychological health Depression and anxiety were screened using the Iranian validated version of Hospital Anxiety and Depression Scale (HADS) which is a brief and useful questionnaire
13
to assess psychological disorders and to measure the symptoms and severity of anxiety disorders and depression [35]. It contains fourteen items and consists of two subscales: anxiety and depression. Each item includes a four-point scale; higher scores indicate an increased level of anxiety and depression. Maximum score is 21 for anxiety and depression. Scores of 8 or more on either subscale were considered as psychological disorders, and scores of 0–7 were defined as ‘normal’ in the current study [35]. Overall, our previous investigations revealed that the questionnaire provides relatively valid measures of mental health [35]. To assess psychological distress, we applied the Iranian validated version of General Health Questionnaire (GHQ) that included 12-items [36]. Each item provides a 4-point rating scale (less than usual, no more than usual, rather more than usual, or much more than usual). To calculate the total score of psychological distress for each participant, we used the bimodal scoring method (0-0-1-1). This method gives total scores ranging from 0 to 12; higher scores indicate a greater degree of psychological distress [37]. In the current study, the score of 4 or more was considered as having psychological distress. A validation study on 748 Iranian adults showed a significant inverse correlation between the GHQ-12 and global quality of life scores (r= − 0.56, P < 0.0001) [37].
Assessment of covariates A self-administered questionnaire was used to collect information on age, gender, marital status (single/married), education (under university/ university graduated), smoking status (non-smoker/former smoker/current smoker), family size (≤ 4/>4 members), home ownership (owner/non-owner), history of diabetes mellitus, current use of anti-psychotic medications (including nortriptyline, amitriptyline or imipramine, fluoxetine, citalopram, fluvoxamine and sertraline) and dietary supplements (including intake of Fe, Ca, vitamins and other dietary supplements). To assess the physical activity of individuals, we used the General Practice Physical Activity Questionnaire (GPPAQ), a simple validated questionnaire reflecting adult people’s physical activity by focusing on current general activities. In the current analysis, participants were classified into two categories: physically active (≥ 1 h/week) and physically inactive (< 1 h/ week). The validity of the GPPAQ for the evaluation of usual physical activity has been previously indicated. We applied a self-administered questionnaire to gather data on anthropometric measures including weight and height. Body mass index (BMI) was calculated as weight in kilograms divided by the height in meters squared.
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Statistical analysis First, we calculated energy-adjusted whole and refined grains using nutrient density method [38]. Then, men and women, separately, were categorized by quartiles of energyadjusted whole and refined grains consumption. One-way analysis of variance (ANOVA) was used to examine significant differences in continuous variables across quartiles of whole and refined grains consumption. To assess the distribution of men and women in terms of categorical variables across quartiles of whole and refined grains consumption, we used Chi-square test. We also applied ANOVA to compare dietary intakes of food groups and nutrients across quartiles of whole and refined grains consumption. The association of whole and refined grains intake with psychological disorders in men and women was assessed using binary logistic regression in different models. In the first model, age (continuous) and energy intake (continuous) were adjusted. Further control was made for marital status (single/married), education (under university/university graduated), smoking status (non-smoker/former smoker/current smoker), family size (≤ 4/>4 members), home ownership (owner/ non-owner), diabetes mellitus (yes/no), dietary supplement use (yes/no) and anti-psychotic medications (yes/no) in the second model. Then, we additionally adjusted for dietary intake of fruits, vegetables, red meat, fish, legumes and nuts, whole grains or refined grains, dairy, tea and coffee in the third model. In the fourth model, additional adjustment was done for BMI (continues) to see if the associations are independent of obesity. In the final model, dietary intakes of B-vitamins including vitamin B1, B2, B3, B5, B6, B12 and folate were adjusted to see if the associations was mediated by these vitamins. In all analyses, the first quartile of whole and refined grains consumption was considered as the reference category. To compute the overall trend of odds ratios across increasing quartiles of whole and refined grains consumption, we used these quartiles as an ordinal variable in the logistic regression models. All statistical analyses were separately done for participants with normal weight and overweight, and also for both genders using SPSS software (version 19.0; SPSS Inc, Chicago IL). P values were considered significant at < 0.05.
Results In total, 3172 participants (1398 men and 1774 women) were included in the statistical analysis. In terms of general characteristics, participants who were included in the current study were not significantly different from those who were excluded. Mean age of participants was 36.5 ± 7.9 years, 55.9% were women. Overall, 20.4% of men and 33.7% of women were scored to be depressed. In addition, 8.4% of
European Journal of Nutrition
men and 17.3% of women were classified as anxious. Based on GHQ questionnaire, psychological distress was prevalent among 16.6% of men and 27.1% of women. General characteristics of men and women across categories of whole and refined grains consumption are presented in Table 1. Men in the top quartile of whole grains consumption were older and more likely to be married and physically active compared with men in the bottom quartile. Among women, those in the highest quartile of whole grains consumption were older and more likely to be educated and use dietary supplements and had lower odds to be married and scored as anxious than those in the first quartile. In terms of refined grains consumption, men in the top quartile of refined grains were younger, have lower BMI and were less likely to be physically active and more likely to be educated than those in the bottom quartile. In addition, women in the highest quartile were less likely to be educated, physically active, home owner, and use dietary supplements and more likely to be depressed, anxious and psychologically distressed compared with those in lowest quartile. No other significant differences were found in general characteristics across quartiles of whole and refined grains consumption. Selected food groups and nutrients intakes of men and women across quartiles of whole and refined grains consumption are indicated in Table 2. Men and women in top quartile of whole grains consumption had greater intake of fruits, vegetables, red meat, fish, legume and nuts, energy, protein, fat, carbohydrate, dietary fiber, vitamin B1, B2, B3, B5, B6, B12, folate, magnesium, iron and n-3 fatty acids, and lower intake of refined grains compared with those in the bottom quartile. Across categories of refined grains consumption, men with the greatest intake had significantly lower intakes of fruits, vegetables, red meat, fish, legume and nuts, whole grains, dairy, protein, fat, dietary fiber, vitamin B6, B2, B12, magnesium and n-3 fatty acids and higher intakes of tea and coffee, energy, carbohydrate, vitamin B1, B3, folate and iron than those with the lowest intake. Such findings were also seen among women except for energy intakes that was higher in participants in the top quartile of refined grains that those in the bottom quartile. Gender-stratified multivariable-adjusted odds ratios for psychological disorders across quartiles of whole and refined grains consumption are shown in Table 3. Compared with the first quartile, women in the third quartile of whole grains consumption had lower odds of anxiety (OR: 0.62, 95% CI: 0.45–0.85); such that even after controlling for potential confounders, women in the third quartile of whole grains consumption were 35% less likely to be anxious than those in the first quartile (OR: 0.65, 95% CI: 0.44–0.96). In terms of refined grains consumption, after all confounders were taken into account, a significant positive association was found between refined grains consumption and risk of depression among women; such that women in the fourth quartile of
refined grains consumption had 79% greater odds of depression compared with those in the first quartile (OR: 1.79, 95% CI: 1.00-3.09). In addition, women with the highest consumption of refined grains had increased risk of anxiety compared with those that consumed the lowest amount of refined grains (OR: 1.80, 95% CI: 1.27–2.56). This association was also significant in fully adjusted model (OR: 2.03, 95% CI: 1.00-4.10). Although a significant positive association was found between refined grains consumption and psychological distress (OR: 1.79, 95% CI: 1.39–2.42), this relationship became non-significant when all confounders were taken into account. Among men, no significant relationship was seen between whole or refined grains consumption and psychological disorders either before or after adjustment for potential confounders. Stratified analysis based on BMI (≥ 25/<25) showed a significant inverse association between whole grains consumption and anxiety among participants with normal weight (OR 0.67, 95% CI 0.46–0.99). However, this association became non-significant in fully adjusted model. In addition, among normal weight individuals, refined grains consumption was positively associated with risk of anxiety (OR 1.60, 95% CI 1.05–2.43). Such positive association was also seen for psychological distress among individuals with overweight (OR 2.01, 95% CI 1.39–2.90). However, both mentioned associations were non-significant when potential confounders were taken into account. No other significant association was found between whole or refined grains consumption and psychological disorders either among normal weight participants or those with overweight (Table 4).
Discussion In the current study, we found a significant inverse association between moderate consumption of whole grains [third quartile] and anxiety among women. This relationship was also seen even after controlling for potential confounders. In contrast, refined grains consumption was positively associated with depression and anxiety in women in fully adjusted model. Such relationships were not observed among men. To the best of our knowledge, this is the first study in the Middle East to examine the association of whole and refined grain consumption with psychological disorders. Based on global burden of diseases, psychological disorders including depression and anxiety are the fifth cause of disability adjusted life years which is associated with increased risk of all non-fatal diseases and mortality [39]. Diet is a potential factor influencing the risk of psychological disorders [40]. Among dietary factors, the association between different types of carbohydrate consumption and psychological disorders has been investigated in earlier studies [14, 15]. However, little attention has been laid down on
13
13 18.4 49 13.7 13.7 3 57.5 14.2 3.2 20.1 8.6 15.2
Physically active (≥ 1 h/week) (%)
Overweight or obese (%)
Family size (> 4 people) (%)
Smoking status (Current smoker) (%)
Diabetes (%)
Home ownership (owner) (%)
Dietary supplement use (%)
Anti-psychotic medications (%)
Depression (%)
Anxiety (%)
Psychological distress (%)
34.53 ± 7.80 24.01 ± 4.10
0 34.45 ± 7.28 24.41 ± 4.21 77.8 66.0 5.9 37.3 11.1 13.1 1.2 59.4 36.7 8.0 37.2 22.2 29.5
Age (year)
BMI (kg/m2)
Marital status (married) (%)
Education (university graduated) (%)
Physically active (≥ 1 h/week) (%)
Overweight or obese (%)
Family size (> 4 people) (%)
Smoking status (Current smoker) (%)
Diabetes (%)
Home ownership (owner) (%)
Dietary supplement use (%)
Anti-psychotic medications (%)
Depression (%)
Anxiety (%)
Psychological distress (%)
Obtained from ANOVA or Chi-square test, where appropriate
a
Data are presented as mean ± standard deviation (SD) or percent
29.3
12.3
33.5
5.4
43.1
59.4
0.8
15.9
13.0
36.0
5.9
71.1
67.7
3.6 ± 0.8
648
Mean ± SD
239
18.6
10.1
22.9
4.0
10.2
60.6
2.2
14.6
11.5
54.4
20.4
52.7
n
Women
52.2
Education (university graduated) (%)
91.5
86.3
Marital status (married) (%)
23.4
15.1
32.0
6.8
45.7
59.9
1.4
13.7
12.8
37.6
8.6
71.6
72.4
24.54 ± 3.83
35.21 ± 7.38
10.8 ± 3.9
444
20.0
8.8
22.9
4.9
11.1
61.4
2.3
12.6
16.3
54.6
21.1
47.1
90.3
25.39 ± 3.40
26.2
16.2
32.3
8.4
47.6
60.9
0.7
12.6
12.9
42.2
7.4
73.8
70.8
24.92 ± 3.94
36.59 ± 7.56
53.9 ± 34.9
443
13.8
7.3
18.8
2.9
10.3
53.9
3.7
17.5
13.8
54.7
29.5
51.3
93.5
25.61 ± 3.44
0.13
0.001
0.24
0.46
0.001
0.31
0.73
0.60
0.75
0.29
0.31
0.03
0.04
0.40
< 0.001
0.10
0.72
0.48
0.48
0.26
0.21
0.63
0.32
0.43
0.27
0.001
0.45
0.03
0.40
25.20 ± 3.43
21.7
14.0
31.7
8.8
49.2
63.7
0.9
14.2
12.6
40.0
9.5
69.1
69.8
24.84 ± 3.97
35.99 ± 7.70
90.1 ± 24.2
443
14.0
7.4
20.1
2.9
11.2
62.2
2.6
16.3
12.9
51
26.9
43.8
88.2
25.39 ± 3.55
39.22 ± 8.70
25.22 ± 3.49
< 0.001
BMI (kg/m2)
39.69 ± 7.93
38.18 ± 7.87
37.16 ± 8.31
Age (year)
39.17 ± 8.46
90.1 ± 24.2
Q1
349 54.2 ± 33.6
Q4
0
11.4 ± 3.8
Q3
26.6
17.1
30.6
7.7
42.3
59.2
1.6
15.3
11.5
38.3
7.7
71.4
75.3
24.64 ± 4.22
35.26 ± 7.74
139.5 ± 10.3
444
15.1
7.4
19.5
5.1
11.1
58.0
3.4
16.0
14.0
57.4
25.4
51.4
92.3
25.77 ± 3.53
39.09 ± 8.14
139.5 ± 10.3
350
Q2
Quartiles of refined grain
Mean ± SD
3.9 ± 1.1
Q2
Pa
n
Men
Q1
Quartiles of whole grain
Table 1 General characteristics of men and women across quartiles of whole and refined grains consumption
27.0
16.4
32.5
5.0
39.2
60.8
0.9
11.7
11.7
38.3
7.7
74.3
73.6
24.17 ± 3.85
34.77 ± 7.22
178.5 ± 13.6
444
18.6
9.6
21.5
4.0
14.0
59.7
2.9
14.0
14.0
52.9
20.0
52.9
89.9
25.26 ± 3.51
37.47 ± 7.94
178.5 ± 13.6
350
Q3
33.2
22.8
42.0
8.4
39.5
56.0
0.9
12.9
13.1
37.2
2.9
65.5
74.5
24.41 ± 4.11
34.74 ± 7.23
253.2 ± 39
443
16.6
9.9
22.5
2.6
10.9
52.4
2.6
11.7
15.2
49.6
16.3
55.0
89.3
25.01 ± 3.15
38.07 ± 8.08
253.2 ± 39
349
Q4
0.002
0.006
0.001
0.12
0.001
0.02
0.69
0.44
0.86
0.87
0.001
0.03
0.18
0.09
0.05
0.24
0.47
0.77
0.25
0.53
0.26
0.89
0.13
0.85
0.17
0.002
0.01
0.50
0.04
0.02
P
European Journal of Nutrition
0
Mean ± SD
212.3 ± 5.1
71.9 ± 2
9.4 ± 0.9
47.7 ± 2
Vegetables
Red meat
Fish
Legume and nuts
386.8 ± 14.9
Tea and coffee
1.6 ± 0.04
1.6 ± 0.03
22.2 ± 0.5
5.7 ± 0.09
1.7 ± 0.03
658.7 ± 16.2
2.8 ± 0.06
Vitamin B1 (mg/day)
Vitamin B2 (mg/day)
Vitamin B3 (mg/day)
Vitamin B5 (mg/day)
Vitamin B6 (mg/day)
Folate (µg/day)
Vitamin B12 (µg/day)
1.5 ± 0.04
n-3 Fatty acids (g/ day)
0
Mean ± SD
7.6 ± 0.3
42.3 ± 1.2
Fish
Legume and nuts
Whole grain
66 ± 1.6
214.2 ± 5
Vegetables
Red meat
306.8 ± 9.4
Fruits
Food groups (g/day)
648
n
Women
21.4 ± 0.5
15.5 ± 0.3
Fe (mg/day)
57.8 ± 2.2
11 ± 0.8
92.4 ± 3.1
279.5 ± 8.9
391.3 ± 19.5
3.6 ± 0.8
239
2.1 ± 0.06
360.2 ± 6.6
Magnesium (mg/day) 227.3 ± 4.7
3.4 ± 0.08
908.4 ± 25.8
2.2 ± 0.04
7.1 ± 0.1
30.4 ± 0.7
2.1 ± 0.04
2.2 ± 0.07
24.8 ± 0.5
18.2 ± 0.3
116.9 ± 2.3
Dietary fiber (g/day)
91.8 ± 1.6
Fat (g/day)
105.2 ± 2.1
2800 ± 50
338.9 ± 7.7
81.5 ± 1.5
477.1 ± 23.1
369.8 ± 17.8
524.8 ± 16.4
64.7 ± 2.8
11.2 ± 0.9
97.7 ± 3.3
257.6 ± 11
284.7 ± 14.1
3.9 ± 1.1
226
Q2
Carbohydrate (g/day) 254.6 ± 5.2
2148 ± 37
Energy (Kcal/day)a
Protein (g/day)
Nutrients
393.5 ± 10.7
339.3 ± 13.9
Refined grain
Dairy
Whole grain
237.9 ± 9.1
Fruits
Food groups (g/day)
473
n
Men
Q1
Quartiles of whole grain
51.7 ± 0.6
11.3 ± 0.6
81.2 ± 2.4
253.9 ± 7.2
348.2 ± 11.9
10.8 ± 3.9
444
1.8 ± 0.04
18.9 ± 0.3
339.1 ± 5.6
3.2 ± 0.07
789.7 ± 17.4
2.1 ± 0.03
6.5 ± 0.1
26.7 ± 0.5
1.9 ± 0.03
1.9 ± 0.05
23.2 ± 0.4
307.5 ± 6
107.1 ± 1.9
95.6 ± 1.8
2545 ± 42
414.9 ± 15.5
351 ± 14.7
416.3 ± 11.1
58.8 ± 1.9
10.3 ± 0.6
91.1 ± 2.6
242.9 ± 6
297 ± 13.4
11.4 ± 3.8
350
Q3
51.6 ± 2.3
11.2 ± 0.5
72.1 ± 2.1
245.7 ± 7.4
366.2 ± 10.8
53.9 ± 34.9
443
1.8 ± 0.04
20.6 ± 0.4
407.6 ± 7.4
3.1 ± 0.07
890.6 ± 18.3
2.2 ± 0.04
6.7 ± 0.1
29.4 ± 0.5
2.1 ± 0.04
2.1 ± 0.04
27.3 ± 0.5
334.4 ± 6.2
106 ± 1.9
100.5 ± 1.8
2653 ± 43
403 ± 17.7
343.6 ± 14.3
363.2 ± 10.6
61.3 ± 2.3
12.7 ± 0.7
86.7 ± 2.8
249.7 ± 6.3
302.7 ± 11.9
54.2 ± 33.6
349
Q4
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.006
0.59
< 0.001
< 0.001
0.04
< 0.001
< 0.001
< 0.001
Pb
85.1 ± 5.6
53.9 ± 1.8
12 ± 0.6
81.7 ± 2.7
276.2 ± 5.8
435.5 ± 14.3
90.1 ± 24.2
443
1.9 ± 0.05
16.6 ± 0.3
367.4 ± 7.9
3.6 ± 0.08
642.5 ± 15.6
2.2 ± 0.04
6.4 ± 0.1
24.3 ± 0.5
2 ± 0.04
1.1 ± 0.03
24.4 ± 0.5
281.5 ± 6.2
110.1 ± 2.3
98.1 ± 2
2462 ± 47
369.2 ± 17.5
434.8 ± 2.5
75.1 ± 6.1
65.2 ± 2.9
15.2 ± 1
93.5 ± 3
261.7 ± 7.9
383 ± 16.9
90.1 ± 24.2
349
Q1
40.5 ± 2.8
52.5 ± 1.4
12 ± 0.6
82.2 ± 2.2
258.1 ± 5.8
412.1 ± 8.1
139.5 ± 10.3
444
1.9 ± 0.04
17.7 ± 0.3
353 ± 6
3.3 ± 0.06
724.6 ± 13.8
2.2 ± 0.03
6.5 ± 0.1
25.8 ± 0.5
1.9 ± 0.03
1.7 ± 0.03
23.4 ± 0.4
288.7 ± 5.1
111.3 ± 1.9
96.8 ± 1.7
2506 ± 39
452.3 ± 17.5
355.4 ± 13.3
55.1 ± 4.1
63.5 ± 2.2
12.7 ± 1.2
94.2 ± 2.8
263.2 ± 6.7
294.3 ± 10.6
139.5 ± 10.3
350
Q2
Quartiles of refined grain
Table 2 Selected food groups and nutrients intakes of men and women across quartiles of whole and refined grains consumption
25.1 ± 2
48 ± 1.6
9.1 ± 0.5
75.4 ± 1.9
236.2 ± 6.2
305.9 ± 9.1
178.5 ± 13.6
444
1.65 ± 0.04
17.5 ± 0.3
316.4 ± 5.8
2.9 ± 0.06
743.9 ± 15.7
1.9 ± 0.03
6.1 ± 0.1
25.1 ± 0.5
1.7 ± 0.03
1.7 ± 0.04
21.3 ± 0.4
282.1 ± 5.5
99.2 ± 1.8
89 ± 1.7
2349 ± 41
415.9 ± 16.7
318.9 ± 12.9
31.7 ± 2.9
53.4 ± 1.8
8.9 ± 1.6
87 ± 2.4
230.7 ± 5.7
244 ± 8.3
178.5 ± 13.6
350
Q3
13.8 ± 1.2
41.7 ± 1.4
6.5 ± 0.4
60.3 ± 1.8
194.2 ± 5.1
220.1 ± 8.1
253.2 ± 39
443
1.6 ± 0.04
22.5 ± 0.5
318.1 ± 6.2
2.4 ± 0.05
1044.7 ± 24.3
1.8 ± 0.03
6.5 ± 0.1
30.7 ± 0.7
1.9 ± 0.04
2.6 ± 0.07
22 ± 0.4
353.5 ± 7.7
92.4 ± 1.7
90.7 ± 1.9
2598 ± 50
412.4 ± 17.4
283.9 ± 10.8
18.9 ± 1.7
44.3 ± 1.8
6.3 ± 0.4
63.5 ± 1.9
190.9 ± 5.7
184.5 ± 7.8
253.2 ± 39
349
Q4
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.03
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.001
0.001
0.009
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
P
European Journal of Nutrition
13
13
332.6 ± 10.7
353 ± 10.9
Tea and coffee
1.5 ± 0.03
1.5 ± 0.02
20.6 ± 0.3
5.4 ± 0.07
1.7 ± 0.02
635.6 ± 12.2
2.6 ± 0.08
Vitamin B1 (mg/day)
Vitamin B2 (mg/d)
Vitamin B3 (mg/day)
Vitamin B5 (mg/day)
Vitamin B6 (mg/day)
Folate (µg/day)
Vitamin B12 (µg/day) 20.3 ± 0.4
14.7 ± 0.2
1.5 ± 0.03
Fe (mg/day)
n-3 Fatty acids (g/ day)
Obtained from ANOVA
b
Energy was not adjusted
a
Data are presented as mean ± standard error (SE)
2 ± 0.06
361.2 ± 5.5
Magnesium (mg/day) 270 ± 3.9
3.3 ± 0.08
852.6 ± 19.4
2.2 ± 0.04
7 ± 0.1
28.7 ± 0.5
2 ± 0.03
2.1 ± 0.05
25.4 ± 0.5
18.6 ± 0.3
114.6 ± 2
Dietary fiber (g/day)
86.7 ± 1.3
Fat (g/day)
99.8 ± 1.7
2749 ± 42
339.5 ± 6.6
74.2 ± 1.1
Protein (g/day)
373.1 ± 16.3
383.5 ± 16.4
483.7 ± 13.5
Q2
Carbohydrate (g/day) 253.7 ± 4.2
2063 ± 30
Energy (Kcal/day)a
Nutrients
381.2 ± 8.6
Dairy
Q1
Quartiles of whole grain
Refined grain
Table 2 (continued)
1.7 ± 0.04
16.5 ± 0.3
316.8 ± 5.2
3 ± 0.06
694.2 ± 13.8
1.9 ± 0.03
6 ± 0.09
23.8 ± 0.4
1.7 ± 0.03
1.6 ± 0.03
22 ± 0.4
279.2 ± 5.1
98.1 ± 1.7
86.3 ± 1.5
2309 ± 37
350 ± 12.3
351.4 ± 12.7
364.4 ± 8.8
Q3
1.7 ± 0.04
18.4 ± 0.3
374.2 ± 6.1
2.7 ± 0.06
802.7 ± 14.5
2 ± 0.03
6.2 ± 0.09
26.2 ± 0.4
2 ± 0.7
2.9 ± 0.03
26.6 ± 0.4
316.2 ± 5.3
95.9 ± 1.7
84.9 ± 1.4
2444 ± 38
356.2 ± 12.2
330.6 ± 11.6
315.3 ± 7.8
Q4
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.72
0.04
< 0.001
Pb
1.9 ± 0.05
15.7 ± 0.3
358.9 ± 6.5
3.2 ± 0.06
632.6 ± 14
2 ± 0.03
6.1 ± 0.09
23.3 ± 0.4
2 ± 0.03
1.6 ± 0.3
25.3 ± 0.5
285.5 ± 5.5
102.9 ± 1.9
90 ± 1.6
2376 ± 41
365.3 ± 3.1
451.7 ± 13.8
Q1
1.8 ± 0.04
16.3 ± 0.2
333.4 ± 4.8
3.1 ± 0.06
672.1 ± 10.7
0.07 ± 0.03
6.2 ± 0.09
23.5 ± 0.4
1.8 ± 0.03
1.6 ± 0.2
23.3 ± 0.3
284.5 ± 4.6
101.6 ± 1.7
89 ± 1.4
2365 ± 13
328.7 ± 11.6
391.4 ± 13.4
Q2
Quartiles of refined grain
1.6 ± 0.03
16.7 ± 0.3
305.5 ± 4.7
2.7 ± 0.04
716.7 ± 12.8
1.8 ± 0.03
5.9 ± 0.08
23.5 ± 0.4
1.7 ± 0.03
1.7 ± 0.3
21.3 ± 0.4
277.1 ± 4.8
93.5 ± 1.4
82.5 ± 1.3
2249 ± 34
365.7 ± 12.4
323 ± 11.4
Q3
1.4 ± 0.02
18.5 ± 0.4
282.5 ± 5.1
2.1 ± 0.04
863.6 ± 18.6
1.6 ± 0.03
5.7 ± 0.1
25.3 ± 0.5
1.5 ± 0.03
2 ± 0.5
19.5 ± 0.4
301.8 ± 16.8
84.4 ± 1.5
76.9 ± 1.5
2259 ± 41
372.3 ± 12.5
244.4 ± 9
Q4
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.001
0.01
< 0.001
< 0.001
< 0.001
0.01
< 0.001
< 0.001
0.02
0.07
< 0.001
P
European Journal of Nutrition
Men n 473 Mean ± SD 0 Depression Crude 1 1 Model 1a 1 Model 2b c 1 Model 3 1 Model 4d 1 Model 5e Anxiety Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1 Model 5 1 Psychological distress Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1 Model 5 1 Women n 648 Mean ± SD 0 Depression Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1 Model 5 1 Anxiety Crude 1
Q1 350 11.4 ± 3.8 1.17 (0.83–1.65) 1.15 (0.78–1.70) 1.17 (0.78–1.75) 1.17 (0.77–1.77) 1.11 (0.72–1.70) 1.15 (0.74–1.79) 1.02 (0.62–1.67) 1.04 (0.57–1.87) 1.06 (0.57–1.95) 1.08 (0.57–2.04) 0.95 (0.48–1.88) 1.14 (0.57–2.30) 1.39 (0.96–2.00) 1.38 (0.91–2.09) 1.44 (0.94–2.22) 1.49 (0.96–2.32) 1.43 (0.90–2.26) 1.59 (0.99–2.55) 444 10.8 ± 3.9 0.79 (0.61–1.03) 0.79(0.61–1.04) 0.82 (0.62–1.09) 0.81 (0.60–1.09) 0.83 (0.61–1.12) 0.83 (0.61–1.13) 0.62 (0.45–0.85)
1.18 (0.8–1.74) 1.10 (0.70–1.72) 1.08 (0.68–1.71) 0.97 (0.60–1.56) 1.11 (0.68–1.80) 1.12 (0.69–1.83)
1.18 (0.68–2.05) 1.22 (0.64–2.31) 1.16 (0.59–2.25) 1.08 (0.54–2.15) 1.23 (0.61–2.49) 1.28 (0.62–2.64)
1.27 (0.83–1.93) 1.18 (0.73–1.90) 1.10 (0.66–1.82) 1.09 (0.65–1.82) 1.14 (0.67–1.93) 1.16 (0.68–1.98)
239 3.6 ± 0.8
0.85 (0.62–1.16) 0.85(0.60–1.20) 0.85 (0.59–1.23) 0.78 (0.54–1.15) 0.81 (0.55–1.20) 0.83 (0.56–1.22)
0.49 (0.31–0.75)
Q3
226 3.9 ± 1.1
Q2
Quartiles of whole grain
0.67 (0.49–0.92)
0.80(0.62–1.04) 0.84(0.64–1.10) 0.87 (0.65–1.16) 0.76 (0.55–1.06) 0.76 (0.54–1.06) 0.75 (0.51–1.10)
443 53.9 ± 34.9
0.88 (0.59–1.31) 0.93 (0.60–1.45) 0.95 (0.59–1.51) 0.98 (0.59–1.62) 0.95 (0.55–1.61) 1.48 (0.79–2.78)
0.83 (0.49–1.40) 0.91 (0.49–1.69) 0.95 (0.50–1.79) 1.00 (0.50–2.00) 1.13 (0.55–2.28) 2.17 (0.93–5.04)
0.91 (0.64–1.30) 0.87 (0.57–1.31) 0.89 (0.58–1.37) 0.89 (0.56–1.42) 0.88 (0.55–1.43) 1.08 (0.61–1.90)
349 54.2 ± 33.6
Q4
p-trend
1
1 1 1 1 1 1
443 90.1 ± 24.2
1 1 1 1 1 1
1 1 1 1 1 1
1 1 1 1 1 1
349 90.1 ± 24.2
Q1
1.26 (0.87–1.82)
0.94 (0.71–1.26) 0.95 (0.71–1.29) 0.99 (0.72–1.36) 0.96 (0.68–1.35) 0.92 (0.65–1.30) 1.06 (0.73–1.53)
444 139.5 ± 10.3
1.09 (0.71–1.66) 0.94 (0.59–1.50) 0.81 (0.49–1.34) 0.72 (0.42–1.23) 0.60 (0.34–1.06) 0.65 (0.36–1.19)
0.99 (0.56–1.77) 0.86 (0.44–1.67) 0.78 (0.39–1.55) 0.72 (0.34–1.52) 0.74 (0.34–1.62) 0.86 (0.37–2.00)
0.96 (0.66–1.40) 0.88 (0.57–1.35) 0.82 (0.52–1.28) 0.69 (0.43–1.12) 0.69 (0.42–1.13) 0.74 (0.43–1.25)
350 139.5 ± 10.3
Q2
Quartiles of refined grain
Table 3 Odds ratio (95% CI) for psychological disorders according to quartiles of whole and refined grains consumption
1.20 (0.83–1.74)
1.03 (0.78–1.37) 0.97 (0.72–1.30) 1.08 (0.79–1.47) 0.90 (0.63–1.28) 0.90 (0.63–1.29) 1.15 (0.75–1.77)
444 178.5 ± 13.6
1.39 (0.93–2.09) 1.40 (0.90–2.18) 1.36 (0.85–2.16) 1.04 (0.61–1.75) 0.92 (0.53–1.59) 1.15 (0.60–2.20)
1.32 (0.77–2.28) 1.20 (0.64–2.22) 1.13 (0.59–2.15) 0.87 (0.42–1.82) 0.88 (0.41–1.89) 1.26 (0.50–3.18)
1.08 (0.75–1.57) 1.17 (0.77–1.77) 1.13 (0.74–1.74) 0.91 (0.56–1.47) 0.83 (0.51–1.37) 0.99 (0.55–1.80)
350 178.5 ± 13.6
Q3
1.80 (1.27–2.56)
1.55 (1.18–2.05) 1.53 (1.15–2.05) 1.49 (1.10–2.03) 1.07 (0.71–1.60) 1.10 (0.73–1.66) 1.76 (1.00-3.09)
443 253.2 ± 39
1.40 (0.93–2.10) 1.19 (0.76–1.87) 1.19 (0.74–1.90) 0.78 (0.40–1.49) 0.77 (0.39–1.50) 1.17 (0.46–2.97)
1.38 (0.80–2.37) 1.19 (0.64–2.20) 1.30 (0.69–2.47) 0.88 (0.37–2.11) 0.98 (0.40–2.40) 2.19 (0.62–7.6)
1.15 (0.79–1.66) 1.03 (0.68–1.56) 1.03 (0.67–1.58) 0.81 (0.44–1.47) 0.79 (0.43–1.47) 1.15 (0.48–2.73)
349 253.2 ± 39
Q4
p-trend
European Journal of Nutrition
13
13 0.61 (0.43–0.85) 0.64 (0.44–0.91) 0.64 (0.44–0.93) 0.65 (0.44–0.94) 0.65 (0.44–0.96) 0.73 (0.55–0.96) 0.78 (0.58–1.04) 0.82 (0.61–1.11) 0.82 (0.60–1.12) 0.79 (0.57–1.08) 0.79 (0.57–1.09)
0.99 (0.71–1.37) 1.02 (0.71–1.45) 1.07 (0.74–1.55) 1.07 (0.73–1.58) 1.11 (0.75–1.64) 1.10 (0.74–1.63)
0.84 (0.64–1.11) 0.92 (0.69–1.23) 0.97 (0.72–1.31) 0.92 (0.66–1.29) 0.94 (0.66–1.33) 0.93 (0.63–1.39)
0.68 (0.49–0.96) 0.75 (0.52–1.08) 0.72 (0.48–1.08) 0.70 (0.46–1.07) 0.82 (0.51–1.33)
Q4
p-trend
1 1 1 1 1 1
1 1 1 1 1
Q1
1.30 (01.96–1.78) 1.32 (0.96–1.82) 1.35 (0.97–1.88) 1.33 (0.94–1.90) 1.35 (0.94–1.94) 1.45 (0.98–2.14)
1.33 (0.90–1.95) 1.51 (1.00-2.28) 1.40 (0.91–2.17) 1.32 (0.85–2.07) 1.51 (0.93–2.43)
Q2
Quartiles of refined grain
1.33 (0.98–1.82) 1.28 (0.93–1.77) 1.33 (0.96–1.86) 1.15 (0.79–1.67) 1.19 (0.81–1.74) 1.31 (0.84–2.06)
1.20 (0.82–1.77) 1.42 (0.94–2.16) 1.19 (0.75–1.88) 1.20 (0.75–1.92) 1.44 (0.83–2.49)
Q3
1.79 (1.32–2.42) 1.71 (1.25–2.34) 1.63 (1.18–2.27) 1.15 (0.75–1.76) 1.19 (0.77–1.83) 1.44 (0.79–2.61)
1.90 (1.31–2.74) 1.98 (1.33–2.96) 1.36 (0.82–2.27) 1.44 (0.86–2.43) 2.03 (1.00-4.10)
Q4
p-trend
Model 4: further controlled for BMI
Model 5: additionally adjusting for B-vitamins including thiamine, riboflavin, niacin, pentatonic acid, pyridoxine, folate and Cobalamin
e
d
Model 3: further adjusted for intake of food groups including fruits, vegetables, red meat, fish, legumes and nuts, whole grains or refined grains, dairy, tea and coffee
c
Model 2: additionally adjusted for marital status, education, family size, smoking status, physical activity, home ownership, diabetes mellitus, dietary supplement use and anti-psychotic medications
b
Q3
0.53 (0.33–0.84) 0.51 (0.31–0.84) 0.51 (0.30–0.85) 0.52 (0.31–0.88) 0.50 (0.29–0.85)
Q2
Model 1: adjusted for age and energy intake
a
Data are OR (95% CI)
Model 1 1 Model 2 1 Model 3 1 Model 4 1 Model 5 1 Psychological distress Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1 Model 5 1
Q1
Quartiles of whole grain
Table 3 (continued)
European Journal of Nutrition
European Journal of Nutrition
whole and refined grains consumption. Based on our findings, moderate consumption of whole grains was inversely associated with anxiety in women. In line with our findings, Gangwisch et al. reported an inverse association between whole grains consumption and psychological disorders in a prospective cohort study [17]. However, this relationship was not seen after taking potential confounders into account. In another study, Kim et al. reported that healthy dietary pattern, characterized by high consumption of whole grains, was inversely associated with mental disorders scores in US women, but not in men [41]. In a cross-sectional study, it was observed that high adherence to mediterranean dietary pattern, which is characterized by high intake of whole grains, was associated with lower odds for having anxiety in Australian adults [42]. In opposite to our findings, some studies found no significant effects of diets rich in whole grains on psychological disorders [43, 44]. Differences in previous findings might be explained by different processing and cooking of whole grain foods in different cultures or different glycemic indices of different whole grain foods. Consumption of whole grains or low-GI foods can decrease the incidence of insulin resistance [45]. It has been shown that insulin resistance is related to neuro-cognitive deficits which are similarly happened in patients with psychological disorders such as depression and anxiety [46]. In addition, whole grain products are rich in carbohydrate and B-vitamins including B1, B3, B6, B9 and B12 which are essential for neuronal function [23, 24]. Carbohydrate and vitamin B6 has been known to increase the synthesis of serotonin in the brain [47, 48]. Although the association between whole grains consumption and anxiety revealed no change after controlling for intakes of B-vitamins, other components of whole grains including dietary fiber and magnesium might have a role in this regard [18, 19, 21]. The lack of significant inverse association between the fourth quartile of whole grains consumption and psychological disorders might be due to the low number of participants with these conditions in this quartile which can in turn result in the wide confidence intervals. It is also possible that the beneficial effects of whole grains consumption on psychological disorders might occur in the range of required energy intake. High energy intake in individuals with high consumption of whole grains might cause obesity which is a known risk factor for depression and anxiety. However, we controlled for total energy intake in the analyses, it must be paid attention that such controlling in the statistical analyses might not entirely exclude the effect of energy intake on the associations. In the current study, refined grains consumption was positively associated with greater odds of having depression and anxiety. Our findings were in line with previous studies reporting the health benefits of diets low in refined grains. Data from a cross-sectional study had shown an
inverse association between dietary diversity score and anxiety [49]. Diverse diets, low in refined grains, were found to be associated with better mental health. Some other studies also support the hypothesis that diets with low amounts of refined grains might reduce the risk of depression or anxiety [50, 51]. In contrast, some other investigations have failed to find any significant association between diets high in refined grain products and risk of psychological disorders [52, 53]. Different findings for psychological distress compared with depression and anxiety might be explained by different psychological processes of these disorders and further studies are needed to shed light on this issue in the future. There are some mechanisms by which refined grains consumption might enhance the risk of depression and anxiety. Consumption of refined grains or high-GI foods increases the risk of inflammation and cardiovascular diseases [54], and these conditions are known as risk factors for psychological disorders [55]. Furthermore, refined grains of high-GI diets results in a postprandial hyperglycemia and hyperinsulinemia [56, 57] and this might decrease blood glucose levels to a concentration which is a threshold for the secretion of autonomic hormones including adrenaline, cortisol, glucagon, and growth hormone [58]. In the current study, we observed a gender disparity in the association of whole and refined grains consumption with psychological disorders. This could be explained by the differential influence of gonadal steroids on mood. In addition, the accuracy of dietary assessment might be different between men and women. Previous studies have indicated that actual food choices [59], self-reported preferences for foods [60] and accuracy of reported dietary intakes [61] are different between men and women. In the current study, no significant association was found between whole or refined grains consumption and psychological disorders either among normal weight participants or those with overweight. Whole grain foods are used in the framework of weight loss diets. Therefore, some obese individuals might consume more whole grain products compared with normal weight people. In addition, it is well known that individuals failed to lose weight are at greater odds of suffering from depression compared with those were successful in this process. Although BMI was controlled for in the multivariate models, it is possible that such controlling may not entirely exclude the effect of BMI from the analysis because losing weight in weight loss diets is low (something between 2 and 4 kg/month). Such a low amount of weight loss cannot significantly affect BMI in short duration. Several limitations should be considered in the interpretation of current findings. Based on the cross-sectional design of our study, we cannot confer a causal link between whole and refined grain intake and psychological disorders. Therefore, our findings should be confirmed by prospective studies. Although a validated FFQ was used to assess dietary
13
13
BMI < 25 n 596 Mean ± SD 0 Depression Crude 1 1 Model 1a 1 Model 2b c 1 Model 3 1 Model 4d Anxiety Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1 Psychological distress Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1 BMI ≥ 25 n 468 Mean ± SD 0 Depression Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1 Anxiety Crude 1 Model 1 1 Model 2 1 Model 3 1 Model 4 1
Q1 402 9.7 ± 3.4 0.86 (0.65–1.14) 0.80 (0.58–1.09) 0.84 (0.61–1.17) 0.81 (0.58–1.14) 0.82 (0.58–1.15) 0.67 (0.46–0.99) 0.63 (0.42–0.96) 0.71 (0.46–1.09) 0.75 (0.48–1.17) 0.83 (0.53–1.31) 0.96 (0.71–1.30) 0.99 (0.71–1.37) 1.06 (0.75–1.49) 1.04 (0.73–1.48) 1.07 (0.75–1.52) 351 12.5 ± 4.1 0.96 (0.71–1.31) 1.02 (0.73–1.43) 1.04 (0.74–1.48) 1.02 (0.71–1.46) 1.03 (0.71–1.49) 0.70 (0.47–1.05) 0.74 (0.48–1.15) 0.72 (0.46–1.15) 0.74 (0.46–1.20) 0.71 (0.44–1.16)
0.92 (0.65–1.3) 0.91 (0.62–1.36) 0.91 (0.60–1.37) 0.86 (0.56–1.33) 0.89 (0.58–1.38)
0.68 (0.42–1.11) 0.67 (0.39–1.15) 0.67 (0.37–1.18) 0.68 (0.37–1.23) 0.69 (0.37–1.26)
1.15 (0.80–1.65) 1.18 (0.78–1.77) 1.16 (0.75–1.78) 1.14 (0.73–1.78) 1.15 (0.73–1.80)
232 4.1 ± 1.2
0.99 (0.69–1.41) 1.05 (0.71–1.56) 1.05 (0.70–1.59) 1.01 (0.66–1.54) 1.01 (0.65–1.55)
0.55 (0.33–0.90) 0.64 (0.37–1.11) 0.59 (0.33–1.06) 0.63 (0.35–1.15) 0.62 (0.34–1.14)
Q3
208 3.4 ± 0.8
Q2
Quartiles of whole grain
0.79 (0.53–1.17) 0.93 (0.60–1.42) 0.93 (0.59–1.46) 1.00 (0.60–1.65) 1.13 (0.63–2.03)
0.90 (0.65–1.23) 0.90 (0.64–1.27) 0.90 (0.63–1.30) 0.79 (0.53–1.18) 0.99 (0.62–1.58)
349 58.7 ± 38.4
0.93 (0.69–1.26) 0.95 (0.68–1.33) 1.01 (0.71–1.43) 0.97 (0.66–1.43) 1.06 (0.67–1.66)
0.71 (0.48–1.04) 0.61 (0.40–0.93) 0.69 (0.44–1.08) 0.67 (0.41–1.11) 1.08 (0.61–1.93)
0.76 (0.57–1.01) 0.77 (0.56–1.05) 0.80 (0.58–1.12) 0.78 (0.54–1.13) 0.73 (0.47–1.12)
402 49.7 ± 30.3
Q4
p-trend
1 1 1 1
349 87.8 ± 25 1 1 1 1 1 1
1 1 1 1 1
1 1 1 1 1
1 1 1 1 1
402 89.2 ± 23.7
Q1
1.33 (0.82–2.14) 1.21 (0.73–2.02) 1.19 (0.69–2.06) 1.35 (0.75–2.45)
351 138.6 ± 10.3 1.38 (0.89–2.16) 0.90 (0.65–1.27) 0.84 (0.58–1.20) 0.73 (0.50–1.07) 0.61 (0.40–0.93) 0.76 (0.48–1.18)
1.08 (0.76–1.52) 1.05 (0.72–1.52) 1.06 (0.72–1.56) 1.07 (0.71–1.61) 1.08 (0.70–1.67)
0.91 (0.58–1.45) 0.89 (0.54–1.48) 0.99 (0.58–1.69) 0.90 (0.51–1.57) 0.94 (0.52–1.70)
0.96 (0.70–1.34) 0.93 (0.65–1.32) 1.03 (0.71–1.49) 1.03 (0.70–1.53) 1.05 (0.69–1.59)
402 140 ± 11.1
Q2
Quartiles of refined grain
Table 4 Odds ratio (95% CI) for psychological disorders according to quartiles of whole and refined grains consumption
0.91 (0.55–1.50) 1.02 (0.60–1.73) 0.96 (0.52–1.74) 1.14 (0.58–2.26)
351 175.8 ± 13.1 1.10 (0.69–1.75) 0.82 (0.58–1.15) 0.77 (0.54–1.12) 0.80 (0.55–1.16) 058 (0.38–0.90) 0.81 (0.49–1.33)
1.57 (1.13–2.19) 1.64 (1.15–2.33) 1.75 (1.21–2.5) 1.53 (1.01–2.30) 1.54 (0.93–2.55)
1.52 (0.99–2.31) 1.59 (1.01–2.50) 1.85 (1.13–3.01) 1.31 (0.76–2.23) 1.55 (0.81–2.98)
1.31 (0.96–1.80) 1.29 (0.92–1.81) 1.48 (1.04–2.11) 1.29 (0.86–1.92) 1.38 (0.85–2.20)
402 180.2 ± 13.5
Q3
1.49 (0.93–2.37) 1.46 (0.89–2.40) 1.26 (0.64–2.46) 1.64 (0.69–3.93)
349 250.7 ± 42.4 1.63 (1.06–2.52) 1.14 (0.82–1.58) 1.13 (0.79–1.60) 1.06 (0.74–1.53) 0.72 (0.43–1.19) 1.35 (0.69–2.64)
1.31 (0.94–1.84) 1.29 (0.90–1.86) 1.24 (0.84–1.81) 0.92 (056–1.50) 0.97 (0.48–1.97)
1.60 (1.05–2.43) 1.83 (1.17–2.86) 1.93 (1.19–3.14) 1.05 (0.57–1.92) 1.59 (0.67–3.81)
1.54 (1.13–2.10) 1.53 (1.10–2.14) 1.54 (1.08–2.20) 1.16 (0.73–1.85) 1.40 (0.72–2.72)
402 250.3 ± 42.1
Q4
p-trend
European Journal of Nutrition
Model 4: additionally adjusting for B-vitamins including thiamine, riboflavin, niacin, pentatonic acid, pyridoxine, folate and Cobalamin
Model 3: further adjusted for intake of food groups including fruits, vegetables, red meat, fish, legumes and nuts, whole grains or refined grains, dairy, tea and coffee
d
Model 1: adjusted for age and energy intake
b
a
Data are OR (95% CI)
c
0.73 (0.52–1.03) 0.82 (0.56–1.18) 0.80 (0.54–1.18) 0.78 (0.50–1.21) 0.96 (0.58–1.59) 0.84 (0.60–1.18) 0.88 (0.62–1.26) 0.91 (0.63–1.33) 0.96 (0.65–1.43) 0.95 (0.64–1.41) 0.86 (0.58–1.26) 0.88 (0.58–1.34) 0.89 (0.57–1.38) 0.88 (0.56–1.39) 0.90 (0.57–1.43) Model 1 Model 2 Model 3 Model 4
1 1 1 1
Psychological distress Crude 1
Model 2: additionally adjusted for marital status, education, family size, smoking status, physical activity, home ownership, diabetes mellitus, dietary supplement use and anti-psychotic medications
2.01 (1.39–2.90) 1.85 (1.26–2.72) 1.86 (1.25–2.78) 1.10 (0.63–1.91) 1.97 (0.95–4.08) 1.14 (0.77–1.68) 1.00 (0.66–1.51) 1.07 (0.70–1.65) 0.76 (0.46–1.23) 1.05 (0.60–1.84) 1.36 (0.93–1.99) 1.28 (0.86–1.91) 1.18 (0.77–1.81) 1.01 (0.64–1.60) 1.27 (0.77–2.07) 1 1 1 1 1
Q3 Q2 Q1 Q2 Q1
Quartiles of whole grain
Table 4 (continued)
Q3
Q4
p-trend
Quartiles of refined grain
Q4
p-trend
European Journal of Nutrition
intakes in our study, the closed-end response nature of the questionnaire might increase the rate of misclassification. Moreover, our study population consist of Isfahani adults. Therefore, the extrapolation of our findings to all Iranian adults must be done cautiously. Although several confounders were adjusted for to assess the association between whole or refined grain foods consumption and psychological disorders, further controlling for other variables such as menopausal status, hormone therapy, number of pregnancy and time between last pregnancy might be needed to reach an independent association. Unfortunately, we did not collect data on these variables in SEPAHAN. In conclusion, moderate consumption of whole grain foods was inversely associated with depression and anxiety in women, but not in men. Furthermore, we found a significant positive association between moderate refined grains consumption and psychological distress in women. Such relationship was not seen among men. Additional studies, particularly of prospective design, are required to confirm our findings. Acknowledgements This study was supported by Isfahan University of Medical Sciences. Dr. Ahmad Esmaillzadeh was supported by a grant from Iran National Science Foundation (INSF).
Compliance with ethical standards Ethics All participants provided signed informed written consent forms. The Bioethics Committee of Isfahan University of Medical Sciences, Isfahan, Iran approved the study [29]. Conflict of interest Authors declared no personal or financial conflicts of interest.
References 1. Murphy JM, Horton NJ, Laird NM, Monson RR, Sobol AM, Leighton AH (2004) Anxiety and depression: a 40-year perspective on relationships regarding prevalence, distribution, and comorbidity. Acta Psychiatr Scand 109:355–375. https://doi. org/10.1111/j.1600-0447.2003.00286.x 2. Mojtabai R (2011) National trends in mental health disability, 1997–2009. Am J Public Health 101:2156–2163. https://doi. org/10.2105/AJPH.2011.300258 3. Olesen J, Gustavsson A, Svensson M, Wittchen HU, Jo¨nsson B (2012) The economic cost of brain disorders in Europe. Eur J Neurol 19:155–162. https://doi. org/10.1111/j.1468-1331.2011.03590.x 4. Sobocki P, Jo¨nsson B, Angst J, Rehnberg C (2006) Cost of depression in Europe. J Ment Health Policy Econ 9:87–98 5. Baxter A, Scott K, Vos T, Whiteford H (2012) Global prevalence of anxiety disorders: a systematic review and metaregression. Psychol Med 10:1–14. https://doi.org/10.1017/ S003329171200147X 6. Ferrari A, Somerville A, Baxter A, Norman R, Patten S, Vos T, Whiteford H (2012) Global variation in the prevalence and incidence of major depressive disorder: a systematic review of the
13
7. 8. 9.
10.
11.
12.
13. 14.
15.
16.
17.
18. 19. 20.
21. 22.
23.
European Journal of Nutrition epidemiological literature. Psychol Med 43:471–481. https://doi. org/10.1017/S0033291712001511 Noorbala AA, Bagheri Yazdi SA, Yasamy MT et al (2004) Mental health survey of the adult population in Iran. Br J Psychiatry 184:70–73 Saveanu RV, Nemeroff CB (2012) Etiology of depression: genetic and environmental factors. Psychiatr Clin North Am 35:51–71. https://doi.org/10.1016/j.psc.2011.12.001 Guo X, Park Y, Freedman ND, Sinha R, Hollenbeck AR, Blair A, Chen H (2014) Sweetened beverages, coffee, and tea and depression risk among older US adults. PLoS One 9:e94715. https://doi. org/10.1371/journal.pone.0094715 Akbaraly TN, Brunner EJ, Ferrie JE, Marmot MG, Kivimaki M, Singh-Manoux A (2009) Dietary pattern and depressive symptoms in middle age. Br J Psychiatry 195:408–413. https://doi. org/10.1192/bjp.bp.108.058925 Sánchez-Villegas A, Toledo E, de Irala J, Ruiz-Canela M, PlaVidal J, Martinez-Gonzalez MA (2012) Fast-food and commercial baked goods consumption and the risk of depression. Public Health Nutr 15:424–432. https://doi.org/10.1017/S1368980011001856 Skarupski KA, Tangney C, Li H, Ouyang B, Evans DA, Morris MC (2010) Longitudinal association of vitamin B-6, folate, and vitamin B-12 with depressive symptoms among older adults over time. Am J Clin Nutr 92:330–335. https://doi.org/10.3945/ ajcn.2010.29413 Hibbeln JR (2009) Depression, suicide and deficiencies of omega-3 essential fatty acids in modern diets. World Rev Nutr Diet 99:17–30. https://doi.org/10.1159/000192992 Cheatham RA, Roberts SB, Das SK, Gilhooly CH, Golden JK, Hyatt R, Lerner D, Saltzman E, Lieberman HR (2009) Long-term effects of providing low and high glycemic load energy diets on mood and cognition. Physiol Behav 98:374–379. https://doi. org/10.1016/j.physbeh Nabb SL, Benton D (2006) The effect of the interaction between glucose tolerance and breakfasts varying in carbohydrate and fibre on mood and cognition. Nutr Neurosci 9:161–168. https://doi. org/10.1080/10284150600955099 Micha R, Rogers PJ, Nelson M (2011) Glycaemic index and glycaemic load of breakfast predict cognitive function and mood in school children: a randomized controlled trial. Br J Nutr 106:1552–1561. https://doi.org/10.1017/S0007114511002303 Gangwisch JE, Hale L, Garcia L, Malaspina D, Opler MG, Payne ME et al (2015) High glycemic index diet as a risk factor for depression: analyses from the Women’s Health Initiative. Am J Clin Nutr 102:454–463. https://doi.org/10.3945/ajcn.114.103846 Slavin J, Jacobs D, Marquart L (1997) Whole grain consumption and chronic disease: protective mechanisms. Nutr Cancer 27:14–21. https://doi.org/10.1080/01635589709514495 Shahyoun N, Jacques P, Zhang X, Joun W et al (2006) Wholegrain intake inversely is associated with the metabolic syndrome and mortality in older adults. Am J Clin Nutr 83:124–131 Yary T, Soleimannejad K, Abd Rahim F, Kandiah M, Aazami S, Poor SJ et al (2010) Contribution of diet and major depression to incidence of acute myocardial infarction (AMI). Lipids Health Dis 9:133. https://doi.org/10.1186/1476-511X-9-133 Serefko A, Szopa A, Poleszak E (2016) Magnesium and depression. Magnesium Res 29:112–119. https://doi.org/10.1684/ mrh.2016.0407 Moylan S, Berk M, Dean OM, Samuni Y, Williams LJ, O’Neil A et al (2014) Oxidative & nitrosative stress in depression: why so much stress? Neurosci Biobehav Rev 45:46–62. https://doi. org/10.1016/j.neubiorev Mikkelsen K, Stojanovska L, Apostolopoulos V (2016) The effects of vitamin B in depression. Current medicinal chemistry. Curr Med Chem 23:4317–4337
13
24. Hvas AM, Juul S, Bech P, Nexo E (2004) Vitamin B6 level is associated with symptoms of depression. Psychother Psychosom 73:340–343. https://doi.org/10.1159/000080386 25. Nguyen PH, Grajeda R, Melgar P, Marcinkevage J, DiGirolamo AM, Flores R et al (2009) Micronutrient supplementation may reduce symptoms of depression in Guatemalan women. Arch Latinoam Nutr 59:278–286 26. Gariballa S (2014) Poor vitamin C status is associated with increased depression symptoms following acute illness in older people. Int J Vitam Nutr Res 84:12–17. https://doi. org/10.1024/0300-9831/a000188 27. Haghighatdoost F, Azadbakht L, Keshteli AH, Feinle-Bisset C, Daghaghzadeh H, Afshar H et al (2016) Glycemic index, glycemic load, and common psychological disorders. Am J Clin Nutr 103:201–209. https://doi.org/10.3945/ajcn.114.105445 28. Murakami K, Miyake Y, Sasaki S, Tanaka K, Yokoyama T, Ohya Y et al (2008) Dietary glycemic index and load and the risk of postpartum depression in Japan: the Osaka Maternal and Child Health Study. J Affect Disord 110:174–179. https://doi. org/10.1016/j.jad.2007.12.230 29. Adibi P, Keshteli AH, Esmaillzadeh A, Afshar H et al (2012) The study on the epidemiology of psychological, alimentary health and nutrition (SEPAHAN): overview of methodology. J Res Med Sci 17:S291-S297 30. Willett W (2013) Nutritional epidemiology. Oxford University Press, Oxford 31. Keshteli A, Esmaillzadeh A, Rajaie S, Askari G, Feinle-Bisset C, Adibi P (2014) A dish based semi-quantitative food frequency questionnaire for assessment of dietary intakes in epidemiologic studies in Iran: design and development. Int J Prev Med 5:29–36 32. Ghaffarpour M, Houshiar-Rad A, Kianfar H (1999) The manual for household measures, cooking yields factors and edible portion of foods. Nashre Olume Keshavarzy, Tehran, pp 1–40 33. Kimura Y, Wada T, Okumiya K et al (2012) Eating alone among community-dwelling Japanese elderly: association with depression and food diversity. J Nutr Health Aging 16:728–731. https:// doi.org/10.1007/s12603-012-0067-3 34. Salehi-Abargouei A, Esmaillzadeh A, Azadbakht L et al (2016) Nutrient patterns and their relation to general and abdominal obesity in Iranian adults: findings from the SEPAHAN study. Eur J Nutr 55:505–518. https://doi.org/10.1007/s00394-015-0867-4 35. Montazeri A, Vahdaninia M, Ebrahimi M, Jarvandi S (2003) The Hospital Anxiety and Depression Scale (HADS): translation and validation study of the Iranian version. Health Qual Life Outcomes 1:14 36. Schmitz N, Kruse J, Heckrath C, Alberti L, Tress W (1999) Diagnosing mental disorders in primary care: the General Health Questionnaire (GHQ) and the Symptom Check List (SCL-90-R) as screening instruments. Soc Psychiatry Psychiatr Epidemiol 34:360–366 37. Montazeri A, Harirchi AM, Shariati M, Garmaroudi G, Ebadi M, Fateh A (2003) The 12-item General Health Questionnaire (GHQ12): translation and validation study of the Iranian version. Health Qual Life Outcomes 1:66. https://doi.org/10.1186/1477-7525-1-66 38. Howe GR, Miller AB, Jain M (1986) Re: Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:157–159 39. Whiteford HA, Degenhardt L, Rehm J, Baxter AJ, Ferrari AJ, Erskine HE, Charlson FJ, Norman RE, Flaxman AD, Johns N (2013) Global burden of disease attributable to mental and substance use disorders: findings from the Global Burden of Disease Study 2010. Lancet 382:1575–1586. https://doi.org/10.1016/ S0140-6736(13)61611-6 40. Opie RS, O’Neil A, Itsiopoulos C, Jacka FN (2014) The impact of whole-of-diet interventions on depression and anxiety: a
European Journal of Nutrition systematic review of randomised controlled trials. Public Health Nutr 18:2074–2093. https://doi.org/10.1017/S1368980014002614 41. Kim WK, Shin D, Song WO (2016) Are Dietary Patterns Associated with Depression in U.S. Adults? J Med Food 19:1074–1084. https://doi.org/10.1089/jmf.2016.0043 42. Crichton GE, Bryan J, Hodgson JM, Murphy KJ (2013) Mediterranean diet adherence and self-reported psychological functioning in an Australian sample. Appetite 70:53–59. https://doi. org/10.1016/j.appet.2013.06.088 43. McMillan L, Owen L, Kras M, Scholey A (2011) Behavioural effects of a 10-day Mediterranean diet. Results from a pilot study evaluating mood and cognitive performance. Appetite 56:143– 147. https://doi.org/10.1016/j.appet.2010.11.149 44. Forster SE, Powers HJ, Foulds GA et al (2012) Improvement in nutritional status reduces the clinical impact of infections in older adults. J Am Geriatr Soc 60:1645–1654. https://doi. org/10.1111/j.1532-5415.2012.04118.x 45. McKeown NM, Meigs JB, Liu S, Saltzman E, Wilson PW, Jacques PF (2004) Carbohydrate nutrition, insulin resistance, and the prevalence of the metabolic syndrome in the Framingham Offspring Cohort. Diabetes Care 27:538–546 46. McIntyre RS, Kenna HA, Nguyen HT, Law CW, Sultan F, Woldeyohannes HO, Adams AK, Cheng JS, Lourenco M, Kennedy SH et al (2010) Brain volume abnormalities and neurocognitive deficits in diabetes mellitus: points of pathophysiological commonality with mood disorders? Adv Ther 27:63–80. https://doi. org/10.1007/s12325-010-0011-z 47. Gougeon L, Payette H, Morais JA, Gaudreau P, Shatenstein B, Gray-Donald K (2016) Intakes of folate, vitamin B6 and B12 and risk of depression in community-dwelling older adults: the Quebec Longitudinal Study on Nutrition and Aging. Eur J Clin Nutr 70:380–385. https://doi.org/10.1038/ejcn.2015.202 48. Wurtman RJ, Wurtman JJ (1995) Brain serotonin, carbohydratecraving, obesity and depression. Obes Res 3:477S-80S 49. Poorrezaeian M, Siassi F, Qorbani M et al (2015) Association of dietary diversity score with anxiety in women. Psychiatry Res 230:622–627. https://doi.org/10.1016/j.psychres.2015.10.016 50. Sánchez-Villegas A, Martínez-González MA, Estruch R et al (2013) Mediterranean dietary pattern and depression: the PREDIMED randomized trial. BMC Med 11:208. https://doi. org/10.1186/1741-7015-11-208 51. Michalak J, Zhang XC, Jacobi F (2012) Vegetarian diet and mental disorders: results from a representative
52.
53.
54.
55. 56.
57.
58. 59.
60. 61.
community survey. Int J Behav Nutr Phys Act 9:67. https://doi. org/10.1186/1479-5868-9-67 Lai JS, Oldmeadow C, Hure AJ et al (2016) Longitudinal diet quality is not associated with depressive symptoms in a cohort of middle-aged Australian women. Br J Nutr 115:842–850. https:// doi.org/10.1017/S000711451500519X Baskin R, Hill B, Jacka FN et al (2015) Antenatal dietary patterns and depressive symptoms during pregnancy and early postpartum. Matern Child Nutr 13:e12218. https://doi.org/10.1111/ mcn.12218 Lopez-Garcia E, Schultze MB, Fung TT, Meigs JB, Rifai N, Manson JE, Hu FB (2004) Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr 80:1029–1035 Rumsfeld JS, Ho PM (2005) Depression and cardiovascular disease: a call for recognition. Circulation 111:250–253. https://doi. org/10.1161/01.CIR.0000154573.62822.89 Bao J, Atkinson F, Petocz P, Willett WC, Brand-Miller JC (2011) Prediction of postprandial glycemia and insulinemia in lean, young, healthy adults: glycemic load compared with carbohydrate content alone. Am J Clin Nutr 93:984–996. https://doi. org/10.3945/ajcn.110.005033 Seaquist ER, Anderson J, Childs B, Cryer P, Dagogo-Jack S, Fish L, Heller SR, Rodriguez H, Rosenzweig J, Vigersky R (2013) Hypoglycemia and diabetes: a report of a workgroup of the American Diabetes Association and The Endocrine Society. Diabetes Care:1384–1395. https://doi.org/10.2337/dc12-2480 Ludwig DS (2002) The glycemic index: physiological mechanisms relating to obesity, diabetes, and cardiovascular disease. JAMA 287:2414–2423 Beer-Borst S, Hercberg S, Morabia A et al (2000) Dietary patterns in six european populations: results from EURALIM, a collaborative European data harmonization and information campaign. Eur J Clin Nutr 54:253–262 O’Doherty Jensen K, Holm L (1999) Preferences, quantities and concerns: socio-cultural perspectives on the gendered consumption of foods. Eur J Clin Nutr 53:351–359 Marks GC, Hughes MC, van der Pols JC (2006) Relative validity of food intake estimates using a food frequency questionnaire is associated with sex, age, and other personal characteristics. J Nutr 136:459–465
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