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ORIGINAL RESEARCH COMMUNICATION |
1 From the National Institute of Health and Nutrition, Tokyo, Japan (KM, SS, YT, and YH); the Department of Nutrition Sciences, Kagawa Nutrition University, Saitama, Japan (HO); the Division of Environmental Medicine, Center for Community Medicine, Jichi Medical University, Tochigi, Japan (HH, EO, and FK); and Core Research for Evolutional Science and Technology, Japan Science and Technology Cooperation, Kawaguchi City, Japan (EO and FK)
2 Supported mainly by grants from the Japanese Ministry of Health, Labor and Welfare, the Ministry of Agriculture and Forestry, and Core Research for Evolutional Science and Technology, Japan Science and Technology Cooperation. 3 Address reprint requests to F Kayama, Division of Environmental Medicine, Center for Community Medicine, Jichi Medical University, 3311-1 Yakushiji, Minami-Kawachi, Kawachi-gun, Tochigi 329-0498, Japan. E-mail: kayamaf{at}jichi.ac.jp.
| ABSTRACT |
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Objective: We examined the cross-sectional associations between dietary GI and GL and several metabolic risk factors in healthy Japanese women with traditional dietary habits.
Design: The subjects were 1354 Japanese female farmers aged 2078 y from 5 regions of Japan. Dietary GI and GL were assessed with a self-administered diet-history questionnaire. Body mass index (BMI) was calculated as weight (kg) divided by the square of height (m). Fasting blood samples were collected for biochemical measurements.
Results: The mean dietary GI was 67, and the mean dietary GL (/1000 kcal) was 88 (GI for glucose = 100). White rice (GI = 77) was the major contributor to dietary GI and GL (58.5%). After adjustment for potential dietary and nondietary confounding factors, dietary GI was positively correlated with BMI (n = 1354; P for trend = 0.017), fasting triacylglycerol (n = 1349; P for trend = 0.001), fasting glucose (n = 764; P for trend = 0.022), and glycated hemoglobin (n = 845; P for trend = 0.038). Dietary GL was independently negatively correlated with HDL cholesterol (n = 1354; P for trend = 0.004) and positively correlated with fasting triacylglycerol (P for trend = 0.047) and fasting glucose (P for trend = 0.012).
Conclusions: Both dietary GI and GL are independently correlated with several metabolic risk factors in subjects whose dietary GI and GL were primarily determined on the basis of the GI of white rice.
Key Words: Glycemic index glycemic load white rice body mass index triacylglycerol glucose glycated hemoglobin HDL cholesterol Japanese women epidemiology Japanese Multi-centered Environmental Toxicants Study JMETS
| INTRODUCTION |
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Recent results from a limited number of observational studies have suggested that diets with a low GI, a low GL, or both have a beneficial effect on several metabolic risk factors for cardiovascular disease and type 2 diabetes, such as body mass index (BMI; in kg/m2) (6), HDL cholesterol (711), triacylglycerol (9, 10, 12), and glycated hemoglobin (Hb A1c) (12, 13). However, almost all studies of dietary GI or dietary GL and metabolic risk factors have been conducted in Western countries, whereas, to our knowledge, only one small study (10) was carried out in Asian countries, including Japan.
For Japanese people, rice is the food that contributes most to total carbohydrate and energy intake (43% and 29%, respectively), which is a characteristic seldom observed in Western people (14). Therefore, a different correlation of dietary GI or dietary GL and metabolic risk factors may exist between Western and Japanese populations. Additionally, whereas cardiovascular disease is the second leading cause of all death in Japan (15), the number of Japanese people with type 2 diabetes is estimated to be no fewer than 6.8 million (16); thus, as is the case in Western people, these are serious health problems in Japan. Consequently, we examined the cross-sectional associations between dietary GI and GL and several metabolic risk factors for cardiovascular disease and type 2 diabetes, including BMI, fasting serum triacylglycerol, fasting plasma glucose, Hb A1c, and serum total, HDL, and LDL cholesterol in a group of apparently healthy Japanese women.
| SUBJECTS AND METHODS |
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A total of 1407 women aged 2078 y completed both a medical examination and the lifestyle-related questionnaires. Subjects excluded from the present study were those with previously diagnosed diabetes (n = 15) or cardiovascular disease (n = 18), those with extremely low or high energy intakes (<600 or >4000 kcal/d; n = 10), and those with missing covariate information (n = 4). Furthermore, subjects with missing information regarding dependent variables, were excluded from the analysis of LDL cholesterol (n = 6), glucose (n = 609), and Hb A1c (n = 527), and subjects who ate breakfast before blood was drawn were excluded from the analysis of fasting triacylglycerol and glucose (n = 5). Thus, the final sample was 1354 for BMI and serum total and HDL cholesterol, 1348 for serum LDL cholesterol, 1349 for fasting serum triacylglycerol, 764 for fasting plasma glucose, and 845 for Hb A1c; however, some subjects were included in more than one exclusion category. Further exclusion of subjects with a diagnosis of hyperglycemia, dyslipidemia, hypercholesterolemia, or a combination thereof (n = 24 for BMI, cholesterol, and triacylglycerol and n = 17 for glucose and Hb A1c) did not alter the findings of the present study; therefore, these subjects were included in the analyses.
Metabolic risk factors
At the medical examination site, each subject's weight (measured while wearing light clothes and no shoes) was measured with a set of balance scales calibrated to 0.01 kg. Body height was also measured at the site. The BMI of each subject was calculated as weight (kg) divided by the square of height (m). Peripheral blood samples were obtained from subjects after an overnight fast. Blood was collected in evacuated tubes containing no additives, allowed to clot, and centrifuged at 3000 x g for 10 min at room temperature to separate the serum. Blood samples for blood sugar measurement were collected in hydrogen fluoridecontaining tubes. All of the following biochemical variables of the samples were assayed at Mitsubishi Kagaku Bio-Clinical Laboratories Inc (Itabashi, Tokyo, Japan) within 3 d of collection to avoid significant degradation. Total cholesterol, HDL cholesterol, and triacylglycerol were measured by enzymatic assay methods. Serum LDL-cholesterol concentrations were calculated by using the Friedewald equation (19) for subjects with fasting serum triacylglycerol concentrations <400 mg/dL. Hb A1c was measured by latex agglutinationturbidimetric immunoassay. In-house quality-control procedures for all of the abovementioned assays were fulfilled at Mitsubishi Kagaku Bio-Clinical Laboratories Inc.
Dietary assessment
Dietary habits during the past month were assessed with a self-administered diet-history questionnaire (DHQ) (2022), which was completed by each subject at home and was checked by
2 dietitians during the medical examination. The DHQ is a 16-page structured questionnaire that consists of the following 7 sections: general dietary behaviors, major cooking methods, consumption frequency and portion size of 6 alcoholic beverages, semiquantitative frequency of intake of 121 selected food and nonalcoholic beverage items, dietary supplements, consumption frequency and amount of 19 staple foods (rice, bread, noodles, and other wheat foods) and miso (fermented soybean paste) soup, and open-ended items for foods consumed regularly (
1 time/wk) but not appearing in the DHQ. The food and beverage items and portion sizes in the DHQ were derived primarily from data in the National Nutrition Survey of Japan and several recipe books for Japanese dishes (20). Measures of dietary intake for 147 food and beverage items, energy, fat, total carbohydrate, alcohol, and dietary fiber were calculated by using an ad hoc computer algorithm developed for the DHQ, which was based on the Standard Tables of Food Composition in Japan (23). Information on dietary supplements and data from the open-ended questionnaire items were not used in the calculation of dietary intake. Detailed descriptions of the methods used for calculating dietary intake and the validity of the DHQ were published elsewhere (2022). Pearson's correlation coefficients between the DHQ and 3-d dietary records were 0.48 for energy, 0.55 for fat, and 0.48 for total carbohydrate in 47 women (20). In addition, Pearson's correlation coefficients between the DHQ and 16-d dietary records were 0.79 for alcohol and 0.69 for dietary fiber in 92 women (S Sasaki, unpublished observations, 2004).
Calculation of dietary GI and GL
The GI of a food is defined as the 2-h incremental area under the blood glucose response curve after consumption of a food portion containing a specific amount (usually 50 g) of available carbohydrate, divided by the corresponding area after consumption of a portion of a reference food (usually glucose or white bread) containing the same amount of available carbohydrate, and multiplied by 100 to be expressed as a percentage (24). We calculated dietary GI by multiplying the percentage contribution of each individual food to daily available carbohydrate intake by the food's GI value and summed these products. Available carbohydrate was calculated as total carbohydrate minus dietary fiber (24). We also calculated dietary GL by multiplying the dietary GI by the total amount of daily available carbohydrate intake (divided by 100).
To determine the GI value of each food for these calculations, each food item on the DHQ was directly matched to foods in the international table of GI (24), in several publications about the GI of Japanese foods (2527), and in a recent article about the GI of potatoes (28). Glucose was used as the reference (GI for glucose = 100). The white breadbased GI values were transformed into glucose-based GI values by multiplying the white breadbased GI by 0.7, as in Western studies (24, 28), or by 0.73 [= 100/137 (white breadbased GI value of white bread/white breadbased GI value of glucose)] as in Japanese studies (27). The white ricebased GI values were transformed into glucose-based GI values by multiplying white ricebased GI by 0.82 [= 100/122 (white rice-based GI of white rice/white rice-based GI of glucose)] (25, 26). When more than one GI value was available, the mean GI values was used. Ten foods for which a GI value had not been determined were assigned a value according to the nearest comparable food, as follows: Chinese noodles were assigned the GI of instant noodles, Japanese-style pancakes were assigned the GI of pizza, jellies were assigned the GI of pudding, lotus roots were assigned the GI of carrots, vegetable juice was assigned the GI of tomato juice, curry and roux in stew were assigned the GI of white rice with curry, nutritional-supplement drinks were assigned the GI of sports drinks, nutritional supplement bars were assigned the GI of a sports bar, and ground fish-meat products and boiled-fish, shellfish, and seaweed in soy sauce were assigned the GI of fish fingers. Although alcoholic beverages contain little carbohydrate, large quantities of several alcoholic beverages, such as beer and sake, may raise glucose concentrations slightly; however, by definition, the GI is based on 50 g available carbohydrate. Thus, we ignored alcoholic beverages during the calculation of dietary GI and GL. Furthermore, foods with a very low available carbohydrate content were excluded because their GI values cannot be tested. The cutoff for exclusion of foods was set at 3.5 g available carbohydrate per serving (6). Of the total 147 food and beverage items included in the DHQ, 6 (4.1%) are alcoholic beverages, 8 (5.4%) contain no available carbohydrate, and 63 (42.9%) contain <3.5 g available carbohydrate per serving. The calculation of dietary GI and GL was thus based on the remaining 70 items with GI values ranging from 16 to 91. The GI value of each item is presented in Table 1
. In the present study, the available carbohydrate content of these 70 items contributed to 94.0 ± 2.5% (
± SD) of total available carbohydrate intake, which is comparable with previous studies (6, 10).
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Statistical analysis
Dietary GI and GL were examined in relation to the 7 metabolic risk factors: BMI; serum total, HDL, and LDL cholesterol; fasting serum triacylglycerol; fasting plasma glucose; and Hb A1c. We used crude values for dietary GI and energy-adjusted values for dietary GL (/1000 kcal) because, by definition, dietary GI is a measure of carbohydrate quality, not quantity, whereas dietary GL is a measure of the combination of carbohydrate quality and quantity. The mean (±SE) values for these metabolic factors were calculated according to quintiles of dietary GI and GL after multivariate adjustment for potential confounding variables. Confounding variables included residential area (5 categories), age (
39, 4049, 5059, 6069, and
70 y), menopausal status (premenopausal or postmenopausal), current smoking (no or yes), dietary supplement use (no or yes), rate of eating (fast, medium, or slow), physical activity level (quintiles), energy intake (quintiles), percentage of energy as fat (quintiles), alcohol intake (nondrinkers, >0 to <1% of energy, or
1% of energy), and energy-adjusted intake (g/1000 kcal) of dietary fiber (quintiles). In the analyses, except for the analysis of BMI, current BMI (quintiles) and BMI at age 20 y (quintiles) were also included as confounding variables. Linear trends with increasing levels of dietary GI and GL were tested by assigning each participant the median value for the category and modeling this value as a continuous variable. All statistical analyses were carried out by using SAS statistical software (version 8.2; SAS Institute Inc, Cary, NC). All reported P values are 2-tailed, and a P value <0.05 was considered statistically significant.
| RESULTS |
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| DISCUSSION |
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Concerns have been expressed regarding the utility of the GI for mixed meals (32, 33). However, many researchers have shown that the GI of a mixed meal can be predicted consistently as the mean of the GI values of each of the component foods, weighted according to their relative contribution to carbohydrate intake (3436). In reality, studies using standardized techniques have observed high correlation coefficients between observed and calculated GI values, ranging from 0.84 to 0.99 (3436). Dietary GI and GL values in the present study were similar when compared with those in a previous Japanese study (67 compared with 64 for GI and 168 compared with 150 for GL) (10). However, the dietary GI and GL values observed in the present and previous (10) Japanese studies were considerably higher than the corresponding values in Western countries (4860 for GI and 84120 for GL) (46, 79, 3740). This may have resulted from the differences in the major food contributors. Dietary GIs and GLs in Western populations are determined by a variety of food items, including potatoes (78%), breakfast cereals (47%), bread (5%), and rice (5%) (4143). However, white rice (GI = 77) was the major contributor in the present and previous (10) Japanese studies, accounting for 59% of dietary GI and GL in the present study.
All self-reported dietary assessment methods are subject to measurement error and selective underestimation or overestimation of dietary intake (44). In the present study, however, we used a previously validated DHQ (2022) to minimize data inaccuracy. Additionally, dietary GI and GL values calculated in the present study are believed to be relatively accurate because the major determinant of dietary GI and GL in the present study, rice (62%), is more accurately reported than are other foods on the DHQ because it is consumed regularly in relatively fixed amounts. Moreover, the same tendency was observed in a repeated analysis of subjects with a physiologically plausible energy intake, ie, subjects with a ratio of energy intake to basal metabolic rate of 1.22.5 (45)
78% of the subjects included in the main analysis (data not shown). Thus, we considered that the correlations observed in the present study reflect true associations, not spurious associations resulting from inaccurate dietary data.
In the present study, dietary GI was positively correlated with BMI. A 5-wk crossover, randomized, controlled trial conducted in overweight nondiabetic men with ad libitum dietary intakes also showed a significantly lower fat mass and a tendency for a higher fat-free mass, but not a lower body weight, after a low-GI diet than after a high-GI diet (46). In contrast, other ad libitum trials conducted in subjects with type 2 diabetes showed no significant differences in body weight change between high-GI and low-GI diets (4749). However, in a 10-wk ad libitum, randomized, controlled trial conducted in healthy overweight women, decreases in body weight and fat mass were larger in a low-GI diet group than in a high-GI diet group, although these differences were not statistically significant (50). Moreover, as was shown in this study, a recent observational study also showed a positive association between dietary GI and BMI and no association between dietary GL and BMI (6).
Dietary GL has consistently been shown to be inversely correlated with HDL cholesterol in cross-sectional studies (811). In contrast, the correlation between dietary GI and HDL cholesterol is not consistent. An inverse correlation has been reported in 3 (7, 8, 10), but not in another 2 (9, 37), cross-sectional studies. Furthermore, recent randomized controlled trials have not supported the beneficial effect of a low-GI diet on HDL cholesterol in contrast with a high-GI diet (4650). In the present study, we also found an inverse correlation between dietary GL and HDL cholesterol, but no correlation between dietary GI and HDL cholesterol.
Both dietary GI and GL were positively correlated with fasting triacylglycerol in 2 cross-sectional studies (9, 10); however, no association between dietary GI and fasting triacylglycerol was observed in a study of elderly men (37). In the present study, both dietary GI and GL were positively associated with fasting triacylglycerol. Several randomized controlled trials have also shown the beneficial effect of a low-GI diet on triacylglycerol (51), although the lack of an effect of GI has been observed in subjects with low triacylglycerol concentrations (52).
We identified a positive correlation between dietary GI and GL and fasting glucose, whereas no correlation was observed in a cross-sectional study of elderly men (37). Several prospective cohort studies (4, 5, 38), but not others (39, 40, 53), in the United States have shown a positive association between dietary GI, GL, or both and the incidence of type 2 diabetes, which is not in conflict with our finding. Recently, several (48, 49), but not all (46, 47, 50), randomized controlled trials have also shown lower fasting glucose concentrations after consumption of a low-GI diet than after a high-GI diet.
We found a positive correlation between dietary GI and Hb A1c. A positive association was also reported in cross-sectional studies conducted in patients with type 2 diabetes treated by dietary restriction alone (12) and in patients with type 1 diabetes (13). Additionally, a low-GI diet reduced Hb A1c more than did a high-GI diet in several randomized controlled trials (48, 49). Furthermore, a recent meta-analysis of 14 randomized controlled trials has shown the amelioration of Hb A1c through a low-GI diet (54).
Both total and LDL cholesterol were not correlated with dietary GI or GL in the present study, although randomized controlled trials have generally shown that low-GI diets result in lower total and LDL cholesterol concentrations (54). However, similar to our findings, no correlation between dietary GI or GL and total or LDL cholesterol was observed in several cross-sectional studies (7, 10, 37).
Our results may not be extrapolated into general Japanese populations because the subjects in the present study were selected female farmers. Additionally, our DHQ, although similar to most previous epidemiologic studies, was not designed specifically to measure dietary GI and GL; however, the satisfactory validity of this DHQ for total carbohydrate (20) provides some reassurance. Moreover, although we attempted to adjust for a wide range of potential confounding variables, we could not rule out residual confounding because of these or other unknown variables. Furthermore, because the study population consisted of generally healthy persons, the clinical relevance of our findings remains to be elucidated. However, our results should provide valuable insight from a prevention perspective.
In summary, after adjustment for a variety of confounding factors, we observed positive correlations between dietary GI and BMI, fasting serum triacylglycerol, fasting plasma glucose, and Hb A1c and between dietary GL and fasting serum triacylglycerol and fasting plasma glucose and negative correlations between dietary GL and serum HDL cholesterol in healthy Japanese female farmers whose dietary GI and GL were primarily determined by white rice. Because the cross-sectional nature of the present study precludes any causal inferences, more observational and experimental studies are needed before any firm conclusions can be drawn with regard to the effect of dietary GI and GL on metabolic risk factors.
| ACKNOWLEDGMENTS |
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KM created a table of glycemic index, conducted the statistical analyses, and wrote the manuscript. SS was involved in the design of the dietary study and assisted in the creation of the table and the manuscript. YT assisted in the creation of the table. HO was involved in the management of the dietary dataset and data collection during the dietary study. YH was involved in the data collection for the dietary study. HH and EO were responsible for the research design, data collection, and data management. FK was responsible for the research design, data collection, and overall management. All authors provided suggestions during the preparation of the manuscript and approved the final version submitted for publication. None of the authors had any conflict of interest to declare.
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