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Dietary patterns and C-reactive protein in Japanese men and women^1,2,3

¹ From the Departments of Preventive Medicine (AN, DY, TY, and SK) and of Medicine and Bioregulatory Science (RT), Faculty of Medical Sciences, Kyushu University, Fukuoka, Japan, and the Department of Epidemiology and International Health, Research Institute, International Medical Center of Japan, Tokyo, Japan (TM)

² Supported by a grant for the 21st Century Center of Excellence (COE) Program (Kyushu University) from the Ministry of Education, Culture, Sports, Science and Technology, Japan.

³ Reprints not available. Address correspondence to A Nanri, Department of Preventive Medicine, Faculty of Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-8582, Japan. E-mail: nnrakiko{at}phealth.med.kyushu-u.ac.jp.

	ABSTRACT

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Background: Inflammation may be involved in the pathogenesis of atherosclerosis, type 2 diabetes mellitus, and cancer. Many studies have reported the relation of specific foods and nutrients to inflammation, but few studies have examined the relation of dietary patterns to inflammatory markers.

Objective: We investigated the relation between dietary patterns and circulating high-sensitivity C-reactive protein (hs-CRP) in Japanese men and women.

Design: The subjects were participants in the baseline survey of an ongoing cohort study of lifestyle-related diseases between February 2004 and July 2006. We excluded persons with life-limiting or possible inflammation-related diseases and those using analgesics. After further exclusion of subjects with a CRP concentration > 3 mg/L, 7802 subjects remained in the analysis. The dietary patterns were derived from principal component analysis of the frequency of consumption of 49 food items ascertained by the food-frequency questionnaire.

Results: We identified 4 dietary patterns: healthy, high-fat, seafood, and Westernized breakfast patterns. The healthy dietary pattern, characterized by high intakes of vegetables, fruit, soy products, and fish, was significantly and inversely related to hs-CRP concentrations, even after adjustment for age, body mass index, smoking, alcohol consumption, and physical activity in both men and women. Although hs-CRP concentrations were slightly elevated in persons with a high score for the seafood pattern, multivariate-adjusted means did not show a significant trend. Neither the high-fat dietary pattern nor the Westernized breakfast pattern was related to hs-CRP concentrations.

Conclusion: The healthy dietary pattern may be related to suppression of inflammation.

	INTRODUCTION

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Inflammation has been implicated in the development and progression of cancer (1, 2) and atherosclerotic disease (3). Obesity-related proinflammatory cytokines have also been linked to insulin resistance and type 2 diabetes mellitus (4, 5). Therefore, much interest has been drawn both to the relation of circulating markers of inflammation with these diseases and to the determinants of inflammatory markers (6, 7). C-reactive protein (CRP) is one of the acute-phase proteins involved in inflammation. The circulating CRP is synthesized and secreted predominantly by hepatocytes in response to proinflammatory cytokines such as tumor necrosis factor-, interleukin-1, and interleukin-6 (7). Whereas obesity (8) and smoking (9) are known as important determinants of circulating CRP, dietary factors have also been of particular interest.

The relation of specific foods and nutrients—eg, vegetables and fruit, antioxidant vitamins, and n–3 fatty acids—to CRP concentrations has been examined in many studies, but the findings are not necessarily consistent (10). Although the effect of a single nutrient, food, or food group on disease risk and morbid conditions has often been investigated, such an effect is difficult to assess in observational studies. Foods and nutrients are consumed in combination, and complex combinations of nutrients are likely to be interactive or to have a synergistic effect (11). Thus, in efforts to overcome the problems related to the close correlation among foods or nutrients, the analysis of dietary patterns has gained much interest (11-13). A dietary pattern is a comprehensive variable that integrates the consumption of several foods or food groups and that has a greater effect on disease risk than does any single nutrient (12, 13). Previously, a prudent dietary pattern characterized by high intakes of vegetables, fruit, and whole grains was shown to be related to lower concentrations of circulating CRP in some (14, 15) but not all (16, 17) studies. In contrast, a Western dietary pattern, representing high intakes of meat, refined grains, and fats, was found to be related to greater concentrations of CRP (14-17). The aim of the present study was to investigate the relation between dietary patterns and circulating CRP in Japanese adults.

	SUBJECTS AND METHODS

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Subjects
The study subjects were participants in the baseline survey of an ongoing cohort study on lifestyle-related diseases. Eligible persons were residents of the East Ward of Fukuoka City who were 50–74 y old at the time of referral to the resident registry. Some areas in the ward were deliberately excluded because of potential emigration (ie, a large proportion of renters), sparse population, or remoteness. Eligible residents were invited by mail to participate in the study. Potential participants were informed of details of the baseline and follow-up surveys.

Between February 2004 and July 2006, a total of 10447 persons (4674 men and 5773 women) participated in the survey. The participation rate was 22.9%. We excluded 1219 subjects who reported to being under current medical care for cardiovascular disease (n = 489), cerebrovascular disease (n = 219), cancer (n = 384), liver disease (n = 206), chronic renal failure (n = 17), and alcohol addiction (n = 2); we also excluded 351 subjects who reported a history of cardiovascular (n = 141), cerebrovascular (n = 98), or liver (n = 120) disease and 516 subjects currently using analgesics. After further exclusion of 550 subjects with a CRP concentration of >3 mg/L and 9 subjects with missing information on covariates, a total of 7802 subjects (3276 men and 4526 women) remained in the analysis.

All subjects gave written informed consent before participating in the study. The study was approved by the Ethics Committee of the Kyushu University Faculty of Medical Sciences.

Baseline survey
All participants completed a self-administered questionnaire and underwent blood pressure measurement, anthropometric measurements (height in cm, body weight in kg, waist in cm, and hip in cm), and venous blood drawing. The questionnaire inquired about smoking, alcohol consumption, physical activity, sleeping, stress, dietary intake, diseases under current or previous treatment, use of drugs and supplements, and family history of selected diseases. The nurse or physician asked participants about any missing or inconsistent answers.

With regard to smoking status, participants were first asked whether they had ever smoked 1 cigarettes/d for 1 y. Those who had done so then reported their age at the time they started smoking, their age when they quit smoking (for past smokers), the total number of years of smoking, and the average number of cigarettes smoked per day. Information on alcohol use was elicited, and alcohol drinkers were defined as those who had consumed alcoholic beverages 1 time/wk over a period of 1 y. Current and past alcohol drinkers were asked about the age at which they began drinking habitually. Current alcohol drinkers responded as to the frequency and amount of consumption for each of 5 alcoholic beverages [ie, sake, shochu (a Japanese distilled beverage), beer, whiskey, and wine]. The frequency of consumption options were almost null, 1–3 times/mo, 1–2 times/wk, 3–4 times/wk, 5–6 times/wk, and daily, and the amount of each beverage was reported. The total ethanol consumption per day was estimated on the basis of beverage-specific ethanol concentrations.

Questions about physical activity elicited information on work-related activity (including domestic housework) and leisure-time activity over the previous year. For the work-related activity, individuals reported the amount of time spent per day in standing, bicycling, walking, and performing strenuous labor by choosing 1 of the 8 options: almost null, <30 min, 30–59 min, 1–2.9 h, 3–4.9 h, 5–6.9 h, 7–8.9 h, or 9 h. For leisure-time activity, the frequency and amount of time per occasion were ascertained for each of 3 categories of exercise in intensity: ie, light activity (resulting in no shortness of breath), moderate activity (causing shortness of breath but not preventing speaking), and heavy activity (causing shortness of breath and difficulty in speaking). The options for the frequency were null, 1–3 times/mo, 1–2 times/wk, 3–4 times/wk, 5–6 times/wk, and almost daily, and those for the amount of time were <30 min, 30–59 min, 1–1.9 h, 2–2.9 h, 3–3.9 h, and 4 h. The intensity of each physical activity was determined in terms of the metabolic equivalent (MET) value (work-related activity: standing, 2; bicycling, 3; walking, 3; and strenuous labor, 6 METs; leisure-time activity: light, 2; moderate, 5; and heavy, 8 METs). Work-related and leisure-time physical activity were each expressed as the sum of MET multiplied by the number of hours of participation in each activity per wk (MET-h/wk).

Body mass index (BMI; in kg/m²) was calculated. Serum concentrations of high-sensitivity CRP (hs-CRP) were measured at an external laboratory (SRL, Hachiohji, Japan) by using a latex-enhanced immunonephelometric assay on a BN II analyzer (Dade Behring, Marburg, Germany). The limit of detection was 0.05 mg/L, and a value of 0.025 mg/L was assigned when the value was below the detection limit.

Dietary assessment
A food-frequency questionnaire (FFQ) was used to assess average intakes of 60 items of foods and beverages over the past year. Dietary questions were primarily derived from a 47-item FFQ developed by Tokudome et al (18); that FFQ was validated with 3-d weighted diet records as the standard for energy and 26 nutrients, and most of the nutrients showed correlation coefficients of 0.4 to 0.6 (19). Because only one item was used for alcohol consumption in that FFQ, this alcohol-related question was replaced in the present study by questions to estimate the consumption of 5 types of alcoholic beverages, which have been used and validated elsewhere (20). We added semiquantitative questions on 6 beverages (ie, green tea, black tea, oolong tea, coffee, vegetable juice, and fruit juice) and questions about the frequency of consumption of 8 specific foods [ie, salted fish guts, tsukudani (seafood simmered in soy and sugar), salted fish, garlic, broiled fish, broiled or barbecued meat, steak or hamburger, and yakitori (broiled meat and offal)]. The FFQ of Tokudome et al included green tea and coffee, but the questions were not quantitative (18). For most items, the participants described consumption frequency by choosing 1 of 8 options (almost null, 1–3 times/mo, 1–2 times/wk, 3–4 times/wk, 5–6 times/wk, 1 time/d, 2 times/d, or 3 times/d). Amounts as well as frequencies were ascertained for 3 items of staple foods (ie, rice, bread, and noodles) eaten at breakfast, lunch, and supper. Six frequency options were given for the staple foods: almost null, 1–3 times/mo, 1–2 times/wk, 3–4 times/wk, 5–6 times/wk, or daily.

In the present analysis, we used a total of 49 food items—46 items of the FFQ of Tokudome et al (excluding the alcohol item) and 3 items of specific foods (ie, salted fish guts, tsukudani, and garlic). Although the amount of consumption was reported for the staple foods, we used only frequency data for these foods. The reported frequency of consuming each food was converted to a frequency of consumption per week. For items other than the staple foods, the following values were assigned: almost null, 0; 1–3 times/mo, 0.5; 1–2 times/wk, 1.5; 3–4 times/wk, 3.5; 5–6 times/wk, 5.5; 1 time/d, 6.5; 2 times/d, 10.5; and 3 times/d, 17.5 times/wk. Regarding each of the staple foods, values of weekly frequency (0–6.5) were summed up over the 3 meals.

Statistical analysis
We performed principal component analysis based on 49 food items to derive dietary patterns. The factors were rotated by orthogonal transformation (varimax rotation) to maintain uncorrelated factors and greater interpretability. We determined 4 factors with eigenvalues, the scree test, and the interpretability of the factors. Dietary patterns were named according to the food items with the highest loadings on each of the 4 factors. The factor scores for each dietary pattern were calculated for each participant by summing intakes of food items weighted by their factor loadings. Quintiles of the factor score of each dietary pattern were used for cutoffs.

The confounding variables considered were age (y), BMI (<22.5, 22.5–24.9, 25.0–27.4, or 27.5), smoking (lifetime nonsmoker, former smoker, or current smoker with a consumption of <20 or 20 cigarettes/d), alcohol consumption (nondrinker, former drinker, or current drinker with a consumption of <30, 30–59, or 60 g ethanol/d), and physical activity (quartile of MET-h/wk). Differences in proportions and means of confounding factors according to quintile categories of each dietary pattern score were statistically tested by using the chi-square test and analysis of variance. In addition, the trend was assessed by using the Mantel-Haenszel chi-square test for categorical variables and linear regression analysis for continuous variables, with ordinal numbers 0–4 assigned to the quintile categories of each dietary pattern.

The distribution of hs-CRP was skewed to higher values, and log transformation was used. To examine the relation of each dietary pattern to hs-CRP concentrations, we performed analysis of covariance and calculated geometric means (and 95% CIs) of hs-CRP for each quintile of the dietary pattern after adjustment for the covariates. The first model was adjusted for age only, and the second model was further adjusted for BMI, smoking, alcohol consumption, and physical activity. The trend of the association was assessed by using multiple linear regression analysis, with ordinal numbers 0–4 assigned to the quintile categories of each dietary pattern. Two-sided P values < 0.05 were regarded as significant. All analyses were performed by using SAS software (version 8.2; SAS Institute, Cary, NC).

	RESULTS

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We identified 4 dietary patterns by principal component analysis (Table 1). The first factor was named a healthy dietary pattern because it represented high intakes of vegetables, fruit, soy products, fish, and yogurt. The second factor was characterized by high intakes of fried food, meat, processed meat, mayonnaise, and egg, and thus it was named a high-fat dietary pattern. The third factor represented high intakes of a variety of seafood, including shellfish, salted fish guts, fish roe, and fish-paste products, and the pattern was named a seafood dietary pattern. The fourth factor was characterized by high intakes of bread, margarine, and coffee and low intakes of rice and miso soup. Because boiled plain rice and miso soup are typical of the traditional Japanese breakfast, the fourth factor was thus named a Westernized breakfast pattern. Dietary patterns 1–4 accounted for 16.8%, 5.5%, 4.8%, and 3.4%, respectively, of the variance in food intakes and together explained 30.5% of the variability.

Table 2

Table 3

Table 4

	DISCUSSION

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Dietary patterns similar to the healthy and high-fat dietary patterns noted in the present study were previously documented in Japan (21-25) and in Western countries (14, 16, 17, 26). In the present study, the healthy dietary pattern was characterized by high intakes of vegetables, fruit, soy products, fish, and yogurt. High intakes of vegetables and fruit have consistently contributed to a healthy or prudent dietary pattern (14-17, 21-26). This pattern was often represented by a high intake of dairy products (21-23, 25). In Japan, soy products and fish were also important components of the healthy dietary pattern (22-24). The high-fat dietary pattern is comparable to the high meat pattern (21), animal food dietary pattern (23, 25), and Western dietary pattern (22, 24) previously documented in Japan. The Western dietary pattern, characterized by red and processed meats, fats, and oils, has also been described in the United States (14, 16) and Europe (26). The Westernized breakfast pattern was defined in one study (21), and this dietary pattern reflected a shift of the staple food from rice to bread. The seafood dietary pattern was unique to the present study.

The present study did not detect the traditional Japanese dietary pattern, characterized by high intakes of rice, fish, and soy products, as suggested in the Seven Countries Study (27). We calculated the score of the traditional Japanese dietary pattern by summing weekly consumption frequencies of rice, fish (2 items), and soy products (4 items). This score was correlated positively with the healthy dietary pattern (Spearman r = 0.56) and seafood dietary pattern (Spearman r = 0.29) and negatively with the Westernized breakfast pattern (Spearman r = –0.56), but it was not correlated with the high-fat dietary pattern (Spearman r = –0.02). Adjusted geometric means of hs-CRP for the lowest to highest quintiles were 0.46, 0.44, 0.46, 0.43, and 0.43 mg/L in men (P for trend = 0.14) and 0.37, 0.38, 0.37, 0.37, and 0.33 mg/L in women (P for trend = 0.0007). The traditional Japanese dietary pattern does not seem to be more favorable than the current healthy dietary pattern in terms of hs-CRP concentrations.

Four studies have previously examined the relation of dietary patterns to circulating CRP concentrations by means of principal component analysis. The prudent and Western dietary patterns were identified in the Health Professionals Follow-up Study (16) and the Nurses' Health Study (14) in the United States. The prudent dietary pattern characterized by high intakes of vegetables, fruit, whole grains, and poultry was inversely related to serum hs-CRP concentrations in the latter (14) but not in the former (16) study. The Western dietary pattern was positively correlated with hs-CRP in both studies (14, 16). In the Multi-Ethnic Study of Atherosclerosis in the United States (17), 4 dietary patterns emerged; circulating hs-CRP was correlated positively with the Western dietary pattern and inversely with a dietary pattern characterized by high intakes of whole grains and fruit, whereas no association was obtained for a dietary pattern characterized by high intakes of vegetables and fish or that characterized by high intakes of beans, tomatoes, and refined grains. In Iran, the healthy dietary pattern was inversely related to hs-CRP concentrations, and the Western dietary pattern was positively related to hs-CRP concentrations (15).

Several studies have addressed the association between a dietary pattern derived from the reduced rank regression method and hs-CRP concentrations (28-30). The reduced rank regression method determines dietary patterns that explain as much variation in intermediate biomarkers for the outcome of primary interest as possible. In studies using 5 biomarkers for coronary artery disease (28) and 6 biomarkers for inflammation and endothelial dysfunction (29), circulating hs-CRP was positively related to a dietary pattern that seemingly corresponded to the combination of the Western dietary pattern and the opposite of the prudent pattern (ie, high intakes of meat, margarine, and refined grains but low intakes of vegetables and wine). In another study (30), a dietary pattern characterized by a high intake of fresh fruit and low intakes of red meat, refined-grain bread, and high-calorie soft drinks was identified in relation to 4 biomarkers for type 2 diabetes mellitus, but this dietary pattern showed no relation to hs-CRP concentrations.

The present findings lend further support to the inverse relation between the prudent or healthy dietary pattern and circulating hs-CRP. Antioxidant vitamins (31), dietary fiber (32), and magnesium (33) may underlie the inverse relation between the healthy dietary pattern and hs-CRP concentrations, but the present study did not intend to clarify the effect of specific nutrients. The present study reinforces the usefulness of a holistic approach in observational studies of diet and health. The prudent or healthy dietary pattern was shown to be related to lower risks of cardiovascular disease (26, 34, 35), type 2 diabetes mellitus (36, 37), and certain cancers (22, 23). The present findings indicate that the healthy dietary pattern ameliorates the process of inflammation, thereby conferring a lower risk of inflammation-related chronic disease. The inverse association between healthy dietary pattern and hs-CRP concentrations may have been mediated by traditional cardiovascular factors, but the reported association did not change after further adjustment for hypertension, hypercholesterolemia, low HDL cholesterol, and elevated concentrations of glycated hemoglobin (data not shown).

The high-fat dietary pattern identified in the present study was not associated with hs-CRP concentrations. The finding may be surprising, in view of the consistent positive association with the Western dietary pattern (14-17). The lack of a positive association with the high-fat dietary pattern may have been ascribed to relatively high loadings of certain vegetables in that pattern in the present study. Alternatively, fat and meat consumption was lower in the study population than in Western and other populations. Fat-derived energy intakes were 31–38% in the Multi-Ethnic Study of Atherosclerosis in the United States (17) and 27–31% in a study of Iranian women (15), whereas fat intake accounted for 25% of total energy intake in Japan (38).

The present study had several advantages in addition to the large size of the study population. Important confounding factors were considered in the analysis. Smoking and obesity have been well documented to be causally related to higher concentrations of circulating CRP (8, 9). Alcohol consumption and physical inactivity also are suspected of being associated with inflammatory markers (39, 40). Most important, persons with potentially life-limiting morbid conditions and those with hs-CRP concentrations > 3 mg/L were excluded. Therefore, the study subjects were free of inflammatory conditions, and their CRP concentrations were in the low-normal range.

Limitations of the present study should also be discussed. An association derived from a cross-sectional study does not necessarily indicate causality. However, we meticulously excluded some of the original participant pool who had life-limiting morbid conditions or some inflammatory conditions so as to reduce the possibility of reverse causality. Another concern is the possibility of selection bias as a result of a low participation rate (23%). The inverse association between a healthy pattern and CRP concentrations could have been due to selection bias if participation had been affected simultaneously by both CRP concentrations and the dietary pattern. Another limitation was the fact that nutrients were not estimated because the modified dietary questionnaire had not been validated. It would be of interest to learn whether fat intake was actually higher in persons with a higher score for the high-fat dietary pattern. Finally, there were limitations in the factor analysis with respect to subjectivity in determining and labeling dietary patterns and extrapolation of the findings to other populations (12, 13, 41).

In conclusion, a healthy dietary pattern characterized by high intakes of vegetables, fruit, soy products, fish, and yogurt was inversely related to circulating hs-CRP concentrations in Japanese men and women. Our findings suggest that a healthy dietary pattern may contribute to the suppression of inflammation.

	ACKNOWLEDGMENTS

 
The authors' responsibilities were as follows—AN: data collection, data analysis, and manuscript preparation; DY and TY: data collection; TM and RT: the design of the study and data collection; SK: the design of the study, data collection, data management, statistical programming support, and manuscript preparation; and all authors: reading and approval of the final manuscript. None of the authors had a personal or financial conflict of interest.

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