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The Jean Mayer U.S. Department of Agriculture Human Nutrition Research Center on Aging at Tufts University, Boston, MA and * Institute of Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, Beijing, China
3To whom correspondence should be addressed. E-mail: Katherine.tucker{at}tufts.edu.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • dietary patterns • homocysteine • B vitamin • cluster analysis • Chinese
Substantial evidence has accumulated linking elevated plasma homocysteine (Hcy)3 to an increased risk of cardiovascular disease (1–4) and mortality (5–7). A linkage between cognitive decline and hyperhomocysteinemia has also been indicated in several cross-sectional (8–10), case-control (11,12) and prospective (13) studies. The relationships between high plasma Hcy concentration and intakes of folate, vitamin B-12 and vitamin B-6 are well established (14–17). Approximately two thirds of a U.S. group of men and women with high plasma Hcy concentration had low blood concentrations of folate, vitamin B-12 or vitamin B-6 (17). B vitamin supplements, especially folic acid, have been found to lower plasma Hcy (18–22). Three clinical trials showed that plasma Hcy can be decreased with increased intakes of fruit and vegetables (23–25). Because a variety of foods are rich in folate, vitamin B-12 and vitamin B-6, the total dietary pattern may have an effect on Hcy status. However, there is little information on the relationships of dietary patterns with plasma Hcy and B vitamin concentrations (25,26).
There has been increasing interest in the identification of dietary patterns to serve as an alternative and complementary approach to single-nutrient analyses in relation to disease outcomes (27–30). Because of high collinearity among many of the nutrients in foods, it is often difficult to identify the effect of a single nutrient on health outcomes. Dietary patterns are characterized on the basis of habitual food consumption (31) and represent a combination of nutrients and foods; thus, they may be a more powerful predictor for health outcomes than any single nutrient alone (32). Furthermore, dietary pattern analysis offers an approach for better understanding the complexities of eating behaviors of different population groups and subgroups, and may be used to effectively develop dietary intervention strategies for target groups (33).
Dietary traditions, culture and social norms in different populations lead to distinct eating patterns (34). Although dietary pattern assessment has been conducted increasingly in Western populations, relatively little work has assessed dietary patterns and their relations to health outcomes in non-Western countries. As reported previously (35), high Hcy was prevalent in a sample of urban Chinese adults and was found to be associated with high intakes of bakery products and sweets. The purpose of the current study was to further characterize existing dietary patterns in this population and to describe the association of dietary patterns with plasma Hcy and B vitamin concentrations.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Subjects included 130 adults (63 men and 67 women, aged 35–49 y) living in Beijing, China. Three of four urban districts were chosen to provide subjects, to include a wide range of economic conditions. Name, age, gender and occupation were obtained from archived records of neighborhood committees for 100–150 randomly selected household residents in each neighborhood. Subjects were selected only if they were in good health, as judged by a normal physical examination, had a normal blood hemoglobin concentration [standard cut-off values used in China are 120–150 g/L for men and 105–135 g/L for women (36)] and were free of any known medical condition that might affect dietary intake or energy metabolism, or prevent them from being physically active, such as heart attack, stroke, diabetes mellitus, cancer and surgeries. Women who were postmenopausal, or who had been pregnant or lactating during the past 2 y were excluded. Additional exclusion criteria included smoking >20 cigarettes/d; drinking >2 alcoholic drinks/d; and weight change of >3 kg or a self-reported change in habitual physical activity level during the past year. After screening examination, 142 subjects were qualified for the study and 130 (92%) were willing to participate. Subject characteristics are provided in Table 1. Relative to Chinese statistical yearbooks in 1999 (37), our population had an average household income similar to the general average for Beijing citizens (both were $262/mo). Similar proportions had a college education (22 vs. 19% for men, and 20 vs. 20% for women, respectively). This sample was less likely to have no high school exposure than the general Beijing population of adults (35 vs. 53% for men, and 17 vs. 46% for women, respectively). However, this is likely true because our sample did not include adults > 50 y old, a group in which a larger proportion did not attend high school. The study was conducted at the Institute of Nutrition and Food Safety, Beijing, with ethical approval obtained from the Human Investigations Review Committees at the Chinese Center for Disease Control and Prevention and New England Medical Center/Tufts University. Written informed consent was obtained from all subjects before the start of the study.
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Usual dietary intake over the preceding 12 mo was assessed with an interviewer-administered Chinese food frequency questionnaire (FFQ) developed from 24-h dietary recall data from the 1992 China Health and Nutrition Survey (38). The major food item contributors to intake from this study were compiled, and some items were deleted or additional items added according to eating practices common in Beijing. The questionnaire lists 170 individual food items. Subjects were asked to recall the frequency of consumption of individual food items (number of times/d, /wk, /mo or /y), and the estimated portion size, using local weight units [liang (50 g) and jin (500 g)] or natural units (small, medium or large). Daily energy intake was calculated using a Chinese food-composition database (39). Comparison of the reported daily energy intake estimated from the Chinese FFQ with total daily energy expenditure determined by the doubly labeled water method (in 73 subjects) showed a significant correlation (r = 0.45, P < 0.01), and a percentage difference of (mean ± SEM) 0.1 ± 5.3% with a 95% CI of ± 11%, indicating that subjects were, to a large extent, accurately reporting their usual energy intake (35).
Biochemical analysis.
Blood was drawn after a 12- to 14-h overnight fast. Within 3 h of collection, plasma was separated by centrifugation at 2500 x g for 20 min at 4°C. All plasma samples were divided into aliquots in airtight storage tubes (Cryos cryogenic vials, Vangard International, Neptune, NJ) and stored at -80°C before shipment on dry ice to the Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, MA.
Plasma Hcy was measured by HPLC with fluorometric detection (40), plasma folate by a 96-well plate microbial (Lactobacillus casei) assay (41), plasma vitamin B-12 by radioassay (Ciba-Corning, Medfield, MA) and plasma pyridoxal-5'-phosphate (PLP, the active circulating form of vitamin B-6) by the tyrosine decarboxylase method (42).
Assessment of other variables.
Information on age, current cigarette smoking (yes or no), household income (Chinese yuan/mo) and education level (middle school or below, high school, and college or above) was collected by questionnaire. For analysis, income was converted from yuan/mo to $/mo assuming 8.2 yuans equal to $1.00. Body weight and height were obtained in triplicate. BMI was calculated as weight (kg)/height (m)2.
Statistical analysis.
Statistical analyses were performed using SAS version 8.1 (SAS Institute, Cary, NC). We collapsed the 170 food items into 25 food groups based on similarity of nutrient content (see Appendix). The percentage of energy contribution from each food group was calculated and used in the cluster analysis. Standardization by energy was performed to control for dietary variations due to differences in sex, age, body size and physical activity and to retain the proportionally based food-intake patterns.
We generated dietary patterns among eligible controls with the FASTCLUS procedure in SAS. Because cluster analysis is sensitive to outliers, we first removed the controls whose energy contribution from any food group was 
6 SD from the mean (n = 6). We then ran the FASTCLUS procedure with a predefined number of 6 clusters and removed individuals who were in clusters with fewer than 4 subjects (n = 5). After these two procedures, 119 subjects were eligible for the cluster analysis. To find the most distinct set of clusters, runs were conducted with a varying number of clusters (from 3 to 6). We compared the ratios of between-cluster variance to within-cluster variance and examined Scree plots to assess the separation of groups within the study population. The 3-cluster set was selected as the one that most clearly identified distinct patterns.
Logarithmic transformations were performed for plasma Hcy and B vitamins to normalize the distribution of the data. Low B vitamin concentrations were defined as <6.8 nmol/L (3 µg/L) for folate, <30 nmol/L for PLP and <221 pmol/L (300 pg/mL) for vitamin B-12 (43). High plasma Hcy concentration was defined as >11 µmol/L for women and 12 µmol/L for men (17). Statistical comparisons were made across the clusters adjusted for the effect of age (y), sex, total energy intake (MJ), BMI (kg/m2), smoking (yes or no), alcohol use (yes or no), income ($/mo) and education level (middle school or below, high school, or college). The General Linear Model procedure in SAS was used for continuous variables. Multiple comparisons were made with Bonferroni adjustment. Mantel-Haenszel 
2 analysis was used for categorical variables. Odds ratios (OR) and 95% CI were calculated by unconditional logistic regression to estimate the relative likelihood between dietary patterns and the risk of high Hcy and low B vitamin status across dietary patterns.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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6.3% in other groups), milk and dairy products (5.9 vs. <3%), and eggs (5.1 vs. 3.6%). This pattern also had the lowest average reported energy intake (8.1 vs. 9.5–11.7 MJ). We considered this pattern to be a healthy dietary pattern based on its relatively higher intake of fruit and milk. The second cluster (n = 54) derived considerably more of its total energy intake from red meat (24.3 vs. <12%). The third cluster (n = 21) distinguished itself from the others by its high intake of refined cereals (white rice and other white flour products such as noodles, buns and bread), accounting for 48.2% of total energy intake vs. 22.5% in the other two groups. Age, BMI, income, education level, smoking and alcohol intake did not differ significantly among the three dietary pattern groups. The percentage of women in the refined cereals pattern group was significantly higher than that in the other two dietary pattern groups (72.7 vs. 38.1 -43.4%; P < 0.05).
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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We identified three distinct dietary patterns among 119 adults living in urban Beijing, i.e., a fruit and milk dietary pattern, a red meat pattern and a refined cereals pattern. These patterns were significantly associated with plasma Hcy and B vitamin status. Those in the refined cereals pattern were at significantly higher risk for high Hcy and low B vitamin status compared with those in the fruit and milk pattern; >40% of the subjects in the refined cereals group had high Hcy and low folate concentrations and up to 67% had low plasma vitamin B-12 concentration. Further analysis suggested that greater consumption of flour products, rather than rice, contributed most to this risk.
These findings are important because high plasma Hcy concentration has been well documented to be a risk factor for cardiovascular diseases, neural tube defects, pregnancy complications, mental disorders and possibly cancer (45,46) A recent study from the Framingham Heart Study showed that after an 8-y follow up, the risk of Alzheimer’s disease was estimated to increase by 40% with each 5 µmol/L increase in plasma Hcy (13). Two recent meta-analyses based on prospective studies demonstrated that every 5 µmol/L increase in Hcy increased the risk for coronary heart disease by 20% (47,48). Therefore, the 4.9 µmol/L difference in plasma Hcy concentration between the refined cereals pattern and the fruit and milk dietary pattern in this population may be associated with 20 and 40% more likelihood of developing coronary heart disease and Alzheimer’s disease, respectively.
Although the patterns identified in this urban Chinese population are culturally specific, they are similar to patterns identified elsewhere. Tucker et al. (49) identified a fruit, milk and breakfast cereal pattern, a bread pattern and a meat pattern in a group of 680 noninstitutionalized predominantly white elderly people living in Massachusetts. Huijbregts et al. (50) identified a meat pattern and a pattern characterized by high fruit, vegetables and grains in a group of Dutch elderly men. In the European SENECA study, Havenman-Nies et al. (51) identified a high meat pattern, and a "healthy" milk and fruit pattern among others. Similar fruit and milk, and meat dietary patterns were identified by Tucker et al. (27) using cluster analysis in the Framingham Osteoporosis Study. The "prudent" and "Western" dietary patterns generated from the Health Professionals’ Health Cohort and the Nurses’ Health Cohort using factor analysis also resembled these two patterns (26,30,31,52,53). These have since been identified with factor analysis in other cohorts as well (54–56).
The refined cereals dietary pattern has not appeared as clearly in most previous studies in Western populations, although a white bread pattern was identified in two Massachusetts studies (27,49). In this Chinese population group, subjects following the refined cereals pattern consumed almost 50% of energy from cereal products, mainly white flour and white rice products. On average, people living in Beijing consumed 395 g/d of refined cereals, and the national average consumption was 439 g/d, based on the data from the third China Health and Nutrition Survey in 1992 (38). In Tianjin, a city close to Beijing, refined cereal products were shown to provide 59 and 75% of energy intakes for individuals living in urban and rural areas, respectively (57), suggesting that the refined cereals consumption pattern was more common in the rural area and in lower income segments of the population. Given this extensive use of refined cereal products in the Chinese population and the observed here between this pattern and deficiencies of B vitamins, the association prevalence of high Hcy in other parts of China may be even greater than that seen in this urban sample. The greater significance of flour product intake (including noodles, steamed buns, breads and fried dough sticks) on B vitamins and Hcy relative to rice intake suggests that these processed foods may contribute to these B vitamin deficiencies. Further investigation of these associations is warranted.
Subjects with the fruit and milk dietary pattern had the highest plasma B vitamin concentrations and lowest plasma Hcy. Fruit, vegetables and dairy products are important sources of B vitamins. Results from the Framingham Heart Study showed that frequent consumption of fruit and vegetables was associated with high plasma folate and low Hcy concentrations (58). Dairy products are important sources of vitamin B-12, and this vitamin B-12 may be more efficiently absorbed than from meat, poultry or fish sources (59,60). Our observations are also consistent with the results from the DASH study, which examined the effect of dietary patterns on serum Hcy, in which 118 participants (aged 23–76 y, 48.3% women) were randomly allocated to three dietary pattern groups, i.e., a control diet (low in fruit, vegetables, and dairy products, with a fat content typical of US consumption), a diet rich in fruit and vegetables but otherwise similar to the control diet and a combination diet rich in fruit, vegetables and low fat dairy products and reduced in saturated and total fat (25). After consuming the diets for 8 wk, the plasma Hcy concentration in the combination diet group was decreased, and the 8-wk change differed significantly from the control diet. Results from the Health Professionals’ Follow-up Study also showed that a prudent diet (characterized by high takes of fruit, vegetables, whole grains, poultry and low fat dairy) was inversely related to plasma Hcy concentration (26).
Refined cereal products, as commonly used in China, are not fortified, and are therefore not good sources of folate or vitamins B-12 or B-6. Furthermore, they appear to displace foods with more nutritional value. In this same urban Chinese population group, Yao et al. (35) reported that higher intake of foods from the refined cereals group was associated with lower HDL and apolipoprotein A-I. Therefore, all of these these results raise concern that a high refined cereals diet may be contributing to greater risk of heart disease and possible cognitive decline in the aging Chinese population. Further studies are required to confirm this observation.
Some limitations of this study should be noted. First, the sample size was small (119 subjects across 3 groups). However, our population had mean plasma Hcy concentrations similar to those in another representative Beijing study. As in any such study, the definition of dietary patterns is limited by the dietary data obtained by self-report using a FFQ. However, we showed previously that the questionnaire measured energy intake remarkably well in relation to doubly labeled water (35). Therefore, the three dietary patterns should be valid within this group and are likely representative of those in the larger urban population. The nutritional implications of these three patterns are useful in that they are generally understandable and offer clear public health guidance.
In summary, of the three dietary patterns identified among urban Beijing adults, the refined cereals pattern was associated with a high prevalence of high plasma Hcy and low B vitamin concentrations, whereas the fruit and milk pattern had the lowest plasma Hcy and the highest B vitamin concentrations. Within the refined cereal group, greater use of flour products, rather than of rice, appeared most associated with these outcomes. These findings highlight the importance of dietary pattern on nutritional status and associated health outcomes and suggest the need for more attention to these issues in Chinese aging populations.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported by National Institutes of Health grant DK53404 and by the U.S. Department of Agriculture, under agreement No. 581950–9-001.
4 Abbreviation used: FFQ, food frequency questionnaire; Hcy, homocysteine; PLP, pyridoxal-5'-phosphate.
Manuscript received 20 June 2003. Initial review completed 7 July 2003. Revision accepted 19 August 2003.
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