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Among older adults, the Mediterranean diet has been inversely related to incident metabolic syndrome (MetSyn); however, this relation has not been studied in young African American and white adults. The objective of this study is to evaluate the relations of a modified Mediterranean diet (mMedDiet) pattern with 25-year incidence of MetSyn in 4,713 African American and white adults enrolled in the Coronary Artery Risk in Young Adults (CARDIA) study. A diet history assessed dietary intake at baseline, years 7 and 20 and a mMedDiet pattern score was created. Cardiovascular risk factors were measured at multiple exams over 25 years. The MetSyn was defined according to ATP III criteria. Cox proportional hazard regression analysis evaluated the relations of incident MetSyn across categories of mMedDiet pattern adjusting for demographics, lifestyle factors, and body mass index. Higher mMedDiet scores represented a diet pattern rich in fruit, vegetables, whole grains, nuts, and fish, but lower in red and processed meat and snack foods. The incidence for MetSyn components abdominal obesity, elevated triglycerides, and low HDL-c was lower in those with higher mMedDiet scores compared to lower scores. Further, the incidence of MetSyn was lower across the 5 categories of mMedDiet score; the hazard ratios and 95% confidence intervals from the 1st category to the 5th were 1.0; 0.94 (0.76, 1.15), 0.84 (0.68, 1.04); 0.73 (0.58, 0.92); and 0.72 (0.54, 0.96), respectively; (ptrend=0.005). These findings suggest that the risk of developing MetSyn is lower when consuming a diet rich in fruit, vegetables, whole grains, nuts, and fish.
Findings from randomized clinical trials have demonstrated a lower the risk of incident and recurrent CVD and its risk factors with consumption of a healthy diet pattern, including a Mediterranean Diet pattern (1,2). The Mediterranean diet is a broadly studied diet pattern, featuring high intake of olive oil, olives, legumes, whole grains, vegetables, fruit, moderate fish intake, low to moderate consumption of dairy products (primarily as cheese and yogurt), and moderate consumption of wine with meals, but low intake of red meat and processed meat (3).
Previous studies have demonstrated inverse associations between the Mediterranean diet pattern and mortality (4,5) and risk of several chronic conditions (6), including the metabolic syndrome (MetSyn), a cluster of several cardiovascular disease (CVD) risk factors. A recent meta-analysis of 50 studies reported that the Mediterranean diet was related to lower risk of MetSyn (7); however, there was significant heterogeneity present in this meta-analysis and the authors concluded that more prospective studies are needed (7). Three previously published prospective studies reporting an inverse relation between a Mediterranean diet score and incident MetSyn were conducted in a Spanish population and in middle-aged U.S. adults (8–10). Few studies examining the relation between diet patterns and MetSyn have used an ‘a priori’ Mediterranean diet pattern score adapted to the U.S. diet (9), especially in a racially diverse young adult population with 25 years of follow-up.
The purpose of this study was to determine the longitudinal relation of a modified Mediterranean diet (mMedDiet) pattern score with risk of developing MetSyn among young black and white adults enrolled in the Coronary Artery Risk Development in Young Adults (CARDIA) study. We hypothesized that the mMedDiet pattern score will be inversely related to the risk of incident MetSyn over 25 years of follow-up.
The CARDIA Study is a multi-center population-based prospective study of cardiovascular disease risk factor evolution in black and white men and women. Details of the CARDIA Study design and participants have been previously reported (11). Briefly, 5,115 participants aged 18–30 years were recruited at baseline (1985–86) from Chicago, IL; Minneapolis, MN; Birmingham, AL; and Oakland, CA. Seven clinical examinations have been conducted, at years 0 (baseline), 2, 5, 7, 10, 15, 20 and 25, with follow-up response rates of 91%, 86%, 81%, 79%, 72% and 72%, respectively (12). Informed consents were obtained from all participants at each exam and the study was approved by institutional review committees at each site.
Participants were excluded from the current analyses for the following reasons: extreme caloric intake at baseline, years 7 and 20 (<800 and >8,000 kcal/day for men and <600 and >6,000 kcal/day for women; n=88); women who reported being pregnant at the year 0 exam (n=7); prevalent metabolic syndrome at baseline (defined below, n=110); or lack of fasting blood sample at baseline (n=147). Measurements taken during pregnancy for years 7, 20 and 25 were treated as missing (n=65). Thus, the sample size for these analyses was 4,713 (1030 black men, 1349 black women, 1110 white men and 1224 white women).
Participants were asked to fast for at least 8 hours and to avoid smoking and heavy physical activity two hours prior to the exam. Blood was drawn using a standard protocol by venipuncture. The plasma levels of lipids were assessed at the Northwest Lipid Research Clinic Laboratory at the University of Washington (Seattle, WA). In particular, the LDL-containing lipoproteins were precipitated with dextran sulfate/magnesium chloride before HDL level was determined (13). Triglycerides were enzymatically measured, using a blank corrected method (14). Fasting glucose levels were quantified by the hexokinase method and standard radioimmunoassay, respectively (15). At each exam, 3 seated blood pressure measurements were obtained on the right arm using a Hawksley random zero sphygmomanometer (WA Baum Company, Copaigue, NY, USA) following a 5-minute rest period. The average of the second and third measurements was used in analyses.
Waist circumference was measured to the nearest 0.5 cm with a tape in duplicate around the minimal abdominal girth. Body weight was measured to the nearest 0.2 kg with a calibrated balance beam scale. Height was measured with a vertical ruler to the nearest 0.5 cm. Body mass index (BMI) was computed as weight in kilograms divided by height in meters squared.
MetSyn is defined as having at least 3 of the following 5 criteria according to the National Cholesterol Education Program Adult Treatment Panel III (ATP III) guidelines (16): waist circumference >88 cm for women or >102 cm for men, elevated systolic or diastolic blood pressure >= 130 or >=85 mmHg, respectively, or on anti-hypertensive medication, elevated fasting triglycerides >= 150 mg/dL, fasting glucose >= 100mg/dL or having diabetes, and low HDL-cholesterol (< 50 mg/dL).
In examinations at years 0, 7, and 20, dietary intake was assessed through an interviewer-administered diet history questionnaire specifically developed for the CARDIA study (17). Participants were asked to self-report dietary intake for the past 28 days, including the frequency, amount, food preparation methods, and type of fat used in preparation or at the table. The validity and reliability of this diet history questionnaire was evaluated and was described in detail (18). Reported foods and beverages were grouped into food groups according to the Nutrient Data Software for Research (NDSR; University of Minnesota, Minneapolis, MN, USA) food grouping scheme (19). Daily intake of each food or beverage group was calculated as the sum of the number of servings consumed per day.
The Mediterranean diet pattern score according to Trichopoulou et al. (4) was modified (mMedDiet) and included 22 food and beverage groups plus a measure of healthy fat intake, i.e., monounsaturated fat + polyunsaturated fat divided by saturated fat (MUFA+PUFA/SFA ratio) with the median as the cutoff. While Americans do not commonly consume olive oil, they do consume meat which contributes MUFA to the diet and vegetable oil which contributes PUFA to the diet. Therefore, a MUFA+PUFA/SFA ratio was included in the score as an alternative to MUFA intake. Furthermore, present day food and beverage habits commonly include coffee, sugar-sweetened beverages and sweet or salty snack foods as reported in both of the Mediterranean and U.S. populations (20–23); therefore, the original Mediterranean diet pattern score was modified to include the majority of reported foods and beverages in the diet. Briefly, a value of 0 or 1 was assigned to each of the food and beverage groups and fat ratio: a value of 1 was assigned to individual intake above the median and 0 for below the median for foods assumed beneficial for health (whole grain products, fruit, vegetables, fruit+vegetable juice, legumes, nuts, poultry, fish, eggs, coffee and tea, and the MUFA+PUFA/SFA ratio). A value of 1 was assigned to individual intakes below the median and 0 for above median intake for foods presumed to be adverse to health (red and processed meat, dairy products, fried vegetables, refined grain, sauces, snack foods, sugar-sweetened beverages, diet beverages). For alcohol, 1 was assigned to men who consumed between 10 and 50 g per day and to women who consumed between 5 and 25 g per day. Thus, the total mMedDiet pattern score ranged from 0 (less healthy diet pattern) to 19 (more healthy diet pattern).
Demographic characteristics (age, sex, race, field center, education at baseline), and lifestyle behaviors (physical activity and cigarette smoking) were obtained via standardized questionnaires across CARDIA examination visits. A validated CARDIA Physical Activity History Questionnaire was administered (24), while vitamin supplement use was queried as a separate question in the CARDIA Diet History (17).
SAS, version 9.2 software (SAS Institute, Cary, NC, USA) was used for all statistical analyses. Baseline characteristics were reported as mean and standard deviation for continuous variables and frequency (%) for categorical variables. The cumulative incidence of components for the MetSyn over 25 years was estimated. Twenty-five year incidence of MetSyn is defined as the first occurrence of MetSyn at any of years 2, 5, 7, 10, 15, 20, or 25.
The mMedDiet score was divided into 5 categories. The average number of servings of food intake for each food group was computed within categories of the mMedDiet score using linear regression, adjusting for sex, age, race, center, education, field center, and energy intake. Time dependent Cox proportional hazards regression analysis was used to evaluate associations of the 25-year incidence of MetSyn, as well as for each MetSyn component, across categories of the mMedDiet score, and to assess whether this relation was modified by race or sex. Time at risk was defined as until first diagnosis or date of last follow-up examination. Hazard ratios were computed for the 2nd through 5th category of the mMedDiet score compared to the 1st category (lowest intake) as the referent group, including interaction terms for race and sex. Cumulative average of dietary intake, which increases the precision of dietary exposure, was used to create food groups and patterns (25). The time-varying diet exposures were modeled as 1) between baseline (year 0) and year 7, diet exposure was based on dietary intake as measured at year 0; 2) year 7 to year 20, diet exposure was based on the average of year 0 and 7 diet; and 3) year 20 to year 25, diet exposure was based on year 20 diet. Three models were developed: model 1, adjusted for energy intake and demographic factors age, race, gender, education, and field center; model 2, adjusted for model 1 plus current smoking, physical activity, and vitamin supplement use at baseline (since food intake may be related to other behaviors); and model 3, adjusted for all variables in model 2 plus baseline BMI and model 4, adjusted for model 3 plus baseline waist circumference (to determine whether the relation of MetSyn and mMedDiet pattern was independent of baseline adiposity). A linear trend across mMedDiet categories was tested with contrast statements using orthogonal polynomial coefficients. The proportional hazards assumption was tested and found to be satisfied (26).
As shown in Table 1, the number of servings for each food group was reported across five categories of the mMedDiet score. Generally, more servings of whole grains, fruit, vegetables, nuts, fish and seafood were observed in those with higher mMedDiet pattern scores; while fewer servings of these foods corresponded to lower scores. Fewer servings of red and processed meat, dairy products, refined grain, snack foods, candy, sugar sweetened beverages, and diet beverages were reported for those with greater mMedDiet scores compared to the lowest scores. The proportion of men and women reporting moderate alcohol intake was 51.2% and 48.8%, respectively. Nutrient intake was supportive of food intake: fiber, vitamin C, and magnesium were greater, while saturated fat intake was lowest in those with the highest mMedDiet pattern scores compared to the lowest category (Table 2).
Baseline characteristics are shown in Table 3. Compared to the lowest category of mMedDiet pattern scores, a greater proportion of participants in the highest mMedDiet score category was older, white, more highly educated, and more physically active. Further, individuals with higher diet scores had lower waist circumference and higher HDL-cholesterol levels. The other CVD risk factors were similar across categories of mMedDiet scores.
The 25-year cumulative incidence of MetSyn components abdominal obesity, high triglycerides, and low HDL-cholesterol levels decreased with higher mMedDiet pattern scores (except for elevated glucose, all ptrend ≤ 0.02) (Table 4). Over 59% of participants assigned to the first mMedDiet pattern category was abdominally obese compared to 42% who reported eating a healthier diet (category 5). Generally, there were fewer participants with adverse MetSyn components with mMedDiet scores in higher categories than those in the lowest.
Further, the incidence of MetSyn was lower with increasing mMedDiet pattern score. Over 25 years of follow-up, hazard ratios (HR) and 95% confidence intervals (95% C.I.) for individuals with mMedDiet scores across categories 1–5 were 1.0; 0.94 (0.76, 1.15); 0.84 (0.68, 1.04); 0.73 (0.58, 0.92); and 0.72 (0.54, 0.96), respectively, adjusting for age, sex, race, education, field center, energy intake, smoking, physical activity, and vitamin supplement use (Table 5; Model 2, (ptrend=0.005). Additional adjustment for BMI and waist circumference at baseline did not influence the observed associations (Models 3 and 4; ptrend=0.004). The proportional hazards assumption was met for the models (p>0.05). No effect modification was observed for sex or race on the relation between the mMedDiet pattern and incident MetSyn (p>0.05).
In this cohort of young adults, the 25-year incidence of MetSyn was inversely related to adherence to a diet pattern similar to a Mediterranean diet that is rich in fruit, vegetables, nuts, fish and seafood, and whole grains, moderate alcohol intake, while low in red and processed meat, dairy products, and snack foods. Although the hallmark of the Mediterranean diet is olive oil, we included a MUFA+PUFA/SFA ratio in the mMedDiet score as Americans do not consume the amount of olive oil as do those in the Mediterranean. Those with higher mMedDiet pattern scores were older, had more years of education, and were more physically active than those with lower scores. Although energy intake was similar across categories of mMedDiet pattern scores, study participants with lower scores consumed over 2 daily servings of snack foods high in solid fat and/or added sugar, such as sugar-sweetened beverages, candy, cake, cookies, pie, donuts, crackers, or chips, compared to those with higher mMedDiet scores who consumed about 1 daily serving of snack foods. These findings suggest that the food choices of study participants who were adherent to a diet pattern similar to a Mediterranean-type diet are consistent with food recommendations of the 2010 U.S. Dietary Guidelines (27).
Although numerous cross-sectional studies have been conducted examining Mediterranean diet-MetSyn relations, findings have been inconsistent (7). Our findings, based on 25 years of follow-up among Caucasian and African American adults ages 18–30 years at baseline, were consistent with those of three previously conducted prospective studies examining the same relationship, but had fewer years of follow-up (8–10). In a study of 2563 Spanish men and women, individuals adhering to a traditional Mediterranean diet pattern were 80% less likely to have MetSyn over 6 years of follow-up than those who did not adhere to this diet pattern (8). However, one limitation of this study was that the components of the MetSyn were self-reported and not measured by trained observers. In a study of 3232 French men and women, three variations of the Mediterranean diet were all related to a lower risk of MetSyn over 6 years of follow-up (10). Among 2730 middle-aged white adult men and women free of diabetes and enrolled in the Framingham Offspring Study, the 7-year incidence of MetSyn was 21% lower among those in the highest quintile of a Mediterranean diet-type pattern compared to those in the lowest quintile (9). Despite differences in study design and methods, including the differing age and race composition of the study populations, diet assessment instrument, data analysis approach, and length of follow-up, the relations between the diverse Mediterranean diet patterns and MetSyn were consistent among the current study and the other 3 prospective studies (8–10).
The Mediterranean diet pattern includes foods and beverages that are rich in a myriad of nutrients, including monounsaturated fat, antioxidants, fiber, calcium, magnesium, phytoestrogens, or other food components (28). The combined influence of these foods (nutrients and food components) has been shown to confer beneficial effects on the individual components of the MetSyn, including a better lipid profile (29), and lower systolic and diastolic blood pressure (30), adiposity (31), and insulin resistance (32). Evidence from studies of individual food intakes relative to components of the MetSyn may also explain underlying mechanisms. In addition, inverse associations have been reported between whole grain foods and glucose concentrations, insulin resistance, and incident diabetes (33). Moderate alcohol intake has been linked with higher HDL-cholesterol (34). Blood pressure may also be beneficially modulated by intakes of fruit and vegetables which are rich in potassium, fiber and antioxidants (35), while plant protein and foods from plant sources were inversely related to blood pressure (36) and elevated blood pressure (35). Meat intake has been positively related to blood pressure and risk of hypertension in several populations (35,37); numerous studies have also shown positive relations between red and processed meat intake and adiposity (38) and type 2 diabetes (39). Finally, fish intake has been inversely associated with CVD risk factors and the metabolic syndrome (40,41) and its individual components blood pressure, glucose, and lipids (41–43).
Olive oil, rich in monounsaturated fatty acids and antioxidants, is a characteristic component of the Mediterranean diet and known for its beneficial effect on CVD risk factors, including lipids, blood pressure, and glucose homeostasis, as well as endothelial function, inflammation and oxidative stress (44). However, Americans do not consume large quantities of olives or olive oil, but they do consume other vegetable oils which are high in PUFA, Thus, the MUFA+PUFA/SFA ratio was greater among adults with a higher mMedDiet score. Higher mMedDiet scores were related to higher polyunsaturated fat and lower monounsaturated fat and saturated fat intake.
Limitations of this study include reliance on self-reported dietary intake, which may induce considerable measurement error (45). However, it is likely that food intake was ranked correctly. Moreover, dietary intake was assessed by trained and certified interviewers at 3 visits using the validated CARDIA diet history questionnaire (17,18) ensuring greater precision of dietary intake compared to a single assessment at baseline (25). Finally, residual confounding may still exist even though statistical models were adjusted for numerous potential factors which may confound the relation between dietary intake and incident MetSyn.
There are several strengths of this study, including the prospective design and study population of African Americans and white men and women aged 18–30 years at baseline, long duration of follow-up, and multiple clinic exams to characterize the components of the Metsyn and assess incident MetSyn. Finally, the CARDIA Diet History allowed for collection of specific fat and oil consumption/use in food preparation and added to foods at the table – which was important to calculate the MUFA+PUFA/SFA ratio included in the mMedDiet pattern score.
The findings from our study with 25 years of followup suggest that the risk of incident MetSyn in young Caucasian and African American adults is lower when consuming a diet pattern rich in fruit, vegetables, whole grains, nuts, and fish. Promoting a Mediterranean diet pattern is beneficial to cardiovascular health.
We wish to thank the CARDIA study participants for their continued participation in this prospective study.
Financial support: The Coronary Artery Risk Development in Young Adults (CARDIA) Study was supported by contracts N01-HC-48047, N01-HC-48048, N01-HC-48049, N01-HC-48050, N01-HC-95095, and N01-HC-45134 from the National Heart, Lung, and Blood Institute (NHLBI) at the National Institutes of Health. NIH/NHLBI had no role in the design or analysis of this article.
Conflict of interest: None.
Authorship: The authors’ responsibilities were as follows—LMS and LVH designed the research; LMS, LVH, and MD wrote the first draft of the manuscript; LMS supervised the statistical analyses; XZ performed the statistical analyses; all authors reviewed the manuscript, participated in the interpretation of the study results and approved the manuscript; LMS had primary responsibility for final content and is the guarantor of the manuscript, having had full access to the data in the study, and takes responsibility for the integrity of the data and the accuracy of the data analysis.