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The relationship between diet and subclinical atherosclerosis: results from the Asklepios Study

Abstract

Background/Objectives:

Nutritional epidemiology shifted its focus from effects of single foods/nutrients toward the overall diet. Food-based dietary guidelines (FBDGs) are promoted worldwide to stimulate a healthy diet, including a variety of foods, to meet nutrient needs and to reduce the risk for non-communicable diseases. The objective of this study was to investigate whether adherence to the FBDG is associated with reduced femoral/carotid atherosclerosis and/or inflammation.

Subjects/Methods:

In October 2002, 2524 healthy men and women aged 35–55 years were recruited for the Belgian Asklepios cohort study. Subjects were extensively phenotyped, including echographic assessment of (carotid and femoral) atherosclerosis. A dietary index consisting of three subscores (dietary quality, diversity and equilibrium) was calculated to measure adherence to the Flemish FBDG, using data from a semi-quantitative food-frequency questionnaire. General linear models were used to investigate associations between these scores and cardiovascular (CV) risk factors and atherosclerosis and inflammation markers.

Results:

Women had better overall dietary scores than men (69 vs 59%). Participants with higher dietary scores showed better age-adjusted CV risk profiles (lower waist/hip ratio, blood pressure, non-high-density lipoprotein-cholesterol, blood triglycerides and homocystein), although most of these associations were only significant in men. Higher dietary scores were also inversely associated with inflammation makers (interleukin-6 and leukocyte count). Associations between diet and atherosclerosis were only found for femoral atherosclerosis and significance disappeared after adjustment for confounders.

Conclusions:

Better adherence to the Flemish FBDG is associated with a better CV risk profile and less inflammation, mainly among men. There was no direct effect on the presence of carotid or femoral atherosclerosis.

Introduction

Cardiovascular diseases (CVDs) remain the leading cause of mortality in industrialized countries and are rapidly becoming a primary cause of death worldwide (Hu et al., 2000; Hu and Willett, 2002). Therefore, the identification of the dietary factors influencing CVD risk is critical.

For a long time, nutritional epidemiology has focused on the effects of single foods (for example, fish, olive oil and red wine) and nutrients (for example, cholesterol, omega-3 polyunsaturated fatty acids and vitamin E) on CVD risk (Davis et al., 2007). As nutrients and foods are consumed in combination rather than separately, interactions are possible. For this reason, there is a recent tendency to study the overall diet, using techniques such as factor analysis to identify dietary patterns in a population (Fung et al., 2001a; Lopez-Garcia et al., 2004), or computing dietary scores, which measure the adherence to dietary guidelines (Kant et al., 2000; McCullough et al., 2000a; Fung et al., 2001a, 2005; Trichopoulou et al., 2003; Chrysohoou et al., 2004; Pitsavos et al., 2005; Panagiotakos et al., 2006).

Food-based dietary guidelines (FBDGs) are developed worldwide to show the population how to eat a well-balanced diet that reduces the risk for non-communicable diseases. In this study, we examined whether adherence to FBDG is associated with reduced risk for femoral and carotid atherosclerosis and/or inflammation. A dietary index consisting of three subscores (dietary quality, diversity and equilibrium) was calculated to measure adherence to the Flemish FBDG, using data from a semi-quantitative food-frequency questionnaire (FFQ) (Huybrechts et al., 2010).

Subjects and methods

Study population and clinical, biochemical and ultrasound examinations

The Asklepios Study is a longitudinal population study focusing on the interplay between ageing, cardiovascular (CV) haemodynamics and inflammation in (preclinical) CVD. At baseline in October 2002, 2524 healthy volunteers aged 35–55 years were recruited. The subjects were randomly sampled from the twinned communities of Erpe-Mere and Nieuwerkerke in Flanders, Belgium. These adjoining communities, approximately 40 km outside the capital Brussels are home to roughly 25 000 inhabitants, of which 8104 were within the target age group (data provided by local authorities). The sampling was by tiered direct postal mailing based on random samples drawn from the population lists. From the onset, partners and relatives of those recruited by mailing were also eligible for study entry (if they inhabited Erpe-Mere or Nieuwerkerken). A total of 703 partners of recruited subjects were included in this manner (Rietzschel et al., 2007). The inclusion criteria were: male or female volunteers aged 35–55 years at study initiation, living in the communities of Erpe-Mere or Nieuwerkerken. Exclusion criteria were the presence of clinical atherosclerosis, major comorbidity, diabetes mellitus, pregnancy, atrial fibrillation, irregular heart cycle and the inability to give informed consent. More details about the inclusion and exclusion criteria used can be found in the methods and baseline characteristics of the Asklepios Study (Rietzschel et al., 2007).

Only the data from the baseline measurement were used for this study (cross-sectional data). In total, 37 (<2%) participants who did not complete the FFQ were excluded, leaving 2487 subjects (1200 men and 1287 women) for analysis. Response rate was 38.3% (36.4% for men; 40.4% for women). Partners who spontaneously entered were not counted in response rates. Except for a slight over-representation of women and married subjects, no important selection bias could be identified through non-participation (Rietzschel et al., 2007).

The participant examination consisted of a self-administered questionnaire (including lifestyle variables), measurement of basic clinical data (body size parameters, blood pressure and electrocardiogram), blood sampling for analysis of classical risk markers and inflammatory markers, an echocardiography and vascular echography and tonometry of the left and right carotid and femoral arteries. Basic clinical data assessment and routine biochemical assays were performed as described previously (Rietzschel et al., 2007). In summary, five markers of inflammation were measured: high-sensitive C-reactive protein, leukocyte count, fibrinogen, oxidized low-density lipoprotein-cholesterol and interleukin 6 (IL-6). The carotid and femoral arteries were carefully scanned over a length as large as possible both longitudinally (anterior-oblique, lateral, and posterior-oblique planes for the carotids) and transversely using two-dimensional, colour flow or pulsed wave Doppler to avoid overlooking poorly visible hypoechogenic plaques. This analysis included plaques in the near as well as the far wall of the vessels. A plaque was defined as a focal widening with protrusion into the lumen, composed of calcified or non-calcified component. For each plaque, we described location, echogenicity and grading of the degree of stenosis if applicable. At the position of the best visibility of the plaque, the biggest cross-sectional area in a longitudinal view (visually judged), quantitative measurements of the protrusion from the media–adventitia interface, length and area were made. Atherosclerosis was defined as the echographical presence of plaques or increased intima-media thickness (IMT >0.9 mm) in the carotid or femoral arteries. A detailed description of the design and methods, laboratory investigations and vascular ultrasound examinations of the Asklepios Study has been published (Rietzschel et al., 2007).

The participants will undergo the second measurement visit starting from December 2010, after 8 years of follow-up.

This study complies with the Declaration of Helsinki. The ethical committee of the Ghent University Hospital approved the study protocol and a written informed consent was obtained from each participant before enrolment.

Dietary intake assessment methods

The participants were asked to complete a semi-quantitative FFQ. The FFQ was specifically designed to assess adherence to the Flemish FBDG and was inspired on pre-existing FFQ's already used in our Belgian population and on the short FFQ developed by W Willett (Willett, 1998; Cade et al., 2002).

This FFQ included questions on the habitual daily consumption of 25 food items during the past year. The 25 food items included in the FFQ are presented in Table 1.

Table 1 The 25 food items included in the semi-quantitative FFQ that was used and the 9 food categories of the Flemish FBDG in which these food items were re-categorized

The participants were asked to indicate how often they consumed each item in a list of frequencies: every day; 5–6 days per week; 2–4 days per week; 1 day per week; 1–3 times per month; never or less than once a month. In addition, the FFQ contained three daily portion size categories per food item and a list of common standard measures as examples. The participants were asked to indicate the portion size category that represents their usual daily portion size most accurately.

On the basis of the FFQ data, an overall dietary index was calculated to measure adherence to the Flemish FBDG (Huybrechts et al., 2010). The overall dietary index consists of three components: dietary diversity, dietary quality and dietary equilibrium.

The dietary diversity score indicates whether a participant eats at least one serving per day from each recommended food group. The nine recommended food groups are presented in Table 1 and include: (1) ‘water’, (2) ‘bread and cereals’, (3) ‘grains and potatoes’, (4) ‘fruit’, (5) ‘vegetables’, (6) ‘milk and milk products’, (7) ‘cheese’, (8) ‘meat and meat products’ and (9) ‘fat’. The dietary diversity score was computed by dividing the number of food groups from which on average at least one serving was consumed by nine (the total number of recommended food groups).

The dietary quality score shows if a person makes the optimal food choices within each food group. In the Flemish FBDG, products have been categorized into three groups: the preference group (for example, dark bread), the moderate group (for example, white bread) and the rest group (energy dense foods like biscuits, which are not necessary in a healthy diet and should be consumed only occasionally). To calculate the dietary quality score, the daily portion size (in grams per day) of preferred foods was multiplied by a factor ‘1’, foods categorized as moderate with a factor ‘0’ and those in the rest group with a factor ‘−1’. For each person, these values (portion size × factor) were summed and divided by the total sum of food quantities eaten per day and multiplied by 100.

The dietary equilibrium score indicates if an individual consumes foods in the right proportions: more from the food groups in the base of the food triangle and less from the food groups in the triangle top. The dietary equilibrium score is disaggregated into an adequacy and moderation score. The adequacy score compares the intake of the participant with the minimal daily recommended intake. If the minimum daily recommended intake is achieved, the participant scores 1 for this food item. If the participant's intake is lower than the minimal recommended intake, he scores proportionally between 0 and 1. The moderation score shows whether the maximal daily recommended intake is exceeded. If the participant has an average daily intake below the maximum daily recommended intake, he scores 0. If his intake exceeds the maximal daily recommendations, he scores proportionally between 0 and −1. The dietary equilibrium score is calculated by summing up the positive adequacy score and the negative moderation score.

The overall dietary score is then computed by summing the three subscores and dividing the result by three. An overall dietary score of 100% indicates full adherence to the Flemish FBDG. Our dietary score was adapted from a diet quality index developed for Flemish preschool children. This index showed good reproducibility (r=0.87) and validity (r=0.82) (Huybrechts et al., 2010).

Statistical analyses

The associations between the dietary scores and CV risk factors and markers of atherosclerosis and inflammation were studied via crude explorative analyses (Spearman correlations and partial correlations) and general linear models. All analyses were conducted using Predictive Analysis Software 18.0 (PASW, 2010).

First, we examined the correlations between the dietary scores and traditional risk factors, adjusting for age and stratified by gender.

Second, we investigated the association between the dietary scores and inflammation markers. We calculated partial Spearman correlations adjusted for age and stratified for genders, between the dietary scores and these markers.

Third, we examined the effect of the dietary scores on atherosclerosis, adjusting for age only. Subsequently we developed a general linear model with the following covariates, which are all known CV risk factors: age, total cholesterol, high-density lipoprotein-cholesterol, waist circumference, height, impaired fasting glycaemia, lipid lowering therapy, systolic blood pressure, antihypertensive therapy, pack-years of cigarette smoking, excessive alcohol consumption, education beyond secondary, physical activity and use of female sex hormones (hormone substitution therapy, oral contraceptives, other). Adjusting for body mass index instead of waist circumference gave similar results (only the results adjusted for waist circumference are included in the paper).

Results

Table 2 shows the baseline characteristics of the Asklepios Study and the average dietary scores for both sexes and for two age groups (30–45 and 45–60 years) separately. Women score generally higher than men (69.3 vs 58.8%). This is mainly due to a difference in dietary quality score (54.9 vs 31.3%). As a result of these clear gender differences, we computed partial correlations adjusted for age between the dietary scores and some CV risk factors and markers of atherosclerosis and inflammation stratified by gender. There is no remarkable difference in dietary scores between the two age groups.

Table 2 Baseline characteristics of the Asklepios study population and average dietary scores±s.d. (%)

Traditional CV risk factors

In Table 3, the relationship between the dietary scores and other CV risk factors is presented. The correlations of the dietary scores with anthropometric variables were in the expected directions for the waist hip ratio, namely inversely correlated with the dietary scores. The correlations between the dietary scores and body mass index were less significant. Although a clear inverse correlation was found between dietary scores and blood pressure and non-high-density lipoprotein-cholesterol in men, no significant association was found in women (Table 3).

Table 3 Relationship between the dietary scores and cardiovascular risk factors (n=2487)

Significant inverse correlations were seen between the dietary scores and blood triglycerides and homocystein in both genders. Smoking and alcohol consumption were strongly associated with lower dietary scores in both genders. SCORE (Conroy et al., 2003) estimates the risk for a fatal CV event in the next 10 years. There was a significant correlation between higher SCORE risks and lower dietary scores in both genders (Table 3).

Inflammation

In Table 4, the relationship between diet and inflammatory markers is presented.

Table 4 Relations between diet and inflammatory markers

There were significant negative correlations, partially adjusted for age, between the overall dietary score, the dietary diversity and equilibrium score and inflammatory markers (high-sensitive C-reactive protein, oxidized low-density lipoprotein-cholesterol and IL-6 in men only, while leukocyte count in both genders) (Table 4).

After multivariate adjustment (full-model), significant inverse correlations remained between the moderation score and the leukocyte count (women: B=−0.028; P<0.001/men: B=−0.020; P=0.004) and between the dietary quality score and raised IL-6 in men (B=−0.001; P=0.015). Although also inverse correlations were found between the dietary quality score and high-sensitive C-reactive protein (women: B=−0.002; P=0.031/men: B=−0.002; P=0.036), these correlations were not statistically significant.

Atherosclerosis

In Table 5, the effect of diet on carotid and femoral atherosclerosis, plaques and IMT is presented.

Table 5 Effect of diet on atherosclerosis

Only significant inverse correlations were found between diet and femoral atherosclerosis. In women, significant correlations with femoral atherosclerosis were found for the adequacy and dietary diversity score, and among men for the overall dietary score and the dietary diversity score (Table 5). In men, the overall dietary score was significantly inversely associated with femoral plaques and with femoral IMT, while not with carotid plaques or IMT.

After multivariate adjustment, the relation between diet and atherosclerosis was no longer significant (values not shown).

Discussion

Main results

Different inverse associations were found between the overall dietary score and the suspected anthropometric (waist/hip), clinical (blood pressure) and biological (non-high-density lipoprotein-cholesterol, triglycerides and homocystein) risk factors presented in Table 3. Although these inverse associations were generally only significant in the male group (except from blood triglycerides and homocystein, which were significantly inversely associated with dietary scores in women as well). Also some subscores were significantly inversely associated with these CVD risk factors.

Adjusting for age and stratifying for genders, showed a significant inverse correlation between dietary scores and the inflammation markers high-sensitive C-reactive protein, oxidized low-density lipoprotein-cholesterol and IL-6 in men only. However, significant inverse correlations between dietary scores and the leukocyte count were found in both genders. After multivariate adjustments, correlations became weaker, but still significant for raised IL-6 in men and for leukocyte count in both genders.

With regard to atherosclerosis, there were only few significant inverse associations between diet and femoral atherosclerosis. However, after adjustments for confounders, none of these associations remained significant. This finding indicates that there was no direct effect of diet on subclinical atherosclerosis, but suggests that the effect of diet on atherosclerosis was mainly mediated through the effect of diet on the traditional risk factors.

Strengths and limitations

This is the first study to our knowledge evaluating the effect of a diet, expressed as a score indicating the level of compliance with the FBDGs, on carotid and femoral atherosclerosis. Both the study size and the in-depth phenotyping, with an important number of biomarkers analyzed in this survey are an important strength of this study.

Although the FFQ is typically used to investigate habitual (long-term) dietary intakes in large-scale surveys, this method also has its limitations. As a result of its closed structure, the flexibility and the degree of between-person variation is limited compared with open methods like food records or 24-h dietary recalls. In addition, does this method rely on the respondents’ memory and their capabilities to interpret those frequency questions. However, important strengths of the FFQ are its low respondent burden and cost and the fact that it gives information about respondents’ usual or habitual dietary intake (Willett, 1998). As mentioned before, the FFQ and the FFQ-based dietary scores that were used derived from previous research among our Belgian population. The FFQ-based dietary quality scores were shown to be reproducible and valid by comparison with a 3-day dietary record approach in a Flemish preschool population (Huybrechts et al., 2010). This FFQ-based dietary quality index is currently being used and evaluated in different national and international surveys and showed good performance in all these studies (data not shown).

Comparison with the literature

Our results are consistent with the results of large European and American studies. The association between higher dietary scores (such as the Recommended Food Score, the Healthy Eating Index, the Mediterranean Diet Scale, the prudent pattern) and a lower CV risk profile was published before in several large-scale studies (Kant et al., 2000; McCullough et al., 2000a,; Fung et al., 2001a,; Trichopoulou et al., 2003; Esposito et al., 2004; Lopez-Garcia et al., 2004; Millen et al., 2004; Fogli-Cawley et al., 2006; Nettleton et al., 2006; Esmaillzadeh et al., 2007).

We observed no direct effect of diet on atherosclerosis, after adjustment for appropriate confounders. This finding is in line with some other studies, where only minor effects of diet on subclinical atherosclerosis were found. Millen et al. (2004) could not demonstrate a lower risk of subclinical atherosclerosis in women with a healthy life style neither. Nettleton et al. (2007) showed only borderline significance between dietary patterns and carotid IMT. None of these studies discussed a complete overview of carotid and femoral atherosclerosis.

More recently, however, Mikkila et al. (2009) found significant independent associations between diet and IMT in men (P<0.01), but not in women (P=0.66) participating in the CV Risk in Young Finns cohort. Also Liese and Kesse-Guyot recently reported significant independent associations between diet and atherosclerosis from two cohort studies (Kesse-Guyot et al., 2010; Liese et al., 2010). These findings were in contrast with our findings. However, it should be noted that the previous studies that did find significant associations with atherosclerosis did not correct for the large battery of CV risk factors as was done in our Asklepios Study.

More investigators have found a relationship between diet and markers of inflammation, even after multivariate adjustment (Fung et al., 2001a; Chrysohoou et al., 2004; Esposito et al., 2004; Lopez-Garcia et al., 2004; Ford et al., 2005; Pitsavos et al., 2005; Nettleton et al., 2006; Panagiotakos et al., 2006; Esmaillzadeh et al., 2007).

Conclusion

We conclude that better adherence to the Flemish FBDGs is associated with a better CV risk profile and less inflammation in men. In women this association was less pronounced. There is no direct effect on the presence of carotid or femoral atherosclerosis, but mediated through traditional CV risk factors and inflammation. Further examinations are needed to answer the question whether adherence to diet equally protects against CV morbidity and mortality.

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Acknowledgements

We want to acknowledge all the participants from the Asklepios Study who voluntarily contributed to this study. The Asklepios Study was partly funded by an FWO Research Grant FWO (G.0427.03).

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Correspondence to I Huybrechts.

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Additional information

Contributors: LIH: statistical analyses, interpretation of the results and drafting of the paper. ERR: conceptualization of the study, statistical analyses, interpretation of the results and contribution to the writing of the paper. ML: laboratory investigations, and contribution to the writing of the paper. MDB: contribution to conceptualization of the study and to the writing of the paper. DDB: contribution to conceptualization of the study and to the writing of the paper. GDB: conceptualization of the study, and contribution to the writing of the paper. LM: concept of FBDGs and dietary quality index, interpretation of the results and contribution to the writing of the paper. TG: conceptualization of the study, interpretation of the results and contribution to the writing of the paper. IH: conceptualization of the dietary intake questionnaire, statistical analyses, interpretation of the results and contribution to the writing of the paper.

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Hoebeeck, L., Rietzschel, E., Langlois, M. et al. The relationship between diet and subclinical atherosclerosis: results from the Asklepios Study. Eur J Clin Nutr 65, 606–613 (2011). https://doi.org/10.1038/ejcn.2010.286

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Keywords

  • diet
  • inflammation
  • atherosclerosis

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