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The Association between Adherence to the Mediterranean Diet and Fasting Indices of Glucose Homoeostasis: The ATTICA Study

Department of Nutrition and Dietetics, Harokopio University (D.B.P, N.T., A.Z.)
First Cardiology Clinic, School of Medicine, University of Athens, Athens, GREECE (C.P., C.C., D.T., C.S.)

Address reprint requests to: Demosthenes B. Panagiotakos, PhD, 46 Paleon Polemiston St., 166 74, Attica, GREECE. E-mail: d.b.panagiotakos{at}usa.net

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS CONCLUSION ACKNOWLEDGMENTS REFERENCES

 
Objective: We investigated the association between adherence to Mediterranean diet and fasting indices of glucose homoeostasis, in a Greek adult population.

Methods: During 2001–2002 we randomly enrolled 1514 men and 1528 women (18–89 years old) without history of CVD, from the Attica area. Diabetes mellitus (type 2) and impaired fasting glucose (IFG) were defined according to the established ADA criteria. Insulin resistance was evaluated by HOMA-IR. Dietary habits were assessed through a validated food frequency questionnaire and a diet score (range 0–55) was developed (higher values means greater adherence to the Mediterranean diet).

Results: The overall prevalence of diabetes type 2 was 7.9% in men and 6.0% in women (P = 0.05). Mean diet score was 26.3 ± 6.8 in normoglycemic, 25.7 ± 6.4 in IFG and 22.2 ± 5.8 in diabetic subjects (p < 0.001). In normoglycemic subjects who were in the upper tertile of the diet score we observed 7% lower glucose (p < 0.05), 5% lower insulin (p < 0.05) and 15% lower HOMA-IR (p < 0.01) levels compared to subjects in the lower tertile of the diet score. Additionally, in diabetic/IFG participants who where in the upper tertile of the diet score we observed 15% lower glucose (p < 0.05), 15% lower insulin (p < 0.05) and 27% lower HOMA-IR (p < 0.01) levels compared to those in the lower tertile. However, multiple regression analysis, adjusted for age, sex, BMI, waist-to-hip ratio, physical activity, smoking status, and presence of hypertension and hypercholesterolemia, confirmed the previous associations in normoglycemic, but not in diabetic/IFG people.

Conclusion: An inverse association was observed between adherence to Mediterranean diet and indices of glucose homeostasis, only in normoglycemic people.

Key words: Mediterranean diet, type 2 diabetes, IFG, insulin resistance, glycemic profile

Abbreviations: IFG = impaired fasting glucose • HOMA-IR = homeostasis model assessment (IR = insulin resistance) • LDL = low-density lipoprotein • HDL = high-density lipoprotein • SFA = saturated fatty acids • MUFA = monounsaturated fatty acids

	INTRODUCTION

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The prevalence of type 2 diabetes mellitus has increased rapidly the last decades and this phenomenon is related to a rise in the prevalence of excess weight and obesity, sedentary lifestyle, unhealthy dietary habits, growth of population and ageing [1–3]. Moreover, the number of people with a diagnosis of impaired fasting glucose (IFG), which is included in the term prediabetes, is expected to rise also [4]. All abovementioned people carry a series of risk factors for cardiovascular disease, including hyperglycaemia, dyslipidemia, and alteration in inflammatory mediators and coagulation parameters [5,6]. The American Diabetic Association recommends attainment and maintenance of an optimum body mass index and a diet according to Diabetes Food Pyramid for prediabetic and diabetic people, but an enormous interest exists also regarding the ideal diet for the general population in order to prevent diabetes and enhance insulin sensitivity [7–9].

Even though there are reports for the advantageous effect of some isolated foods or food groups like fruits, vegetables, fiber etc., on glucose metabolism [10], several investigators now propose the study of whole dietary patterns, in order to overcome potential interactions and inter-correlations among single nutrients and foods [11,12]. Such a whole dietary pattern, the Mediterranean diet, has evidently a beneficial effect on dyslipidemia—also to individuals with diabetes and an atheroprotective effect [13–15]. Nevertheless its role to the fasting indices of glucose homoeostasis and its effect to insulin resistance has not yet been elucidated, at population level. The aim of this work was to examine the association between adherence to the Mediterranean diet and fasting indices of glucose homoeostasis in adults without any clinical evidences of cardiovascular disease, randomly selected from the general population.

	METHODS

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The "ATTICA" epidemiological study has been carried out in the province of Attica (including 78% urban and 22% rural areas). From May 2001 to December 2002, 4056 inhabitants from the area were randomly selected and asked to participate. 3042 of them (age range 18–89 years) agreed to participate (75% participation rate). All participants were interviewed by trained personnel (cardiologists, general practitioners, dieticians and nurses), who used standard questionnaires that evaluated lifestyle habits and various socio-demographic, clinical and biological characteristics. Five percent of men and 3% of women were excluded from the study because they reported history of cardiovascular or any other atherosclerotic disease, as well as chronic viral infections. Moreover, participants who had had a cold or flu, acute respiratory infection, dental problems or any type of surgery during the past weeks were also excluded.

All participants underwent the fasting plasma glucose test. Diabetes was defined according to the American Diabetes Association diagnostic criteria. In particular, blood glucose levels greater or equal to 126 mg/dl classified participants as having diabetes while glucose levels between 100 to 125 mg/dl classified participants as IFG [16], a pre-diabetic condition. However, it should be mentioned that the use of this cut-off for defining IFG is still controversial [17]. In this work the population studied was divided into those with diabetes mellitus (type 2), IFG and with normal fasting glucose levels. However, since it has been reported that diabetic and IFG patients have higher risk for cardiovascular morbidity compared to normoglycemic [4], in most analyses we have merged the two groups to increase the number of people in this category. Patients with type 1 were excluded from the analysis due to their small sample size (i.e. < 1% of the study's population). Power analysis showed that the number of enrolled participants is adequate to evaluate two-sided standardised differences between subgroups of the study and the investigated parameters greater than 0.5 (power > 0.90 at < 0.05 significance level).

The study was approved by the Medical Research Ethics Committee of our Institution and was carried out in accordance with the Declaration of Helsinki (1989) of the World Medical Association.

Dietary Assessment
Usual dietary intake over the year preceding enrollment was assessed by a validated, semi-quantitative food frequency questionnaire, including 156 foods and beverages commonly consumed in Greece [18,19]. We asked all participants to report the daily or weekly average intake of several food items that they consumed. Then, the frequency of consumption was quantified approximately in terms of the number of times a month this food was consumed. Alcohol consumption was measured in wineglasses (100 ml) and quantified by ethanol intake (grams per drink). One wineglass was equal to 12 g ethanol concentration. Based on a dietary pyramid that has been developed to describe the Mediterranean dietary pattern [18] and the reported consumption of the 9 major food groups non-refined cereals, fruit, vegetables, legumes, potatoes, fish, meat and meat products, poultry, full fat dairy products, as well as olive oil and alcohol intake, we calculated a special diet score that assessed adherence to this dietary pattern. In particular, for the consumption of items presumed to be part of the recommended Mediterranean pattern (i.e. those suggested on a daily basis or more than 4 servings per week; non-refined cereals, fruits, vegetables, legumes, olive oil, fish, and potatoes) we assigned score = 0 when someone reported no consumption, score = 1 when they reported consumption of 1 to 4 servings/month, score = 2 for 5 to 8 servings/month, score = 3 for 9 to 12 servings/month, score = 4 for 13 to 18 servings/month and score = 5 for more than 18 servings per month. For the consumption of foods presumed not to be part of the recommended Mediterranean pattern (i.e. consumption of meat and meat products, poultry and full fat dairy products) we assigned the scores on a reverse scale (i.e. 5 when someone reported no consumption to 0 when they reported almost daily consumption). Especially for alcohol we assigned score 5 for consumption of less than 3 wineglasses per day, score 0 for consumption of more than 7 wineglasses per day and scores 4 to 1 for consumption of 3, 4 to 5, 6 and 7 or 0 wineglasses per day. Thus, the range of the diet score was between 0–55. Higher values of this diet score indicates greater adherence to the Mediterranean diet.

Socio-Demographic And Lifestyle Variables
We recorded mean annual income during the past three years and the educational level of the participants in years of school (as a proxies of social status). Current smokers were defined as those who smoked at least one cigarette per day; former smokers were defined as those who had stopped smoking for at least one year and the rest of the participants were defined as non-smokers. Occasional smokers (less than 7 cigarettes per week) were recorded and combined with current smokers due to their small sample size. For a more accurate evaluation of smoking habits we calculated the pack-years (cigarette packs per day x years of smoking), adjusted for a nicotine content of 0.8 mg/cigarette.

For the ascertainment of physical activity status we used the International Physical Activity Questionnaire (IPAQ, [20]), as an index of weekly energy expenditure using frequency (times per week), duration (in minutes per time) and intensity of sports or other habits related to physical activity. Particularly, intensity was gradated in qualitative terms such as: light (expended calories < 4 Kcal/min, i.e. walking slowly, cycling stationary, light stretching etc.), moderate (expended calories 4–7 Kcal/min, i.e. walking briskly, cycling outdoor, swimming moderate effort etc.) and high (expended calories > 7 Kcal/min, i.e. walking briskly uphill, long distance running, cycling fast or racing, swimming fast crawl etc.). Participants who did not report any physical activities were defined as sedentary. For the rest of the participants we calculated a combined score by multiplying the weekly frequency, duration and intensity of physical activity.

Anthropometric, Clinical and Biochemical Characteristics
Standing height and weight were recorded, and body mass index was calculated as weight (in kilograms) divided by standing height (in meters squared). According to standard guidelines obesity was defined as BMI greater than 29.9 kg/m². Arterial blood pressure was measured three times, at the end of the physical examination with the subject in sitting position. Before blood pressure evaluation all participants were at least 30 minutes at rest. Patients whose average blood pressure levels were greater or equal to 140/90 mmHg or who were under anti-hypertensive medication were classified as hypertensive. Venous fasting blood samples were collected and measured immediately with a Beckman Glucose Analyzer (Beckman Instruments, Fullerton, CA, USA). Serum insulin concentrations were assayed by means of radioimmunoassay (RIA100, Pharmacia Co., Erlangen, Germany). Insulin resistance was assessed by the calculation of a homeostasis model assessment (HOMA-IR) approach (glucose in mmol/l x insulin in µU/mL/22.5) [21]. As the ability of the ß-cell to respond to insulin resistance with an increase in hormone secretion is disrupted in type 2 diabetes, especially when insulin-treated, insulin levels were not measured from the samples of the diabetic patients with insulin treatment. Moreover, HOMA-IR was not calculated for people with diabetes. Total cholesterol was measured using chromatographic enzymic method (Technicon automatic analyzer RA 1000, Tarrytown, NY, USA). Hypercholesterolemia was defined as total serum cholesterol levels greater than 200 mg/dl or the use of lipid lowering agents.

Further details about the design and methods of the ATTICA study have been presented elsewhere [22].

Statistical Analysis
Associations between categorical variables were tested by the calculation of chi-squared test, while differences between categorical and several biochemical, clinical and nutritional variables were tested by the use of Student's t-test and Mann-Whitney criterion (for the normally distributed and the skewed variables, respectively). Due to multiple comparisons we used the Bonferroni correction in order to account for the increase in Type I error. A multiple linear regression model was applied to test the association between the different glycemic control indices and the diet score, after controlling for several potential confounders. Collinearity between independent variables was evaluated through the condition index and the Durbin-Watson criterion, while model's goodness of fit was graphically evaluated (standardized residuals against fitted values). All reported P-values are based on two-sided tests and compared to a significance level of 5%. SPSS 12 (SPSS Inc., Chicago, IL, USA) software was used for all the statistical calculations.

	RESULTS

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The overall prevalence of diabetes type 2 was 118 out of 1514 men (7.8%) and 92 out of 1528 women (6.0%), (P for gender differences = 0.05). Prevalence of IFG was 310 out of 1514 men (21%) and 184 out of 1528 women (12%), (P for gender differences = 0.05).

Table 1 illustrates various characteristics of the participants by glucose tolerance status. As we progress from normal towards diabetic subjects, we observed that people are older and less active and less insulin sensitive, in greater proportion males and smokers. The prevalence of obesity increased, waist and BMI levels were higher and co-morbidities rates (hypercholesterolemia and hypertension) were more elevated also. Compared to normal subjects, diabetic subjects had lower levels of the diet score (p = 0.001). Moreover, mean HOMA-IR levels in normal people were 2.5 ± 0.48 and in IFG were 3.8 ± 0.43.

	DISCUSSION

The association found between Mediterranean diet and glucose homeostasis indices in normoglycemic people are in agreement with the results of several intervention trials. In particular, Perez-Himenez et al. [23] report that Mediterranean diet (enriched in MUFA) improved insulin sensitivity in healthy young men and women. These findings are in accordance also with the KANWU study, where the substitution of SFA for MUFA improved insulin sensitivity in healthy men and women [24] and the Pizarra study where oleic acid and olive oil, the major component of Mediterranean diet was associated with lower insulin resistance in a general population [25].

Some intervention studies reveal a favourable effect of Mediterranean diet on glucose metabolism in people with diabetes or the metabolic syndrome. Hence, Esposito et al. report that the Mediterranean-style diet is associated with increased insulin sensitivity in people with metabolic syndrome [26]. In addition, the results of the "Mediterranean life style program" referring to postmenopausal women with type 2 diabetes demonstrate an improvement in glucose control with the adoption of the Mediterranean diet [27]. Nevertheless, the present work did not show a relationship between adherence to the Mediterranean diet and fasting indices of glucose homoeostasis in diabetic or IFG people, probably because of the large variation of diet score observed within this group (Table 3) and because HOMA-IR is not a reliable measure in individuals with diabetes. Moreover, for diabetic people, the major concern is achievement of glycemic control through different means: diet and physical activity for attainment and maintenance of ideal weight and pharmaceutical treatment when necessary [28,29]. It seems that various types of diet can achieve the goal of glycemic control [30–33]. Though, glycemic control is not the only therapeutical goal in diabetic people; control of blood lipids and hypertension are additional targets and there are now adequate evidences that Mediterranean diet can contribute to accomplish them [34,35]. Considering that all studies of lifestyle intervention on diabetes incidence found a clear benefit for diet and exercise [36] and the fact that Mediterranean diet is more readily acceptable by the general population than the current recommendations, we must further investigate its preventive role in the development of diabetes and cardiovascular complications.

Limitations
Due to its cross-sectional character, this study could not establish causal relationships, but only states hypotheses about the link between fasting indices of glucose homoeostasis and lifestyle characteristics of the participants. Moreover, inverse causality may exist, i.e. a portion of diabetic people may be attached to a non-Mediterranean diet, due to an incorrect belief that a diet with more protein and less starches is more appropriate and at the same time non diabetic people may feel free to choose to eat a lot of fruits, starches, olive oil. Additionally, there is a possibility that the recommendations for a diabetic diet may somehow influence certain components of adherence to a Mediterranean diet, in a positive or negative way, like reducing carbohydrate intake. Misreporting of food items consumed could influence the calculation of the diet score and bias the results for the data analysis. This particular be the case for individuals with diabetes, since obese people underreport to a larger extend than non-obese [37]. In this study, we did not use the gold standard, the euglycaemic-hyperinsulinaemic clamp in assessment of insulin sensitivity. However, some investigators reported that HOMA-IR is strongly related to clamp-measured insulin resistance in both nondiabetic and diabetic subjects [38–40]. Finally the lack of HbAlc data is another limitation of the study.

	CONCLUSION

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Despite the limitations of the present study, we provide current evidence about the association between Mediterranean diet and fasting indices of glucose homoeostasis. To the best of our knowledge this is the first, non interventional study, that reveals an inverse association between greater adherence to Mediterranean diet and levels of fasting glucose, insulin and insulin resistance in normoglycemic subjects, coming from the general, "free-eating," population. There is a great need to further investigate the role of Mediterranean diet as a potential public health measure for the prevention of diabetes and related cardiovascular complications through metabolic, interventional studies.

	ACKNOWLEDGMENTS

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The ATTICA study was supported by research grants from the Hellenic Cardiological Society (HCS2002). The authors would like to thank the filed investigators of "ATTICA" study: Dr. Y. Skoumas (physical examination, head), Dr. M. Toutouza (biochemical analyses, head), Dr. A. Zeimbekis (physical examination), Dr. N. Papaioannou (physical examination), Dr. E. Tsetsekou (physical examination), Dr. L. Papadimitriou (physical examination), Dr. C. Massoura (physical examination), Dr. S. Vellas (physical examination), Dr. A. Katinioti (physical examination), Ms. C. Vassiliadou (genetic evaluation), Mr. E. Kambaxis (nutritional evaluation), Ms. K. Paliou (nutritional evaluation), Ms. C. Tselika (biochemical analyses), Ms. S. Poulopoulou (biochemical analyses) and Ms. M. Toutouza (data base management).

Received December 6, 2005. Accepted April 20, 2006.

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