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Lipids and cardiovascular/metabolic health

Effects of Mediterranean-style diet on glycemic control, weight loss and cardiovascular risk factors among type 2 diabetes individuals: a meta-analysis

Abstract

Background/Objectives:

Studies suggest that the Mediterranean-style diet (MSD) may improve glucose metabolism in patients with type 2 diabetes (T2D), but the results are inconsistent. We conducted a meta-analysis of randomized controlled trials (RCTs) to explore the effects of MSD on glycemic control, weight loss and cardiovascular risk factors in T2D patients.

Subjects/Methods:

We performed searches of EMBASE, Cochrane Library and PubMed databases up to February 2014. We included RCTs that compared the MSD with control diets in patients with T2D. Effect size was estimated as mean difference with 95% confidence interval (CI) by using random effect models.

Results:

The meta-analysis included nine studies with 1178 patients. Compared with control diets, MSD led to greater reductions in hemoglobin A1c (mean difference, −0.30; 95% CI, −0.46 to −0.14), fasting plasma glucose (−0.72 mmol/l; CI, −1.24 to −0.21), fasting insulin (−0.55 μU/ml; CI, −0.81 to −0.29), body mass index (−0.29 kg/m2; CI, −0.46 to −0.12) and body weight (−0.29 kg; CI, −0.55 to −0.04). Likewise, concentrations of total cholesterol and triglyceride were decreased (−0.14 mmol/l; CI, −0.19 to −0.09 and −0.29 mmol/l; CI, −0.47 to −0.10, respectively), and high-density lipoprotein was increased (0.06 mmol/l; CI, 0.02 to 0.10). In addition, MSD was associated with a decline of 1.45 mm Hg (CI, −1.97 to −0.94) for systolic blood pressure and 1.41 mm Hg (CI, −1.84 to −0.97) for diastolic blood pressure.

Conclusions:

The present meta-analysis provides evidence that MSD improves outcomes of glycemic control, body weight and cardiovascular risk factors in T2D patients.

Introduction

Type 2 diabetes (T2D) is a global epidemic and a main threat to human health. It is estimated that about 552 million cases worldwide will suffer from T2D by the year 2030,1 with an accompanying increase in diabetes-related complications and health-care expenditures. In view of its severity, there is a need for new therapeutic approaches to manage T2D. It is well established that lifestyle interventions, including dietary changes, have a vital role in preventing the progression of impaired fasting glucose or impaired glucose tolerance to T2D.2, 3, 4, 5, 6 However, there is limited evidence on appropriate dietary strategy to manage hyperglycemia in T2D patients.

The Mediterranean diet has been widely reported to be the optimal diet for contributing to a beneficial health status.7, 8 The diet was originally described by Ancel Keys in the 1960s, on the basis of epidemiological data linking the dietary pattern of people in the Mediterranean region with low rates of cardiovascular disease.9 Notably, there is no single Mediterranean diet, because the populations in different countries bordering the Mediterranean Sea have their own eating habits. As a result, the 'Mediterranean-style diet (MSD)' is used to represent a collection of food habits traditionally followed by people of different regions in the Mediterranean basin, and it is characterized by a high consumption of vegetables, monounsaturated fatty acids (primarily from olive oil), fruits, cereals and legumes, a low consumption of red or processed meat and a low-to-moderate consumption of red wine during meals.10

Increased epidemiological evidence has suggested that a greater adherence to MSD is associated with a lower risk of diabetes.11, 12, 13, 14, 15, 16, 17, 18 However, relatively few studies have explored the link between the MSD and glycemic control in T2D patients, and the results are inconsistent. Some reported positive effect on glycemic control,19, 20, 21, 22, 23, 24 others did not.25, 26, 27 Therefore, we did a meta-analysis of randomized controlled trials (RCTs) to offer a comprehensive and updated overview of the effects of MSD on glycemic control, weight loss and cardiovascular risk factors in patients with T2D.

Materials and methods

Design

The present meta-analysis was conducted and reported in accordance with the statement of the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA).28

Data sources and search strategy

We performed a systematic electronic search of PubMed, Cochrane Library and EMBASE databases up to February 2014 for RCTs assessing the effect of MSD compared with control diet on the management of T2D. The search terms comprising Medical Subject Headings, free text and word variants were as follows: 'Diet, Mediterranean' or 'Mediterranean diet' or 'Mediterranean eating pattern' or 'Mediterranean-style diet' and 'Diabetes Mellitus, type 2' or 'type 2 diabetes' or 'diabetes type 2' or 'diabetic'. Furthermore, the reference lists of relevant original reports and review articles were retrieved manually.

Study selection

Studies were considered eligible if they (1) were RCTs (either parallel or cross-over design), (2) enrolled adult patients with already diagnosed T2D, (3) evaluated the effect of MSD with a minimum intervention period of 4 weeks and (4) reported at least hemoglobin A1c (HbA1c) outcome data. Studies were excluded if they (1) were clinical trials that reported lack of randomization or control diet group, (2) had a cohort, case-control or cross-sectional design, (3) included subjects with type 1 diabetes, gestational diabetes or at high risk for diabetes, (4) did not report relevant data or (5) performed a post hoc analysis of previous studies. In addition, we excluded commentaries, reviews, letters, editorials, duplications, nonhuman studies and extensions of original studies. Two researchers independently assessed the eligibility of all potentially relevant studies, and any discordance in opinion was reconciled by group discussion.

Data extraction and outcomes

The following information were extracted from the eligible studies: name of the first author, year of publication, study design, country of origin, sample size for each group, intervention period, participants’ characteristics (age, race, sex and duration of T2D), contents of intervention and control conditions, as well as main study findings.

Outcome measures were classified into three aspects: (1) glycemic control including changes in HbA1c, fasting plasma glucose (FPG), fasting insulin and homeostasis model assessment of insulin resistance; (2) weight control including changes in body weight, body mass index (BMI) and waist circumference; and (3) cardiovascular risk factors including changes in total cholesterol, triglyceride, high-density lipoprotein cholesterol and low-density lipoprotein cholesterol, as well as systolic and diastolic blood pressure. If data were reported in diverse units, they were converted into uniform units for consistency of the results. For multiple papers of the same study, we collected data from the most updated or complete report.

Quality assessment

We assessed risk of bias of RCTs based on the Cochrane Collaboration’s tool.29 The categories were random sequence generation, allocation concealment, blinding (participants, study personnel and outcome assessors), incomplete outcome data, selective outcome reporting and other sources of bias. Two investigators independently evaluated the above risk of bias domains and classified each study as a low risk of bias, an uncertain risk of bias or a high risk of bias. Discrepancies in opinion between the two investigators were resolved by consensus.

Statistical analysis

In our meta-analysis, the mean differences with 95% confidence intervals (CIs) between MSD and control diet were calculated as the effect size for continuous outcomes. For some studies, missing standard deviations of the changes were computed from standard errors, 95% CIs or P-values.30 We performed primary analyses using a random effects model that adequately accounts for between-study variability.

Heterogeneity among studies was examined by the Cochrane Q-test and I2 statistic. A level of P-value 0.10 was considered as statistically significant heterogeneity. The I2 statistic provides an estimate of the extent of inconsistency attributable to inter-study heterogeneity. I2 values of 25, 50 and 75% indicate low, moderate and high levels of heterogeneity, respectively.31, 32 If results showed substantial heterogeneity, we explored potential sources of heterogeneity through subgroup analysis and sensitivity analysis when required. We visually assessed potential publication bias using funnel plots, in which the effect size was plotted against its corresponding standard error for each outcome. Furthermore, publication bias was formally assessed by Begg’s33 and Egger’s tests.34

All statistical analyses were performed by means of Stata statistical software version 12.0 (StataCorp, College Station, TX, USA), and a two-sided P-value <0.05 was considered statistically significant.

Results

Search results

The study selection process is presented in Figure 1. We identified 1102 potentially relevant records, of which 1076 records from the initial electronic searches of three major online databases and 26 additional records from hand searches of other sources (reference lists of high-quality systematic reviews and other articles). After excluding duplicates and studies that clearly could not fulfill our inclusion criteria, 63 articles remained for further evaluation of full texts. Of these, we excluded 54 studies for the following reasons: 28 studies included mixed populations of individuals with and without T2D with no separate data provided for the T2D groups; 24 studies did not report at least one of our required clinical outcomes; one study35 was only published as an abstract and the full paper was not available; and another study36 was a parallel clinical trial but not a randomized one, because it was a post hoc analysis of the PREDIMED study. Finally, nine studies involving a total of 1178 patients met the inclusion criteria and entered into this meta-analysis.

Figure 1
figure1

Flow diagram of literature search and study selection.

Study characteristics

Table 1 summarizes baseline characteristics of the included studies, all of which were published as full text articles in the English language. Follow-up periods ranged from 4 weeks to 4 years. Participants’ ages varied from 26 to 77 years at the time of intervention. All included studies were RCTs that comprised seven parallel trials19, 20, 21, 23, 24, 26, 27 and two cross over trials.22, 25 The trials were conducted in the United States,19, 24, 27 Greece,26 Israel,20, 23 Italy,21 Spain25 and Australia.22 With the exception of one study by Shai et al.,20 the remaining eight studies enrolled only participants with T2D. Although the study by Shai et al. included subjects with and without T2D, it provided separate data on changes in HbA1c, FPG, fasting insulin and homeostasis model assessment of insulin resistance for T2D subjects, and thus these outcomes were included in our meta-analysis.

Table 1 Study characteristics of included randomized controlled trials

All included trials studied the role of the MSD in T2D patients. Two of the studies compared three separate diets, one study20 compared a MSD versus two types of control diets, and the other one23 compared two versions of MSD versus a control diet. We treated these arms in isolation. Therefore, nine RCTs with 11 arms were included in the quantitative analysis, of which the control diets comprised low-fat diet, usual dietary habits, nonrestricted-calorie low-carbohydrate diet, the 2003 American Diabetes Association (ADA) diet and high-carbohydrate diet. Reports of MSD varied across studies, but all of the included trials comprised the basic characteristics of this diet. In particular, two trials25, 27 emphasized high-monounsaturated fatty acid-enriched intervention diet, whereas we chose to include these two trials because actually consumed study diets were comparable to the traditional Mediterranean diet (Table 1).

Quality of studies

Among the nine eligible studies, random sequence generation was adequate in three21, 24, 25 and unclear in six.19, 20, 22, 23, 26, 27 Concealment of group allocation was described adequately in three studies,21, 23, 24 whereas in the remaining six studies, it remained unclear. Blinding of participants and key study personnel for dietary intervention are difficult; therefore, none of the included studies reported the success of blinding. Outcome assessors were blinded in four studies21, 23, 24, 27 and unclear in the rest of the studies. In addition, none of the studies had incomplete outcome data or reporting bias (Supplementary Table 1).

Outcomes

Glycemic control (HbA1c, FPG, fasting insulin and homeostasis model assessment of insulin resistance)

Nine studies with 11 arms (n=1178) contributed data in our main analysis for the change in HbA1c from baseline (Figure 2a). Compared with control diets, the MSD was associated with a significant reduction in HbA1c (mean difference, −0.30; 95% CI, −0.46 to −0.14) by using a random effects model. We found evidence of between-study heterogeneity in this analysis (I2=67.2%; P=0.001).

Figure 2
figure2

Forest plots assessing the effects of MSD on HbA1c (a), FPG (b) and fasting insulin (c). A random effects model was used to calculate the mean difference between MSD and control diet. Shai-1 is the comparison between a MSD and a low-fat diet arm of the study. Shai-2 is the comparison between a MSD and a low-carbohydrate diet arm of the study. Elhayany-1 is the comparison between a low-carbohydrate Mediterranean diet and an ADA diet arm of the study. Elhayany-2 is the comparison between a traditional Mediterranean diet and an ADA diet arm of the study. ADA, American Diabetes Association; FPG, fasting plasma glucose; HbA1c, hemoglobin A1c; MSD, Mediterranean-style diet.

Changes in FPG levels were pooled for six studies with seven arms (n=580). Subjects who consumed MSD had decreased FPG levels (−0.72 mmol/l; CI, −1.24 to −0.21) compared with subjects who consumed control diet (Figure 2b). Heterogeneity of the effect measures on FPG was detected (I2=66.1%; P=0.007).

Five studies with six arms (n=531) measured fasting insulin and reported data that could be pooled in the analysis. Compared with control diet, there was a minimal but statistically significant decline in fasting insulin levels (−0.55 μU/ml; CI, −0.81 to −0.29) for MSD (Figure 2c). No heterogeneity was observed (I2=0.0%; P=0.46).

With regard to homeostasis model assessment of insulin resistance, although the beneficial effect of MSD compared with control diet was not statistically significant (mean difference, −0.55; CI, −1.53 to 0.42), the MSD had greater probability on improving insulin resistance. Moderate heterogeneity was present between the studies (I2=45.8%; P=0.137).

BMI, body weight and waist circumference

Six studies with seven arms reported the change in BMI from baseline (Figure 3a). We conducted a random effects meta-analysis comprising 520 patients randomly assigned to the MSD and 500 assigned to the control diets. The MSD was more effective in decreasing BMI compared with those in the control diets (mean difference, −0.29 kg/m2; 95% CI, −0.46 to −0.12; I2=0.0%; P=0.976).

Figure 3
figure3

Forest plots assessing the effects of MSD on BMI (a) and body weight (b). Elhayany-1 is the comparison between a low-carbohydrate Mediterranean diet and an ADA diet arm of the study. Elhayany-2 is the comparison between a traditional Mediterranean diet and an ADA diet arm of the study. ADA, American Diabetes Association; BMI, body mass index; MSD, Mediterranean-style diet.

Concerned about body weight, six studies involving 835 patients demonstrated that MSD was associated with a significant weight loss of 0.29 kg (CI, −0.55 to −0.04; I2=0.0%; P=0.924) as compared with control diets (Figure 3b).

In addition, only three studies with four arms (n=416) provided data on waist circumference and showed no significant reduction in waist circumference when MSD was compared with control diets (−0.41 cm; CI, −0.89 to 0.08; I2=0.0%; P=0.97). Evidence of heterogeneity in these outcomes was lacking among studies.

Cardiovascular risk factors (lipid profile and blood pressure)

Random effects meta-analyses found that the MSD significantly decreased concentrations of total cholesterol (mean difference, −0.14 mmol/l; 95% CI, −0.19 to −0.09; Figure 4a) and triglyceride (−0.29 mmol/l; CI, −0.47 to −0.10; Figure 4b) and increased high-density lipoprotein cholesterol (0.06 mmol/l; CI, 0.02 to 0.10; Figure 4c), but the reduction in low-density lipoprotein cholesterol was not significant as compared with control diets (−0.11 mmol/l; CI, −0.24 to 0.01; Figure 4d). There were moderate heterogeneity for the analyses of triglyceride (I2=58.0%; P=0.03) and high-density lipoprotein (I2=53.6%; P=0.04) cholesterol and none for others.

Figure 4
figure4

Forest plots assessing the effects of MSD on TC (a), triglyceride (b), HDL cholesterol (c) and LDL cholesterol (d). Elhayany-1 is the comparison between a low-carbohydrate Mediterranean diet and an ADA diet arm of the study. Elhayany-2 is the comparison between a traditional Mediterranean diet and an ADA diet arm of the study. ADA, American Diabetes Association; HDL, high-density lipoprotein; LDL, low-density lipoprotein; MSD, Mediterranean-style diet; TC, total cholesterol.

Moreover, the summary estimate of MSD showed a trend towards reduction in systolic blood pressure (−1.45 mm Hg; CI, −1.97 to −0.94; I2=0.0%; P=0.58). Likewise, we found a similar trend for lower diastolic blood pressure in the MSD group (−1.41 mm Hg; CI, −1.84 to −0.97; I2=0.0%; P=0.95).

Publication bias

We found no evidence of substantial publication bias from Begg’s test (P>0.05) for any outcome examined. However, some evidence of potential publication bias was detected for HbA1c (P=0.001) and total cholesterol (P=0.025) by using Egger’s test (Supplementary Table 2).

Subgroup and sensitivity analyses

Significant heterogeneity was observed in the primary outcome of HbA1c, and therefore we performed further analyses. The subgroup analyses were stratified by country of origin (Mediterranean or non-Mediterranean countries), number of participants, duration of the intervention and quality of the studies. These analyses resulted in similar results to the primary analysis (Table 2). In sensitivity analyses, the effect estimate was consistent when primary meta-analysis was repeated using a fixed effects model. Moreover, omission of any individual study from the meta-analysis did not alter the pooled effects. When we excluded the two small trials with a cross-over design,22, 25 effect estimate and heterogeneity were unchanged (mean difference, −0.33%; 95% CI, −0.49 to −0.17; I2=68.3%; P for heterogeneity=0.001).

Table 2 Subgroup analyses for primary outcome of HbA1c

Discussion

This meta-analysis includes data from all available RCTs comparing the effects of MSD with control diets in T2D patients. The results demonstrate that MSD has beneficial effects on glycemic control, weight loss and cardiovascular risk factors.

Our study conclusion regarding glycemic control is consistent with a meta-analysis by Ajala et al.,37 which evaluated the effects of various diets on the nutritional management of T2D and found a significant benefit in terms of HbA1c reduction in MSD. Another network meta-analysis38 that compared MSD with other diets evidenced that MSD slightly lowered HbA1c in T2D. However, above both meta-analyses did not show a reduction in FPG and fasting insulin. Actually, our study showed that MSD ameliorated FPG and fasting insulin in T2D patients, which is agreeable with some clinical studies.20, 21, 23

Concerning weight control, our results that MSD reduced BMI and body weight are similar to the study by Ajala et al.,37 which showed that MSD was effective in inducing weight loss in T2D. Recently, a post hoc analysis of the PREDIMED study showed that MSD was associated with a significant decline in body weight for T2D patients after 1 year of follow-up.36 In addition, Esposito et al.39 conducted a meta-analysis that specifically evaluated MSD’s effect on weight control in subjects with various co-morbidities and also found that MSD significantly reduced BMI and body weight. The beneficial effect of MSD on weight loss may be due to plenty of plant-based foods that supply an abundance of dietary fiber and low-carbohydrate load.40

The MSD improved cardiovascular risk factors such as blood pressure and lipid profile in our study, which is in accordance with previous publications.41, 42 Two reviews showed an association between MSD and improved cardiovascular risk factors, including decreases in blood pressure, total cholesterol and triglyceride and an increase in high-density lipoprotein cholesterol.43, 44

Mechanisms underlying these associations probably attribute to increased intake of healthy nutrients and decreased consumption of red and processed meat. The main component of MSD like olive oil (rich in monounsaturated fatty acid) together with other protective components, such as vegetables, fruits, whole grains and red wine, can offer anti-inflammatory and anti-oxidative effects as the serum levels of adiponectin, and dietary polyphenols and fiber were increased in the individuals consuming MSD.45, 46, 47 On the other hand, MSD is low in red and processed meat, which contributes to reduced consumption of saturated fatty acids and dietary cholesterol, and thus lead to improvement in glucose metabolism, body weight and cardiovascular risk factors.48, 49

Strengths and limitations

The present meta-analysis includes a large number of trials and a much more available outcome assessing the effects of MSD on glycemic control, weight loss and cardiovascular risk factors in patients with T2D. Our study includes nine RCTs involving a total of 1178 patients, compared with a previous meta-analysis,37 which included only three trials with 308 T2D patients in the Mediterranean-diet arm; the high heterogeneity between the three trials was detected (I2=82%; P=0.004). Furthermore, our study recruited only subjects with T2D, and this may eliminate the interference caused by mixed populations of individuals with and without T2D. A published network meta-analysis38 that evaluated the MSD’s effect on glucose control showed that MSD improved HbA1c but not FPG or fasting insulin, which is different from ours. However, the studies included in the network meta-analysis comprised participants not only with T2D but also without T2D.38

Nevertheless, several limitations should be recognized. First, the MSD is not a homogenous pattern; however, all of the included studies comprised the basic characteristics of this diet. Second, control diets vary across studies, including low-fat, non-restricted-calorie low-carbohydrate, ADA, high-carbohydrate and regular diets. Certain diets such as low-carbohydrate diet and ADA diet are also recommended to patients with T2D and may have beneficial effect in terms of metabolic controls. Therefore, effect of MSD on glycemic control, weight loss and cardiovascular risk factors may be underestimated in our study. Third, although we detected possible publication bias for HbA1c outcome, further subgroup analysis revealed that studies with larger number of participants (200 subjects) and higher quality showed more prominent effects of MSD on HbA1c reduction compared with studies with small sample size and low quality (Table 2). Finally, for some outcomes, the relatively insufficient number of trials limits our ability to perform appropriate subgroup analysis.

Conclusions and clinical implications

In summary, our meta-analysis provides convincing evidence that MSD has a more prominent role in the management of T2D. The results suggest that MSD is effective in improving glycemic control (HbA1c, FPG and fasting insulin), losing weight (BMI and body weight) and meliorating lipid profile and blood pressure in people with T2D. These findings are of considerable public health interest, particularly for helping health administrators to identify effective dietary strategy of T2D.

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Acknowledgements

This study was funded by the research grants from National Nature Science Foundation of China (30772207 to X Yu).

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Correspondence to X Yu.

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Supplementary Information accompanies this paper on European Journal of Clinical Nutrition website

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Huo, R., Du, T., Xu, Y. et al. Effects of Mediterranean-style diet on glycemic control, weight loss and cardiovascular risk factors among type 2 diabetes individuals: a meta-analysis. Eur J Clin Nutr 69, 1200–1208 (2015). https://doi.org/10.1038/ejcn.2014.243

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