The Mediterranean Diet, Its Microbiome Connections, and Cardiovascular Health: A Narrative Review
Abstract
:1. Introduction
2. The Mediterranean Diet Components
2.1. Extra-Virgin Olive Oil (EVOO)
2.2. Legumes, Cereals, and Nuts
2.3. Fruits and Vegetables
2.4. Dairy Products
2.5. Fish
2.6. Wine
3. MD and Cardiovascular Outcomes: Clinical, Epidemiological, and Intervention Studies
4. Favorable Mechanisms of MD on Cardiovascular Health
- (a)
- Favorable effects on multiple specific cardiovascular risk factors [85,86] through a specific plasma metabolomic profile (mainly triglycerides and medium/long-chain acylcarnitines, amino acids, and steroids). MD improves insulin resistance, increases adiponectin concentrations [87], and decreases the hepatic fat content [88] with beneficial effects on diabetes mellitus and metabolic syndrome [89,90]. The lipid profile improves, too, with a decrease in plasma cholesterol [91], oxidized low-density lipoprotein [87,92], LDL-cholesterol, ApoB, and the ApoB/ApoA-I ratio and an increase in ApoA-I [93,94]. There are also putative favorable changes in the blood fatty acid profile, with increased levels of eicosapentaenoic and docosahexaenoic acid [95]. Then, both systolic and diastolic blood pressure decrease [94]. Finally, the MD-style diet may influence the potential negative relationship between elevated plasma ceramide concentrations and CVD [96];
- (b)
- (c)
- Protection against oxidative stress and inflammation. MD is associated with lower concentrations of inflammatory mediators, like C-reactive protein, interleukin-6, sICAM, P-selectin, and tumor necrosis factor-α [94], hallmarks of inflammaging, the peculiar low-grade, chronic, and “sterile” inflammatory state characterizing old age that represents a background pathogenetic mechanism linking metabolic risk factors to increased risk of chronic degenerative diseases [96,99,100]. The MD modulates the immune system, induces induction of detoxification enzymes [101], and has a low dietary inflammatory index [102] and is associated with lower intracellular reactive oxygen species production [103], an increase in serum markers of atheroma plaque stability, and a reduction in CD40 expression on monocyte surface [94]. Flavonoids, in particular, provide a variety of nutraceutical functions including antioxidant, antimicrobial, anti-inflammatory, antiangiogenic, antitumor, and improved pharmacokinetic properties [104]. The MD was also significantly associated with lower levels of subclinical gut inflammation, defined by fecal calprotectin [105] and higher concentrations of fecal short-chain acids (FSCAs) (propionate and butyrate) [106];
- (d)
- Anti-atherosclerotic effects. Increase in endothelial progenitor cells [103,107] and endothelial-mediated nitric oxide (NO) synthesis leads to higher NO bioavailability [100,108] and consequent significant improvements in endothelial function [86], flow-mediated microvascular vasodilation [103,109], and arterial stiffness [110,111], as well as carotid intima-media thickness [112];
- (e)
- Decrease in platelet aggregation and blood coagulation [87];
- (f)
- Inhibition of nutrient sensing pathways by specific amino acid restriction [113];
- (g)
- And, last but not least, gut microbiota-mediated production of beneficial metabolites [114].
5. Microbiota: Definitions and Functions
6. Western Diet, Microbiome, and Cardiovascular Diseases
7. Effects of Mediterranean Diet on Microbiome
8. MD, Microbiome, and Cardiovascular Health
9. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Author, Year | Study Setting | Findings |
---|---|---|
De Lorgeril et al., 1999 [69] | Secondary prevention, intervention | Three composite outcomes (COs) combining either cardiac death and nonfatal myocardial infarction (CO 1), or the preceding plus major secondary end points (unstable angina, stroke, heart failure, and pulmonary or peripheral embolism) (CO 2), or the preceding plus minor events requiring hospital admission (CO 3) were studied. In the Mediterranean diet group, CO 1 was reduced (14 events versus 44 in the prudent Western-type diet group, p = 0.0001), as were CO 2 (27 events versus 90, p = 0.0001) and CO 3 (95 events versus 180, p = 0. 0002). |
Martinez-Gonzalez et al., 2002 [77] | Observational case-control | For each additional point in the a priori Mediterranean pattern (observed range: 9–38) the odds ratio (95% CI) was 0.92 (0.86–0.98). This estimate was 0.55 (0.42–0.73) when using the post hoc pattern (range: 0–8). |
Panagiotakos et al., 2002 [54] | Observational case-control | MeDiet reduces the risk of developing acute coronary syndromes by 17% (odds ratio = 0.83, 95% CI 0.73–0.88, p < 0.01) in controlled hypertensive subjects, and by 20% (odds ratio = 0.80, 95% CI 0.71–0.89, p < 0.01) in normotensive subjects. |
Pitsavos et al., 2002 [56] | Observational case-control | The combination of a MeDiet and statin medical therapy is associated with an additional reduction in the coronary risk (odds ratio = 0.57, p < 0.01), independently from cholesterol levels and the other cardiovascular factors. |
Panagiotakos et al., 2006 [55] | Observational | In acute coronary syndrome, an increment in the diet score was associated with a significant decrease in troponin I and creatine phosphokinase-MB levels (p < 0.01) after adjusting for various potential confounders. Moreover, diet score was associated with lower risk of recurrent events (odds ratio = 0.81, 95% CI 0.61–0.98). |
Fung et al., 2009 [65] | Observational | Women in the top aMed quintile were at lower risk for both CHD and stroke compared with the bottom quintile (RR = 0.71 (95% CI = 0.62–0.82; p trend < 0.0001) for CHD; RR = 0.87 (95% CI = 0.73–1.02; p trend = 0.03) for stroke). CVD mortality was significantly lower among women in the top quintile of the aMed (RR = 0.61, 95% CI = 0.49–0.76, p trend < 0.0001). |
Levitan et al., 2013 [61] | Observational, longitudinal | Multivariable-adjusted HRs were 1 (reference), 1.05 (95% CI 0.89–1.24), 0.97 (95% CI 0.81–1.17), and 0.85 (95% CI 0.70–1.02) across quartiles of the Mediterranean diet score (p-trend = 0.08) |
Tektonidis et al., 2015 [57] | Observational, longitudinal | A high adherence to the mMED score (6–8), compared to low, was associated with a lower risk of MI (RR: 0.74, 95% CI: 0.61–0.90, p = 0.003), HF (RR: 0.79, 95% CI: 0.68–0.93, p = 0.004) and ischemic stroke (RR: 0.78, 95% CI: 0.65–0.93, p = 0.007) but not hemorrhagic stroke (RR: 0.88, 95% CI: 0.61–1.29, p = 0.53). |
Tong et al., 2016 [67] | Observational | The Mediterranean diet score (MDS) was significantly associated with lower incidence of the cardiovascular outcomes, with hazard ratios (95% confidence intervals) of 0.95 (0.92–0.97) per one standard deviation for incident CVD and 0.91 (0.87–0.96) for CVD mortality. Associations were similar for composite incident ischaemic heart disease and all-cause mortality. |
Liyanage et al., 2016 [76] | Meta-analysis | Evidence of protection against major vascular events (RR 0.63, 95% confidence interval 0.53–0.75), coronary events (0.65, 0.50–0.85), stroke (0.65, 0.48–0.88), and heart failure (0.30, 0.17–0.56) but not for all-cause mortality (1.00, 0.86–1.15) or cardiovascular mortality (0.90, 0.72–1.11). |
Grosso et al., 2017 [78] | Meta-analysis | Individuals in the highest quantile of adherence to the diet had lower incidence [relative risk (RR): 0.76, 95% CI: 0.68, 0.83] and mortality (RR: 0.76, 95% CI: 0.68, 0.83) from CVD compared to those least adherent. A significant reduction in risk was found also for coronary heart disease (CHD) (RR: 0.72, 95% CI: 0.60, 0.86), myocardial infarction (MI) (RR: 0.67; 95% CI: 0.54, 0.83), and stroke (RR: 0.76; 95% CI: 0.60, 0.96) incidence. |
Stefler et al., 2017 [68] | Observational | One standard deviation (SD) increase in the MDS (equivalent to a 2.2-point increase in the score) was found to be inversely associated with death from all causes (HR, 95% CI 0.93, 0.88–0.98) and CVD (0.90, 0.81–0.99) even after multivariable adjustment. An inverse but statistically not significant link was found for CHD (0.90, 0.78–1.03) and stroke (0.87, 0.71–1.07). |
Bonaccio et al., 2017 [53] | Observational | A retrospective analysis of 18,991 men and women aged ≥35 years from the general population of the Moli-sani cohort (Italy). Overall, a two-point increase in MDS was associated with a 15% reduced CVD risk (95% confidence interval: 1% to 27%). Such association was evident in highly (HR = 0.43; 0.25–0.72) but not in less (HR = 0.94; 0.78–1.14) educated subjects (p for interaction = 0.042). Similarly, CVD advantages associated with the MD were confined to the high household income group (HR = 0.39; 0.23–0.66 and HR = 1.01; 0.79–1.29 for high- and low-income groups, respectively); p for interaction = 0.0098. |
Dinu et al., 2018 [81] | Umbrella review of 13 meta-analyses of observational studies and 16 meta-analyses of RCTs | Robust evidence, supported by a p-value < 0.001, a large simple size, and a not considerable heterogeneity between studies, for a greater adherence to the Mediterranean diet and a reduced risk of overall mortality, cardiovascular diseases, coronary heart disease, myocardial infarction, overall cancer incidence, neurodegenerative diseases, and diabetes was found. |
Waldeyer et al., 2018 [60] | Observational study | In patients undergoing coronary angiography, adherence to MD represented by a higher MDS was significantly associated with a reduced probability for a medium/high risk SYNTAX score of ≥23 with an odds ratio (OR) of 0.923 per point increase in MDS (95% confidence interval 0.869–0.979; p = 0.0079). |
Shikany et al., 2018 [62] | Observational, longitudinal | In multivariable-adjusted models, the Mediterranean diet score was inversely associated with the hazard of recurrent CHD events (hazard ratio for highest score versus lowest score, 0.78; 95% confidence interval, 0.62–0.98; PTrend = 0.036). |
Hodge et al., 2018 [63] | Observational, longitudinal | The hazard ratio for the total was 0.86 (95% CI: 0.80–0.93) comparing the highest and lowest three categories of MDS. |
Mirò et al., 2018 [59] | Observational, longitudinal | In patients diagnosed with AHF after a mean follow-up period of 2 years, no differences were observed in survival between adherent and nonadherent patients (HR of adherents 0.86; 95% CI: 0.73 to 1.02). Adherence to the MD was associated with decreased rates of rehospitalization during the next year. |
Rosato et al., 2019 [79] | Meta-analysis | The RR for the highest versus the lowest category of the MDS was 0.81 (95% CI: 0.74–0.88) for the 11 studies that considered unspecified CVD. The corresponding pooled RR for CHD/AMI risk was 0.70 (95% CI: 0.62–0.80). The overall RR for the six studies that considered unspecified stroke was 0.73 (95% CI: 0.59–0.91) for the highest versus the lowest category of the MDS. The corresponding values were 0.82 (95% CI: 0.73–0.92) for ischemic (five studies) and 1.01 (95% CI: 0.74–1.37) for hemorrhagic stroke. |
Saulle et al., 2019 [75] | Systematic review | The Mediterranean diet may be a useful means of preventing stroke; the 6 meta-analyses especially highlighted that high adherence to the Mediterranean diet was protective against stroke, with a relative risk ranging from 0.64 (95% CI: 0.48–0.88) to 0.90 (95% CI: 0.87–0.93). |
Delgado-Lista et al., 2022 [71] | Secondary prevention, intervention | Multivariable-adjusted hazard ratios (HRs) of the different models ranged from 0.719 (95% CI: 0.541–0.957) to 0.753 (0.568–0.998) in favor of the Mediterranean diet. |
Chang et al., 2022 [64] | observational | The alternate Mediterranean diet index aMED 3 (vs. <3) was not associated with a lower risk of all-cause (adjusted HR 0.797, 95% CI: 0.599–1.059, p = 0.116) and cardiovascular (adjusted HR 0.911, 95% CI: 0.539–1.538, p = 0.724) mortality in participants with a history of heart failure. |
Liang et al., 2022 [66] | Observational | In Cox regression analysis, a higher absolute aMED score (HR 0.798, p = 0.0079) or an above-median aMED score (score 4–9) (HR 0.646, p = 0.0013) was negatively associated with all-cause mortality. In contrast, a higher aMEDscore was not associated with less cardiovascular mortality. |
Gupta et al., 2023 [73] | Systematic review | Consumption of an MD associated with longer life and lower incidence of heart disease. |
Laffond et al., 2023 [74] | Systematic review | Higher adherence to the MD is associated with a reduced risk of overall mortality, both in the general population and in patients with previous CVDs. Moreover, evidence suggests that following this dietary pattern likely decreases the risk of CVDs such as heart attacks, various types of coronary artery disease, stroke, and cardiovascular mortality. |
Cangemi et al., 2023 [52] | Observational | In multivariate Cox regression analysis, a greater adherence remained inversely associated with major adverse cardiovascular events (HR: 0.49; 95% CI: 0.29–0.82; p = 0.006) after adjusting for confounding factors. |
Pant et al., 2023 [80] | Meta-analysis | In women, higher adherence to a Mediterranean diet was associated with a lower CVD incidence (HR 0.76, 95% CI: 0.72 to 0.81; I2 = 39%, p test for heterogeneity = 0.07), total mortality (HR 0.77, 95% CI: 0.74 to 0.80; I2 = 21%, p test for heterogeneity = 0.28), and coronary heart disease (HR 0.75, 95% CI: 0.65 to 0.87; I2 = 21%, p test for heterogeneity = 0.28). Stroke incidence was lower in women with higher Mediterranean diet adherence (HR 0.87, 95% CI: 0.76 to 1.01; I2 = 0%, p test for heterogeneity = 0.89), but this result was not statistically significant. |
Disease/Condition | Main Microbial Agents |
---|---|
Cardiovascular risk factors | Prevotella 2, Prevotella 7, Tyzzerella and Tyzzerella 4 genera, Bacteroides uniformis and B. vulgatus (low prevalence of Alloprevotella Prevotella copri and Catenibacterium) |
Arterial hypertension | Catabacter, Robinsoleilla, Serratia, Enterobacteriaceae, Ruminococcus torques, Parasutterella, Escherichia, Shigella, and Klebsiella (decreased abundance of Sporobacter, Roseburia hominis, Romboutsia spp., and Roseburia) |
Atrial fibrillation | Enorma and Bifidobacterium genera |
Diabetes mellitus | Order Rhizobiales, family Desulfovibrionaceae, genus Romboutsia |
Coronary heart disease | Proteobacteria and Actinobacteria phyla, Bacteroides, Prevotella, Firmicutes, Veillonella, Clostridium, Lactobacillaceae (Lactobacillus plantarum) and Streptococcus (decreased prevalence of Caulobacterales order and Caulobacteraceae family, aminococcaceae and Odoribacteraceae) |
Cerebrovascular disease | Firmicutes, Proteobacteria, and Actinobacteria phyla |
Heart failure | Ruminococcus gnavus, Escherichia Shigella, Streptococcus sp. (sanguinus and parasanguinis), Veillonella sp., and Actinobacteria (relative depletion of Eubacterium, Prevotella, Faecalibacterium, SMB53, aminococcaceae, Odoribacteraceae and Megamonas) |
Cardiovascular mortality | Genera Kocuria and Enhydrobacter (genera Paracoccus was inversely related) |
Increase | Decrease |
---|---|
Akkermansia muciniphila, Anaerostipes hadrus, Bacteroides thetaiotaomicron, Bifidobacteria animalis, Candida albicans, Catenibacterium, Christensenellaceae, Clostridium (cluster XIVa, leptum) Enterorhabdus, Eubacterium rectale, Faecalibacterium (Lactococcus, prausnitzii) Lachnoclostridium, Lachnospiraceae, Oscillospira (Flavonifractor), Parabacteroides, Phascolarctobacterium, Prevotellaceae, Prevotellae, Proteobacteria, Roseburia faecis, Ruminococcaceae bromii and plautii, Sphingobacteriaceae | Actinomyces lignae, Butyricicoccus, Catenibacterium, Clostridium ramosum, Collinsella aerofaciens, Coprococcus Anaerostipes and comes, Dorea formicigenerans, Escherichia coli, Eubacterium hallii, Firmicutes, Flavonifractor plautii, Haemophilus, Lachnospiraceae Megamonas, Ruminiclostridium, Ruminococcus gnavus and torques Veillonella dispar |
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Abrignani, V.; Salvo, A.; Pacinella, G.; Tuttolomondo, A. The Mediterranean Diet, Its Microbiome Connections, and Cardiovascular Health: A Narrative Review. Int. J. Mol. Sci. 2024, 25, 4942. https://doi.org/10.3390/ijms25094942
Abrignani V, Salvo A, Pacinella G, Tuttolomondo A. The Mediterranean Diet, Its Microbiome Connections, and Cardiovascular Health: A Narrative Review. International Journal of Molecular Sciences. 2024; 25(9):4942. https://doi.org/10.3390/ijms25094942
Chicago/Turabian StyleAbrignani, Vincenzo, Andrea Salvo, Gaetano Pacinella, and Antonino Tuttolomondo. 2024. "The Mediterranean Diet, Its Microbiome Connections, and Cardiovascular Health: A Narrative Review" International Journal of Molecular Sciences 25, no. 9: 4942. https://doi.org/10.3390/ijms25094942