Mediterranean Diet and Endothelial Function: A Review of its Effects at Different Vascular Bed Levels
Abstract
:1. Introduction
2. Mediterranean Diet and Microvascular Endothelial Function
3. The Mediterranean Diet and Flow-Mediated Vasodilation of the Brachial Artery
4. Mediterranean Diet, Intima-Media Thickness and Atherosclerotic Plaques
5. Effect of Mediterranean Diet at Molecular and Cellular Levels
5.1. At the Molecular Level
5.1.1. Mediterranean Diet and Genotype Relationship
5.1.2. Effects of Mediterranean Diet on miRNAs
5.2. At the Cellular Level
5.2.1. The Positive Impact of the Mediterranean Diet on Endothelial Progenitor Cells
5.2.2. Release of Microparticles Regulated by the Mediterranean Diet
Author Contributions
Funding
Conflicts of Interest
References
- Estruch, R.; Ros, E.; Salas-Salvadó, J.; María-Isabel, C.; Corella, D.; Borau, F.A.; Gómez-Gracia, E.; Ruiz-Gutierrez, V.; Fiol, M.; Lapetra, J.; et al. Primary Prevention of Cardiovascular Disease with a Mediterranean Diet Supplemented with Extra-Virgin Olive Oil or Nuts. N. Engl. J. Med. 2018, 378, e34. [Google Scholar] [CrossRef] [PubMed]
- Lacatusu, C.; Grigorescu, E.-D.; Floria, M.; Onofriescu, A.; Mihai, B. The Mediterranean Diet: From an Environment-Driven Food Culture to an Emerging Medical Prescription. Int. J. Environ. Res. Public Health 2019, 16, 942. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boccardi, V.; Calvani, R.; Limongi, F.; Marseglia, A.; Mason, A.; Noale, M.; Rogoli, D.; Veronese, N.; Crepaldi, G.; Maggi, S. Consensus paper on the “executive summary of the international conference on Mediterranean diet and health: A lifelong approach” an Italian initiative supported by the Mediterranean Diet Foundation and the Menarini Foundation. Nutrition 2018, 51, 38–45. [Google Scholar] [CrossRef] [PubMed]
- Arrebola-Moreno, A.L.; Laclaustra, M.; Kaski, J.-C. Noninvasive Assessment of Endothelial Function in Clinical Practice. Rev. Española Cardiol. 2012, 65, 80–90. [Google Scholar] [CrossRef] [PubMed]
- Levy, B.I.; Schiffrin, E.L.; Mourad, J.J.; Agostini, D.; Vicaut, E.; Safar, M.E.; Struijker-Boudier, H.A. Impaired tissue perfusion: A pathology common to hypertension, obesity, and diabetes mellitus. Circulation 2008, 118, 968–976. [Google Scholar] [CrossRef]
- Mordi, I.R.; Mordi, N.; Delles, C.; Tzemos, N. Endothelial dysfunction in human essential hypertension. J. Hypertens. 2016, 34, 1464–1472. [Google Scholar] [CrossRef] [Green Version]
- Settergren, M.; Bohm, F.; Ryden, L.; Pernow, J.; Kalani, M. Lipid lowering versus pleiotropic effects of statins on skin microvascular function in patients with dysglycaemia and coronary artery disease. J. Intern. Med. 2009, 266, 492–498. [Google Scholar] [CrossRef]
- Ruano-Ruíz, J.A.; López-Miranda, J.; Fuentes, F.; Moreno, J.A.; Bellido, C.; Perez-Martinez, P.; Lozano, A.; Gómez, P.; Jiménez, Y.; Pérez-Jiménez, F. Phenolic Content of Virgin Olive Oil Improves Ischemic Reactive Hyperemia in Hypercholesterolemic Patients. J. Am. Coll. Cardiol. 2005, 46, 1864–1868. [Google Scholar] [CrossRef] [Green Version]
- Valls, R.M.; Farràs, M.; Suárez, M.; Fernández-Castillejo, S.; Fitó, M.; Konstantinidou, V.; Fuentes, F.; López-Miranda, J.; Giralt, M.; Covas, M.-I.; et al. Effects of functional olive oil enriched with its own phenolic compounds on endothelial function in hypertensive patients. A randomised controlled trial. Food Chem. 2015, 167, 30–35. [Google Scholar] [CrossRef]
- Fernández, J.M.; Rosado-Álvarez, D.; Da Silva-Grigoletto, M.E.; Rangel-Zuñiga, O.A.; Landaeta-Díaz, L.L.; Caballero-Villarraso, J.; López-Miranda, J.; Jiménez, F.P.; Fuentes-Jiménez, F. Moderate-to-high-intensity training and a hypocaloric Mediterranean diet enhance endothelial progenitor cells and fitness in subjects with the metabolic syndrome. Clin. Sci. 2012, 123, 361–373. [Google Scholar] [CrossRef]
- Klonizakis, M.; Alkhatib, A.; Middleton, G.; Smith, M.F. Mediterranean diet- and exercise-induced improvement in age-dependent vascular activity. Clin. Sci. 2013, 124, 579–587. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rogerson, D.; Maçãs, D.; Milner, M.; Liu, Y.; Klonizakis, M. Contrasting Effects of Short-Term Mediterranean and Vegan Diets on Microvascular Function and Cholesterol in Younger Adults: A Comparative Pilot Study. Nutrients 2018, 10, 1897. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marín, C.; Ramírez, R.; Gomez-Delgado, F.; Carracedo, J.; Garcia-Rios, A.; Rodríguez, F.; Gómez, P.; López-Miranda, J.; Yubero-Serrano, E.M.; Perez-Martinez, P.; et al. Mediterranean diet reduces endothelial damage and improves the regenerative capacity of endothelium. Am. J. Clin. Nutr. 2010, 93, 267–274. [Google Scholar] [CrossRef] [PubMed]
- Torres-Peña, J.D.; Garcia-Rios, A.; Delgado-Casado, N.; Gomez-Luna, P.; Alcalá-Díaz, J.F.; Yubero-Serrano, E.M.; Delgado, F.G.; Leon-Acuña, A.; Lopez-Moreno, J.; Camargo, A.; et al. Mediterranean diet improves endothelial function in patients with diabetes and prediabetes: A report from the CORDIOPREV study. Atherosclerosis 2018, 269, 50–56. [Google Scholar] [CrossRef]
- Rallidis, L.S.; Lekakis, J.; Kolomvotsou, A.; Zampelas, A.; Vamvakou, G.; Efstathiou, S.; Dimitriadis, G.; Raptis, S.A.; Kremastinos, D.T. Close adherence to a Mediterranean diet improves endothelial function in subjects with abdominal obesity. Am. J. Clin. Nutr. 2009, 90, 263–268. [Google Scholar] [CrossRef] [PubMed]
- Davis, C.R.; Hodgson, J.M.; Woodman, R.; Bryan, J.; Wilson, C.; Murphy, K.J. A Mediterranean diet lowers blood pressure and improves endothelial function: Results from the MedLey randomized intervention trial. Am. J. Clin. Nutr. 2017, 105, ajcn146803. [Google Scholar] [CrossRef] [Green Version]
- Ceriello, A.; Esposito, K.; La-Sala, L.; Pujadas, G.; De Nigris, V.; Testa, R.; Bucciarelli, L.; Rondinelli, M.; Genovese, S. The protective effect of the Mediterranean diet on endothelial resistance to GLP-1 in type 2 diabetes: A preliminary report. Cardiovasc. Diabetol. 2014, 13, 140. [Google Scholar] [CrossRef]
- Buscemi, S.; Verga, S.; Tranchina, M.R.; Cottone, S.; Cerasola, G. Effects of hypocaloric very-low-carbohydrate diet vs. Mediterranean diet on endothelial function in obese women. Eur. J. Clin. Investig. 2009, 39, 339–347. [Google Scholar] [CrossRef]
- Jaacks, L.M.; Sher, S.; De Staercke, C.; Porkert, M.; Alexander, W.R.; Jones, D.P.; Vaccarino, V.; Ziegler, T.R.; Quyyumi, A.A. Pilot randomized controlled trial of a Mediterranean diet or diet supplemented with fish oil, walnuts, and grape juice in overweight or obese US adults. BMC Nutr. 2018, 4, 26. [Google Scholar] [CrossRef]
- Thomazella, M.C.D.; Góes, M.F.; Andrade, C.R.; Debbas, V.; Barbeiro, D.F.; Correia, R.L.; Marie, S.K.; Cardounel, A.J.; Daluz, P.L.; Laurindo, F.R. Effects of High Adherence to Mediterranean or Low-Fat Diets in Medicated Secondary Prevention Patients. Am. J. Cardiol. 2011, 108, 1523–1529. [Google Scholar] [CrossRef] [Green Version]
- Shai, I.; Spence, J.D.; Schwarzfuchs, D.; Henkin, Y.; Parraga, G.; Rudich, A.; Fenster, A.; Mallett, C.; Liel-Cohen, N.; Tirosh, A.; et al. Dietary Intervention to Reverse Carotid Atherosclerosis. Circulation 2010, 121, 1200–1208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gardener, H.; Wright, C.B.; Cabral, D.; Scarmeas, N.; Gu, Y.; Cheung, K.; Elkind, M.S.; Sacco, R.L.; Rundek, T. Mediterranean diet and carotid atherosclerosis in the Northern Manhattan Study. Atherosclerosis 2014, 234, 303–310. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Murie-Fernandez, M.; Irimia, P.; Toledo, E.; Martínez-Vila, E.; Buil-Cosiales, P.; Serrano-Martínez, M.; Ruíz-Gutierrez, V.; Ros, E.; Estruch, R.; Martínez-González, M.Á. Carotid intima-media thickness changes with Mediterranean diet: A randomized trial (PREDIMED-Navarra). Atherosclerosis 2011, 219, 158–162. [Google Scholar] [CrossRef] [PubMed]
- Sala-Vila, A.; Romero-Mamani, E.D.; Gilabert, R.; Núñez, I.; de la Torre, R.; Corella, D.; Ruiz-Gutiérrez, V.; López-Sabater, M.A.; Pintó, X.; Rekondo, J. Changes in ultrasound-assessed carotid intima-media thickness and plaque with a Mediterranean diet: A substudy of the PREDIMED trial. Arterioscler. Thromb. Vasc. Biol. 2014, 34, 439–445. [Google Scholar] [CrossRef] [Green Version]
- Giannini, C.; Diesse, L.; D’Adamo, E.; Chiavaroli, V.; De Giorgis, T.; Di Iorio, C.; Chiarelli, F.; Mohn, A. Influence of the Mediterranean diet on carotid intima–media thickness in hypercholesterolaemic children: A 12-month intervention study. Nutr. Metab. Cardiovasc. Dis. 2014, 24, 75–82. [Google Scholar] [CrossRef]
- Maiorino, M.I.; Bellastella, G.; Petrizzo, M.; Gicchino, M.; Caputo, M.; Giugliano, D.; Esposito, K. Effect of a Mediterranean diet on endothelial progenitor cells and carotid intima-media thickness in type 2 diabetes: Follow-up of a randomized trial. Eur. J. Prev. Cardiol. 2016, 24, 399–408. [Google Scholar] [CrossRef]
- Delgado, F.G.; Alcala-Diaz, J.F.; Leon-Acuña, A.; Lopez-Moreno, J.; Delgado, F.G.; Gomez-Marin, B.; Ramos, I.R.; Yubero-Serrano, E.M.; Rangel-Zuñiga, O.A.; Delgado, C.V.; et al. Apolipoprotein E genetic variants interact with Mediterranean diet to modulate postprandial hypertriglyceridemia in coronary heart disease patients: Cordioprev study. Eur. J. Clin. Investig. 2019, 49, e13146. [Google Scholar] [CrossRef]
- Corella, D.; Asensio, E.M.; Coltell, O.; Sorlí, J.V.; Estruch, R.; Martínez-González, M.Á.; Salas-Salvadó, J.; Castañer, O.; Arós, F.; Lapetra, J.; et al. Clock gene variation is associated with incidence of type-2 diabetes and cardiovascular diseases in type-2 diabetic subjects: Dietary modulation in the PREDIMED randomized trial. Cardiovasc. Diabetol. 2016, 15, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Delgado, F.G.; Delgado, F.G.; Lopez-Moreno, J.; Rangel-Zuñiga, O.A.; Alcalá-Díaz, J.F.; Leon-Acuña, A.; Corina, A.; Yubero-Serrano, E.M.; Torres-Peña, J.D.; Camargo, A.; et al. Telomerase RNA Component Genetic Variants Interact With the Mediterranean Diet Modifying the Inflammatory Status and its Relationship With Aging: CORDIOPREV Study. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 2016, 73, 327–332. [Google Scholar] [CrossRef] [Green Version]
- Delgado, F.G.; Alcalá-Díaz, J.F.; Garcia-Rios, A.; Delgado, F.G.; Ortiz-Morales, A.; Rangel-Zuñiga, O.A.; Tinahones, F.J.; Gonzalez-Guardia, L.; Malagón, M.M.; Bellido-Muñoz, E.; et al. Polymorphism at the TNF -alpha gene interacts with Mediterranean diet to influence triglyceride metabolism and inflammation status in metabolic syndrome patients: From the Cordioprev clinical trial. Mol. Nutr. Food Res. 2014, 58, 1519–1527. [Google Scholar] [CrossRef]
- Jiménez-Morales, A.I.; Ruano, J.; Fernandez, J.M.; Camargo, A.; Lopez-Segura, F.; Caballero-Villarraso, J.; Fuentes-Jiménez, F.; López-Miranda, J.; Jiménez, F.P. NOS3 Glu298Asp Polymorphism Interacts with Virgin Olive Oil Phenols to Determine the Postprandial Endothelial Function in Patients with the Metabolic Syndrome. J. Clin. Endocrinol. Metab. 2011, 96, 1694–1702. [Google Scholar] [CrossRef]
- D’Amore, S.; Vacca, M.; Cariello, M.; Graziano, G.; D’Orazio, A.; Salvia, R.; Sasso, R.C.; Sabbà, C.; Palasciano, G.; Moschetta, A. Genes and miRNA expression signatures in peripheral blood mononuclear cells in healthy subjects and patients with metabolic syndrome after acute intake of extra virgin olive oil. Biochim. Biophys. Acta 2016, 1861, 1671–1680. [Google Scholar] [CrossRef] [PubMed]
- Marques-Rocha, J.L.; Milagro, F.I.; Mansego, M.L.; Zulet, M.A.; Bressan, J.; Martínez, J.A. Expression of inflammation-related miRNAs in white blood cells from subjects with metabolic syndrome after 8 wk of following a Mediterranean diet–based weight loss program. Nutrition 2016, 32, 48–55. [Google Scholar] [CrossRef] [Green Version]
- Daimiel, L.; Micó, V.; Valls, R.M.; Pedret, A.; Motilva, M.J.; Rubió, L.; Fitó, M.; Farrás, M.; Covas, M.; Solá, R.; et al. Impact of Phenol-Enriched Virgin Olive Oils on the Postprandial Levels of Circulating microRNAs Related to Cardiovascular Disease. Mol. Nutr. Food Res. 2020, e2000049. [Google Scholar] [CrossRef] [PubMed]
- Cesari, F.; Sofi, F.; Molino-Lova, R.; Vannetti, F.; Pasquini, G.; Cecchi, F.; Marcucci, R.; Gori, A.; Macchi, C.; Boni, R.; et al. Aging process, adherence to Mediterranean diet and nutritional status in a large cohort of nonagenarians: Effects on endothelial progenitor cells. Nutr. Metab. Cardiovasc. Dis. 2018, 28, 84–90. [Google Scholar] [CrossRef]
- Chiva-Blanch, G.; Crespo, J.; Suades, R.; Arderiu, G.; Padró, T.; Vilahur, G.; Cubedo, J.; Corella, D.; Salas-Salvadó, J.; Arós, F.; et al. CD142+/CD61+, CD146+ and CD45+ microparticles predict cardiovascular events in high risk patients following a Mediterranean diet supplemented with nuts. Thromb. Haemost. 2016, 116, 103–114. [Google Scholar] [CrossRef] [Green Version]
- Chiva-Blanch, G.; Sala-Vila, A.; Crespo, J.; Ros, E.; Estruch, R.; Badimon, L. The Mediterranean diet decreases prothrombotic microvesicle release in asymptomatic individuals at high cardiovascular risk. Clin. Nutr. 2020. [Google Scholar] [CrossRef] [PubMed]
- Nabel, E.G.; Selwyn, A.P.; Ganz, P. Large coronary arteries in humans are responsive to changing blood flow: An endothelium-dependent mechanism that fails in patients with atherosclerosis. J. Am. Coll. Cardiol. 1990, 16, 349–356. [Google Scholar] [CrossRef] [Green Version]
- Halcox, J.; Schenke, W.H.; Zalos, G.; Mincemoyer, R.; Prasad, A.; Waclawiw, M.A.; Nour, K.R.; Quyyumi, A.A. Prognostic value of coronary vascular endothelial dysfunction. Circulation 2002, 106, 653–658. [Google Scholar] [CrossRef]
- Gokce, N.; Keaney, J.; Hunter, L.M.; Watkins, M.T.; Nedeljkovic, Z.S.; Menzoian, J.O.; Vita, J.A. Predictive value of noninvasively determined endothelial dysfunction for long-term cardiovascular events in patients with peripheral vascular disease. J. Am. Coll. Cardiol. 2003, 41, 1769–1775. [Google Scholar] [CrossRef] [Green Version]
- Karatzis, E.N.; Ikonomidis, I.; Vamvakou, G.D.; Papaioannou, T.G.; Protogerou, A.D.; Andreadou, I.; Voidonikola, P.T.; Karatzi, K.N.; Papamichael, C.M.; Lekakis, J.P. Long-Term Prognostic Role of Flow-Mediated Dilatation of the Brachial Artery After Acute Coronary Syndromes Without ST Elevation. Am. J. Cardiol. 2006, 98, 1424–1428. [Google Scholar] [CrossRef] [PubMed]
- Santos-García, D.; Blanco, M.; Serena, J.; Rodríguez-Yáñez, M.; Leira, R.; Castillo, J. Impaired Brachial Flow-Mediated Dilation Is a Predictor of a New-Onset Vascular Event after Stroke. Cerebrovasc. Dis. 2011, 32, 155–162. [Google Scholar] [CrossRef] [PubMed]
- Schroeder, S.; Enderle, M.D.; Ossen, R.; Meisner, C.; Baumbach, A.; Pfohl, M.; Herdeg, C.; Oberhoff, M.; Haering, H.U.; Karsch, K.R. Noninvasive determination of endothelium-mediated vasodilation as a screening test for coronary artery disease: Pilot study to assess the predictive value in comparison with angina pectoris, exercise electrocardiography, and myocardial perfusion imaging. Am. Heart J. 1999, 138, 731–739. [Google Scholar] [CrossRef]
- Delgado, F.G.; Perez-Martinez, P.; Garcia-Rios, A.; Alcalá-Díaz, J.F.; Perez-Caballero, A.I.; Delgado, F.G.; Fuentes, F.; Quintana-Navarro, G.; Lopez-Segura, F.; Ortiz-Morales, A.M.; et al. Diet Intervention with Olive oil and cardiovascular PREVention study (the CORDIOPREV study): Rationale, methods, and baseline characteristics: A clinical trial comparing the efficacy of a Mediterranean diet rich in olive oil versus a low-fat diet on cardiovascular disease in coronary patients. Am. Heart J. 2016, 177, 42–50. [Google Scholar] [CrossRef] [Green Version]
- Inaba, Y.; Chen, J.A.; Bergmann, S.R. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: A meta-analysis. Int. J. Cardiovasc. Imaging 2010, 26, 631–640. [Google Scholar] [CrossRef]
- Schwingshackl, L.; Hoffmann, G. Mediterranean dietary pattern, inflammation and endothelial function: A systematic review and meta-analysis of intervention trials. Nutr. Metab. Cardiovasc. Dis. 2014, 24, 929–939. [Google Scholar] [CrossRef] [PubMed]
- Shannon, O.M.; Mendes, I.; Köchl, C.; Mazidi, M.; Ashor, A.W.; Rubele, S.; Minihane, A.M.; Mathers, J.C.; Siervo, M. Mediterranean Diet Increases Endothelial Function in Adults: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. J. Nutr. 2020, 150, 1151–1159. [Google Scholar] [CrossRef]
- Ambring, A.; Friberg, P.; Axelsen, M.; Laffrenzen, M.; Taskinen, M.-R.; Basu, S.; Johansson, M. Effects of a Mediterranean-inspired diet on blood lipids, vascular function and oxidative stress in healthy subjects. Clin. Sci. 2004, 106, 519–525. [Google Scholar] [CrossRef] [Green Version]
- Esposito, K.; Marfella, R.; Ciotola, M. Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: A randomized trial. JAMA 2004, 13, 16–17. [Google Scholar] [CrossRef]
- Tardif, J.-C.; Heinonen, T.; Orloff, D.; Libby, P. Vascular Biomarkers and Surrogates in Cardiovascular Disease. Circulation 2006, 113, 2936–2942. [Google Scholar] [CrossRef] [Green Version]
- Lorenz, M.W.; Sitzer, M.; Markus, H.S.; Bots, M.L.; Rosvall, M. Response to Letter Regarding Article, “Prediction of Clinical Cardiovascular Events With Carotid Intima-Media Thickness: A Systematic Review and Meta-Analysis”. Circulation 2007, 116, e318. [Google Scholar] [CrossRef]
- Millen, B.E.; Quatromoni, P.A.; Nam, B.-H.; Pencina, M.J.; Polak, J.F.; Kimokoti, R.W.; Ordovas, J.M.; D’Agostino, R.B. Compliance with expert population-based dietary guidelines and lower odds of carotid atherosclerosis in women: The Framingham Nutrition Studies. Am. J. Clin. Nutr. 2005, 82, 174–180. [Google Scholar] [CrossRef] [PubMed]
- Nettleton, J.A.; Schulze, M.B.; Jiang, R.; Jenny, N.S.; Burke, G.L.; Jacobs, D.R. A priori–defined dietary patterns and markers of cardiovascular disease risk in the Multi-Ethnic Study of Atherosclerosis (MESA)2. Am. J. Clin. Nutr. 2008, 88, 185–194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wildman, R.; Schott, L.; Brockwell, S. A dietary and exercise intervention slows menopause-associated progression of subclinical atherosclerosis as measured by intima-media thickness of the carotid arteries. J. Am. Coll. Cardiol. 2004, 13, 36. [Google Scholar] [CrossRef]
- Višković, K.; Rutherford, G.W.; Sudario, G.; Stemberger, L.; Brnić, Z.; Begovac, J. Ultrasound measurements of carotid intima-media thickness and plaque in HIV-infected patients on the Mediterranean diet. Croat. Med. J. 2013, 54, 330–338. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ding, M.; Ellervik, C.; Huang, T.; Jensen, M.K.; Curhan, G.C.; Pasquale, L.R.; Kang, J.H.; Wiggs, J.L.; Hunter, D.J.; Willett, W.C.; et al. Diet quality and genetic association with body mass index: Results from 3 observational studies. Am. J. Clin. Nutr. 2018, 108, 1291–1300. [Google Scholar] [CrossRef]
- Pérez-Martínez, P.; Moreno-Conde, M.; Cruz-Teno, C.; Ruano, J.; Fuentes, F.; Delgado, F.G.; Garcia-Rios, A.; Marín, C.; Gómez-Luna, M.J.; Jiménez, F.P.; et al. Dietary fat differentially influences regulatory endothelial function during the postprandial state in patients with metabolic syndrome: From the LIPGENE study. Atherosclerosis 2010, 209, 533–538. [Google Scholar] [CrossRef]
- Shang, X.; Pati, P.; Anea, C.B.; Fulton, D.J.; Rudic, R.D. Differential Regulation of BMAL1, CLOCK, and Endothelial Signaling in the Aortic Arch and Ligated Common Carotid Artery. J. Vasc. Res. 2016, 53, 269–278. [Google Scholar] [CrossRef]
- Kura, B.; Parikh, M.; Slezak, J.; Pierce, G. The Influence of Diet on MicroRNAs that Impact Cardiovascular Disease. Molecules 2019, 24, 1509. [Google Scholar] [CrossRef] [Green Version]
- Quintanilha, B.J.; Reis, B.Z.; Duarte, G.B.S.; Cozzolino, S.M.F.; Rogero, M.M. Nutrimiromics: Role of microRNAs and Nutrition in Modulating Inflammation and Chronic Diseases. Nutrients 2017, 9, 1168. [Google Scholar] [CrossRef]
- Maiorino, M.I.; Bellastella, G.; Caputo, M.; Castaldo, F.; Improta, M.R.; Giugliano, D.; Esposito, K. Effects of Mediterranean diet on sexual function in people with newly diagnosed type 2 diabetes: The MÈDITA trial. J. Diabetes Complicat. 2016, 30, 1519–1524. [Google Scholar] [CrossRef] [PubMed]
- Minhajat, R.; Nilasari, D.; Bakri, S. The Role of Endothelial Progenitor Cell in Cardiovascular Disease Risk Factors. Acta Med. Indones. 2015, 47, 340–347. [Google Scholar] [PubMed]
- Estruch, R.; Sacanella, E.; Mota, F.; Chiva-Blanch, G.; Antúnez, E.; Casals, E.; Deulofeu, R.; Rotilio, D.; Andres-Lacueva, C.; Lamuela-Raventos, R.M. Moderate consumption of red wine, but not gin, decreases erythrocyte superoxide dismutase activity: A randomised cross-over trial. Nutr. Metab. Cardiovasc. Dis. 2011, 21, 46–53. [Google Scholar] [CrossRef] [PubMed]
- Werner, N.; Kosiol, S.; Schiegl, T.; Ahlers, P.; Walenta, K.; Link, A.; Böhm, M.; Nickenig, G. Circulating endothelial progenitor cells and cardiovascular outcomes. N. Engl. J. Med. 2005, 353, 999–1007. [Google Scholar] [CrossRef] [PubMed]
- Roberts, N.; Jahangiri, M.; Xu, Q. Progenitor cells in vascular disease. J. Cell. Mol. Med. 2005, 9, 583–591. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Golab-Janowska, M.; Paczkowska, E.; Machalinski, B.; Meller, A.; Kotlega, D.; Safranow, K.; Wankowicz, P.; Nowacki, P. Statins Therapy is Associated with Increased Populations of Early Endothelial Progenitor (CD133+/VEGFR2+) and Endothelial (CD34-/CD133- /VEGFR2+) Cells in Patients with Acute Ischemic Stroke. Curr. Neurovasc. Res. 2018, 15, 120–128. [Google Scholar] [CrossRef]
- Nomura, S.; Ozaki, Y.; Ikeda, Y. Function and role of microparticles in various clinical settings. Thromb. Res. 2008, 123, 8–23. [Google Scholar] [CrossRef]
- Baron, M.; Boulanger, C.M.; Staels, B.; Tailleux, A. Cell-derived microparticles in atherosclerosis: Biomarkers and targets for pharmacological modulation? J. Cell. Mol. Med. 2012, 16, 1365–1376. [Google Scholar] [CrossRef]
Authors (Ref) | Study Design | Population Health Status | Target | Sample Size | Duration | Type of Intervention | Type of Control | Main Findings |
---|---|---|---|---|---|---|---|---|
Fernandez et al. 2012 [10] | Parallel control trial | Metabolic syndrome patients | IRH by laser doppler | 45 | 12 weeks | Mediterranean diet + moderate-to-high-intensity training | Hypocaloric Mediterranean diet | IRH was only improved after the Mediterranean diet plus training intervention. |
Ruano et al. 2005 [8] | Crossover trial | Hypercholesterolemic | IRH by laser doppler | 21 | - | Olive oil (400 ppm of phenols) | Olive oil (80 ppm of phenols) | High-phenolic virgin olive oil improves IRH in the postprandium |
Marin et al. 2011 [13] | Crossover trial | Healthy older subjects | IRH by laser doppler | 20 | 4 | Mediterranean diet | Saturated fat diet and a low-fat, high-carbohydrate diet. | IRH was higher after consumption of the Mediterranean diet compared to the two control diets (p < 0.05). |
Klonizakis et al. 2013 [11] | Parallel | Healthy older subjects | CVC by laser doppler | 22 | 8 | Mediterranean diet + exercise | Non-Mediterranean diet + exercise | Mediterranean diet group showed greater improvement of endothelial function compared to non-Mediterranean diet group (p = 0.02) |
Rogerson et al. 2018 [12] | Parallel | Healthy young people | CVC by laser doppler | 24 | 4 weeks | Mediterranean diet | Vegan diet | Mediterranean diet led to improvements in microvascular function (p = 0.005) |
Torres Peña et al. 2018 [14] | Parallel | Coronary heart disease with and without T2DM and pre-diabetes | Brachial artery FMD | 805 | 1.5 years | Mediterranean diet | Low-fat diet | Mediterranean diet enhanced FMD in patients with diabetes (5.2 at 1.5 years vs. 3.8 at baseline; p = 0.04) and pre-diabetes (4.9 ± 0.4 vs. 3.8 ± 0.4; p = 0.04) Mediterranean diet induced an improvement in endothelial function after 1.5 years compared to low-fat diet in patients with diabetes (5.2 (Mediterranean diet) vs. 3.7 (Low-fat diet); p = 0.01) |
Rallidis et al. 2009 [15] | Parallel | Healthy with abdominal obesity | Brachial artery FMD | 90 | 2 months | Mediterranean diet plus close supervision | Mediterranean diet | The intervention increased FMD by 2.05%. Close adherence to a Mediterranean diet with dietitians’ advice improves endothelial function in obese individuals. |
Davis et al. 2017 [16] | Parallel | Healthy older subjects | Brachial artery FMD | 166 | 6 months | Mediterranean diet | Habitual diet | FMD was higher by 1.3% in the Mediterranean diet group. |
Ceriello et al. 2014 [17] | Parallel | T2DM | Brachial artery FMD | 24 | 3 months | Mediterranean diet | Low-fat diet | Mediterranean diet improved FMD compared to low-fat diet |
Buscemi et al. 2009 [18] | Parallel | Overweight/obese | Brachial artery FMD | 20 | 5 days and 60 days evaluation | Mediterranean diet | Very low-carbohydrate diet | Cardiovascular risk can be higher in the early days of a very low-carbohydrate diet compared to a Mediterranean diet. p = 0.007 for diet × time interaction |
Jaacks et al. 2018 [19] | Parallel | Overweight/obese | Brachial artery FMD | 30 | 8 weeks | Mediterranean diet. 3 arms: Mediterranean or habitual high-fat American-type diet + fish oil, walnuts and grape juice | High-fat American-type diet | No changes between groups were observed |
Thomazella et al. 2011 [20] | Parallel | Stable coronary heart disease | Brachial artery FMD | 40 | 3 months | Mediterranean diet | Low-fat Therapeutic Lifestyle Changes Diet | The 2 diets did not modify FMD in the brachial artery. |
Shai et al. 2010 [21] | Parallel | Obese | IMT | 140 | 2 years | Mediterranean diet; Low-carbohydrate diet | Low-fat diet | No differences in regression in intima-media thickness between groups. |
Gardener et al. 2014 [22] | Observational | Primary and secondary prevention; multiethnic | IMT | 1374 | - | Mediterranean diet adherence score ranges. | - | Moderate and strict adherence to a Mediterranean diet may protect against a higher burden of carotid atherosclerotic plaque. |
Murie-Fernández et al. 2011 [23] | Parallel | High-cardiovascular-risk asymptomatic subjects | IMT | 187 | 1 year | Mediterranean diet + virgin olive oil and Mediterranean diet + nuts | Low-fat diet | Mediterranean diets + virgin olive oil or nuts were not effective in inducing regression IMT after one year. However, they were effective among subjects with high baseline IMT |
Sala-Vila et al. 2014 [24] | Parallel | High-cardiovascular-risk asymptomatic subjects | IMT | 175 | 2.4 years | Mediterranean diet + virgin olive oil and Mediterranean diet + nuts | Low-fat diet | Compared with a control diet |
Giannini et al. 2013 [25] | Cross-sectional study | Hypercholesterolemic children | IMT | 68 | 12 months | Mediterranean diet | - | A reduction in IMT was documented after intervention |
Maiorino et al. 2016 [26] | Parallel | Newly diagnosed T2DM | IMT | 215 | 8.1 years | Mediterranean diet | Low-fat diet | Mediterranean diet is associated with a reduction in the progression of subclinical atherosclerotic disease, compared to control diet |
Gómez-Delgado et al. 2019 [27] | Intervention trial | Coronary heart disease patients | Genotyping of Apolipoprotein E genetic variants and the relationship with lipid metabolism | 506 | 3 years; postprandial state after 4 h | Mediterranean diet | Low-fat diet | After long-term consumption of a Mediterranean diet, subjects carrying the T allele have lower postprandial levels and smaller AUC in triglycerides, TRLs and large TRLs than patients carrying the CC allele. |
Corella et al. 2016. [28] | Longitudinal study | Free CVD patients (high-risk participants). | The study analyzed the relationship between CLOCK-rs4580704 gene variant and incidence of T2D and CVD. | 7098 | 4.8 years | Mediterranean diet supplemented with extra virgin olive oil or Mediterranean diet supplemented with mixed nuts | Low-fat diet | The study showed that the Mediterranean diet increased the protective effects of the G allele against T2D and demonstrated the association between the G allele and protection against stroke in T2D subjects |
Gómez-Delgado et al. 2018. [29] | Intervention trial | Coronary heart disease patients | Interaction between TERC gene variants with monounsaturated fatty acids and the effect on leukocyte telomere length, glucose metabolism and inflammation status | 926 | 12 months | Mediterranean diet | Low-fat diet | After consumption of a Mediterranean diet, subjects carrying the CC allele have a protective capacity slowing down telomeric shortening and decreasing the hs-CRP levels in CVD patients |
Gómez-Delgado et al. 2014 [30] | Intervention trial | Metabolic syndrome | Interaction between TNFα gene variation rs1800629 and the Mediterranean diet. Effect on triglycerides and inflammatory markers | 507 | 12 months | Mediterranean diet | Low-fat diet | The Mediterranean diet induced a silencing of a genetic variant of the TNF gene to improve the metabolism of triglycerides and the inflammatory markers associated with risk of endothelial dysfunction |
Jiménez-Morales et al. 2011 [31] | Metabolic syndrome | Interaction between NOS3 Glu298Asp polymorphism and the phenol content of virgin olive oil. Effect on postprandial endothelial dysfunction | 55 | Postprandial state at 4 h | High, medium and low polyphenol extra virgin olive oil intake | --- | Virgin olive oil with high content of polyphenols induces protection against the genetic variant NOS3 Glu298Asp, regulating NOS3 activity and decreasing the oxidative stress associated with endothelial damage. | |
D’Amore et al. 2016 [32] | Cross-sectional study | Metabolic syndrome | Deregulation of genes and microRNAs in response to extra virgin olive oil intake | 12 | Postprandial state at 4 h | High- and low-polyphenol extra virgin olive oil intake | ---- | The study showed the deregulation of miRNAs expressed differentially between healthy subjects and patients with metabolic syndrome. The deregulation of these miRNAs was associated with an anti-inflammatory, anti-oxidant status. |
Marques-Rocha et al. 2016 [33] | Cross-sectional study | Metabolic syndrome | Effect of dietary strategy for weight loss on inflammation-related microRNAs | 40 | 8 weeks | Hypocaloric diet based on the Mediterranean dietary pattern | ---- | Increased expression of miR-155-3p and decreased of Let-7b was observed in white blood cells. Changes in the expression profile were associated with atherogenic mechanisms related to disease development. |
Daimiel et al. 2020 [34] | Crossover trial | Healthy subjects | Postprandial deregulation of miRNAs related to cardiovascular disease | 12 | Postprandial state at 6 h | Low, medium and high content of total phenols in extra virgin olive oil | ---- | Deregulation of miRNAs in response to olive oil polyphenols was associated with improved lipid metabolism and reduced oxidative stress |
Fernandez et al. 2012 [10] | Parallel control trial | Metabolic syndrome patients | Effect of Mediterranean diet on endothelial progenitor cells (EPC) number. | 45 | 12 weeks | Mediterranean diet plus moderate-to-high intensity endurance training | Hypocaloric Mediterranean diet | Mediterranean diet improved the regenerative capacity of the endothelium and the cardiometabolic risk factors in metabolic syndrome patients, mediated by an increase in EPC. |
Cesari et al. 2017. [35] | Cross-sectional study | Elderly patients (nonagenarians) | Adherence of Mediterranean diet and endothelial progenitor cells (EPC) number. | 421 | Mediterranean diet | --- | Strict adherence to the Mediterranean diet and a high consumption of its foods induces an increase in EPCs in elderly patients, suggesting a lower cardiovascular risk. | |
Marín et al. 2011 [13] | Crossover trial | Healthy older subjects | Effect of Mediterranean diet on biomarkers of regenerative capacity of endothelium | 20 | 4 weeks | Mediterranean diet | Saturated fatty acid diet and low-fat, high-carbohydrate diet | The intake of the Mediterranean diet induced a decrease in microparticle levels and an increase in EPC, associated with an improvement in oxidative stress markers and high ischemic reactive hyperemia, suggesting an improvement in the regenerative capacity of the endothelium |
Maiorino et al. 2016 [26] | Parallel | Newly-diagnosed type 2 diabetes patients | Effect of Mediterranean diet on EPC and IMT | 215 | 4 years | Mediterranean diet | Low-fat diet | EPC levels increased with the Mediterranean diet and were associated with the regression of intima-media thickness and other markers of endothelial regeneration. |
Chiva-Blanch et al. 2016 [36] | Case-control study | Patients with cardiovascular events and at high risk of a cardiovascular event | Microparticles released from different vascular cells as biomarkers of endothelial damage. | 50 | 1 year | Mediterranean diet supplemented with virgin olive oil and Mediterranean diet supplemented with nuts | Low-fat diet | A Mediterranean diet rich in nuts promoted the reduction of endothelial damage markers, such as endothelial and platelet microparticles. |
Chiva-Blanch et al. 2016 [37] | Prospective study | High cardiovascular risk participants free of cardiovascular events | Long-term effect of a Mediterranean diet on microparticles derived from blood cells | 155 | 5 years | Mediterranean diet supplemented with virgin olive oil and Mediterranean diet supplemented with nuts | Low-fat diet | The Mediterranean diet induced changes in the microparticles, generating a lower prothrombotic and procoagulant endothelial environment and reducing the risk of cardiovascular events. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Torres-Peña, J.D.; Rangel-Zuñiga, O.A.; Alcala-Diaz, J.F.; Lopez-Miranda, J.; Delgado-Lista, J. Mediterranean Diet and Endothelial Function: A Review of its Effects at Different Vascular Bed Levels. Nutrients 2020, 12, 2212. https://doi.org/10.3390/nu12082212
Torres-Peña JD, Rangel-Zuñiga OA, Alcala-Diaz JF, Lopez-Miranda J, Delgado-Lista J. Mediterranean Diet and Endothelial Function: A Review of its Effects at Different Vascular Bed Levels. Nutrients. 2020; 12(8):2212. https://doi.org/10.3390/nu12082212
Chicago/Turabian StyleTorres-Peña, Jose D., Oriol A. Rangel-Zuñiga, Juan F. Alcala-Diaz, Jose Lopez-Miranda, and Javier Delgado-Lista. 2020. "Mediterranean Diet and Endothelial Function: A Review of its Effects at Different Vascular Bed Levels" Nutrients 12, no. 8: 2212. https://doi.org/10.3390/nu12082212