Advertisement
Research Article| Volume 269, P50-56, February 2018

Download started.

Ok

Mediterranean diet improves endothelial function in patients with diabetes and prediabetes: A report from the CORDIOPREV study

  • Jose D. Torres-Peña
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Antonio Garcia-Rios
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Nieves Delgado-Casado
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Purificacion Gomez-Luna
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Juan F. Alcala-Diaz
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Elena M. Yubero-Serrano
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Francisco Gomez-Delgado
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Ana Leon-Acuña
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Javier Lopez-Moreno
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Antonio Camargo
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Francisco J. Tinahones
    Affiliations
    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain

    Biomedical Research Institute of Malaga (IBIMA), Virgen de la Victoria Hospital, University of Malaga, Malaga, Spain
    Search for articles by this author
  • Javier Delgado-Lista
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Jose M. Ordovas
    Affiliations
    Jean Mayer U.S. Department of Agriculture Human Nutrition Research Center on Aging, Tufts University School of Medicine, Boston, MA, USA

    Madrid Institute of Advanced Studies–Food, Madrid, Spain

    National Centre of Cardiovascular Research (CNIC), Madrid, Spain
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.
    Pablo Perez-Martinez
    Correspondence
    Corresponding author. Reina Sofia University Hospital, Lipid and Atherosclerosis Research Unit. Avda. Menéndez Pidal, s/n. 14004 Córdoba, Spain.
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.
    Jose Lopez-Miranda
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    Lipid and Atherosclerosis Unit, Department of Internal Medicine / IMIBIC/Reina Sofia University Hospital/University of Cordoba, Spain

    CIBER Fisiopatologia Obesidad y Nutricion (CIBEROBN), Instituto de Salud Carlos III, Spain
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.

      Highlights

      • Long-term consumption of a MedDiet improves endothelial function in patients with prediabetes and diabetes.
      • MedDiet is associated with an improvement of endothelial function compared to LF diet in patients with diabetes.
      • Our findings advocate use of the MedDiet in patients with prediabetes and diabetes to prevent cardio-metabolic complications.

      Abstract

      Background and aims

      Endothelial dysfunction (ED) plays a key role in the development of atherosclerotic cardiovascular disease (ASCVD). Likewise, type 2 diabetes (T2D) is a major CVD risk factor. Therefore, our objective was to explore whether long-term consumption of a Mediterranean diet (MedDiet) rich in olive oil or a low-fat diet (LF diet) was associated with an improvement in ED and whether the potential benefits were similar in patients with or without T2D in the CORDIOPREV clinical trial (NCT00924937).

      Methods

      Endothelial function was measured in 805 participants who had completed follow-up ultrasound image studies, using ultrasonography of brachial artery to calculate flow mediated vasodilatation (FMD) before and after 1.5 years of intervention with a MedDiet [35% of calories from fat (22% monounsaturated) and 50% from carbohydrates] and LF diet [28% fat (12% monounsaturated) and 55% of calories from carbohydrates]. We categorized participants as patients with T2D, prediabetes, and without T2D according to the American Diabetes Association (ADA) criteria.

      Results

      MedDiet increased FMD in patients with T2D [5.2 ± 0.4 at 1.5 years vs. 3.8 ± 0.4 at baseline; p=0.04] and prediabetes [4.9 ± 0.4 vs. 3.8 ± 0.4; p=0.04] and induced an improvement in FMD compared to LF diet in patients with diabetes [5.2 ± 0.4 (MedDiet) vs.3.7 ± 0.4 (LF diet); p=0.01]; whereas both diets maintained FMD stable in patients without diabetes.

      Conclusions

      Habitual consumption of a MedDiet rich in extra virgin olive oil improves endothelial function in patients with prediabetes and diabetes. This takes great importance given that diet must be the cornerstone of treatment of patients with diabetes at high cardiovascular risk.

      Keywords

      Abbreviations:

      ADA (American Diabetes Association), ASCVD (atherosclerotic cardiovascular disease), BMI (body mass index), CVD (cardiovascular disease), CHD (coronary heart disease), FMD (flow mediated vasodilation), HDL-C (high-density lipoprotein cholesterol), LDL-C (low density lipoprotein), LF (low fat), MedDiet (Mediterranean diet), NO (nitric oxide), TC (total cholesterol), TG (triglycerides), T2D (type 2 diabetes)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Atherosclerosis
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Risk N.C.D.
        Worldwide trends in diabetes since 1980 : a pooled analysis of 751 population-based studies with 4.4 million participants.
        Lancet. 2008; 387: 1513-1530
        • Buse J.B.
        • Ginsberg H.N.
        • Bakris G.L.
        • Clark N.G.
        • Costa F.
        • Eckel R.
        • et al.
        Primary prevention of cardiovascular diseases in people with diabetes mellitus.
        Circulation. 2007; 115: 114
        • Ford E.S.
        • Ajani U.A.
        • Croft J.B.
        • Critchley J.A.
        • Labarthe D.R.
        • Kottke T.E.
        • et al.
        Explaining the decrease in U.S. Deaths from coronary disease, 1980–2000.
        N. Engl. J. Med. 2007; 356: 2388-2398
        • Franco M.
        • Cooper R.
        • Bilal U.
        • Fuster V.
        Control of coronary heart disease risk factors and evidence-based therapies: joint efforts for coronary heart disease prevention in Spain.
        Rev. Española Cardiol. English Ed. 2011; 64: 962-964
        • Jernberg T.
        • Hasvold P.
        • Henriksson M.
        • Hjelm H.
        • Thuresson M.
        • Janzon M.
        Cardiovascular risk in post-myocardial infarction patients: nationwide real world data demonstrate the importance of a long-term perspective.
        Eur. Heart J. 2015; 36: 1163-1170
        • Brunner H.
        • Cockcroft J.R.
        • Deanfield J.
        • Donald A.
        • Ferrannini E.
        • Halcox J.
        • et al.
        Endothelial function and dysfunction. Part II: association with cardiovascular risk factors and diseases. A statement by the working group on endothelins and endothelial factors of the european society of hypertension*.
        J. Hypertens. 2005; 23: 233-246
        • Halcox J.P.
        • Schenke W.H.
        • Zalos G.
        • Mincemoyer R.
        • Prasad A.
        • Waclawiw M.A.
        • et al.
        Prognostic value of coronary vascular endothelial dysfunction.
        Ciruclation. 2002; 106: 653-658
        • Corrado E.
        • Rizzo M.
        • Coppola G.
        • Fattouch K.
        • Novo G.
        • Marturana I.
        • et al.
        An update on the role of markers of inflammation in atherosclerosis.
        J. Atheroscler. Thrombosis. 2010; 17: 1-11
        • Francesco C.
        • Elena T.
        • Stefano M.
        • Andrea M.
        Genetic and molecular determinants of atherosclerotic plaque instability.
        Curr. Vasc. Pharmacol. 2010; 8: 545-552
      1. Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, et al. Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet.340(8828):1111–1115.

        • Anderson T.J.
        • Uehata A.
        • Gerhard M.D.
        • Meredith I.T.
        • Knab S.
        • Delagrange D.
        • et al.
        Close relation of endothelial function in the human coronary and peripheral circulations.
        J. Am. Coll. Cardiol. 1995; 26: 1235-1241
        • Enderle M.
        • Schroeder S.
        • Ossen R.
        • Meisner C.
        • Baumbach A.
        • Haering H.
        • et al.
        Comparison of peripheral endothelial dysfunction and intima media thickness in patients with suspected coronary artery disease.
        Heart. 1998; 80: 349-354
        • Schroeder S.
        • Enderle M.
        • Ossen R.
        • Meisner C.
        • Baumbach A.
        • Pfohl M.
        • et al.
        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
        • Fathi R.
        • Haluska B.
        • Isbel N.
        • Short K.
        The relative importance of vascular structure and function in predicting cardiovascular events.
        J. Am. Coll. Cardiol. 2004; 43: 616-623
        • Veerasamy M.
        • Bagnall A.
        • Neely D.
        • Allen J.
        • Sinclair H.
        • Kunadian V.
        Endothelial dysfunction and coronary artery disease: a state of the art review.
        Cardiol. Rev. 2015; 23: 119-129
        • Ceriello A.
        • Esposito K.
        • Sala L.L.
        • Pujadas G.
        • De Nigris V.
        • Testa R.
        • et al.
        The protective effect of the Mediterranean diet on endothelial resistance to GLP-1 in type 2 diabetes: a preliminary report.
        Cardiovasc. Diabetol. 2014; 13: 1-9
        • Bansal N.
        Prediabetes diagnosis and treatmen: a review.
        World J. Diabetes. 2015; 6: 296-303
        • Delgado-Lista J.
        • Perez-Martinez P.
        • Garcia-Rios A.
        • Alcala-Diaz J.F.
        • Perez-Caballero A.I.
        • Gomez-Delgado F.
        CORonary 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): 177
      2. Standards of medical care in diabetes-2017:summary of revisions.
        Diabetes Care. 2016; (S4 LP-S5)
        • Corretti M.C.
        • Anderson T.J.
        • Benjamin E.J.
        • Celermajer D.
        • Charbonneau F.
        • Creager M.A.
        • et al.
        Guidelines for the ultrasound assesment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force.
        J. Am. Coll. Cardiol. 2002; 39: 257-265
        • Fuentes F.
        • Lopez-Miranda J.
        • Sanchez E.
        • et al.
        Mediterranean and low-fat diets improve endothelial function in hypercholesterolemic men.
        Ann. Intern. Med. 2001; 134: 1115-1119
        • Perez-Martinez P.
        • Moreno-Conde M.
        • Cruz-Teno C.
        • Ruano J.
        • Fuentes F.
        • Delgado-Lista J.
        • 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
        • Storniolo C.E.
        • Casillas R.
        • Bullo M.
        • Castañer O.
        • Ros E.
        • Saez G.T.
        • et al.
        A Mediterranean diet supplemented with extra virgin olive oil or nuts improves endothelial markers involved in blood pressure control in hypertensive women.
        Eur. J. Nutr. 2015; : 1-9
        • Ryan M.
        • McInerney D.
        • Owens D.
        • Collins P.
        • Johnson a
        • Tomkin G.H.
        Diabetes and the Mediterranean diet: a beneficial effect of oleic acid on insulin sensitivity, adipocyte glucose transport and endothelium-dependent vasoreactivity.
        QJM Mon. J. Assoc. Physicians. 2000; 93: 85-91
        • Seligman B.G.S.
        • Polanczyk C.A.
        • Santos A.S.B.
        • Foppa M.
        • Junges M.
        • Bonzanini L.
        • et al.
        Intensive practical lifestyle intervention improves endothelial function in metabolic syndrome independent of weight loss: a randomized controlled trial.
        Metabolism Clin. Exp. 2011; 60: 1736-1740
        • Mohler E.R.
        • Sibley A.A.
        • Stein R.
        • Davila-Roman V.
        • Wyatt H.
        • Badellino K.
        • et al.
        Endothelial function and weight loss: Comparison of low- carbohydrate and low-fat diets.
        Obesity (Silver Spring, Md). 2013; 21: 504-509
        • Hodson L.
        • Harnden K.E.
        • Roberts R.
        • Dennis aL.
        • Frayn K.N.
        Does the DASH diet lower blood pressure by altering peripheral vascular function?.
        J. Hum. Hypertens. 2010; 24: 312-319
        • Peter K.
        • Nawroth P.
        • Conradt C.
        • Weiss T.
        • Boehme M.
        • et al.
        Circulating vascular cell adhesion molecule-1 correlates with the extent of human atherosclerosis in contrast to circulating intercellular adhesion molecule-1, E-selectin, P-selectin, and thrombomodulin.
        Arter. Thromb. Vasc. Biol. 1997; 17: 505-512
      3. Perez-Jimenez F, Castro P, Lopez-Miranda J, Paz-Rojas E, Blanco A, Lopez-Segura F, et al. Circulating levels of endothelial function are modulated by dietary monounsaturated fat. Atherosclerosis1452:351–358.

        • Fuentes F.
        • Lopez-Miranda J.
        • Perez-Martinez P.
        • Jimenez Y.
        • Marin C.
        • Gomez P.
        • et al.
        Chronic effects of a high-fat diet enriched with virgin olive oil and a low-fat diet enriched with α-linolenic acid on postprandial endothelial function in healthy men.
        Br. J. Nutr. 2008; 100: 159-165
        • Ruano J.
        • Lopez-Miranda J.
        • Fuentes F.
        • Moreno J.A.
        • Bellido C.
        • Perez-Martinez P.
        • et al.
        Phenolic content of virgin olive oil improves ischemic reactive hyperemia in hypercholesterolemic patients.
        J. Am. Coll. Cardiol. 2005; 46: 1864-1868
        • Harris W.S.
        • Park Y.
        • Isley W.L.
        Cardiovascular disease and long-chain omega-3 fatty acids.
        Curr. Opin. Lipidol. 2003; 14: 9-14
        • Hu F.B.
        Dietary pattern analysis: a new direction in nutritional epidemiology.
        Curr. Opin. Lipidol. 2002; 13: 3-9
        • Moradipoor S.
        • Ismail P.
        • Etemad A.
        • Wan Sulaiman W.A.
        • Ahmadloo S.
        • Khazaei S.
        Expression profiling of genes related to endothelial cells biology in patients with type 2 diabetes and patients with prediabetes.
        BioMed Res. Int. 2017; 2017: 1
        • Suwaidi J.A.
        • Hamasaki S.
        • Higano S.T.
        • Nishimura R.A.
        • Holmes D.R.
        • Lerman A.
        Long-term follow-up of patients with mild coronary artery disease and endothelial dysfunction.
        Circulation. 2000; 101: 948-954
        • Celermajer D.S.
        • Sorensen K.E.
        • Bull C.
        • Robinson J.
        • Deanfield J.E.
        Endothelium-dependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction.
        J. Am. Coll. Cardiol. 1994; 24: 1468-1474
      4. Laclaustra M, Frangi AF, Frangi AG, Casasnovas JA, Cia P. Association of endothelial function and vascular data with LDL-c and HDL-c in a homogeneous population of middle-aged, healthy military men: evidence for a critical role of optimal lipid levels. Int. J. Cardiol..125(3):376–382.

        • Witte D.R.
        • Westerink J.
        • de Koning E.J.
        • van der Graaf Y.
        • Grobbee D.E.
        • Bots M.L.
        Is the association between flow-mediated dilation and cardiovascular risk limited to low-risk populations?.
        J. Am. Coll. Cardiol. 2005; 45: 1987-1993
        • Gokce N.
        • Keaney J.F.
        • Hunter L.M.
        • Watkins M.T.
        • Nedeljkovic Z.S.
        • Menzoian J.O.
        • et al.
        Predictive value of non invasively determined endothelial dysfunction for long-term cardiovascular events in patients with peripheral vascular disease.
        J. Am. Coll. Cardiol. 2003; 41: 1769-1775
      5. Karatzis EN, Ikonomidis I, Vamvakou GD, Papaioannou TG, Protogerou AD, Andreadou I, et al. Long-term prognostic role of flow-mediated dilatation of the brachial artery after acute coronary syndromes without ST elevationAm. J. Cardiol..98(11):1424–1428.

        • Anderson E.A.
        • Mark A.L.
        Flow-mediated and reflex changes in large peripheral artery tone in humans.
        Circulation. 1989; 79: 93-100
        • 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
        • Huang Y.
        • Cai X.
        • Mai W.
        • Li M.
        • Hu Y.
        Association between prediabetes and risk of cardiovascular disease and all cause mortality: systematic review and meta-analysis.
        BMJ. 2016; 355 (i5953)