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European Journal of Nutrition

, Volume 56, Issue 1, pp 89–97 | Cite as

A Mediterranean diet supplemented with extra virgin olive oil or nuts improves endothelial markers involved in blood pressure control in hypertensive women

  • C. E. Storniolo
  • R. Casillas
  • M. Bulló
  • O. Castañer
  • E. Ros
  • G. T. Sáez
  • E. Toledo
  • R. Estruch
  • V. Ruiz-Gutiérrez
  • M. Fitó
  • M. A. Martínez-González
  • J. Salas-Salvadó
  • M. T. Mitjavila
  • J. J. MorenoEmail author
Original Contribution

Abstract

Purpose

Serum nitric oxide (NO) reduction and increased endothelin-1 (ET-1) play a pivotal role in endothelial dysfunction and hypertension. Considering that traditional Mediterranean diet (TMD) reduces blood pressure (BP), the aim of this study was to analyze whether TMD induced changes on endothelial physiology elements such as NO, ET-1 and ET-1 receptors which are involved in BP control.

Methods

Non-smoking women with moderate hypertension were submitted for 1 year to interventions promoting adherence to the TMD, one supplemented with extra virgin olive oil (EVOO) and the other with nuts versus a control low-fat diet (30 participants/group). BP, NO, ET-1 and related gene expression as well as oxidative stress biomarkers were measured.

Results

Serum NO and systolic BP (SBP) or diastolic BP (DBP) were negatively associated at baseline, as well as between NO and ET-1. Our findings also showed a DBP reduction with both interventions. A negative correlation was observed between changes in NO metabolites concentration and SBP or DBP after the intervention with TMD + EVOO (p = 0.033 and p = 0.044, respectively). SBP reduction was related to an impairment of serum ET-1 concentrations after the intervention with TMD + nuts (p = 0.008). We also observed changes in eNOS, caveolin 2 and ET-1 receptors gene expression which are related to NO metabolites levels and BP.

Conclusions

The changes in NO and ET-1 as well as ET-1 receptors gene expression explain, at least partially, the effect of EVOO or nuts on lowering BP among hypertensive women.

Keywords

Endothelin-1 Hypertension Nitric oxide PREDIMED study Oxidative stress 

Notes

Acknowledgments

The authors thank the participants in the PREDIMED study for their continued collaboration. The Fundación Patrimonio Comunal Olivarero, Hojiblanca SA (Málaga, Spain), California Walnut Commission (Sacramento, CA, USA), Borges SA (Reus, Spain) and Morella Nuts SA (Reus, Spain) donated the olive oil, walnuts, almonds and hazelnuts, respectively. We also thank the Scientific and Technical services of the University of Barcelona for malondialdehyde determinations. This study was supported by the Spanish Ministry of Health (FIS PI10/0082, G03/140, RD06/0045), Fondo Europeo de Desarrollo Regional, the Spanish Ministry of Science (BFU2007-61727/BFI) and the Generalitat de Catalunya (2009SGR00438).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Jousilahti P, Toumilehto J, Vartiainen E, Korhonen HJ, Pitkäniemi J, Nissinen A, Puska P (1995) Importance of risk factor clustering in coronary heart disease mortality and incidence in eastern Finland. J Cardiovasc Risk 2:63–70CrossRefGoogle Scholar
  2. 2.
    Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265–9269CrossRefGoogle Scholar
  3. 3.
    Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, Yazaki Y, Goto K, Masaki T (1988) A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332:411–415CrossRefGoogle Scholar
  4. 4.
    Furchgott RF, Zawadzki JV (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288:373–376CrossRefGoogle Scholar
  5. 5.
    Griendling KK, Alexander RW (1997) Oxidative stress and cardiovascular disease. Circulation 96:3264–3265Google Scholar
  6. 6.
    Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferranini E, Halcox J, Kiowski W, Lüscher TF, Mancia G, Natali A, Oliver JJ, Pessina AC, Rizzoni D, Rossi GP, Salvetti A, Spieker LE, Taddei S, Webb DJ (2005) 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 23:233–246CrossRefGoogle Scholar
  7. 7.
    Dhaun N, Goddard J, Kohan DE, Pollock DM, Schiffrin EL, Webb DJ (2008) Role of endothelin-1 in clinical hypertension: 20 years on. Hypertension 52:452–459CrossRefGoogle Scholar
  8. 8.
    Epstein BJ, Anderson S (2009) Endothelin receptor antagonists as antihypertensives: the next frontier. Expert Rev Cardiovasc Ther 7:675–687CrossRefGoogle Scholar
  9. 9.
    Mancia G, De Backer G, Dominiczak A, Cifkova R, Fagard R, Germano G, Grassi G, Heagerty AM, Kjeldsen SE, Laurent S, Narkiewicz K, Ruilope L, Rynkiewicz A, Schmieder RE, Boudier HA, Zanchetti A, Vahanian A, Camm J, De Caterina R, Dean V, Dickstein K, Filippatos G, Funck-Brentano C, Hellemans I, Kristensen SD, McGregor K, Sechtem U, Silber S, Tendera M, Widimsky P, Zamorano JL, Erdine S, Kiowski W, Agabiti-Rosei E, Ambrosioni E, Lindholm LH, Viigimaa M, Adamopoulos S, Agabiti-Rosei E, Ambrosioni E, Bertomeu V, Clement D, Erdine S, Farsang C, Gaita D, Lip G, Mallion JM, Manolis AJ, Nilsson PM, O’Brien E, Ponikowski P, Redon J, Ruschitzka F, Tamargo J, van Zwieten P, Waeber B, Williams B (2007) Guidelines for the management of arterial hypertension: the task force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). J Hypertens 25:1105–1187CrossRefGoogle Scholar
  10. 10.
    Strazzullo P, Ferro-Luzzi A, Siani A, Scaccini C, Sette S, Catasta G, Mancini M (1986) Changing the Mediterranean diet: effects on blood pressure. J Hypertens 4:407–412CrossRefGoogle Scholar
  11. 11.
    Casas-Agustench P, López-Uriarte P, Ros E, Bulló M, Salas-Salvadó J (2011) Nuts, hypertension and endothelial function. Nutr Metabol Cardiovasc Dis 21:S21–S33CrossRefGoogle Scholar
  12. 12.
    Martínez-González MA, Corella D, Salas-Salvadó J, Ros E, Covas MI, Fiol M, Wärnberg J, Arós F, Ruíz-Gutiérrez V, Lamuela-Raventós RM, Lapetra J, Muñoz MA, Martínez JA, Sáez G, Serra-Majem L, Pintó X, Mitjavila MT, Tur JA, Portillo MP, Estruch R, PREDIMED Study Investigators (2012) Cohort profile: design and methods of the PREDIMED study. Int J Epidemiol 41:377–385CrossRefGoogle Scholar
  13. 13.
    Estruch R, Martínez-González MA, Corella D, Salas-Salvadó J, Ruiz-Gutiérrez V, Covas MI, Fiol M, Gómez-Gracia E, López-Sabater MC, Vinyoles E, Arós F, Conde M, Lahoz C, Lapetra J, Sáez G, Ros E, PREDIMED Study Investigators (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145:1–11CrossRefGoogle Scholar
  14. 14.
    Toledo E, Hu FB, Estruch R, Buil-Cosiales P, Corella D, Salas-Salvado J, Covas MI, Arós F, Gómez-Gracia E, Fiol M, Lapetra J, Serra-Majem L, Pinto X, Lamuela-Raventós RM, Saez G, Bulló M, Ruiz-Gutiérrez V, Ros E, Sorli JV, Martinez-Gonzalez MA (2013) Effect of the Mediterranean diet on blood pressure in the PREDIMED trial: results from a randomized controlled trial. BMC Med 11:207CrossRefGoogle Scholar
  15. 15.
    Nigg CR, Burbank PM, Padula C, Dufresne R, Rossi JS, Velicer WF, Laforge RG, Prochaska JO (1999) Stages of change across ten health risk behaviors for older adults. Gerontologist 9:473–482CrossRefGoogle Scholar
  16. 16.
    Fernández-Ballart JD, Piñol JL, Zazpe I, Corella D, Carrasco P, Toledo E, Perez-Bauer M, Martínez-González MA, Salas-Salvadó J, Martín-Moreno JM (2010) Relative validity of a semi-quantitative food-frequency questionnaire in an elderly Mediterranean population of Spain. Br J Nutr 103:1808–1816CrossRefGoogle Scholar
  17. 17.
    Elosua R, Marrugat J, Molina L, Pons S, Pujol E (1994) Validation of the Minnesota Leisure Time Physical Activity Questionnaire in Spanish men. The MARATHOM Investigators. Am J Epidemiol 139:1197–1209Google Scholar
  18. 18.
    Cheng GW, Wu HL, Huang YL (2008) Simultaneous determination of malondialdehyde and ofloxacin in plasma using an isocratic high-performance liquid chromatography/fluorescence detection system. Anal Chim Acta 616:230–234CrossRefGoogle Scholar
  19. 19.
    Celermajer DS, Sorensen KE, Gooch VM, Spiegelhalter DJ, Miller OI, Sullivan ID, Lloyd JK, Deanfield JE (1992) Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340:1111–1115CrossRefGoogle Scholar
  20. 20.
    Perticone A, Ceravolo R, Pujia A, Ventura G, Iacopino S, Scozzafava A, Chello M, Mastroroberto P, Verdecchia P, Schillaci G (2001) Prognostic significance of endothelial dysfunction in hypertensive patients. Circulation 104:191–196CrossRefGoogle Scholar
  21. 21.
    Giannotti G, Doerries C, Mocharla PS, Mueller MF, Bahlmann FH, Horvàth T, Jiang H, Sorrentino SA, Steenken N, Manes C, Marzilli M, Rudolph KL, Lüscher TF, Drexler H, Landmesser U (2010) Impaired endothelial repair capacity of early endothelial progenitor cells in prehypertension: relation to endothelial dysfunction. Hypertension 55:1389–1397CrossRefGoogle Scholar
  22. 22.
    Ghiadoni L, Versari D, Magagna A, Kardasz I, Plantinga Y, Giannarelli C, Taddei S, Salvetti A (2007) Ramipril dose-dependently increases nitric oxide availability in the radial artery of essential hypertension patients. J Hypertens 25:361–366CrossRefGoogle Scholar
  23. 23.
    Stauffer BL, Westby CM, DeSouza CA (2008) Endothelin-1, aging and hypertension. Curr Opin Cardiol 23:350–355CrossRefGoogle Scholar
  24. 24.
    Weil BR, Westby CM, Greiner JJ, Stauffer BL, DeSouza CA (2012) Elevated endothelin-1 vasoconstrictor tone in prehypertensive adults. Can J Cardiol 28:347–353CrossRefGoogle Scholar
  25. 25.
    Kleinbongard P, Dejam A, Lauer T, Rassaf T, Schindler A, Picker O, Scheeren T, Gödecke A, Schrader J, Schulz R, Heusch G, Schaub GA, Bryan NS, Feelisch M, Kelm M (2003) Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals. Free Radic Biol Med 35:790–796CrossRefGoogle Scholar
  26. 26.
    Kelm M (1999) Nitric oxide metabolism and breakdown. Biochim Biophys Acta 1411:273–289CrossRefGoogle Scholar
  27. 27.
    Leung JW, Wong WT, Koon HW, Mo FM, Tam S, Huang Y, Vanhoutte PM, Chung SS, Chung SK (2011) Transgenic mice over-expressing ET-1 in the endothelial cells develop systemic hypertension with altered vascular reactivity. PLoS One 6:e26994CrossRefGoogle Scholar
  28. 28.
    Edwards DL, Arora CP, Bui DT, Castro LC (1996) Long-term nitric oxide blockade in the pregnant rat: effects on blood pressure and plasma levels of endothelin-1. Am J Obstet Gynecol 175:484–488CrossRefGoogle Scholar
  29. 29.
    Bourque SL, Davidge ST, Adams MA (2011) The interaction between endothelin-1 and nitric oxide in the vasculature: new perspectives. Am J Physiol Regul Integr Comp Physiol 300:R1288–R1295CrossRefGoogle Scholar
  30. 30.
    Stamler R (1991) Implications of the INTERSALT Study. Hypertension 17:16–20CrossRefGoogle Scholar
  31. 31.
    Estruch R, Ros E, Salas-Salvadó J, Covas MI, Corella D, Arós F, Gómez-Gracia E, Ruiz-Gutiérrez V, Fiol M, Lapetra J, Lamuela-Raventos RM, Serra-Majem L, Pintó X, Basora J, Muñoz MA, Sorlí JV, Martínez JA, Martínez-González MA (2013) Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med 4:1279–1290CrossRefGoogle Scholar
  32. 32.
    Medina-Remón A, Tresserra-Rimbau A, Pons A, Tur JA, Martorell M, Ros E, Buil-Cosiales P, Sacanella E, Covas MI, Corella D, Salas-Salvadó J, Gómez-Gracia E, Ruiz-Gutiérrez V, Ortega-Calvo M, García-Valdueza M, Arós F, Saez GT, Serra-Majem L, Pinto X, Vinyoles E, Estruch R, Lamuela-Raventos RM (2015) Effects of total dietary polyphenols on plasma nitric oxide and blood pressure in a high cardiovascular risk cohort. The PREDIMED randomized trial. Nutr Metab Cardiovasc Dis 25:60–67CrossRefGoogle Scholar
  33. 33.
    Esposito K, Marfella R, Ciotola M, Di Palo C, Giugliano F, Giugliano G, D’Armiento M, D’Andrea F, Giugliano D (2004) Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial. JAMA 292:1440–1446CrossRefGoogle Scholar
  34. 34.
    Ros E, Nuñez I, Pérez-Heras A, Serra M, Gilabert R, Casals E, Deulofeu R (2004) A walnut diet improves endothelial function in hypercholesterolemic subjects: a randomized crossover trial. Circulation 109:1609–1614CrossRefGoogle Scholar
  35. 35.
    Cortés B, Nuñez I, Cofán M, Gilabert R, Pérez-Heras A, Casals E, Deulofeu R, Ros E (2006) Acute effects of high-fat meals enriched with walnuts or olive oil on postprandial endothelial function. J Am Coll Cardiol 48:1666–1671CrossRefGoogle Scholar
  36. 36.
    Konstantinidou V, Covas MI, Muñoz-Aguayo D, Khymenets O, de la Torre R, Saez G, Tormos Mdel C, Toledo E, Marti A, Ruiz-Gutiérrez V, Ruiz Mendez MV, Fito M (2010) In vivo nutrigenomic effects of virgin olive oil polyphenols within the frame of the Mediterranean diet: a randomized controlled trial. FASEB J 24:2546–2557CrossRefGoogle Scholar
  37. 37.
    Fleming I (2010) Molecular mechanisms underlying the activation of eNOS. Pflugers Arch 459:793–806CrossRefGoogle Scholar
  38. 38.
    Weber MA, Black H, Bakris G, Krum H, Linas S, Weiss R, Linseman JV, Wiens BL, Warren MS, Lindholm LH (2009) A selective endothelin-receptor antagonist to reduce blood pressure in patients with treatment-resistant hypertension: a randomized, double-blind, placebo-controlled trial. Lancet 374:1423–1431CrossRefGoogle Scholar
  39. 39.
    Walter MF, Jacob RF, Jeffers B, Ghadanfar MM, Preston GM, Buch J, Mason RP (2004) Serum levels of thiobarbituric acid reactive substances predict cardiovascular events in patients with stable coronary artery disease. J Am Coll Cardiol 44:1996–2002CrossRefGoogle Scholar
  40. 40.
    Mitjavila MT, Fandos M, Salas-Salvadó J, Covas MI, Borrego S, Estruch R, Lamuela-Raventós R, Corella D, Martínez-Gonzalez MA, Sánchez JM, Bulló M, Fitó M, Tormos C, Cerdá C, Casillas R, Moreno JJ, Iradi A, Zaragoza C, Chaves J, Sáez GT (2013) The Mediterranean diet improves the systemic lipid and DNA oxidative damage in metabolic syndrome individuals. A randomized, controlled, trial. Clin Nutr 32:172–178CrossRefGoogle Scholar
  41. 41.
    Fitó M, Guxens M, Corella D, Sáez G, Estruch R, de la Torre R, Francés F, Cabezas C, López-Sabater Mdel C, Marrugat J, García-Arellano A, Arós F, Ruiz-Gutierrez V, Ros E, Salas-Salvadó J, Fiol M, Solá R, Covas MI, PREDIMED Study Investigators (2007) Effect of a traditional Mediterranean diet on lipoprotein oxidation: a randomized controlled trial. Arch Intern Med 167:1195–1203CrossRefGoogle Scholar
  42. 42.
    Moreno-Luna R, Muñoz-Hernandez R, Miranda ML, Costa AF, Jimenez-Jimenez L, Vallejo-Vaz AJ, Muriana FJ, Villar J, Stiefel P (2012) Olive oil polyphenols decrease blood pressure and improve endothelial function in young women with mild hypertension. Am J Hypertens 25:1299–1304Google Scholar
  43. 43.
    Storniolo CE, Roselló-Catafau J, Pintó X, Mitjavila MT, Moreno JJ (2014) Polyphenol fraction of extra virgin olive oil protects against endothelial dysfunction induced by high glucose and free fatty acids through modulation of nitric oxide and endothelin-1. Redox Biol 2C:971–977CrossRefGoogle Scholar
  44. 44.
    Perona JS, Martínez-González J, Sanchez-Domínguez JM, Badimon L, Ruiz-Gutierrez V (2004) The unsaponifiable fraction of virgin olive oil in chylomicrons from men improves the balance between vasoprotective and prothrombotic factors released by endothelial cells. J Nutr 134:3284–3289Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • C. E. Storniolo
    • 1
  • R. Casillas
    • 1
  • M. Bulló
    • 2
    • 9
  • O. Castañer
    • 3
    • 9
  • E. Ros
    • 4
    • 9
  • G. T. Sáez
    • 5
    • 9
  • E. Toledo
    • 6
    • 9
  • R. Estruch
    • 7
    • 9
  • V. Ruiz-Gutiérrez
    • 8
    • 9
  • M. Fitó
    • 3
    • 9
  • M. A. Martínez-González
    • 6
    • 9
  • J. Salas-Salvadó
    • 2
    • 9
  • M. T. Mitjavila
    • 1
  • J. J. Moreno
    • 1
    Email author
  1. 1.Department of PhysiologyUniversity of BarcelonaBarcelonaSpain
  2. 2.Human Nutrition Unit, HSPVRovira i Virgili UniversityReusSpain
  3. 3.Cardiovascular Risk and Nutrition Research GroupIMIM-Institut de Recerca Hospital del MarBarcelonaSpain
  4. 4.Endocrinology and Nutrition ServiceHospital ClinicBarcelonaSpain
  5. 5.Department of Biochemistry and Molecular Biology, Clinical Analysis Service-CDB HGUVUniversity of ValenciaValenciaSpain
  6. 6.Department of Preventive Medicine and Public HealthUniversity of NavarraPamplonaSpain
  7. 7.Department of Internal MedicineUniversity of BarcelonaBarcelonaSpain
  8. 8.Instituto de la GrasaConsejo Superior de Investigaciones CientíficasSevilleSpain
  9. 9.Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y NutriciónInstituto de Salud Carlos IIIMadridSpain

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