Effect of consumption of tomato juice enriched with n-3 polyunsaturated fatty acids on the lipid profile, antioxidant biomarker status, and cardiovascular disease risk in healthy women

Abstract

Purpose

We compared the effects of consumption of n-3 polyunsaturated fatty acids (PUFA)-enriched tomato juice versus plain tomato juice on the serum lipid profile and levels of biomarkers related to antioxidant status and cardiovascular disease (CVD) risk in women.

Methods

Eighteen healthy women participated in a 2-week intervention trial involving the daily intake of 500 mL of n-3 PUFA-enriched juice (n = 11) or plain tomato juice (n = 7). Each serving of enriched juice provided 250 mg of eicosapentaenoic acid (EPA) plus docosahexanoic acid (DHA). Both juices provided natural antioxidant compounds such as phenolics (181 mg) and lycopene (26.5 mg).

Results

Intervention with the enriched juice had no effect on the lipid profile, and serum levels of triglycerides and cholesterol (total, LDL, and HDL) remained unchanged. The serum antioxidant status improved following juice intake, as revealed by an increase in total antioxidant capacity and a slight decrease in lipid peroxidation. The serum levels of homocysteine, a cardiovascular risk factor, decreased following n-3 PUFA-enriched juice consumption. A decrease in vascular adhesion molecule 1 (VCAM-1) levels was also noted after intake of either plain or enriched tomato juice, whereas intercellular adhesion molecule 1 (ICAM-1) levels only decreased following intake of the enriched juice.

Conclusions

Overall, stronger positive amelioration of CVD risk factors was observed following the intake of n-3 PUFA-enriched juice than after plain tomato juice consumption, which suggested a possible synergistic action between n-3 PUFAs and tomato antioxidants.

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References

  1. 1.

    Das UN (2008) Essential fatty acids and their metabolites could function as endogenous HMG-CoA reductase and, and cardioprotective molecules. Lipids Health Dis 7:37–55

    Article  Google Scholar 

  2. 2.

    Leal J, Luengo-Fernandez R, Gray A, Petersen S, Rayner M (2006) ACE enzyme inhibitors, anti-arrhytmic, anti-hypertensive, anti-atherosclerotic, anti-inflammatory, cytoprotective. Economic burden of cardiovascular diseases in the enlarged European Union. Eur Heart J 27(13):1610–1619

    Article  Google Scholar 

  3. 3.

    Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J (2010) Heart disease and stroke statistics-2010 Update. A report from the American Heart Association. Circulation 121:e46–e215

    Article  Google Scholar 

  4. 4.

    Maas R, Böger RH (2003) Old and new cardiovascular risk factors: from unresolved issues to new opportunities. Atheroscler Suppl 4:5–17

    Article  Google Scholar 

  5. 5.

    Bhatnagar D, Durrington PN (2003) Omega-3 fatty acids: their role in the prevention and treatment of atherosclerosis related risk factors and complications. Int J Clin Pract 57:305–314

    CAS  Google Scholar 

  6. 6.

    Nishida C, Uauy R, Kumanyika S, Shetty P (2004) The Joint WHO/FAO Expert Consultation on diet, nutrition and the prevention of chronic diseases: process, product and policy implications. Public Health Nutr 7:245–250

    Google Scholar 

  7. 7.

    De Caterina R, Massaro M (2005) Omega-3 fatty acids and the regulation of expression of endothelial pro-atherogenic and pro-inflammatory genes. J Membr Biol 206:103–116

    Article  Google Scholar 

  8. 8.

    Calder PC, Yaqoob P (2009) Omega-3 polyunsaturated fatty acids and human health outcomes. Biofactors 35:266–272

    Article  CAS  Google Scholar 

  9. 9.

    Lavie CJ, Milani RV, Mehra MR, Ventura HO (2009) Omega-3 polyunsaturated fatty acids and cardiovascular diseases. J Am Coll Cardiol (JACC) 54:585–594

    Article  CAS  Google Scholar 

  10. 10.

    Patel JV, Tracey I, Hughes EA, Lip GYH (2000) Omega-3 polyunsaturated fatty acids: a necessity for a comprehensive secondary prevention strategy. Vasc Health Risk Manag 5:801–810

    Google Scholar 

  11. 11.

    De Roos B, Mavromatis Y, Brouwer IA (2009) Long-chain n-3 polyunsaturated fatty acids: new insights into mechanisms relating to inflammation and coronary heart disease. Br J Pharmacol 158:413–428

    Article  Google Scholar 

  12. 12.

    Vrablik M, Prusikova M, Snejdrlova M, Zlatohlavek L (2009) Omega-3 fatty acids and cardiovascular disease risk. Do we understand the relationship? Physiol Res 58((Suppl 1)):S19–S26

    CAS  Google Scholar 

  13. 13.

    He K (2009) Fish, long-chain omega-3 polyunsaturated fatty acids and prevention of cardiovascular disease-Eat fish or take fish oil supplement? Prog Cardiovasc Dis 52:95–114

    Article  CAS  Google Scholar 

  14. 14.

    World Health Organization (1985) Energy and protein requirements. Technical Report Series, No. 724. Report of a Joint FAO/WHO/UNU Expert Consultation. World Health Organization. Geneva

  15. 15.

    Baghurst K (2005) Executive summary of nutrient reference values for Australia and New Zealand including recommended dietary intakes. Commonwealth department of health and ageing, Australia. Ministryof health, New Zealand. National Health and Medical Research. Council. http://www.nhmrc.gov.au/publications/synopses/n35syn.htm

  16. 16.

    Kris-Etherton PM, Grieger JA, Etherton TD (2009) Dietary reference intakes for DHA and EPA. Prostag Leukotr Ess 81:99–104

    Article  CAS  Google Scholar 

  17. 17.

    Wallace JM, McCabe AJ, Robson PJ, Keogh MK, Murray CA, Kelly PM, Marquez-Ruiz G, McGlynn H, Gilmore WS, Strain JJ (2000) Bioavailability of n-3 polyunsaturated fatty acids (PUFA) in foods enriched with microencapsulated fish oil. Ann Nutr Metab 44:157–162

    Article  CAS  Google Scholar 

  18. 18.

    Whelan J, Rust C (2006) Innovative dietary sources of n-3 fatty acids. Ann Rev Nutr 26:75–103

    Article  CAS  Google Scholar 

  19. 19.

    Kolanowsky W, Swiderski F, Berger S (1999) Possibilities of fish oil application for food products enrichment with omega-3 PUFA. Int J Food Sci Nutr 50:39–49

    Article  Google Scholar 

  20. 20.

    Metcalf RG, James MJ, Mantzioris E, Cleland LG (2003) A practical approach to increasing intakes of n-3 polyunsaturated fatty acids: use of novel foods enriched with n-3 fats. Eur J Clin Nutr 57:1605–1612

    Article  CAS  Google Scholar 

  21. 21.

    Martin L, Zarn D, Hansen AM, Wismer W, Mazurak V (2008) Food products as vehicles for n-3 fatty acid supplementation. Can J Diet Pract Res 69:203–207

    Article  Google Scholar 

  22. 22.

    Periago MJ, García-Alonso FJ, Jacob K, Olivares AB, Bernal MJ, Iniesta MD, Martínez C, Ros G (2008) Bioactive compounds, folates and antioxidant properties of tomatoes (Lycopersicum esculentum) during vine ripening. Int J Food Sci Nutr 12:1–15

    Article  Google Scholar 

  23. 23.

    Garcia-Alonso FJ, Bravo S, Casas J, Pérez-Conesa D, Jacob K, Periago MJ (2009) Changes in antioxidant compounds during the shelf life of commercial tomato juices in different packaging materials. J Agric Food Chem 57:6815–6822

    Article  CAS  Google Scholar 

  24. 24.

    Rao AV (2002) Lycopene, tomatoes, and the prevention of coronary heart disease. Exp Biol Med 227:908–913

    CAS  Google Scholar 

  25. 25.

    Wilcox JK, Catignani GL, Lazarus S (2003) Tomatoes and cardiovascular health. Crit Rev Food Sci Nutr 43(1):1–18

    Article  Google Scholar 

  26. 26.

    Iniesta MD, Pérez-Conesa D, García-Alonso FJ, Ros G, Periago MJ (2009) Folate content in tomato (Lycopersicum esculentum). Influence of cultivar, ripeness, year of harvest and pasteurization and storage temperatures. J Agric Food Chem 57:4739–4745

    Article  CAS  Google Scholar 

  27. 27.

    Aguilar B, Rojas JC, Collados MT (2004) Metabolism of homocysteine and its relationship with cardiovascular disease. J Thromb Thrombolys 18:75–87

    Article  CAS  Google Scholar 

  28. 28.

    Jacob K, Periago MJ, Böhm V, Berruezo GR (2008) Influence of lycopene and vitamin C from tomato juice on biomarkers of oxidative stress and inflammation. Br J Nutr 99:137–146

    Article  CAS  Google Scholar 

  29. 29.

    Castelli WP (1988) Cholesterol and lipids in the risk of coronary artery disease. The Framingham Heart Study. Can J Cardiol 4(Suppl A):5A–10A

    Google Scholar 

  30. 30.

    Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Method Enzymol 52:302–310

    Article  CAS  Google Scholar 

  31. 31.

    Nourooz-Zadeh J, Tajaddini-Sarmadi J, Wolf SP (1994) Measurement of plasma hydroperoxide concentrations by the ferrous oxidation-xylenol orange assay in conjunction with triphenilphosphine. Anal Biochem 220:403–409

    Article  CAS  Google Scholar 

  32. 32.

    Miller NJ, Sampson J, Candeias LP, Bramley PM, Rice-Evans CA (1996) Antioxidant activities of carotenes and xanthophylls. Fed Eur Biochem Soc Lett 384:240–242

    Article  CAS  Google Scholar 

  33. 33.

    Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76

    Article  CAS  Google Scholar 

  34. 34.

    Esteve MJ, Farré R, Frígola A, López JC, Romera JM, Ramírez M, Gil A (1995) Comparison of voltammetric and high performance liquid chromatographic methods for ascorbic acid determination in infant formulas. Food Chem 52:99–102

    Article  CAS  Google Scholar 

  35. 35.

    MacCrehan WA (1990) Determination of retinol, α-tocopherol and β-carotene in serum by liquid chromatography. Method Enzymol 189:172–181

    Article  CAS  Google Scholar 

  36. 36.

    Baró L, Fonollá J, Peña JL, Martínez-Férez A, Lucena A, Jiménez J, Boza JJ, López-Huertas E (2003) n-3 fatty acids plus oleic acid and vitamin supplemented milk consumption reduces total and LDL cholesterol, homocysteine and levels of endothelial adhesion molecules in healthy humans. Clin Nutr 22:175–182

    Article  Google Scholar 

  37. 37.

    Carrero JJ, Fonollá J, Mart JL, Jimenez J, Boza JJ, Lopez-Huertas E (2007) Intake of fish oil, oleic acid, folic acid, and vitamins B-6 and E for 1 year decreases plasma-C-reactive protein and reduces coronary heart disease risk factors in male patients in a cardiac rehabilitation program. J Nutr 137:384–390

    CAS  Google Scholar 

  38. 38.

    Benito P, Caballero J, Moreno J, Gutiérrez-Alcántara C, Muñoz C, Rojo G, Garcia S, Soriguer FC (2006) Effects of milk enriched with ω-3 fatty acid, oleic acid and folic acid in patients with metabolic syndrome. Clin Nutr 25:581–587

    Article  CAS  Google Scholar 

  39. 39.

    Raghu B, Venkatesan P (2008) Effect of n-3 fatty acid supplementation on blood glucose, lipid profile and cytokines in humans: a pilot study. Ind J Clin Biochem 23:85–88

    Article  CAS  Google Scholar 

  40. 40.

    Fuhrman B, Elis A, Aviram M (1997) Hypocholesterolemic effect of lycopene and β-carotene is related to suppression of cholesterol synthesis and augmentation of LDL receptor activity in macrophages. Biochem Bioph Res Co 233(3):658–662

    Article  CAS  Google Scholar 

  41. 41.

    Schmidt EB, Lervang HH, Varming K, Madsen P, Dyeberg J (1992) Lon-term supplementation with n-3 fatty acids, I: effect on blood lipids, haemostasis and blood pressure. Scand J Clin Lab Inv 52:221–228

    Article  CAS  Google Scholar 

  42. 42.

    Ridker P (2003) Expert opinions: clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 107:363–369

    Article  Google Scholar 

  43. 43.

    López-García E, Schulze MB, Manson JE, Meigs JB, Albert CM, Rifai N, Willett WC, Hu FB (2004) Consumption of (n-3) fatty acids is related to plasma biomarkers of inflammation and endothelial activation in women. J Nutr 134:1086–1811

    Google Scholar 

  44. 44.

    Shen YC, Chen SL, Wang CK (2007) Contribution of tomato phenolics to antioxidation and down-regulation of blood lipids. J Agric Food Chem 55:6475–6481

    Article  CAS  Google Scholar 

  45. 45.

    Thorlaksdottir AY, Skuladottir GV, Petursdottir AL, Tryggvadottir L, Ogmundsdottir HM, Eyfjord JE, Jonsson JJ, Hardardottir I (2006) Positive association between plasma antioxidant capacity and n-3 PUFA in red blood cells from women. Lipids 41:119–126

    Article  CAS  Google Scholar 

  46. 46.

    Erdogan H, Fadillioglu E, Ozgocmen S, Sogut S, Ozyurt B, Akyol O, Ardicoglu O (2004) Effect of fish oil supplementation on plasma oxidant/antioxidant status in rats. Prostag Leukotr Ess 71:149–152

    Article  CAS  Google Scholar 

  47. 47.

    Clarke R, Armitage J (2000) Vitamin supplements and cardiovascular risk: review of the randomized trials of homocysteine-lowering vitamin supplements. Semin Thromb Hemost 26:341–348

    Article  CAS  Google Scholar 

  48. 48.

    Stanger O, Semmelrock HJ, Wonisch W, Bös U, Pabst E, Wascher TC (2002) Effects of folate treatment and homocysteine lowering on resistance vessel reactivity in atherosclerotic subjects. J Pharmacol Exp Ther 303:158–162

    Article  CAS  Google Scholar 

  49. 49.

    Ueland PM, Refsum H, Beresford SA, Wollset SE (2000) The controversy over homocysteine and cardiovascular risk. Am J Clin Nutr 72:324–332

    CAS  Google Scholar 

  50. 50.

    Ford ES, Smith SJ, Stroup DF, Steinberg KK, Mueller PW, Thacker SB (2002) Homocysteine and cardiovascular disease: a systematic review of the evidence with special emphasis on case control studies. Int J Epidemiol 31:59–70

    Article  Google Scholar 

  51. 51.

    Huang T, Wahlqvist ML, Li D (2010) Docosahexaenoic acid decreases plasma homocysteine via regulating enzyme activity and nRNA expression involved in methionine metabolism. Nutrition 26:112–119

    Article  CAS  Google Scholar 

  52. 52.

    Grundt H, Nilsen DWT, Mansoor MA, Hetland O, Nordoy A (2003) Reduction in homocysteine by n-3 polyunsaturated fatty acids after 1 year in a randomized double-blind study following an acute myocardial infarction: no effect on endothelial adhesion properties. Pathophysiol Haemost Thromb 33:88–95

    Article  CAS  Google Scholar 

  53. 53.

    Chi Z, Melendez AJ (2007) Role of cell adhesion molecules and immune-cell migration in the initiation, onset and development of atherosclerosis. Cell Adh Migr 1:171–175

    Article  Google Scholar 

  54. 54.

    Miles EA, Thies F, Wallace FA, Powell JR, Hurst TL, Newsholme EA, Calder PC (2001) Influence of age and dietary fish oil on plasma soluble adhesion molecule concentrations. Clin Sci (Lond) 100:91–100

    Article  CAS  Google Scholar 

  55. 55.

    Liu X, Qu D, He F, Lu Q, Wang J, Cai D (2007) Effect of lycopene on the vascular endothelial function and expression of inflammatory agents in hyperhomocysteinemic rats. Asia Pac J Clin Nutr 16:244–248

    CAS  Google Scholar 

  56. 56.

    Blum A, Moni M, Khazim K, Peleg A, Blum N (2007) Tomato-rich (Mediterranean) diet does not modify inflammatory markers. Clin Invest Med 30(2):E70–E74

    CAS  Google Scholar 

  57. 57.

    Upchurch GR, Welch GN, Fabian AJ, Freedman JE, Johnson JL, Keaney JF Jr, Loscalzo J (1997) Homocysteine decreases bioavailable nitric oxide by a mechanism involving glutathione peroxidase. J Biol Chem 272:17012–17017

    Article  CAS  Google Scholar 

  58. 58.

    Mestas J, Ley K (2008) Monocyte-endothelial cell interactions in the development of atherosclerosis. Trends Cardiovasc Med 18:228–232

    Article  CAS  Google Scholar 

  59. 59.

    Rizzo M, Kotur-Stevuljevic J, Berneis K, Spinas G, Rini BG, Jelic-Ivanovic Z, Spasojevic-Kalimanovska V, Vekic J (2009) Atherogenic dyslipidemia and oxidative stress: a new look. Transl Res 153:217–223

    Article  CAS  Google Scholar 

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Acknowledgments

We thank to Hero España S.A. and Denomega Nutritional Oil for providing the samples and ingredients of this study. The authors are grateful to the Ministry of Education and Science of the Spanish Government for the project AGL 2006-26965-E, and to the Fundación Seneca of the Murcia Regional Government for the project 05774/PI/07.

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Correspondence to M. J. Periago.

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García-Alonso, F.J., Jorge-Vidal, V., Ros, G. et al. Effect of consumption of tomato juice enriched with n-3 polyunsaturated fatty acids on the lipid profile, antioxidant biomarker status, and cardiovascular disease risk in healthy women. Eur J Nutr 51, 415–424 (2012). https://doi.org/10.1007/s00394-011-0225-0

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Keywords

  • Cardiovascular diseases (CVD)
  • PUFAs
  • Tomato juice
  • Antioxidants
  • Homocysteine
  • Lipid oxidation
  • VCAM-1
  • ICAM-1