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Dietary antioxidant capacity is associated with improved serum antioxidant status and decreased serum C-reactive protein and plasma homocysteine concentrations

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Abstract

Purpose

To investigate the associations of dietary TAC from diet and supplements with serum antioxidant concentrations and serum C-reactive protein (CRP) and plasma total homocysteine (tHcy) in US adults.

Methods

This was a cross-sectional study. Food consumption data, serum antioxidant levels, and serum CRP and Plasma tHcy concentrations of 4,391 US adults aged ≥19 years in the National Health and Nutrition Examination Survey 2001–2002 were analyzed. The USDA flavonoid and proanthocyanidin databases and dietary supplement data as well as antioxidant capacities of 43 antioxidants were also utilized.

Result

Serum CRP and plasma tHcy concentrations were higher in older adults, smokers, and those with lower non-leisure time physical activity levels (P < 0.05). Energy-adjusted daily total antioxidant capacity (TAC) from diet and supplements was positively associated with serum vitamin E and carotenoid concentrations (P < 0.05). Adjusted odds ratio (OR) for plasma tHcy >13 μmol/L significantly decreased across quartiles of TAC from diet and supplements (Q1 = 2.18 (1.56–2.77); Q2 = 1.30 (1.00–2.07); Q3 = 1.34 (0.84–2.28); Q4 = 1.00; P for linear trend <0.001). A negative trend across quartiles of TAC from diet and supplements was also observed in OR for serum CRP ≥3 mg/L (Q1 = 1.26 (0.97–1.70); Q2 = 1.21 (0.91–1.66); Q3 = 0.97 (0.80–1.24); Q4 = 1.00; P for linear trend <0.05).

Conclusions

These findings indicated that dietary TAC provided an integrated conceptual tool in assessing serum antioxidants and investigating the associations between antioxidant intake and CVD risk. The implicated applicability of dietary TAC needs further validation in prospective cohort studies.

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References

  1. Genkinger JM, Platz EA, Hoffman SC, Comstock GW, Helzlsouer KJ (2004) Fruit, vegetable, and antioxidant intake and all-cause, cancer, and cardiovascular disease mortality in a community-dwelling population in Washington County, Maryland. Am J Epidemiol 160:1223–1233

    Article  Google Scholar 

  2. Heidemann C, Schulze MB, Franco OH, van Dam RM, Mantzoros CS, Hu FB (2008) Dietary patterns and risk of mortality from cardiovascular disease, cancer, and all causes in a prospective cohort of women. Circulation 118:230–237

    Article  Google Scholar 

  3. Oude Griep LM, Verschuren WM, Kromhout D, Ocke MC, Geleijnse JM (2011) Raw and processed fruit and vegetable consumption and 10-year stroke incidence in a population-based cohort study in the Netherlands. Eur J Clin Nutr 65:791–799

    Article  CAS  Google Scholar 

  4. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G et al (2010) Heart disease and stroke statistics-- 2010 update: a report from the American Heart Association. Circulation 121:e46–e215

    Google Scholar 

  5. Singh U, Devaraj S, Jialal I (2005) Vitamin E, oxidative stress, and inflammation. Annu Rev Nutr 25:151–174

    Article  CAS  Google Scholar 

  6. Pepys MB, Hirschfield GM (2003) C-reactive protein: a critical update. J Clin Invest 111:1805–1812

    CAS  Google Scholar 

  7. Nygard O, Vollset SE, Refsum H, Brattstrom L, Ueland PM (1999) Total homocysteine and cardiovascular disease. J Intern Med 246:425–454

    Article  CAS  Google Scholar 

  8. Ridker PM (2005) C-reactive protein, inflammation, and cardiovascular disease: clinical update. Tex Heart Inst J 32:384–386

    Google Scholar 

  9. Suliman ME, Stenvinkel P, Baranyi P, Heimburger O, Anderstam B, Lindholm B (2003) Hyperhomocysteinemia and its relationship to cardiovascular disease in ESRD: influence of hypoalbuminemia, malnutrition, inflammation, and diabetes mellitus. Am J Kidney Dis 41:S89–S95

    Article  CAS  Google Scholar 

  10. Kaptoge S, Di Angelantonio E, Lowe G, Pepys MB, Thompson SG, Collins R, Danesh J (2010) C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet 375:132–140

    Article  Google Scholar 

  11. de Ferranti SD, Rifai N (2007) C-reactive protein: a nontraditional serum marker of cardiovascular risk. Cardiovasc Pathol 16:14–21

    Article  Google Scholar 

  12. van’t Veer P, Jansen MC, Klerk M, Kok FJ (2000) Fruits and vegetables in the prevention of cancer and cardiovascular disease. Public Health Nutr 3:103–107

    Google Scholar 

  13. Hermsdorff HH, Zulet MA, Puchau B, Martinez JA (2010) Fruit and vegetable consumption and proinflammatory gene expression from peripheral blood mononuclear cells in young adults: a translational study. Nutr Metab (Lond) 7:42

    Article  Google Scholar 

  14. Pellegrini N, Salvatore S, Valtuena S, Bedogni G, Porrini M, Pala V, Del Rio D, Sieri S, Miglio C, Krogh V, Zavaroni I, Brighenti F (2007) Development and validation of a food frequency questionnaire for the assessment of dietary total antioxidant capacity. J Nutr 137:93–98

    CAS  Google Scholar 

  15. Martin K, Wu D, Meydani M (2000) The effect of carotenoids on the expression of cell surface adhesion molecules and binding of monocytes to human aortic endothelial cells. Atherosclerosis 150:265–274

    Article  CAS  Google Scholar 

  16. Kaur G, Rao LV, Agrawal A, Pendurthi UR (2007) Effect of wine phenolics on cytokine-induced C-reactive protein expression. J Thromb Haemost 5:1309–1317

    Article  CAS  Google Scholar 

  17. Libinaki R, Tesanovic S, Heal A, Nikolovski B, Vinh A, Widdop RE, Gaspari TA, Devaraj S, Ogru E (2010) Effect of tocopheryl phosphate on key biomarkers of inflammation: implication in the reduction of atherosclerosis progression in a hypercholesterolaemic rabbit model. Clin Exp Pharmacol Physiol 37:587–592

    Article  CAS  Google Scholar 

  18. El-Mowafy AM, El-Mesery ME, Salem HA, Al-Gayyar MM, Darweish MM (2010) Prominent chemopreventive and chemoenhancing effects for resveratrol: unraveling molecular targets and the role of C-reactive protein. Chemotherapy 56:60–65

    Article  CAS  Google Scholar 

  19. Suzuki K, Inoue T, Hashimoto S, Ochiai J, Kusuhara Y, Ito Y, Hamajima N (2010) Association of serum carotenoids with high molecular weight adiponectin and inflammation markers among Japanese subjects. Clin Chim Acta 411:1330–1334

    Article  CAS  Google Scholar 

  20. Scheurig AC, Thorand B, Fischer B, Heier M, Koenig W (2008) Association between the intake of vitamins and trace elements from supplements and C-reactive protein: results of the MONICA/KORA Augsburg study. Eur J Clin Nutr 62:127–137

    Article  CAS  Google Scholar 

  21. Vivekananthan D, Penn M, Sapp S, Hsu A, Topol E (2003) Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials. Lancet 361:2017–2023

    Article  CAS  Google Scholar 

  22. Kushi LH, Folsom AR, Prineas RJ, Mink PJ, Wu Y, Bostick RM (1996) Dietary antioxidant vitamins and death from coronary heart disease in postmenopausal women. N Engl J Med 334:1156–1162

    Article  CAS  Google Scholar 

  23. Serafini M, Del Rio D (2004) Understanding the association between dietary antioxidants, redox status and disease: is the total antioxidant capacity the right tool? Redox Rep 9:145–152

    Article  CAS  Google Scholar 

  24. Brighenti F, Valtuena S, Pellegrini N, Ardigo D, Del Rio D, Salvatore S, Piatti P, Serafini M, Zavaroni I (2005) Total antioxidant capacity of the diet is inversely and independently related to plasma concentration of high-sensitivity C-reactive protein in adult Italian subjects. Br J Nutr 93:619–625

    Article  CAS  Google Scholar 

  25. Yang M, Chung S-J, Chung C, Kim D-O, Song WO, Koo SI, Chun OK (2010) Estimation of total antioxidant capacity from diet and supplements in U.S. adults. Br J Nutr 106:254–263

    Article  Google Scholar 

  26. National Center for Health Statistics (2004) National Health and Nutrition Examination Survey, 2001-2002 Data Files. Hyattsville, MD: Centers for Disease Control. http://www.cdc.gov/nchs/nhanes/nhanes2001-2002/nhanes01_02.htm. Accessed by May, 2004

  27. Botman S, Moore T, Moriarity C, Parsons V (2000) Design and estimation for the national health interview survey, 1995-2004. National Center for Health Statistics. Vital Health Stat 2(130). http://www.cdc.gov/nchs/data/series/sr_02/sr02_130.pdf

  28. National Center for Health Statistics (2004) General information about the NHANES 2001-2002, laboratory methodology and public data files. Hyattsville, MD: Centers for Disease Control. http://www.cdc.gov/nchs/data/nhanes/nhanes_01_02/l36_b_doc.pdf. Accessed May, 2004

  29. Chun OK, Floegel A, Chung S-J, Chung C, Song WO, Koo SI (2010) Estimation of antioxidant intakes from diet and supplements in U.S. adults. J Nutr 140:317–324

    Article  CAS  Google Scholar 

  30. Agricultural Research Service, US Department of Agriculture (2003) Database for the flavonoid content of selected foods. Agricultural Research Service, Beltsville. http://www.nal.usda.gov/fnic/foodcomp/Data/Flav/flav.pdf. Accessed March, 2003

  31. Agricultural Research Service, US Department of Agriculture (2002) USDA-Iowa State University database on the isoflavone content of foods, release 1.3. Agricultural Research Service, Beltsville. http://www.nal.usda.gov/fnic/foodcomp/Data/isoflav/isoflav.html. Accessed 2002

  32. Agricultural Research Service, US Department of Agriculture (2004) Database for the Proanthocyanidin Content of Selected Foods. Agricultural Research Service, Beltsville. http://www.nal.usda.gov/fnic/foodcomp/Data/PA/PA.html. Accessed 2004

  33. Floegel A, Kim D-O, Chung SJ, Song WO, Fernandez ML, Bruno RS, Koo SI, Chun OK (2010) Development and validation of an algorithm to establish a total antioxidant capacity database of the US diet. Int J Food Sci Nutr 61:600–623

    Article  CAS  Google Scholar 

  34. Kim D-O, Chun OK, Kim YJ, Moon HY, Lee CY (2003) Quantification of polyphenolics and their antioxidant capacity in fresh plums. J Agric Food Chem 51:6509–6515

    Article  CAS  Google Scholar 

  35. Kim D-O, Lee KW, Lee HJ, Lee CY (2002) Vitamin C equivalent antioxidant capacity (VCEAC) of phenolic phytochemicals. J Agric Food Chem 50:3713–3717

    Article  CAS  Google Scholar 

  36. Chun OK, Kim D-O, Smith N, Schroeder D, Han JT, Lee CY (2005) Daily consumption of phenolics and total antioxidant capacity from fruits and vegetables in the American diet. J Sci Food Agric 85:1715–1724

    Article  CAS  Google Scholar 

  37. Blake GJ, Rifai N, Buring JE, Ridker PM (2003) Blood pressure, C-reactive protein, and risk of future cardiovascular events: a prospective study among 15,215 women. Circulation 108:2993–2999

    Article  CAS  Google Scholar 

  38. de Luis DA, Fernandez N, Arranz ML, Aller R, Izaola O, Romero E (2005) Total homocysteine levels relation with chronic complications of diabetes, body composition, and other cardiovascular risk factors in a population of patients with diabetes mellitus type 2. J Diabetes Complicat 19:42–46

    Article  Google Scholar 

  39. Detopoulou P, Panagiotakos DB, Chrysohoou C, Fragopoulou E, Nomikos T, Antonopoulou S, Pitsavos C, Stefanadis C (2010) Dietary antioxidant capacity and concentration of adiponectin in apparently healthy adults: the ATTICA study. Eur J Clin Nutr 64:161–168

    Article  CAS  Google Scholar 

  40. Puchau B, Zulet MA, de Echavarri AG, Hermsdorff HHM, Martinez JA (2010) Dietary total antioxidant capacity is negatively associated with some metabolic syndrome features in healthy young adults. Nutrition 26:534–541

    Article  CAS  Google Scholar 

  41. Kim D-O, Lee CY (2004) Comprehensive study on vitamin C equivalent antioxidant capacity (VCEAC) of various polyphenolics in scavenging a free radical and its structural relationship. Crit Rev Food Sci Nutr 44:253–273

    Article  CAS  Google Scholar 

  42. Wang Y, Yang M, Lee SG, Davis CG, Kenny A, Koo SI, Chun OK (2012) Plasma total antioxidant capacity is associated with dietary intake and plasma level of antioxidants in postmenopausal women. J Nutr Biochem 23:1725–1731

    Google Scholar 

  43. Wang Y, Yang M, Lee SG, Davis CG, Masterjohn C, Kenny A, Bruno R, Chun OK (2010) Total antioxidant capacity: a useful tool in assessing antioxidant intake status. In: Diederich M (ed) Natural compounds and apoptosis. Springer, New York

    Google Scholar 

  44. Valtuena S, Del Rio D, Pellegrini N, Ardigo D, Franzini L, Salvatore S, Piatti PM, Riso P, Zavaroni I, Brighenti F (2007) The total antioxidant capacity of the diet is an independent predictor of plasma beta-carotene. Eur J Clin Nutr 61:69–76

    Article  CAS  Google Scholar 

  45. Puchau B, Zulet MA, de Echavarri AG, Hermsdorff HH, Martinez JA (2009) Dietary total antioxidant capacity: a novel indicator of diet quality in healthy young adults. J Am Coll Nutr 28:648–656

    Article  Google Scholar 

  46. Jansen MC, Van Kappel AL, Ocke MC, Van’t Veer P, Boshuizen HC, Riboli E, Bueno-de-Mesquita HB (2004) Plasma carotenoid levels in Dutch men and women, and the relation with vegetable and fruit consumption. Eur J Clin Nutr 58:1386–1395

    Article  CAS  Google Scholar 

  47. Baldrick FR, Woodside JV, Elborn JS, Young IS, McKinley MC (2011) Biomarkers of fruit and vegetable intake in human intervention studies: a systematic review. Crit Rev Food Sci Nutr 51:795–815

    Article  CAS  Google Scholar 

  48. Del Rio D, Valtuena S, Pellegrini N, Bianchi MA, Ardigo D, Franzini L, Scazzina F, Monti L, Zavaroni I, Brighenti F (2009) Intervention study with a high or low antioxidant capacity diet: effects on circulating beta-carotene. Eur J Clin Nutr 63:1220–1225

    Article  Google Scholar 

  49. McNaughton SA, Marks GC, Gaffney P, Williams G, Green A (2005) Validation of a food-frequency questionnaire assessment of carotenoid and vitamin E intake using weighed food records and plasma biomarkers: the method of triads model. Eur J Clin Nutr 59:211–218

    Article  CAS  Google Scholar 

  50. Dixon LB, Subar AF, Wideroff L, Thompson FE, Kahle LL, Potischman N (2006) Carotenoid and tocopherol estimates from the NCI diet history questionnaire are valid compared with multiple recalls and serum biomarkers. J Nutr 136:3054–3061

    CAS  Google Scholar 

  51. Satia JA, Watters JL, Galanko JA (2009) Validation of an antioxidant nutrient questionnaire in whites and African Americans. J Am Diet Assoc 109:502–508

    Article  Google Scholar 

  52. Yang M, Wang Y, Davis CG, Lee SG, Fernandez ML, Koo SI, Cho E, Song WO, Chun OK (2012) Validation of an FFQ to assess short-term antioxidant intake against 30d food records and plasma biomarkers. Public Health Nutr. doi:10.1017/S1368980012005071

  53. Wang Y, Yang M, Lee SG, Davis CG, Koo SI, Chun OK (2012) Dietary total antioxidant capacity is associated with diet and plasma antioxidant status in healthy young adults. J Acad Nutr Diet 112:1626–1635

    Article  CAS  Google Scholar 

  54. Carr AC, Zhu BZ, Frei B (2000) Potential antiatherogenic mechanisms of ascorbate (vitamin C) and alpha-tocopherol (vitamin E). Circ Res 87:349–354

    Article  CAS  Google Scholar 

  55. Berliner JA, Heinecke JW (1996) The role of oxidized lipoproteins in atherogenesis. Free Radic Biol Med 20:707–727

    Article  CAS  Google Scholar 

  56. Rimm EB, Stampfer MJ, Ascherio A, Giovannucci E, Colditz GA, Willett WC (1993) Vitamin E consumption and the risk of coronary heart disease in men. N Engl J Med 328:1450–1456

    Article  CAS  Google Scholar 

  57. Stampfer MJ, Hennekens CH, Manson JE, Colditz GA, Rosner B, Willett WC (1993) Vitamin E consumption and the risk of coronary disease in women. N Engl J Med 328:1444–1449

    Article  CAS  Google Scholar 

  58. van Herpen-Broekmans WMR, Klopping-Ketelaars IAA, Bots ML, Kluft C, Princen H, Hendriks HFJ, Tijburg LBM, van Poppel G, Kardinaal AFM (2004) Serum carotenoids and vitamins in relation to markers of endothelial function and inflammation. Eur J Epidemiol 19:915–921

    Article  Google Scholar 

  59. Ito Y, Kurata M, Suzuki K, Hamajima N, Hishida H, Aoki K (2006) Cardiovascular disease mortality and serum carotenoid concentrations: a Japanese population-based follow-up study. J Epidemiol 16:154–160

    Article  Google Scholar 

  60. Rissanen TH, Voutilainen S, Nyyssonen K, Lakka TA, Sivenius J, Salonen R, Kaplan GA, Salonen JT (2001) Low serum lycopene concentration is associated with an excess incidence of acute coronary events and stroke: the Kuopio Ischaemic Heart Disease Risk Factor Study. Brit J Nutr 85:749–754

    Article  CAS  Google Scholar 

  61. Dalgård C, Nielsen F, Morrow J, Enghusen-Poulsen H, Jonung T, Hørder M, de Maat M (2009) Supplementation with orange and blackcurrant juice, but not vitamin E, improves inflammatory markers in patients with peripheral arterial disease. Br J Nutr 101:263–269

    Article  Google Scholar 

  62. Lee IM, Cook NR, Gaziano JM, Gordon D, Ridker PM, Manson JE, Hennekens CH, Buring JE (2005) Vitamin E in the primary prevention of cardiovascular disease and cancer: the Women’s Health Study: a randomized controlled trial. JAMA 294:56–65

    Article  CAS  Google Scholar 

  63. Redberg RF (2005) Vitamin E and cardiovascular health: does sex matter? JAMA 294:107–109

    Article  CAS  Google Scholar 

  64. Sesso HD, Buring JE, Christen WG, Kurth T, Belanger C, MacFadyen J, Bubes V, Manson JE, Glynn RJ, Gaziano JM (2008) Vitamins E and C in the prevention of cardiovascular disease in men: the Physicians’ Health Study II randomized controlled trial. JAMA 300:2123–2133

    Article  CAS  Google Scholar 

  65. Miller ER III, Pastor-Barriuso R, Dalal D, Riemersma RA, Appel LJ, Guallar E (2005) Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 142:37–46

    Article  CAS  Google Scholar 

  66. Omenn GS, Goodman GE, Thornquist MD, Balmes J, Cullen MR, Glass A, Keogh JP, Meyskens FL, Valanis B, Williams JH, Barnhart S, Hammar S (1996) Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. N Engl J Med 334:1150–1155

    Article  CAS  Google Scholar 

  67. Cummings DM, King DE, Mainous AG, Geesey ME (2006) Combining serum biomarkers: the association of C-reactive protein, insulin sensitivity, and homocysteine with cardiovascular disease history in the general US population. Eur J Cardiovasc Prev Rehabil 13:180–185

    Article  Google Scholar 

  68. Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L, Hu FB, Willett WC (2007) Dietary patterns and markers of systemic inflammation among Iranian women. J Nutr 137:992–998

    CAS  Google Scholar 

  69. Ford ES, Liu S, Mannino DM, Giles WH, Smith SJ (2003) C-reactive protein concentration and concentrations of blood vitamins, carotenoids, and selenium among United States adults. Eur J Clin Nutr 57:1157–1163

    Article  CAS  Google Scholar 

  70. Bertran N, Camps J, Fernandez-Ballart J, Arija V, Ferre N, Tous M, Simo D, Murphy MM, Vilella E, Joven J (2005) Diet and lifestyle are associated with serum C-reactive protein concentrations in a population-based study. J Lab Clin Med 145:41–46

    Article  CAS  Google Scholar 

  71. Block G, Jensen C, Dietrich M, Norkus EP, Hudes M, Packer L (2004) Plasma C-reactive protein concentrations in active and passive smokers: influence of antioxidant supplementation. J Am Coll Nutr 23:141–147

    Article  CAS  Google Scholar 

  72. Nanri A, Moore MA, Kono S (2007) Impact of C-reactive protein on disease risk and its relation to dietary factors. Asian Pac J Cancer Prev 8:167–177

    Google Scholar 

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Acknowledgments

This research was fully funded by the Beginning Grant in Aid No. 0865092E from the American Heart Association. This article was partially presented at the 2010 Experimental Biology Meeting, Anaheim, CA, in April 2010.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Nutritional Sciences, University of Connecticut, 3624 Horsebarn Road Extension Unit 4017, Storrs, CT, 06269-4017, USA

    Meng Yang, Sung I. Koo & Ock K. Chun

  2. Department of Foods and Nutrition, Kookmin University, Seoul, 136-702, Korea

    Sang-Jin Chung

  3. Department of Epidemiology, German Institute of Human Nutrition, Potsdam-Rehbruecke, 14558, Nuthetal, Germany

    Anna Floegel

  4. Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI, 48824, USA

    Won O. Song

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  1. Meng Yang
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Yang, M., Chung, SJ., Floegel, A. et al. Dietary antioxidant capacity is associated with improved serum antioxidant status and decreased serum C-reactive protein and plasma homocysteine concentrations. Eur J Nutr 52, 1901–1911 (2013). https://doi.org/10.1007/s00394-012-0491-5

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