NOTICE: We are experiencing technical issues with Academy members trying to log into the JAND site using Academy member login credentials. We are working to resolve the issue as soon as possible. Alternatively, if you are an Academy member, you can access the JAND site by registering for an Elsevier account and claiming access using the links at the top of the JAND site. Email us at [email protected] for assistance. Thanks for your patience!

Self-Report of Fruit and Vegetable Intake that Meets the 5 A Day Recommendation Is Associated with Reduced Levels of Oxidative Stress Biomarkers and Increased Levels of Antioxidant Defense in Premenopausal Women

Published:March 19, 2013DOI:https://doi.org/10.1016/j.jand.2013.01.019

      Abstract

      Background

      Oxidative stress has been associated with a variety of chronic diseases and reproductive disorders. Fruits and vegetables (F/V) may contribute to antioxidant vitamin and micronutrient levels and reduce oxidative stress.

      Objective

      To investigate the effect of meeting the 5 A Day For Better Health Program recommendation for F/V consumption on biomarkers of oxidative damage and antioxidant defense.

      Design

      In this longitudinal study, healthy premenopausal women (n=258) were followed for ≤2 menstrual cycles with ≤16 oxidative stress measures timed to cycle phase.

      Main outcome measures

      Plasma concentrations of F2-isoprostane, 9-hydroxyoctadecadieneoic acid, 13-hydroxyoctadecadieneoic acid, erythrocyte activity of superoxide dismutase, glutathione reductase, and glutathione peroxidase, as well as blood micronutrient concentrations were measured. Dietary intake was assessed by food frequency questionnaires (FFQs) (1 per cycle), and 24-hour recalls (≤4 per cycle).

      Statistical analyses performed

      Fruit and vegetable servings were dichotomized based on the recommendation to consume five servings of F/V each day. Linear mixed models with repeated measures were used to analyze lipid peroxidation markers, antioxidant vitamins, and antioxidant enzymes by cycle phase and in association with usual F/V intake.

      Results

      For both 24-hour recall (timed to cycle phase) and cycle-specific FFQ, meeting the recommendation to consume five servings of F/V each day was associated with decreased F2-isoprostanes (24-hour recall β=−.10 [95% CI, −0.12 to −0.07]; FFQ β= −.14 [95% CI, −0.18 to −0.11]). Glutathione reductase was lower in association with typical consumption of five or more servings of F/V by FFQ but not in the phase-specific analysis. Higher levels of ascorbic acid, lutein, beta carotene, and beta cryptoxanthin were observed with both intake measures.

      Conclusions

      Meeting the 5 A Day For Better Health Program recommendation was associated with lower oxidative stress and improved antioxidant status in analyses of typical diet (via FFQ) and in menstrual cycle phase-specific analyses using 24-hour recalls. Green salads were commonly eaten and increasing intake of salads may be a useful strategy to influence oxidation in reproductive aged women.

      Keywords

      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 Journal of the Academy of Nutrition and Dietetics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Sies H.
        • Stahl W.
        • Sevanian A.
        Nutritional, dietary and postprandial oxidative stress.
        J Nutr. 2005; 135: 969-972
        • Rayman M.P.
        The importance of selenium to human health.
        Lancet. 2000; 356: 233-241
        • Murray A.A.
        • Molinek M.D.
        • Baker S.J.
        • et al.
        Role of ascorbic acid in promoting follicle integrity and survival in intact mouse ovarian follicles in vitro.
        Reproduction. 2001; 121: 89-96
        • Murphy A.A.
        • Santanam N.
        • Parthasarathy S.
        Endometriosis: A disease of oxidative stress?.
        Semin Reprod Endocr. 1998; 16: 263-273
        • Samborskaia E.
        • Ferdman T.
        Mechanism of abortion induced by ascorbic acid.
        Biull Eksp Biolol Med. 1966; 62: 96-98
        • Jenkins C.
        • Wilson R.
        • Roberts J.
        • Miller H.
        • McKillop J.H.
        • Walker J.J.
        Antioxidants: Their role in pregnancy and miscarriage.
        Antioxid Redox Sign. 2000; 2: 623-628
        • Kim Y.J.
        • Hong Y.C.
        • Lee K.H.
        • et al.
        Oxidative stress in pregnant women and birth weight reduction.
        Reprod Toxicol. 2005; 19: 487-492
        • Halliwell B.
        • Chirico S.
        Lipid peroxidation: Its mechanism, measurement, and significance.
        Am J Clin Nutr. 1993; 57: 715S-724S
        • Epplein M.
        • Franke A.A.
        • Cooney R.V.
        • et al.
        Association of plasma micronutrient levels and urinary isoprostane with risk of lung cancer: The multiethnic cohort study.
        Cancer Epidemiol Biomarkers Prev. 2009; 18: 1962-1970
        • Polidori M.C.
        • Pratico D.
        • Parente B.
        • et al.
        Elevated lipid peroxidation biomarkers and low antioxidant status in atherosclerotic patients with increased carotid or iliofemoral intima media thickness.
        J Investig Med. 2007; 55: 163-167
        • Brevik A.
        • Gaivao I.
        • Medin T.
        • et al.
        Supplementation of a western diet with golden kiwifruits (Actinidia chinensis var. 'Hort 16A'): Effects on biomarkers of oxidation damage and antioxidant protection.
        Nutr J. 2011; 10: 54
        • Fowke J.H.
        • Morrow J.D.
        • Motley S.
        • Bostick R.M.
        • Ness R.M.
        Brassica vegetable consumption reduces urinary F2-isoprostane levels independent of micronutrient intake.
        Carcinogenesis. 2006; 27: 2096-2102
        • Visioli F.
        • Riso P.
        • Grande S.
        • Galli C.
        • Porrini M.
        Protective activity of tomato products on in vivo markers of lipid oxidation.
        Eur J Nutr. 2003; 42: 201-206
        • Thompson H.J.
        • Heimendinger J.
        • Sedlacek S.
        • et al.
        8-Isoprostane F2alpha excretion is reduced in women by increased vegetable and fruit intake.
        Am J Clin Nutr. 2005; 82: 768-776
        • Thompson H.J.
        • Heimendinger J.
        • Haegele A.
        • et al.
        Effect of increased vegetable and fruit consumption on markers of oxidative cellular damage.
        Carcinogenesis. 1999; 20: 2261-2266
        • Sanchez-Moreno C.
        • Cano M.P.
        • de Ancos B.
        • et al.
        Mediterranean vegetable soup consumption increases plasma vitamin C and decreases F2-isoprostanes, prostaglandin E2 and monocyte chemotactic protein-1 in healthy humans.
        J Nutr Biochem. 2006; 17: 183-189
        • Miller 3rd, E.R.
        • Erlinger T.P.
        • Sacks F.M.
        • et al.
        A dietary pattern that lowers oxidative stress increases antibodies to oxidized LDL: Results from a randomized controlled feeding study.
        Atherosclerosis. 2005; 183: 175-182
        • Nelson J.L.
        • Bernstein P.S.
        • Schmidt M.C.
        • Von Tress M.S.
        • Askew E.W.
        Dietary modification and moderate antioxidant supplementation differentially affect serum carotenoids, antioxidant levels and markers of oxidative stress in older humans.
        J Nutr. 2003; 133: 3117-3123
        • Dragsted L.O.
        • Pedersen A.
        • Hermetter A.
        • et al.
        The 6-A-Day study: Effects of fruit and vegetables on markers of oxidative stress and antioxidative defense in healthy nonsmokers.
        Am J Clin Nutr. 2004; 79: 1060-1072
        • Rytter E.
        • Vessby B.
        • Asgard R.
        • et al.
        Supplementation with a combination of antioxidants does not affect glycaemic control, oxidative stress or inflammation in type 2 diabetes subjects.
        Free Radic Res. 2010; 44: 1445-1453
        • Heart Protection Study Collaborative Group
        MRC/BHF Heart Protection Study of antioxidant vitamin supplementation in 20,536 high-risk individuals: A randomised placebo-controlled trial.
        Lancet. 2002; 360: 23-33
        • The Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group
        The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers.
        N Engl J Med. 1994; 330: 1029-1035
        • Omenn G.S.
        • Goodman G.E.
        • Thornquist M.D.
        • et al.
        Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease.
        N Engl J Med. 1996; 334: 1150-1155
        • Greenwald P.
        • Anderson D.
        • Nelson S.A.
        • Taylor P.R.
        Clinical trials of vitamin and mineral supplements for cancer prevention.
        Am J Clin Nutr. 2007; 85: 314S-317S
      1. Nutrition and Your Health: Dietary Guidelines for Americans, 2010. 7th ed. US Government Printing Office, Washington, DC2010
        • National Cancer Institute
        5 A Day for Better Health Program Evaluation Report. Executive Summary.
        (Updated March 1, 2006. Accessed March 6, 2013)
        • Moshfegh A.J.
        • Goldman J.D.
        • Cleveland L.E.
        What We Eat in America, NHANES 2001-2002: Usual Nutrient Intakes from Food Compared to Dietary Reference Intakes.
        US Department of Agriculture, Agricultural Research Service, Washington, DC2005
        • Heimendinger J.
        • Van Duyn M.A.
        • Chapelsky D.
        • Foerster S.
        • Stables G.
        The national 5 A Day for Better Health Program: A large-scale nutrition intervention.
        J Public Health Manag Pract. 1996; 2: 27-35
        • Gaskins A.J.
        • Rovner A.J.
        • Mumford S.L.
        • et al.
        Adherence to a Mediterranean diet and plasma concentrations of lipid peroxidation in premenopausal women.
        Am J Clin Nutr. 2010; 92: 1461-1467
        • Schisterman E.
        • Gaskins A.J.
        • Mumford S.L.
        • et al.
        Influence of endogenous reproductive hormones on F2-isoprostane levels in premenopausal women: The BioCycle Study.
        Am J Epidemiol. 2010; 172: 430-439
        • Wactawski-Wende J.
        • Schisterman E.F.
        • Hovey K.M.
        • et al.
        BioCycle study: Design of the longitudinal study of oxidative stress and hormone variation during the menstrual cycle.
        Paediatr Perinat Epidemiol. 2009; 23: 171-184
        • Howards P.P.
        • Schisterman E.F.
        • Wactawski-Wende J.
        • Reschke J.E.
        • Frazer A.A.
        • Hovey K.M.
        Timing clinic visits to phases of the menstrual cycle by using a fertility monitor: The BioCycle Study.
        Am J Epidemiol. 2009; 169: 105-112
        • Browne R.W.
        • Bloom M.S.
        • Schisterman E.F.
        • et al.
        Analytical and biological variation of F2-isoprostanes during the menstrual cycle.
        Clin Chem. 2009; 55: 1245-1247
        • Schakel S.F.
        Procedures for estimating nutrient values for food composition databases.
        J Food Comp and Anal. 1997; 10: 102-114
        • Thompson F.E.
        • Subar A.F.
        • Smith A.F.
        • et al.
        Fruit and vegetable assessment: Performance of 2 new short instruments and a food frequency questionnaire.
        J Am Diet Assoc. 2002; 102: 1764-1772
        • Milne G.L.
        • Sanchez S.C.
        • Musiek E.S.
        • Morrow J.D.
        Quantification of F2-isoprostanes as a biomarker of oxidative stress.
        Nat Protoc. 2007; 2: 221-226
        • Browne R.W.
        • Bloom M.S.
        • Schisterman E.F.
        • et al.
        Analytical and biological variation of F2-isoprostanes during the menstrual cycle.
        Clin Chem. 2009; 55: 1245-1247
        • Browne R.W.
        • Bloom M.S.
        • Schisterman E.F.
        • et al.
        Analytical and biological variation of biomarkers of oxidative stress during the menstrual cycle.
        Biomarkers. 2008; 13: 160-183
        • Browne R.W.
        • Armstrong D.
        Simultaneous determination of polyunsaturated fatty acids and corresponding monohydroperoxy and monohydroxy peroxidation products by HPLC.
        Methods Mol Biol. 2002; 186: 13-20
        • Browne R.W.
        • Armstrong D.
        Simultaneous determination of serum retinol, tocopherols, and carotenoids by HPLC.
        Methods Mol Biol. 1998; 108: 269-275
        • Chalmers A.H.
        • McWhinney B.C.
        Two spectrophotometric methods compared for measuring low concentrations of ascorbate in plasma and urine.
        Clin Chem. 1986; 32: 1412-1413
        • Pippenger C.E.
        • Browne R.W.
        • Armstrong D.
        Regulatory antioxidant enzymes.
        Methods Mol Biol. 1998; 108: 299-313
        • Craig C.L.
        • Marshall A.L.
        • Sjostrom M.
        • et al.
        International physical activity questionnaire: 12-country reliability and validity.
        Med Sci Sports Exerc. 2003; 35: 1381-1395
        • Holt E.M.
        • Steffen L.M.
        • Moran A.
        • et al.
        Fruit and vegetable consumption and its relation to markers of inflammation and oxidative stress in adolescents.
        J Am Diet Assoc. 2009; 109: 414-421
        • Tomey M.
        • Sowers M.
        • Li X.
        • McConnell D.S.
        • et al.
        Dietary fat subgroups, zinc, and vegetable components are related to urine f2a-isoprostane concentration, a measure of oxidative stress, in midlife women.
        J Nutr. 2007; 137: 2412-2419
        • Salminen A.
        • Vihko V.
        Endurance training reduces the susceptibility of mouse skeletal muscle to lipid peroxidation in vitro.
        Acta Physiol Scand. 1983; 117: 109-113
        • Kalra J.
        • Rajput A.H.
        • Mantha S.V.
        • Prasad K.
        Serum antioxidant enzyme activity in Parkinson's disease.
        Mol Cell Biochem. 1992; 110: 165-168
        • Heroux M.
        • Janssen I.
        • Lam M.
        • et al.
        Dietary patterns and the risk of mortality: Impact of cardiorespiratory fitness.
        Int J Epidemiol. 2010; 39: 197-209
        • Kondo Y.
        • Higashi C.
        • Iwama M.
        • et al.
        Bioavailability of vitamin C from mashed potatoes and potato chips after oral administration in healthy Japanese men.
        Br J Nutr. 2012; 107: 885-892
        • Rao A.V.
        • Shen H.
        Effect of low dose lycopene intake on lycopene bioavailability and oxidative stress.
        Nutr Res. 2002; 22: 1125-1131

      Biography

      S. M. Rink is a dietetic intern, Department of Nutrition, School of Nursing, Loyola University Chicago, Chicago, IL; at the time of the study, she was a summer intern, Division of Epidemiology, Statistics, and Prevention Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD.

      Biography

      P. Mendola is an investigator, Division of Epidemiology, Statistics, and Prevention Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD.

      Biography

      S. L. Mumford is an investigator, Division of Epidemiology, Statistics, and Prevention Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD.

      Biography

      N. J. Perkins is a staff scientist, Division of Epidemiology, Statistics, and Prevention Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD.

      Biography

      E. F. Schisterman is a senior investigator and branch chief, Division of Epidemiology, Statistics, and Prevention Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD.

      Biography

      J. K. Poudrier is a biostatistician, John P. Murtha Cancer Center at Walter Reed National Military Medical Center, Henry M. Jackson Foundation, Rockville, MD; at the time of the study, she was a summer intern, Division of Epidemiology, Statistics, and Prevention Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD.

      Biography

      R. W. Browne is an associate professor, Department of Biotechnical and Clinical Laboratory Sciences, University at Buffalo, The State University of New York, Buffalo.

      Biography

      J. Wactawski-Wende is professor and associate chair, Department of Social and Preventive Medicine, University at Buffalo, The State University of New York, Buffalo.