Research Original Research| Volume 114, ISSUE 5, P700-708.e2, May 2014

Download started.


Cruciferous Vegetable Intake Is Inversely Correlated with Circulating Levels of Proinflammatory Markers in Women

Published:March 13, 2014DOI:



      Higher intakes of cruciferous vegetables or their constituents have been shown to lower inflammation in animal studies. However, evidence for this anti-inflammatory effect of cruciferous vegetable consumption in humans is scarce.


      In this cross-sectional analysis, we evaluated associations of vegetable intake with a panel of inflammatory and oxidative stress markers among 1,005 middle-aged Chinese women. Dietary intake of foods was assessed by a food frequency questionnaire.


      Multivariable-adjusted circulating concentrations of tumor necrosis factor-α (TNF-α), interlukin-1β (IL-1β), and IL-6 were lower among women with higher intakes of cruciferous vegetables. The differences in concentrations of inflammatory biomarkers between extreme quintiles of cruciferous vegetable intake were 12.66% for TNF-α (Ptrend=0.01), 18.18% for IL-1β (Ptrend=0.02), and 24.68% for IL-6 (Ptrend=0.02). A similar, but less apparent, inverse association was found for intakes of all vegetables combined but not for noncruciferous vegetables. Levels of the urinary oxidative stress markers F2-isoprostanes and their major metabolite, 2,3-dinor-5,6-dihydro-15-F2t-IsoP, were not associated with intakes of cruciferous vegetables or all vegetables combined.


      This study suggests that the previously observed health benefits of cruciferous vegetable consumption may be partly associated with the anti-inflammatory effects of these vegetables.


      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 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


        • Block G.
        • Patterson B.
        • Subar A.
        Fruit, vegetables, and cancer prevention: A review of the epidemiological evidence.
        Nutr Cancer. 1992; 18: 1-29
        • Zhang X.
        • Shu X.O.
        • Xiang Y.B.
        • et al.
        Cruciferous vegetable consumption is associated with a reduced risk of total and cardiovascular disease mortality.
        Am J Clin Nutr. 2011; 94: 240-246
        • World Cancer Research Fund, American Institute for Cancer Research
        Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective.
        AICR, Washington, DC2007
        • Fenwick G.R.
        • Heaney R.K.
        • Mullin W.J.
        Glucosinolates and their breakdown products in food and food plants.
        Crit Rev Food Sci Nutr. 1983; 18: 123-201
        • Zhang Y.
        • Talalay P.
        Anticarcinogenic activities of organic isothiocyanates: Chemistry and mechanisms.
        Cancer Res. 1994; 54: S1976-S1981
        • Fahey J.W.
        • Zhang Y.
        • Talalay P.
        Broccoli sprouts: An exceptionally rich source of inducers of enzymes that protect against chemical carcinogens.
        Proc Natl Acad Sci U S A. 1997; 94: 10367-10372
        • Mi L.
        • Hood B.L.
        • Stewart N.A.
        • et al.
        Identification of potential protein targets of isothiocyanates by proteomics.
        Chem Res Toxicol. 2011; 24: 1735-1743
        • Youn H.S.
        • Kim Y.S.
        • Park Z.Y.
        • et al.
        Sulforaphane suppresses oligomerization of TLR4 in a thiol-dependent manner.
        J Immunol. 2010; 184: 411-419
        • Xue M.
        • Qian Q.
        • Adaikalakoteswari A.
        • Rabbani N.
        • Babaei-Jadidi R.
        • Thornalley P.J.
        Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease.
        Diabetes. 2008; 57: 2809-2817
        • Zakkar M.
        • Van der Heiden K.
        • Luong L.A.
        • et al.
        Activation of Nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state.
        Arterioscler Thromb Vasc Biol. 2009; 29: 1851-1857
        • Brown K.K.
        • Blaikie F.H.
        • Smith R.A.
        • et al.
        Direct modification of the proinflammatory cytokine macrophage migration inhibitory factor by dietary isothiocyanates.
        J Biol Chem. 2009; 284: 32425-32433
        • Navarro S.L.
        • Li F.
        • Lampe J.W.
        Mechanisms of action of isothiocyanates in cancer chemoprevention: An update.
        Food Function. 2011; 2: 579-587
        • Lampe J.W.
        • Peterson S.
        Brassica, biotransformation and cancer risk: Genetic polymorphisms alter the preventive effects of cruciferous vegetables.
        J Nutr. 2002; 132: 2991-2994
        • Lam T.K.
        • Gallicchio L.
        • Lindsley K.
        • et al.
        Cruciferous vegetable consumption and lung cancer risk: A systematic review.
        Cancer Epidemiol Biomarkers Prev. 2009; 18: 184-195
        • Moore L.E.
        • Huang W.Y.
        • Chatterjee N.
        • et al.
        GSTM1, GSTT1, and GSTP1 polymorphisms and risk of advanced colorectal adenoma.
        Cancer Epidemiol Biomarkers Prev. 2005; 14: 1823-1827
        • Yang G.
        • Gao Y.T.
        • Shu X.O.
        • et al.
        Isothiocyanate exposure, glutathione S-transferase polymorphisms, and colorectal cancer risk.
        Am J Clin Nutr. 2010; 91: 704-711
        • Wu L.
        • Noyan A.M.
        • Facci M.
        • et al.
        Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system.
        Proc Natl Acad Sci U S A. 2004; 101: 7094-7099
        • Wu S.H.
        • Shu X.O.
        • Chow W.H.
        • et al.
        Soy food intake and circulating levels of inflammatory markers in Chinese women.
        J Acad Nutr Diet. 2012; 112: 996-1004
        • Zheng W.
        • Chow W.H.
        • Yang G.
        • et al.
        The Shanghai Women's Health Study: Rationale, study design, and baseline characteristics.
        Am J Epidemiol. 2005; 162: 1123-1131
        • Shu X.O.
        • Yang G.
        • Jin F.
        • et al.
        Validity and reproducibility of the food frequency questionnaire used in the Shanghai Women's Health Study.
        Eur J Clin Nutr. 2004; 58: 17-23
        • Lee S.A.
        • Kallianpur A.
        • Xiang Y.B.
        • et al.
        Intra-individual variation of plasma adipokine levels and utility of single measurement of these biomarkers in population-based studies.
        Cancer Epidemiol Biomarkers Prev. 2007; 16: 2464-2470
        • Morrow J.D.
        • Hill K.E.
        • Burk R.F.
        • Nammour T.M.
        • Badr K.F.
        • Roberts L.N.
        A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism.
        Proc Natl Acad Sci U S A. 1990; 87: 9383-9387
        • 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
        • Milne G.L.
        • Yin H.
        • Brooks J.D.
        • Sanchez S.
        • Jackson R.L.N.
        • Morrow J.D.
        Quantification of F2-isoprostanes in biological fluids and tissues as a measure of oxidant stress.
        Methods Enzymol. 2007; 433: 113-126
        • Harrell F.J.
        • Shih Y.C.
        Using full probability models to compute probabilities of actual interest to decision makers.
        Int J Technol Assess Health Care. 2001; 17: 17-26
        • D'Hoore W.
        • Bouckaert A.
        • Tilquin C.
        Practical considerations on the use of the Charlson comorbidity index with administrative data bases.
        J Clin Epidemiol. 1996; 49: 1429-1433
        • Pearson T.A.
        • Mensah G.A.
        • Alexander R.W.
        • et al.
        Markers of inflammation and cardiovascular disease: Application to clinical and public health practice: A statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association.
        Circulation. 2003; 107: 499-511
        • Belsley D.A.
        • Kuh E.
        • Welsch R.E.
        Regression Diagnostics: Identifying Influential Data and Sources of Collinearity.
        Wiley, New York, NY1980
        • Cotton S.C.
        • Sharp L.
        • Little J.
        • Brockton N.
        Glutathione S-transferase polymorphisms and colorectal cancer: A HuGE review.
        Am J Epidemiol. 2000; 151: 7-32
        • 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
        • Esfahani A.
        • Wong J.M.
        • Truan J.
        • et al.
        Health effects of mixed fruit and vegetable concentrates: A systematic review of the clinical interventions.
        J Am Coll Nutr. 2011; 30: 285-294
        • Jayakumar T.
        • Chen W.F.
        • Lu W.J.
        • et al.
        A novel antithrombotic effect of sulforaphane via activation of platelet adenylatecyclase: Ex vivo and in vivo studies.
        J Nutr Biochem. 2013; 24: 1086-1095
        • Tsai J.T.
        • Liu H.C.
        • Chen Y.H.
        Suppression of inflammatory mediators by cruciferous vegetable-derived indole-3-carbinol and phenylethylisothiocyanate in lipopolysaccharide-activated macrophages.
        Mediators Inflamm. 2010; 293642: 1-5
        • Tiku A.B.
        • Abraham S.K.
        • Kale R.K.
        Protective effect of the cruciferous vegetable mustard leaf (Brassica campestris) against in vivo chromosomal damage and oxidative stress induced by gamma-radiation and genotoxic chemicals.
        Environ Mol Mutagen. 2008; 49: 335-342
        • van den Berg R.
        • van Vliet T.
        • Broekmans W.M.
        • et al.
        A vegetable/fruit concentrate with high antioxidant capacity has no effect on biomarkers of antioxidant status in male smokers.
        J Nutr. 2001; 131: 1714-1722
        • Paterson E.
        • Gordon M.H.
        • Niwat C.
        • et al.
        Supplementation with fruit and vegetable soups and beverages increases plasma carotenoid concentrations but does not alter markers of oxidative stress or cardiovascular risk factors.
        J Nutr. 2006; 136: 2849-2855
        • Hopkins M.H.
        • Fedirko V.
        • Jones D.P.
        • Terry P.D.
        • Bostick R.M.
        Antioxidant micronutrients and biomarkers of oxidative stress and inflammation in colorectal adenoma patients: Results from a randomized, controlled clinical trial.
        Cancer Epidemiol Biomarkers Prev. 2010; 19: 850-858
        • Braga M.
        • Bissolati M.
        • Rocchetti S.
        • Beneduce A.
        • Pecorelli N.
        • Di Carlo V.
        Oral preoperative antioxidants in pancreatic surgery: A double-blind, randomized, clinical trial.
        Nutrition. 2012; 28: 160-164
        • Roberts L.J.
        • Morrow J.D.
        Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo.
        Free Radic Biol Med. 2000; 28: 505-513
        • London S.J.
        • Yuan J.M.
        • Chung F.L.
        • et al.
        Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms, and lung-cancer risk: A prospective study of men in Shanghai, China.
        Lancet. 2000; 356: 724-729
        • Seow A.
        • Yuan J.M.
        • Sun C.L.
        • Van Den Berg D.
        • Lee H.P.
        • Yu M.C.
        Dietary isothiocyanates, glutathione S-transferase polymorphisms and colorectal cancer risk in the Singapore Chinese Health Study.
        Carcinogenesis. 2002; 23: 2055-2061
        • Lin H.J.
        • Probst-Hensch N.M.
        • Louie A.D.
        • et al.
        Glutathione transferase null genotype, broccoli, and lower prevalence of colorectal adenomas.
        Cancer Epidemiol Biomarkers Prev. 1998; 7: 647-652
        • Tijhuis M.J.
        • Wark P.A.
        • Aarts J.M.
        • et al.
        GSTP1 and GSTA1 polymorphisms interact with cruciferous vegetable intake in colorectal adenoma risk.
        Cancer Epidemiol Biomarkers Prev. 2005; 14: 2943-2951
        • Cornelis M.C.
        • El-Sohemy A.
        • Campos H.
        GSTT1 genotype modifies the association between cruciferous vegetable intake and the risk of myocardial infarction.
        Am J Clin Nutr. 2007; 86: 752-758


      Y. Jiang is deputy chief, Division of Chronic Disease Control and Prevention, Changning Center for Disease Control and Prevention, Shanghai, China, and a research fellow trainee, Division of Epidemiology, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      S.-H. Wu is a research fellow, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      X.-O. Shu is a professor, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      W. Zheng is a professor, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      Q. Cai is an associate professor, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      X. Zhang is an assistant professor, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      G. Yang is a research associate professor, Division of Epidemiology, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      G. L Milne is a research associate professor, Division of Clinical Pharmacology, Department of Medicine, Vanderbilt University School of Medicine, Nashville, TN.


      Y.-B. Xiang is a professor, Shanghai Cancer Institute, Shanghai, China.


      Y.-T. Gao is a professor, Shanghai Cancer Institute, Shanghai, China.


      B.-T. Ji is a staff scientist, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Bethesda, MD.