Effects of long-term consumption of broccoli sprouts on inflammatory markers in overweight subjects

Published:March 13, 2018DOI:https://doi.org/10.1016/j.clnu.2018.03.006


      Background & aims

      Broccoli sprouts represent an interesting choice of healthy food product as they are rich in glucosinolates and their cognate bioactive metabolites, isothiocyanates able to counteract the negative effects of diverse pathologies. As obesity is linked to an inflammatory component, the aim of the study was to evaluate the anti-inflammatory action of broccoli sprouts in overweight adult subjects.


      An in vivo controlled study was performed in 40 healthy overweight subjects (ClinicalTrials.gov ID NCT 03390855). Treatment phase consisted on the consumption of broccoli sprouts (30 g/day) during 10 weeks and the follow-up phase of 10 weeks of normal diet without consumption of these broccoli sprouts. Anthropometric parameters as body fat mass, body weight, and BMI were determined. Inflammation status was assessed by measuring levels of TNF-α, IL-6, IL-1β and C-reactive protein.


      IL-6 levels significantly decreased (mean values from 4.76 pg/mL to 2.11 pg/mL with 70 days of broccoli consumption, p < 0.001) and during control phase the inflammatory levels were maintained at low grade (mean values from 1.20 pg/mL to 2.66 pg/mL, p < 0.001). C-reactive protein significantly decreased as well.


      This study represents an advance in intervention studies as the broccoli sprouts were included in a daily dietary pattern in quantities that reflect a real consumption. Further studies are necessary to elucidate the role of this healthy rich and nutritious food product, but these promising results support the current evidence on the healthy properties of Brassica varieties.


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        • West L.G.
        • Meyer K.A.
        • Balch B.A.
        • Rossi F.J.
        • Schultz M.R.
        • Haas G.W.
        Glucoraphanin and 4-hydroxyglucobrassicin contents in seeds of 59 cultivars of broccoli, raab, kohlrabi, radish, cauliflower, brussels sprouts, kale, and cabbage.
        J Agric Food Chem. 2004; 52: 916-926
        • Baenas N.
        • García-Viguera C.
        • Moreno D.A.
        Elicitation: a tool for enriching the bioactive composition of foods.
        Molecules (Basel, Switzerland). 2014; 19: 13541-13563
        • Dinkova-Kostova A.T.
        • Kostov R.V.
        Glucosinolates and isothiocyanates in health and disease.
        Trends Mol Med. 2012; 18: 337-347
        • Wu Q.-J.
        • Yang Y.
        • Wang J.
        • Han L.-H.
        • Xiang Y.-B.
        Cruciferous vegetable consumption and gastric cancer risk: a meta-analysis of epidemiological studies.
        Cancer Sci. 2013; 104: 1067-1073
        • Hu J.
        • Hu Y.
        • Hu Y.
        • Zheng S.
        Intake of cruciferous vegetables is associated with reduced risk of ovarian cancer: a meta-analysis.
        Asia Pac J Clin Nutr. 2015; 24: 101-109
        • Abdull Razis A.
        • Nicola G.
        • Pagnotta E.
        • Iori R.
        • Ioannides C.
        4-Methylsulfanyl-3-butenyl isothiocyanate derived from glucoraphasatin is a potent inducer of rat hepatic phase II enzymes and a potential chemopreventive agent.
        Arch Toxicol. 2012; 86: 183-194
        • Jeffery E.H.
        • Araya M.
        Physiological effects of broccoli consumption.
        Phytochemistry Rev. 2009; 8: 283-298
        • Moschen A.R.
        • Molnar C.
        • Enrich B.
        • Geiger S.
        • Ebenbichler C.F.
        • Tilg H.
        Adipose and liver expression of interleukin (IL)-1 family members in morbid obesity and effects of weight loss.
        Mol Med (Cambridge, Mass.). 2011; 17: 840-845
        • Lumeng C.N.
        • Saltiel A.R.
        Inflammatory links between obesity and metabolic disease.
        J Clin Invest. 2011; 121: 2111-2117
        • Baenas N.
        • Villaño D.
        • García-Viguera C.
        • Moreno D.A.
        Optimizing elicitation and seed priming to enrich broccoli and radish sprouts in glucosinolates.
        Food Chem. 2016; 204: 314-319
        • Houghton C.A.
        • Fassett R.G.
        • Coombes J.S.
        Sulforaphane: translational research from laboratory bench to clinic.
        Nutr Rev. 2013; 71: 708-726
        • Palermo M.
        • Pellegrini N.
        • Fogliano V.
        The effect of cooking on the phytochemical content of vegetables.
        J Sci Food Agric. 2014; 94: 1057-1070
        • Vermeulen M.
        • Klöpping-Ketelaars I.W.
        • van den Berg R.
        • Vaes W.H.
        Bioavailability and kinetics of sulforaphane in humans after consumption of cooked versus raw broccoli.
        J Agric Food Chem. 2008; 56: 10505-10509
        • Baenas N.
        • Suárez-Martínez C.
        • García-Viguera C.
        • Moreno D.A.
        Bioavailability and new biomarkers of cruciferous sprouts consumption.
        Food Res Int (Ottawa, Ont.). 2017; 100: 497-503
        • Dominguez-Perles R.
        • Medina S.
        • Moreno D.A.
        • García-Viguera C.
        • Ferreres F.
        • Gil-Izquierdo A.
        A new ultra-rapid UHPLC/MS/MS method for assessing glucoraphanin and sulforaphane bioavailability in human urine.
        Food Chem. 2014; 143: 132-138
        • Kang Y.E.
        • Kim J.M.
        • Joung K.H.
        • Lee J.H.
        • You B.R.
        • Choi M.J.
        • et al.
        The roles of adipokines, proinflammatory cytokines, and adipose tissue macrophages in obesity-associated insulin resistance in modest obesity and early metabolic dysfunction.
        PLoS One. 2016; 11 (e0154003–e0154003)
        • Jorge A.S.B.
        • Jorge G.C.
        • Paraíso A.F.
        • Franco R.M.
        • Vieira L.J.
        • Hilzenderger A.M.
        • et al.
        Brown and white adipose tissue expression of IL6, UCP1 and SIRT1 are associated with alterations in clinical, metabolic and anthropometric parameters in obese humans.
        Exp Clin Endocrinol Diabetes. 2017; 125: 163-170
        • Bienvenu J.
        • Monneret G.
        • Fabien N.
        • Revillard J.P.
        The clinical usefulness of the measurement of cytokines.
        Clin Chem Lab Med. 2000; 38: 267-285
        • Whelton S.P.
        • Roy P.
        • Astor B.C.
        • Zhang L.
        • Hoogeveen R.C.
        • Ballantyne C.M.
        • et al.
        Elevated high-sensitivity C-Reactive protein as a risk marker of the attenuated relationship between serum cholesterol and cardiovascular events at older age.
        Am J Epidemiol. 2013; 178: 1076-1084
        • Medina S.
        • Domínguez-Perles R.
        • Moreno D.A.
        • García-Viguera C.
        • Ferreres F.
        • Gil J.I.
        • Gil-Izquierdo A.
        The intake of broccoli sprouts modulates the inflammatory and vascular prostanoids but not the oxidative stress-related isoprostanes in healthy humans.
        Food Chem. 2015; 173: 1187-1194
        • Riso P.
        • Vendrame S.
        • Del Bo C.
        • Martini D.
        • Martinetti A.
        • Seregni E.
        • et al.
        Effect of 10-day broccoli consumption on inflammatory status of young healthy smokers.
        Int J Food Sci Nutr. 2014; 65: 106-111
        • Navarro S.L.
        • Schwarz Y.
        • Song X.
        • Wang C.-Y.
        • Cheng C.
        • Trudo S.P.
        • et al.
        Cruciferous vegetables have variable effects on biomarkers of systemic inflammation in a randomized controlled trial in healthy young adults.
        J Nutr. 2014; 144: 1850-1857
        • Fahey J.W.
        • Zhang Y.
        • Talalay P.
        Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against.
        Proc Natl Acad Sci U S A. 1997; 94: 10367
        • Bones A.M.
        • Rossiter J.T.
        The enzymic and chemically induced decomposition of glucosinolates.
        Phytochemistry. 2006; 67: 1053-1067
        • Angelino D.
        • Jeffery E.
        Glucosinolate hydrolysis and bioavailability of resulting isothiocyanates: focus on glucoraphanin.
        J Funct Foods. 2014; 7: 67-76
        • Joseph M.A.
        • Moysich K.B.
        • Freudenheim J.L.
        • Shields P.G.
        • Bowman E.D.
        • Zhang Y.
        • et al.
        Cruciferous vegetables, genetic polymorphisms in glutathione S-transferases M1 and T1, and prostate cancer risk.
        Nutr Cancer. 2004; 50: 206-213
        • Higdon J.V.
        • Delage B.
        • Williams D.E.
        • Dashwood R.H.
        Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis.
        Pharmacol Res. 2007; 55: 224-236
        • Sayeed M.A.
        • Bracci M.
        • Lazzarini R.
        • Tomasetti M.
        • Amati M.
        • Lucarini G.
        • et al.
        Use of potential dietary phytochemicals to target miRNA: promising option for breast cancer prevention and treatment?.
        J Funct Foods. 2017; 28: 177-193
        • Fujioka N.
        • Ainslie-Waldman C.E.
        • Upadhyaya P.
        • Carmella S.G.
        • Fritz V.A.
        • Rohwer C.
        • et al.
        Urinary 3,3'-diindolylmethane: a biomarker of glucobrassicin exposure and indole-3-carbinol uptake in humans.
        Cancer Epidemiol Biomarkers Prev. 2014; 23: 282-287
        • Houghton C.A.
        • Fassett R.G.
        • Coombes J.S.
        Sulforaphane and Other Nutrigenomic Nrf2 activators: can the Clinician's expectation Be matched by the reality?.
        Oxid Med Cell Longev. 2016; 2016 (7857186–7857186)
        • Hu C.
        • Eggler A.L.
        • Mesecar A.D.
        • van Breemen R.B.
        Modification of keap1 cysteine residues by sulforaphane.
        Chem Res Toxicol. 2011; 24: 515-521
        • Riedl M.A.
        • Saxon A.
        • Diaz-Sanchez D.
        Oral sulforaphane increases Phase II antioxidant enzymes in the human upper airway.
        Clin Immunol. 2009; 130: 244-251
        • Wagner A.E.
        • Boesch-Saadatmandi C.
        • Dose J.
        • Schultheiss G.
        • Rimbach G.
        Anti-inflammatory potential of allyl-isothiocyanate–role of Nrf2, NF-(κ) B and microRNA-155.
        J Cell Mol Med. 2012; 16: 836-843
        • Sturm C.
        • Wagner A.E.
        Brassica-derived plant bioactives as modulators of chemopreventive and inflammatory signaling pathways.
        Int J Mol Sci. 2017; 18
        • Heiss E.
        • Herhaus C.
        • Klimo K.
        • Bartsch H.
        • Gerhäuser C.
        Nuclear factor kappa B is a molecular target for sulforaphane-mediated anti-inflammatory mechanisms.
        J Biol Chem. 2001; 276: 32008-32015
        • Dinkova-Kostova A.T.
        • Fahey J.W.
        • Wade K.L.
        • Jenkins S.N.
        • Shapiro T.A.
        • Fuchs E.J.
        • et al.
        Induction of the phase 2 response in mouse and human skin by sulforaphane-containing broccoli sprout extracts.
        Cancer Epidemiol Biomarkers Prev: A Publ Am Assoc Cancer Res Cospons Am Soc Prev Oncol. 2007; 16: 847-851
        • Harvey C.J.
        • Thimmulappa R.K.
        • Sethi S.
        • Kong X.
        • Yarmus L.
        • Brown R.H.
        • et al.
        Targeting Nrf2 signaling improves bacterial clearance by alveolar macrophages in patients with COPD and in a mouse model.
        Sci Transl Med. 2011; 3 (78ra32-78ra32)
        • Cho H.J.
        • Seon M.R.
        • Lee Y.M.
        • Kim J.
        • Kim J.K.
        • Kim S.G.
        • et al.
        3,3'-Diindolylmethane suppresses the inflammatory response to lipopolysaccharide in murine macrophages.
        J Nutr. 2008; 138: 17-23
        • Jeon E.-J.
        • Davaatseren M.
        • Hwang J.-T.
        • Park J.H.
        • Hur H.J.
        • Lee A.S.
        • et al.
        Effect of oral administration of 3,3'-diindolylmethane on dextran sodium sulfate-induced acute colitis in mice.
        J Agric Food Chem. 2016; 64: 7702-7709
        • Kim Y.H.
        • Kwon H.-S.
        • Kim D.H.
        • Shin E.K.
        • Kang Y.H.
        • Park J.H.
        • et al.
        3,3'-diindolylmethane attenuates colonic inflammation and tumorigenesis in mice.
        Inflamm Bowel Dis. 2009; 15: 1164-1173
        • Clarke J.D.
        • Hsu A.
        • Riedl K.
        • Bella D.
        • Schwartz S.J.
        • Stevens J.F.
        • et al.
        Bioavailability and inter-conversion of sulforaphane and erucin in human subjects consuming broccoli sprouts or broccoli supplement in a cross-over study design.
        Pharmacol Res. 2011; 64: 456-463
        • Choi Y.
        • Kim Y.
        • Park S.
        • Lee K.W.
        • Park T.
        Indole-3-carbinol prevents diet-induced obesity through modulation of multiple genes related to adipogenesis, thermogenesis or inflammation in the visceral adipose tissue of mice.
        J Nutr Biochem. 2012; 23: 1732-1739