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Broccoli sprouts reduce oxidative stress in type 2 diabetes: a randomized double-blind clinical trial

Abstract

Background/Objectives:

In vitro and animal studies have reported that young broccoli sprouts improve oxidative stress status in diabetic condition. The objective of this double-blind, placebo-controlled, randomized clinical trial was to investigate the effects of broccoli sprouts powder (BSP) on some oxidative stress parameters in type 2 diabetes patients.

Subjects/Methods:

A total of 81 patients with type 2 diabetes were randomly assigned to one of three treatment groups for 4 weeks. The groups received either 10 g/d BSP (n=27), 5 g/d BSP (n=29) or placebo (n=25). Serum total antioxidant capacity (TAC), total oxidant status (TOS), oxidative stress index (OSI), malondialdehyde (MDA) and oxidized low density lipoprotein (LDL) cholesterol were measured at baseline and at 4 weeks after treatment.

Results:

In all, 63 patients in three groups were included in the analysis: 10 g/d BSP (n=21), 5 g/d (n=22) and placebo (n=20). After 4 weeks, consumption of BSP resulted in significant decrease in MDA (P=0.001 for treatment effect), oxidized low density lipoprotein cholesterol (P=0.03 for treatment effect), OSI (P=0.001 for treatment effect) and significant increase in TAC (P=0.001 for treatment effect). No effects were found on TOS.

Conclusion:

BSP had favorable effects on oxidative stress status in type 2 diabetes patients.

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References

  • Altomare E, Vendemiale G, Chicco D, Procacci V, Cirelli F (1992). Increased lipid peroxidation in type 2 poorly controlled diabetic patients. Diabete Metab 18, 264–271.

    CAS  PubMed  Google Scholar 

  • Angeloni C, Leoncini E, Malaguti M, Angelini S, Hrelia P, Hrelia S (2009). Modulation of Phase II enzymes by sulforaphane: Implications for its cardioprotective potential. J Agric Food Chem 57, 5615–5622.

    Article  CAS  PubMed  Google Scholar 

  • Aslan M, Sabuncu T, Kocyigit A, Celik H, Selek S (2007). Relationship between total oxidant status and severity of diabetic nephropathy in type 2 diabetic patients. Nutr Metab Cardiovasc Dis 17, 734–740.

    Article  CAS  PubMed  Google Scholar 

  • Bekyarova GY, Ivanova DG, Madjova VH (2007). Molecular mechanisms associating oxidative stress with endothelial dysfunction in the development of various vascular complications in diabetes mellitus. Folia Med 49, 13–19.

    Google Scholar 

  • Cao Z, Tsang M, Zhao H, Li Y (2003). Induction of endogenous antioxidants and phase 2 enzymes by alpha-lipoic acid in rat cardiac H9C2 cells: protection against oxidative injury. Biochem Biophys Res Commun 310, 979–985.

    Article  CAS  PubMed  Google Scholar 

  • Carvajal M, Berenguer C, Viguera C (2006). Chemical and biological characterisation of nutraceutical compounds of broccoli. J Pharma Biochem Anal 41, 1508–1522.

    Article  Google Scholar 

  • Chisolm GM, Steinberg D (2000). The oxidative modification hypothesis of atherogenesis: an overview. Free Radic Biol Med 28, 1815–1826.

    Article  CAS  PubMed  Google Scholar 

  • Cho EJ, Lee YA, Yoo HH, Yokozawa T (2006). Protective effects of broccoli (Brassica oleracea) against oxidative damage in vitro and in vivo. J Nutr Sci Vitaminol 52, 437–444.

    Article  CAS  PubMed  Google Scholar 

  • Cumurcu BE, Ozyurt H, Etikan I, Demir S, Karlidag R (2009). Total antioxidant capacity and total oxidant status in patients with major depression: impact of antidepressant treatment. Psychiatry Clin Neurosci 63, 639–645.

    Article  CAS  PubMed  Google Scholar 

  • Dembinska-Kiec A, Mykkänen O, Kiec-Wilk B, Mykkänen H (2008). Antioxidant phytochemicals against type 2 diabetes. Br J Nutr 99, ES109–ES117.

    Article  PubMed  Google Scholar 

  • Dinkova-Kostova AT, Fahey JW, Wade KL, Jenkins SN, Shapiro TA, Fuchs EJ (2007). Induction of the Phase 2 response in mouse and human skin by sulforaphane-containing broccoli sprouts extracts. Cancer Epidemiol Biomarkers Prev 16, 847–851.

    Article  CAS  PubMed  Google Scholar 

  • Erel O (2004a). A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37, 277–285.

    Article  CAS  PubMed  Google Scholar 

  • Erel O (2004b). A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 37, 112–119.

    Article  CAS  PubMed  Google Scholar 

  • Evans JL, Goldfine ID, Maddux BA, Grodsky GM (2002). Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr Rev 23, 599–622.

    Article  CAS  Google Scholar 

  • Fahey J, Talalay P (1999). Antioxidant function of sulforaphane: a potent inducer of phase 2 detoxyfication enzymes. Food Chem Toxicol 37, 973–979.

    Article  CAS  PubMed  Google Scholar 

  • Goycheva V, Gadjeva B, Popov (2004). Oxidative stress and its complications in diabetes mellitus. Trakia J Sci 4, 1–8.

    Google Scholar 

  • Jeffery E, Araya M (2009). Physiological effects of broccoli consumption. Phytochem Rev 8, 283–298.

    Article  CAS  Google Scholar 

  • Jurlink B (2001). Therapeutic potential of dietary phase 2 enzyme inducer in ameliorating diseases that have an underlying inflammatory component. Can J Physiol Pharmacol 79, 266–282.

    Article  Google Scholar 

  • Keum Y, Jeong W, Kong T (2004). Chemoprevention by isothiocyanates and underlying molecular signaling mechanisms. Mut Res 555, 191–202.

    Article  CAS  Google Scholar 

  • Likidlilid A, Patchanans N, Peerapatdit T, Sriratanasathavorn C (2010). Lipid peroxidation and antioxidant enzyme activities in erythrocytes of type 2 diabetic patients. J Med Assoc Thai 93, 682–693.

    PubMed  Google Scholar 

  • Memişoğullari R, Bakan E (2004). Levels of ceruloplasmin, transferrin, and lipid peroxidation in the serum of patients with type 2 diabetes mellitus. J Diabetes Complications 18, 193–197.

    Article  PubMed  Google Scholar 

  • Menke T, Niklowitz P, de Sousa G, Reinehr T, Andler W (2004). Comparison of coenzyme Q10 plasma levels in obese and normal weight children. Clin Chim Acta 349, 121–127.

    Article  CAS  PubMed  Google Scholar 

  • Murashima M, Watanabe S, Zhuo XG, Uehara M, Kurashige A (2004). Phase 1 study of multiple biomarkers for metabolism and oxidative stress after one-week intake of broccoli sprouts. Biofactors 22, 271–275.

    Article  CAS  PubMed  Google Scholar 

  • Nakhjavani M, Esteghamati A, Nowroozi S, Asgarani F, Rashidi A, Khalilzadeh O (2010). Type 2 diabetes mellitus duration: an independent predictor of serum malondialdehyde levels. Singapore Med J 51, 582–585.

    CAS  PubMed  Google Scholar 

  • Opara EC, Abdel-Rahman E, Soliman S (1999). Depletion of total antioxidant capacity in type 2 diabetes. Metabolism 48, 1414–1417.

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Matute P, Zulet MA, Martínez JA (2009). Reactive species and diabetes: counteracting oxidative stress to improve health. Curr Opin Pharmacol 9, 771–779.

    Article  PubMed  Google Scholar 

  • Piao XL, Kim HY, Yokozawa T, Lee YA, Piao XS, Cho EJ (2005). Protective effects of broccoli (Brassica oleracea) and its active components against radical-induced oxidative damage. J Nutr Sci Vitaminol 51, 142–147.

    Article  CAS  PubMed  Google Scholar 

  • Ping Z, Liu W, Kang Z et al (2010). Sulforaphane protects brains against hypoxic-ischemic injury through induction of Nrf2-dependent phase 2 enzyme. Brain Res 1343, 178–185.

    Article  CAS  PubMed  Google Scholar 

  • Rabus M, Demirbağ R, Sezen Y (2008). Plasma and tissue oxidative stress index in patients with rheumatic and degenerative heart valve disease. Turk Kardiyol Dern Ars 36, 536–540.

    PubMed  Google Scholar 

  • Riedl MA, Saxon A, Diaz-Sanchez D (2009). Oral sulforaphane increases Phase II antioxidant enzymes in the human upper airway. Clin Immunol 130, 244–251.

    Article  CAS  PubMed  Google Scholar 

  • Schulz KF, Altman DG, Moher D (2010). CONSORT 2010 Statement: updated guidelines for reporting parallel group randomized trials. J Clin Epidemiol 63, 834–840.

    Article  PubMed  Google Scholar 

  • Son SM (2007). Role of vascular reactive oxygen species in development of vascular abnormalities in diabetes. Diabetes Res Clin Pract 77, S65–S70.

    Article  CAS  PubMed  Google Scholar 

  • Stranges S, Dorn J, Donahue R (2008). Oxidation, type 2 diabetes, and coronary heart disease: A complex interaction. Diabetes Care 31, 1864–1866.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S (2002). Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res 62, 5196–5203.

    CAS  PubMed  Google Scholar 

  • Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39, 44–84.

    Article  CAS  Google Scholar 

  • Verkerk R, Schreiner M, Krumbein A (2009). Glucosinolates in brassica vegetable: the influence of the food supply chain on intake, bioavailability and human health. Mol Nutr Food Res 53 (Suppl 2), S219–S266.

    Article  PubMed  Google Scholar 

  • Whiteside CI (2005). Cellular mechanisms and treatment of diabetes vascular complications converge on reactive oxygen species. Curr Hypertens Rep 7, 148–154.

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Juurlink BH (2001). The impaired glutathione system and its up-regulation by sulforaphane in vascular smooth muscle cells from spontaneously hypertensive rats. J Hypertens 19, 1819–1825.

    Article  CAS  PubMed  Google Scholar 

  • Wu L, Noyan MH, Facci M (2004). Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proc Natl Acad Sci 101, 7094–7099.

    Article  CAS  PubMed  Google Scholar 

  • Xue M, Qian Q, Adaikalakoteswari A, Rabbani N, Babaei-Jadidi R, Thornalley PJ (2008). Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease. Diabetes 57, 2809–2817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu H, Jia Z, Strobl JS, Ehrich M, Misra HP, Li Y (2008). Potent induction of total cellular and mitochondrial antioxidants and phase 2 enzymes by cruciferous sulforaphane in rat aortic smooth muscle cells: cytoprotection against oxidative and electrophilic stress. Cardiovasc Toxicol 8, 115–125.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by the Research Institute of Endocrine Sciences, Shahid Beheshti University of Medical Sciences (Tehran, Iran). The authors express appreciation to the participants of this study and would like to acknowledge the assistance given by Dr N Shakeri in data analysis and Ms N Shiva for language editing of the manuscript. None of the authors had any personal or financial conflicts of interest. The project was designed and implemented by PM and ZB. Serum sample were obtained and analyzed by ZB and MH. The data were analyzed and interpreted by ZB. The manuscript was prepared by PM, ZB, FH, SH and FA. PM and FA supervised overall project and approved the final version of the manuscript for submission.

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Correspondence to P Mirmiran.

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Bahadoran, Z., Mirmiran, P., Hosseinpanah, F. et al. Broccoli sprouts reduce oxidative stress in type 2 diabetes: a randomized double-blind clinical trial. Eur J Clin Nutr 65, 972–977 (2011). https://doi.org/10.1038/ejcn.2011.59

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