Investigation of cytokines, oxidative stress, metabolic, and inflammatory biomarkers after orange juice consumption by normal and overweight subjects

Grace K Z S Dourado, Thais B Cesar, Grace K Z S Dourado, Thais B Cesar

Abstract

Background: Abdominal adiposity has been linked to metabolic abnormalities, including dyslipidemia, oxidative stress, and low-grade inflammation.

Objective: To test the hypothesis that consumption of 100% orange juice (OJ) would improve metabolic, oxidative, and inflammatory biomarkers and cytokine levels in normal and overweight subjects with increased waist circumference.

Design: Subjects were divided into two groups in accordance with their body mass index: normal and overweight. Both groups of individuals consumed 750 mL of OJ daily for 8 weeks. Body composition (weight, height, percentage of fat mass, and waist circumference); metabolic biomarkers (total cholesterol, low-density lipoprotein-cholesterol [LDL-C], high-density lipoprotein-cholesterol [HDL-C], triglycerides, glucose, insulin, HOMA-IR, and glycated hemoglobin); oxidative biomarkers (malondialdehyde and DPPH(•)); inflammatory biomarkers (high-sensitivity C-reactive protein [hsCRP]); cytokines (IL-4, IL-10, IL-12, TNF-α, and IFN-γ); and diet were evaluated before and after consumption of OJ for 8 weeks.

Results: The major findings of this study were: 1) no alteration in body composition in either group; 2) improvement of the lipid profile, evidenced by a reduction in total cholesterol and LDL-C; 3) a potential stimulation of the immune response due to increase in IL-12; 4) anti-inflammatory effect as a result of a marked reduction in hsCRP; and 5) antioxidant action by the enhancement of total antioxidant capacity and the reduction of lipid peroxidation, in both normal and overweight subjects.

Conclusions: OJ consumption has a positive effect on important biomarkers of health status in normal and overweight subjects, thereby supporting evidence that OJ acts as functional food and could be consumed as part of a healthy diet to prevent metabolic and chronic diseases.

Keywords: biomarkers; clinical trial; cytokines; orange juice; overweight; oxidative stress.

References

    1. Magrone T, Perez de Heredia F, Jirillo E, Morabito G, Marcos A, Serafini M. Functional foods and nutraceuticals as therapeutic tools for the treatment of diet-related diseases. Can J Physiol Pharmacol. 2013;91:387–96.
    1. Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw. 2006;17:4–12.
    1. Ceriello A, Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovasculardisease? Arterioscler Thromb Vasc Biol. 2004;24:816–23.
    1. Coelho RC, Hermsdorff HH, Bressan J. Anti-inflammatory properties of orange juice: possible favorable molecular and metabolic effects. Plant Foods Hum Nutr. 2013;68:1–10.
    1. Mastrodi Salgado J, Baroni Ferreira TR, de Oliveira Biazotto F, Dos Santos Dias CT. Increased antioxidant content in juice enriched with dried extract of pomegranate (Punica granatum) peel. Plant Foods Hum Nutr. 2012;67:39–43.
    1. Chanet A, Milenkovic D, Manach C, Mazur A, Morand C. Citrus flavanones: what is their role in cardiovascular protection? J Agric Food Chem. 2012;12:8809–22.
    1. Benavente-García O, Castillo J. Update on uses and properties of citrus flavonoids: new findings in anticancer, cardiovascular, and anti-inflammatory activity. J Agric Food Chem. 2008;56:6185–205.
    1. Liu RH. Dietary bioactive compounds and their health implications. J Food Sci. 2013;78(Suppl 1):A18–25.
    1. Yao LH, Jiang YM, Shi J, Tomás-Barberán FA, Datta N, Singanusong R, et al. Flavonoids in food and their health benefits. Plant Foods Hum Nutr. 2004;59:113–22.
    1. Ghanim H, Sia CL, Upadhyay M, Korzeniewski K, Viswanathan P, Abuaysheh S, et al. Orange juice neutralizes the proinflammatory effect of a high-fat, high-carbohydrate meal and prevents endotoxin increase and toll-like receptor expression. Am J Clin Nutr. 2010;91:940–9.
    1. O'Neil CE, Nicklas TA, Rampersaud GC, Fulgoni VL., 3rd 100% orange juice consumption is associated with better diet quality, improved nutrient adequacy, decreased risk for obesity, and improved biomarkers of health in adults: National Health and Nutrition Examination Survey, 2003–2006. Nutr J. 2012;11:107.
    1. Murphy MM, Barraj LM, Rampersaud GC. Consumption of grapefruit is associated with higher nutrient intakes and diet quality among adults, and more favorable anthropometrics in women, NHANES 2003–2008. Food Nutr Res. 2014;58:22179. doi: .
    1. Johnston CS, Dancho CL, Strong GM. Orange juice ingestion and supplemental vitamin C are equally effective at reducing plasma lipid peroxidation in healthy adult women. J Am Coll Nutr. 2003;22:519–23.
    1. Buscemi S, Rosafio G, Arcoleo G, Mattina A, Canino B, Montana M, et al. Effects of red orange juice intake on endothelial function and inflammatory markers in adult subjects with increased cardiovascular risk. Am J Clin Nutr. 2012;95:1089–95.
    1. Rampersaud GC, Valim MF. 100% Citrus juice: nutritional contribution, dietary benefits, and association with anthropometric measures. Crit Rev Food Sci Nutr. 2015 [Epub ahead of print]
    1. Livesey G, Taylor R. Fructose consumption and consequences for glycation, plasma triacylglycerol, and body weight: meta-analyses and meta-regression models of intervention studies. Am J Clin Nutr. 2008;88:1419–37.
    1. AOAC International. Gaithersburg: AOAC International; 1995. Official methods of analysis of AOAC International (vol. II)
    1. Singleton VL, Rossi JA. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic. 1965;16:144–58.
    1. Yu Z, Dahlgren RA. Evaluation of methods for measuring polyphenols in conifer foliage. J Chem Ecol. 2000;26:2119–40.
    1. Zhishen J, Mengcheng T, Jianming W. The determination of flavonoid content in mulberry and their scavenging effects on superoxide radicals. Food Chem. 1999;64:555–9.
    1. Rodriguez-Amaya DB. Washington, DC: International Life Sciences Institute Press; 1999. A guide for carotenoid analysis in foods.
    1. Bocco A, Cuvelier ME, Richard H, Berset C. Antioxidant activity and phenolic composition of citrus peel and seed extracts. J Agric Food Chem. 1998;46:2123–9.
    1. World Health Organization. Geneva: WHO; 2000. Obesity: preventing and managing the global epidemic. WHO Technical Report Series no. 894.
    1. FDA (U.S. Food and Drug Administration) Title 21 – food and drugs. Part 101 – food labeling. 2011. Available from: [cited 15 May 2015]
    1. Cesar TB, Aptekmann NP, Araujo MP, Vinagre CC, Maranhão RC. Orange juice decreases low-density lipoprotein cholesterol in hypercholesterolemic subjectsand improves lipid transfer to high-density lipoprotein in normal and hypercholesterolemic subjects. Nutr Res. 2010;30:689–94.
    1. Aptekmann NP, Cesar TB. Orange juice improved lipid profile and blood lactate of overweight middle-aged women subjected to aerobic training. Maturitas. 2010;67:343–7.
    1. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499–502.
    1. Geloneze B, Repetto EM, Geloneze SR, Tambascia MA, Ermetice MN. The threshold value for insulin resistance (HOMA-IR) in an admixtured population IR in the Brazilian Metabolic Syndrome Study. Diabetes Res Clin Pract. 2006;72:219–20.
    1. Yagi K. Simple assay for the level of total lipid peroxides in serum or plasma. Methods Mol Biol. 1998;108:101–6.
    1. Chrzczanowicz J, Gawron A, Zwolinska A, Graft J. Simple method for determining human serum 2,2-diphenyl-1-picryl-hydrazyl (DPPH•) radical scavenging activity – possible application in clinical studies on dietary antioxidants. Clin Chem Lab Med. 2008;46:342–9.
    1. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2014;37(Suppl 1):S81–90.
    1. Stone NJ, Robinson JG, Lichtenstein AH, Bairey Merz CN, Lloyd-Jones DM, Blum CB, et al. American College of Cardiology/American Heart Association Task Force on Practice Guidelines. 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol. 2014 63(25 Pt B): 2889–934. Erratum in: J Am Coll Cardiol 2014; 63(25 Pt B): 3024–3025.
    1. Nieto-Vazquez I, Fernández-Veledo S, Krämer DK, Vila-Bedmar R, Garcia-Guerra L, Lorenzo M. Insulin resistance associated to obesity: the link TNF-alpha. Arch Physiol Biochem. 2008;114:183–94.
    1. Basile LG, Lima CG, César TB. Daily intake of pasteurized orange juice decreases serum cholesterol, fasting glucose, and diastolic blood pressure in adults. Proc Fla State Horticult Soc. 2010;123:228–33.
    1. Cesar TB, Paiva AC. Functional properties of orange juice on lipid and glucose metabolism, appetite, and oxidative stress on humans. In: 246th American Chemistry Society National Meeting, 2013, Indianapolis, IN, USA.
    1. Clarke R, Frost C, Collins R, Appleby P, Peto R. Dietary lipids and blood cholesterol: quantitative meta-analysis of metabolic ward studies. BMJ. 1997;314:112–17.
    1. Ford ES, Capewell S. Trends in total and low-density lipoprotein cholesterol among U.S. adults: contributions of changes in dietary fat intake and use of cholesterol-lowering medications. PLoS One. 2013;8:e65228.
    1. Aptekmann NP, Cesar TB. Long-term orange juice consumption is associated with low LDL-cholesterol and apolipoprotein B in normal and moderately hypercholesterolemic subjects. Lipids Health Dis. 2013;12:119.
    1. Wang X, Hasegawa J, Kitamura Y, Wang Z, Matsuda A, Shinoda W, et al. Effects of hesperidin on the progression of hypercholesterolemia and fatty liver induced by high-cholesterol diet in rats. J Pharmacol Sci. 2011;117:129–38.
    1. Rampersaud GC. A comparison of nutrient density scores for 100% fruit juices. J Food Sci. 2007;72:S261–6.
    1. O'Neil CE, Nicklas TA, Rampersaud GC, Fulgoni VL., 3rd One hundred percent orange juice consumption is associated with better diet quality, improved nutrient adequacy, and no increased risk for overweight/obesity in children. Nutr Res. 2011;31:673–82.
    1. Assini JM, Mulvihill EE, Huff MW. Citrus flavonoids and lipid. Curr Opin Lipidol. 2013;24:34–40.
    1. Mehta S, Farmer JA. Obesity and inflammation: a new look at an old problem. Curr Atheroscler Rep. 2007;9:134–8.
    1. Bienvenu J, Monneret G, Fabien N, Revillard JP. The clinical usefulness of the measurement of cytokines. Clin Chem Lab Med. 2000;38:267–85.
    1. Sinigaglia F, D'Ambrosio D, Panina-Bordignon P, Rogge L. Regulation of the IL-12/IL-12R axis: a critical step in T-helper cell differentiation and effector function. Immunol Rev. 1999;170:65–72.
    1. Langrish CL, McKenzie BS, Wilson NJ, de Waal Malefyt R, Kastelein RA, Cua DJ. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev. 2004;202:96–105.
    1. Zanotti Simoes Dourado GK, de Abreu Ribeiro LC, Zeppone Carlos I, Borges César T. Orange juice and hesperidin promote differential innate immune response in macrophages ex vivo. Int J Vitam Nutr Res. 2013;83:162–7.
    1. Ridker PM, Cannon CP, Morrow D, Rifai N, Rose LM, McCabe CH, et al. C-reactive protein levels and outcomes after statin therapy. N Engl J Med. 2005;352:20–8.
    1. Sánchez-Moreno C, Cano MP, de Ancos B, Plaza L, Olmedilla B, Granado F, et al. High-pressurized orange juice consumption affects plasma vitamin C, antioxidative status and inflammatory markers in healthy humans. J Nutr. 2003;133:2204–9.
    1. Asgary S, Keshvari M, Afshani MR, Amiri M, Laher I, Javanmard SH. Effect of fresh orange juice intake on physiological characteristics in healthy volunteers. ISRN Nutr. 2014;2014:405867.
    1. Devaraj S, Autret BC, Jialal I. Reduced-calorie orange juice beverage with plant sterols lowers C-reactive protein concentrations and improves the lipid profile in human volunteers. Am J Clin Nutr. 2006;84:756–61.
    1. Halliwell B, Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr. 1993;57:715S–24S.
    1. Franke AA, Cooney RV, Henning SM, Custer LJ. Bioavailability and antioxidant effects of orange juice components in humans. J Agric Food Chem. 2005;53:5170–8.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere