Short-term cactus pear [Opuntia ficus-indica (L.) Mill] fruit supplementation ameliorates the inflammatory profile and is associated with improved antioxidant status among healthy humans
Background: Dietary ingredients and food components are major modifiable factors protecting immune system and preventing the progression of a low-grade chronic inflammation responsible for age-related diseases.
Objective: Our study explored whether cactus pear (Opuntia ficus-indica, Surfarina cultivar) fruit supplementation modulates plasma inflammatory biomarkers in healthy adults. Correlations between inflammatory parameters and antioxidant status were also assessed in parallel.
Design: In a randomised, 2-period (2 weeks/period), crossover, controlled-feeding study, conducted in 28 healthy volunteers [mean age 39.96 (±9.15) years, BMI 23.1 (±1.5) kg/m2], the effects of a diet supplemented with cactus pear fruit pulp (200 g, twice a day) were compared with those of an equivalent diet with isocaloric fresh fruit substitution.
Results: With respect to control, cactus pear diet decreased ( p < 0.05) the pro-inflammatory markers such as tumour necrosis factor-α (TNF-α), interleukin (IL)-1β, interferon-γ (INF)-γ, IL-8, C-reactive protein (CRP) and erythrocyte sedimentation rate (ESR), whereas it increased ( p < 0.05) the anti-inflammatory marker IL-10. Moreover, the diet decreased ratios between pro-inflammatory biomarkers (CRP, IL-6, IL-8, TNF-α) and anti- inflammatory biomarker (IL-10) ( p < 0.05). Cactus pear supplementation caused an increase ( p < 0.05) in dermal carotenoids (skin carotenoid score, SCS), a biomarker of the body antioxidant status, with correlations between SCS and CRP (r = −0.905, p < 0.0001), IL-8 (r = −0.835, p < 0.0001) and IL-10 (r = 0.889, p < 0.0001).
Conclusions: The presently observed modulation of both inflammatory markers and antioxidant balance suggests cactus pear fruit as a novel and beneficial component to be incorporated into current healthy dietary habits.
- Neale EP, Batterham MJ, Tapsell LC. Consumption of a healthy dietary pattern results in significant reductions in C-reactive protein levels in adults: a meta-analysis. Nutr Res 2016; 36(5): 391–401.
- Calder PC, Ahluwalia N, Albers R, Bosco N, Bourdet-Sicard R, Haller D, et al. A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr 2013; 109(Suppl 1): S1–34.
- Danesh J, Kaptoge S, Mann AG, Sarwar N, Wood A, Angleman SB, et al. Long-term interleukin-6 levels and subsequent risk of coronary heart disease: two new prospective studies and a systematic review. PLoS Med 2008; 5(4): e78.
- Clearfield MB. C-reactive proteIn: a new risk assessment tool for cardiovascular disease. J Am Osteopath Assoc 2005; 105(9): 409–16.
- Sabat R, Grutz G, Warszawska K, Kirsch S, Witte E, Wolk K, et al. Biology of interleukin-10. Cytokine Growth Factor Rev 2010; 21(5): 331–44.
- Filippi CM, von Herrath MG. IL-10 and the resolution of infections. J Pathol 2008; 214(2): 224–30.
- Wyczalkowska-Tomasik A, Czarkowska-Paczek B, Zielenkiewicz M, Paczek L. Inflammatory markers change with age, but do not fall beyond reported normal ranges. Arch Immunol Ther Exp (Warsz). 2016; 64(3): 249–54.
- Butera D, Tesoriere L, Di Gaudio F, Bongiorno A, Allegra M, Pintaudi AM, et al. Antioxidant activities of Sicilian prickly pear (Opuntia ficus indica) fruit extracts and reducing properties of its betalains: betanin and indicaxanthin. J Agr Food Chem 2002; 50(23): 6895–901.
- Tesoriere L, Allegra M, Butera D, Gentile C, Livrea MA. Cytoprotective effects of the antioxidant phytochemical indicaxanthin in beta-thalassemia red blood cells. Free Radic Res 2006; 40(7): 753–61.
- Tesoriere L, Allegra M, Butera D, Gentile C, Livrea MA. Kinetics of the lipoperoxyl radical-scavenging activity of indicaxanthin in solution and unilamellar liposomes. Free Radic Res 2007; 41(2): 226–33.
- Tesoriere L, Attanzio A, Allegra M, Gentile C, Livrea MA. Phytochemical indicaxanthin suppresses 7-ketocholesterol-induced THP-1 cell apoptosis by preventing cytosolic Ca(2+) increase and oxidative stress. Br J Nutr 2013; 110(2): 230–40.
- Tesoriere L, Gentile C, Angileri F, Attanzio A, Tutone M, Allegra M, et al. Trans-epithelial transport of the betalain pigments indicaxanthin and betanin across Caco-2 cell monolayers and influence of food matrix. Eur J Nutr 2013; 52(3): 1077–87.
- Allegra M, D’Acquisto F, Tesoriere L, Attanzio A, Livrea MA. Pro-oxidant activity of indicaxanthin from Opuntia ficus indica modulates arachidonate metabolism and prostaglandin synthesis through lipid peroxide production in LPS-stimulated RAW 264.7 macrophages. Redox Biol 2014; 2: 892–900.
- Allegra M, Ianaro A, Tersigni M, Panza E, Tesoriere L, Livrea MA. Indicaxanthin from cactus pear fruit exerts anti-inflammatory effects in carrageenin-induced rat pleurisy. J Nutr 2014; 144(2): 185–92.
- Tesoriere L, Attanzio A, Allegra M, Gentile C, Livrea MA. Indicaxanthin inhibits NADPH oxidase (NOX)-1 activation and NF-kappaB-dependent release of inflammatory mediators and prevents the increase of epithelial permeability in IL-1beta-exposed Caco-2 cells. Br J Nutr 2014; 111(3): 415–23.
- Allegra M, Carletti F, Gambino G, Tutone M, Attanzio A, Tesoriere L, et al. Indicaxanthin from Opuntia ficus-indica crosses the blood-brain barrier and modulates neuronal bioelectric activity in rat hippocampus at dietary-consistent amounts. J Agr Food Chem. 2015; 63(33): 7353–60.
- Tesoriere L, Attanzio A, Allegra M, Livrea MA. Dietary indicaxanthin from cactus pear (Opuntia ficus-indica, L. Mill) fruit prevents eryptosis induced by oxysterols in a hypercholesterolaemia-relevant proportion and adhesion of human erythrocytes to endothelial cell layers. Br J Nutr 2015; 114(3): 368–75.
- Tesoriere L, Butera D, Pintaudi AM, Allegra M, Livrea MA. Supplementation with cactus pear (Opuntia ficus-indica) fruit decreases oxidative stress in healthy humans: a comparative study with vitamin C. Am J Clin Nutr 2004; 80(2): 391–5.
- Bonaccio M, Cerletti C, Iacoviello L, de Gaetano G. Mediterranean diet and low-grade subclinical inflammation: the Moli-sani study. Endocr Metab Immune Disord Drug Targets 2015; 15(1): 18–24.
- Rocha VZ, Ras RT, Gagliardi AC, Mangili LC, Trautwein EA, Santos RD. Effects of phytosterols on markers of inflammation: a systematic review and meta-analysis. Atherosclerosis 2016; 248: 76–83.
- 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(4): 756–61.
- Labonte ME, Cyr A, Abdullah MM, Lepine MC, Vohl MC, Jones P, et al. Dairy product consumption has no impact on biomarkers of inflammation among men and women with low-grade systemic inflammation. J Nutr 2014; 144(11): 1760–7.
- Yu Z, Malik VS, Keum N, Hu FB, Giovannucci EL, Stampfer MJ, et al. Associations between nut consumption and inflammatory biomarkers. Am J Clin Nutr 2016; 104(3): 722–8.
- Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 2010; 49(11): 1603–16.
- Tesoriere L, Fazzari M, Allegra M, Livrea MA. Biothiols, taurine, and lipid-soluble antioxidants in the edible pulp of Sicilian cactus pear (Opuntia ficus-indica) fruits and changes of bioactive juice components upon industrial processing. J Agric Food Chem 2005; 53(20): 7851–5.
- Zello GA. Dietary Reference Intakes for the macronutrients and energy: considerations for physical activity. Appl Physiol Nutr Metab 2006; 31(1): 74–9.
- Chang S, Koegel K. Back to basics: all about myPlate food groups. J Acad Nutr Diet. 2017; 117(9): 1351–3.
- Strojnik T, Smigoc T, Lah TT. Prognostic value of erythrocyte sedimentation rate and C-reactive protein in the blood of patients with glioma. Anticancer Res 2014; 34(1): 339–47.
- Perrone A, Pintaudi AM, Traina A, Carruba G, Attanzio A, Gentile C, et al. Raman spectroscopic measurements of dermal carotenoids in breast cancer operated patients provide evidence for the positive impact of a dietary regimen rich in fruit and vegetables on body oxidative stress and BC prognostic anthropometric parameters: a five-year study. Oxid Med Cell Longev 2016; 2016: 2727403.
- Devaraj S, O’Keefe G, Jialal I. Defining the proinflammatory phenotype using high sensitive C-reactive protein levels as the biomarker. J Clin Endocrinol Metab 2005; 90(8): 4549–54.
- Wang XH, Liu SQ, Wang YL, Jin Y. Correlation of serum high-sensitivity C-reactive protein and interleukin-6 in patients with acute coronary syndrome. Genet Mol Res 2014; 13(2): 4260–6.
- Ridker PM. From C-reactive protein to interleukin-6 to interleukin-1: moving upstream to identify novel targets for atheroprotection. Circ Res 2016; 118(1): 145–56.
- Albers R, Bourdet-Sicard R, Braun D, Calder PC, Herz U, Lambert C, et al. Monitoring immune modulation by nutrition in the general population: identifying and substantiating effects on human health. Br J Nutr 2013; 110(Suppl 2): S1–30.
- Gonzalez-Gallego J, Garcia-Mediavilla MV, Sanchez-Campos S, Tunon MJ. Fruit polyphenols, immunity and inflammation. Br J Nutr 2010; 104(Suppl 3): S15–27.
- Koenig W. Predicting risk and treatment benefit in atherosclerosis: the role of C-reactive protein. Int J Cardiol 2005; 98(2): 199–206.
- Il’yasova D, Ivanova A, Morrow JD, Cesari M, Pahor M. Correlation between two markers of inflammation, serum C-reactive protein and interleukin 6, and indices of oxidative stress in patients with high risk of cardiovascular disease. Biomarkers 2008; 13(1): 41–51.
- Ivashchenko Y, Kramer F, Schafer S, Bucher A, Veit K, Hombach V, et al. Protein kinase C pathway is involved in transcriptional regulation of C-reactive protein synthesis in human hepatocytes. Arterioscler Thromb Vasc Biol 2005; 25(1): 186–92.
- Kluft C, de Maat MP. Genetics of C-reactive proteIn: new possibilities and complications. Arterioscler Thromb Vasc Biol 2003; 23(11): 1956–9.
- Tesoriere L, Allegra M, Butera D, Livrea MA. Absorption, excretion, and distribution of dietary antioxidant betalains in LDLs: potential health effects of betalains in humans. Am J Clin Nutr 2004; 80(4): 941–5.
- Mayne ST, Cartmel B, Scarmo S, Jahns L, Ermakov IV, Gellermann W. Resonance Raman spectroscopic evaluation of skin carotenoids as a biomarker of carotenoid status for human studies. Arch Biochem Biophys 2013; 539(2): 163–70.
- Forman HJ, Davies KJ, Ursini F. How do nutritional antioxidants really work: nucleophilic tone and para-hormesis versus free radical scavenging in vivo. Free Radic Biol Med 2014; 66: 24–35.
- Panickar KS, Jewell DE. The beneficial role of anti-inflammatory dietary ingredients in attenuating markers of chronic low-grade inflammation in aging. Horm Mol Biol Clin Investig 2015; 23(2): 59–70.
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