The effects of fish-based and milk-based diets on liver tissue antioxidant enzymes and lipid peroxidation in female Wistar rats: A pilot study

Nevena Vidović; Slavica Ranković; Zorana Oreščanin-Dušić; Jasmina Debeljak-Martačić; Tamara Popović; Mirko Tomić; Marija Glibetić

doi:10.2298/VSP180326122V

Nevena Vidović University of Belgrade, Institute for Medical Research Centre of Research Excellence in Nutrition and Metabolism, Belgrade, Serbia
Slavica Ranković University of Belgrade, Institute for Medical Research Centre of Research Excellence in Nutrition and Metabolism, Belgrade, Serbia
Zorana Oreščanin-Dušić University of Belgrade, Institute for Biological Research “Siniša Stanković”, Belgrade, Serbia
Jasmina Debeljak-Martačić University of Belgrade, Institute for Medical Research Centre of Research Excellence in Nutrition and Metabolism, Belgrade, Serbia
Tamara Popović University of Belgrade, Institute for Medical Research Centre of Research Excellence in Nutrition and Metabolism, Belgrade, Serbia
Mirko Tomić University of Belgrade, Institute for Biological Research “Siniša Stanković”, Belgrade, Serbia
Marija Glibetić University of Belgrade, Institute for Medical Research Centre of Research Excellence in Nutrition and Metabolism, Belgrade, Serbia

DOI: https://doi.org/10.2298/VSP180326122V

Keywords: antioxidants, catalase, enzymes, fatty acids, omega-3, fishes, food, lipid peroxidation, milk, rats, superoxide dismutase

Abstract

Background/Aim. Recently, there has been an increased interest in novel dietary antioxidants, including omega-3 fatty acids and bioactive proteins present in milk. The aim of this study was to examine potential antioxidant effects of four-weeks long fish-based and milk-based diets in female Wistar rats. Methods. Four-months old rats were divided into three groups receiving either: control diet, diet enriched with fish meal, or diet enriched with milk. The activities of antioxidant enzymes: glutathione peroxidase (GPx), superoxide dismutase (SOD) and catalase (CAT), and concentration of thiobarbituric acid reactive substances (TBARS) were determined in liver homogenates obtained at the end of the treatment period. Results. Statistically significant higher activities of GPx (3.52 ± 0.73 U/mg) and CAT (147.25 ± 15.93 U/mg) were detected in rats fed with fish-based meal in comparison with both the control (GPx: 1.93 ± 0.11 U/mg; CAT: 99.37 ± 10.03 U/mg) and the group fed with milk-based diet (GPx: 1.72 ± 0.52 U/mg; CAT: 104.18 ± 37.49 U/mg). Despite somewhat lower concentration of TBARS in the milk-treated group (0.88 ± 0.23 nmoL/mg), no significant differences were detected in comparison with other groups (the control group: 1.00 ± 0.08 nmoL/mg; the fish-based diet group: 1.13 ± 0.15 nmoL/mg). Conclusion. Diet enriched with fish could improve one’s oxidative status by enhancing activities of antioxidant enzymes in the liver tissue. On the contrary, we failed to obtain results suggesting that milk could serve as a source of dietary antioxidants.

References

Del Rio D, Rodriguez-Mateos A, Spencer JP, Tognolini M, Borges G, Crozier A. Dietary (poly)phenolics in human health: struc-tures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal 2013; 18(14): 1818–92.

Hooper L, Kroon PA, Rimm EB, Cohn JS, Harvey I, Le Cornu KA, et al. Flavonoids, flavonoid-rich foods, and cardiovascular risk: a meta-analysis of randomized controlled trials. Am J Clin Nutr 2008; 88(1): 38–50.

Calder PC. Functional Roles of Fatty Acids and Their Effects on Human Health. JPEN J Parenter Enteral Nutr 2015; 39(Suppl 1): 18S–32S.

Mozaffarian D, Wu JH. Omega-3 fatty acids and cardiovascular disease: effects on risk factors, molecular pathways, and clini-cal events. J Am Coll Cardiol 2011; 58(20): 2047–67.

Wander RC, Du SH. Oxidation of plasma proteins is not in-creased after supplementation with eicosapentaenoic and do-cosahexaenoic acids. Am J Clin Nutr 2000; 72(3): 731–7.

Tsuduki T, Honma T, Nakagawa K, Ikeda I, Miyazawa T. Long-term intake of fish oil increases oxidative stress and decreases lifespan in senescence-accelerated mice. Nutrition 2011; 27(3): 334–7.

Iraz M, Erdogan H, Ozyurt B, Ozugurlu F, Ozgocmen S, Fadillioglu E. Brief communication: omega-3 essential fatty acid supple-mentation and erythrocyte oxidant/antioxidant status in rats. Ann Clin Lab Sci 2005; 35(2): 169–73.

Arnal E, Miranda M, Johnsen-Soriano S, Alvarez-Nolting R, Diaz-Llopis M, Araiz J, et al. Beneficial effect of docosahexanoic acid and lutein on retinal structural, metabolic, and functional abnormalities in diabetic rats. Curr Eye Res 2009; 34(11): 928–38.

Priyamvada S, Khan SA, Khan MW, Khan S, Farooq N, Khan F, et al. Studies on the protective effect of dietary fish oil on ura-nyl-nitrate-induced nephrotoxicity and oxidative damage in rat kidney. Prostaglandins Leukot Essent Fatty Acids 2009; 82(1): 35–44.

Zanatta AL, Miranda DT, Dias BC, Campos RM, Massaro MC, Michelotto PV Jr, et al. Fish oil supplementation decreases oxi-dative stress but does not affect platelet-activating factor bio-activity in lungs of asthmatic rats. Lipids 2014; 49(7): 665–75.

Ide T. Physiological activities of the combination of fish oil and α-lipoic acid affecting hepatic lipogenesis and parameters related to oxidative stress in rats. Eur J Nutr 2018; 57(4): 1545–61.

Power-Grant O, McCormack WG, Ramia De Cap M, Amigo-Benavent M, Fitzgerald RJ, Jakeman P. Evaluation of the antiox-idant capacity of a milk protein matrix in vitro and in vivo in women aged 50-70 years. Int J Food Sci Nutr 2016; 67(3): 325–34.

Da Silva MS, Rudkowska I. Novel functional foods for optimal oxidative status in healthy ageing. Maturitas 2016; 93: 100–7.

Tong X, Li W, Xu JY, Han S, Qin LQ. Effects of whey protein and leucine supplementation on insulin resistance in non-obese insulin-resistant model rats. Nutrition 2014; 30(9): 1076–80.

Kim J, Paik HD, Yoon YC, Park E. Whey protein inhibits iron overload-induced oxidative stress in rats. J Nutr Sci Vitaminol (Tokyo) 2013; 59(3): 198–205.

Świeca M, Reguła J, Suliburska J, Złotek U, Gawlik-Dziki U. Ef-fects of gluten-free breads, with varying functional supple-ments, on the biochemical parameters and antioxidant status of rat serum. Food Chem 2015; 182: 268–74.

Alférez MJ, Rivas E, Díaz-Castro J, Hijano S, Nestares T, Moreno M, et al. Folic acid supplemented goat milk has beneficial ef-fects on hepatic physiology, haematological status and antiox-idant defence during chronic Fe repletion. J Dairy Res 2015; 82(1): 86–94.

Ranković S, Popović T, Debeljak-Martačić J, Petrović S, Tomić M, Ig-njatović Đ, et al. Liver phospholipids fatty acids composition in response to different types of diets in rats of both sexes. Li-pids Health Dis 2017; 16(1): 94.

Girotti MJ, Khan N, McLellan BA. Early measurement of sys-temic lipid peroxidation products in the plasma of major blunt trauma patients. J Trauma 1991; 31(1): 32–5.

Aebi H. Catalase in vitro. Methods Enzymol 1984; 105: 121–6.

Bu J, Dou Y, Tian X, Wang Z, Chen G. The Role of Omega-3 Polyunsaturated Fatty Acids in Stroke. Oxid Med Cell Longev 2016; 2016: 6906712.

An WS, Kim HJ, Cho KH, Vaziri ND. Omega-3 fatty acid supplementation attenuates oxidative stress, inflammation, and tubulointerstitial fibrosis in the remnant kidney. Am J Physiol Renal Physiol 2009; 297(4): F895–903.

Venkatraman JT, Chandrasekar B, Kim JD, Fernandes G. Effects of n-3 and n-6 fatty acids on the activities and expression on hepatic antioxidant enzymes in autoimmune-prone NZBxNZW F mice. Lipids 1994; 29(8): 561–8.

Dotan Y, Lichtenberg D, Pinchuk I. Lipid peroxidation cannot be used as a universal criterion of oxidative stress. Prog Lipid Res 2004; 43(3): 200–27.

Lluís L, Taltavull N, Muñoz-Cortés M, Sánchez-Martos V, Romeu M, Giralt M, et al. Protective effect of the omega-3 polyun-saturated fatty acids: Eicosapentaenoic acid/Docosahexaenoic acid 1:1 ratio on cardiovascular disease risk markers in rats. Lipids Health Dis 2013; 12: 140.

Hernández-Ledesma B, Dávalos A, Bartolomé B, Amigo L. Prepa-ration of antioxidant enzymatic hydrolysates from alpha-lactalbumin and beta-lactoglobulin. Identification of active peptides by HPLC-MS/MS. J Agric Food Chem 2005; 53(3): 588–93.

Pan D, Guo Y, Jiang X. Anti-fatigue and antioxidative activi-ties of peptides isolated from milk proteins. J Food Biochem 2011; 35(4): 1130–44.