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Dietary resveratrol impairs body weight gain due to reduction of feed intake without affecting fatty acid composition in Atlantic salmon

Published online by Cambridge University Press:  23 April 2018

D. Menoyo*
Affiliation:
Departamento de Producción Agraria, Universidad Politécnica de Madrid, ETS Ingenieros Agrónomos, 28040 Madrid, Spain
G. Kühn
Affiliation:
Departamento de Producción Agraria, Universidad Politécnica de Madrid, ETS Ingenieros Agrónomos, 28040 Madrid, Spain Institute of Human Nutrition and Food Science, University of Kiel, Hermann-Rodewald-Straße 6-8, D-24118 Kiel, Germany
N. Ruiz-Lopez
Affiliation:
Departamento de Producción Agraria, Universidad Politécnica de Madrid, ETS Ingenieros Agrónomos, 28040 Madrid, Spain
K. Pallauf
Affiliation:
Institute of Human Nutrition and Food Science, University of Kiel, Hermann-Rodewald-Straße 6-8, D-24118 Kiel, Germany
I. Stubhaug
Affiliation:
Skretting Aquaculture Research Centre (ARC), P.O. Box 319, N-4002 Stavanger, Norway
J. J. Pastor
Affiliation:
Lucta S.A., Can Parellada 28, 08170, Montornés del Vallés, Barcelona. Spain
I. R. Ipharraguerre
Affiliation:
Institute of Human Nutrition and Food Science, University of Kiel, Hermann-Rodewald-Straße 6-8, D-24118 Kiel, Germany
G. Rimbach
Affiliation:
Institute of Human Nutrition and Food Science, University of Kiel, Hermann-Rodewald-Straße 6-8, D-24118 Kiel, Germany
*
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Abstract

Recent studies suggest that the use of vegetable oils at expense of fish oil in aquaculture feeds might have potential negative effects on fish redox homeostasis and adiposity. Resveratrol (RESV) is a lipid-soluble phytoalexin present in fruits and vegetables with proven in vivo antioxidant function in animals. The present study aims to assess the potential use of RESV in Atlantic salmon feeds. To this end, post-smolt salmons with an initial BW of 148±3 g were fed four experimental diets for 15 weeks. A diet low in fish oil served as a control and was supplemented with 0, 0.5, 1.5 and 2.5 g/kg of RESV, respectively. The effect of the experimental diets on animal performance, tissue fatty acid composition, and the expression of genes encoding proteins involved in antioxidant signalling, lipid peroxidation, and metabolism were studied. Resveratrol significantly reduced feed intake and final BW of the salmon. Feeding RESV did not affect the sum of saturated and monounsaturated fatty acids or total lipids in the fillet. While the content of total polyunsaturated fatty acids was not affected, the percentages of some fatty acids in the liver and fillet were changed by RESV. Furthermore, in liver, the relative expression of glutathione peroxidase 4b, nuclear factor-like 2, and arachidonate 5-lipoxygenase remained unchanged across treatment groups. In conclusion, the negative impact of dietary RESV on FI and hence reduction of the BW discourages its inclusion in low fish oil diets for Atlantic salmon.

Type
Research Article
Copyright
© The Animal Consortium 2018 

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Footnotes

a

Present address: Department of Biochemistry and Molecular Biology, Edificio I+D, Campus de Teatinos Universidad de Málaga 29010, Málaga, Spain.

References

Avila, P, Marques, SO, Luciano, TF, Vitto, MF, Engelmann, J, Souza, DR, Pereira, SV, Pinho, RA, Lira, FS and De Souza, CT 2013. Resveratrol and fish oil reduce catecholamine-induced mortality in obese rats: role of oxidative stress in the myocardium and aorta. British Journal of Nutrition 110, 15801590.Google Scholar
Azorín-Ortuño, M, Yáñez-Gascón, MJ, Vallejo, F, Pallarés, FJ, Larrosa, M, Lucas, R, Morales, JC, Tomás-Barberán, FA, García-Conesa, MT and Espín, JC 2011. Metabolites and tissue distribution of resveratrol in the pig. Molecular Nutrition and Food Research 55, 11541168.Google Scholar
Bou, M, Berge, GM, Baeverfjord, G, Sigholt, T, Østbye, T-K and Ruyter, B 2017. Low levels of very-long-chain n-3 PUFA in Atlantic salmon (Salmo salar) diet reduce fish robustness under challenging condition in sea cages. Journal of Nutritional Science 6, e32.Google Scholar
Calder, PC 2012. The role of marine omega-3 (n-3) fatty acids in inflammatory processes, atherosclerosis and plaque stability. Molecular Nutritrition Food Research 56, 10731080.Google Scholar
Caro, M, Sansone, A, Amézaga, J, Navarro, V, Ferreri, C and Tueros, I 2017. Wine lees modulate lipid metabolism and induce fatty acid remodelling in Zebrafish. Food & Function 8, 16521659.Google Scholar
Fiesel, A, Gessner, DK, Most, E and Eder, K 2014. Effects of dietary polyphenol-rich plant products from grape or hop on pro-inflammatory gene expression in the intestine, nutrient digestibility and faecal microbiota of weaned pigs. BMC Veterinary Research 10, 196.Google Scholar
Gilbert, NC, Bartlett, SG, Waight, MT, Neau, DB, Boeglin, WE, Brash, AR and Newcomer, ME 2011. The structure of human 5-lipoxygenase. Science 331, 217219.Google Scholar
Grahl-Nielsen, O and Barnung, T 1985. Variations in the fatty acid profile of marine animals caused by environmental and developmental changes. Marine Environmental Research 17, 218221.Google Scholar
Hamre, K, Torstensen, BE, Maage, A, Waagbø, R, Berge, RK and Albrektsen, S 2010. Effects of dietary lipid, vitamins and minerals on total amounts and redox status of glutathione and ubiquinone in tissues of Atlantic salmon (Salmo salar): a multivariate approach. British Journal of Nutrition 104, 980988.Google Scholar
Keum, Y-S and Choi, BY 2014. Molecular and chemical regulation of the Keap1-Nrf2 signaling pathway. Molecules 19, 1007410089.Google Scholar
Kim, S, Lee, YH, Han, M, Mar, W, Kim, W and Nam, K 2010. Resveratrol, purified from the stem of vitis coignetiae pulliat, inhibits food intake in C57BL/6J mice. Archives of Pharmacology Research 33, 775780.Google Scholar
La Porte, C, Voduc, N, Zhang, G, Seguin, I, Tardiff, D, Singhal, N and Cameron, DW 2010. Steady-state pharmacokinetics and tolerability of trans-resveratrol 2000 mg twice daily with food, quercetin and alcohol (ethanol) in healthy human subjects. Clinical Pharmacokinetics 49, 449454.Google Scholar
Leaver, MJ, Villeneuve, LA, Obach, A, Jensen, L, Bron, JE, Tocher, DR and Taggart, JB 2008. Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genomics 9, 299.Google Scholar
López-Vélez, M, Martínez-Martínez, F and Del Valle-Ribes, C 2003. The study of phenolic compounds as natural antioxidants in wine. Critical Reviews in Food Science and Nutrition 43, 233244.Google Scholar
Malhotra, A, Bath, S and Elbarbry, F 2015. An organ system approach to explore the antioxidative, anti-inflammatory, and cytoprotective actions of resveratrol. Oxidative Medicine and Cellular Longevity 2015, 803971.Google Scholar
Martinez-Rubio, L, Evensen, Ø, Krasnov, A, Jørgensen, SM, Wadsworth, S, Ruohonen, K, Vecino, JLG and Tocher, DR 2014. Effects of functional feeds on the lipid composition, transcriptomic responses and pathology in heart of Atlantic salmon (Salmo salar L.) before and after experimental challenge with piscine myocarditis virus (PMCV). BMC Genomics 15, 462.Google Scholar
Menoyo, D, Sanz-Bayón, C, Nessa, AH, Esatbeyoglu, T, Faizan, M, Pallauf, K, de Diego, N, Wagner, AE, Ipharraguerre, I, Stubhaug, I and Rimbach, G 2014. Atlantic salmon (Salmo salar L.) as a marine functional source of gamma-tocopherol. Marine Drugs 12, 59445959.Google Scholar
Minghetti, M, Leaver, MJ and Tocher, DR 2011. Transcriptional control mechanisms of genes of lipid and fatty acid metabolism in the Atlantic salmon (Salmo salar L.) established cell line, SHK-1. Biochimica et Biophysica Acta 1811, 194202.Google Scholar
Momchilova, A, Petkova, D, Staneva, G, Markovska, T, Pankov, R, Skrobanska, R, Nikolova-Karakashian, M and Koumanov, K 2014. Resveratrol alters the lipid composition, metabolism and peroxide level in senescent rat hepatocytes. Chemico-Biological Interactions 207, 7480.Google Scholar
Moreno, JJ 2000. Resveratrol modulates arachidonic acid release, prostaglandin synthesis, and 3T6 fibroblast growth. Journal of Pharmacology and Experimental Therapeutics 294, 333338.Google Scholar
National Research Council (NRC) 2011. Nutrient requirements of fish and shrimp, 2nd revised (edition. National Academy Press, Washington, DC, USA.Google Scholar
Pallarès, V, Calay, D, Cedó, L, Castell-Auví, A, Raes, M, Pinent, M, Ardévol, A, Arola, L and Blay, M 2012. Enhanced anti-inflammatory effect of resveratrol and EPA in treated endotoxin-activated RAW 264.7 macrophages. British Journal of Nutrition 108, 15621573.Google Scholar
Robb, EL, Page, MM, Wiens, BE and Stuart, JA 2008. Molecular mechanisms of oxidative stress resistance induced by resveratrol: specific and progressive induction of MnSOD. Biochemical and Biophysical Research Communications 367, 406412.Google Scholar
Saera-Vila, A, Benedito-Palos, L, Sitjà-Bobadilla, A, Nácher-Mestre, J, Serrano, R, Kaushik, S and Pérez-Sánchez, J 2009. Assessment of the health and antioxidant trade-off in gilthead sea bream (Sparus aurata L.) fed alternative diets with low levels of contaminants. Aquaculture 296, 8795.Google Scholar
Schiller Vestergren, A, Wagner, L, Pickova, J, Rosenlund, G, Kamal-Eldin, A and Trattner, S 2012. Sesamin modulates gene expression without corresponding effects on fatty acids in Atlantic salmon (Salmo salar L.). Lipids 47, 897911.Google Scholar
Segura, J and López-Bote, CJ 2014. A laboratory efficient method for intramuscular fat analysis. Food Chemistry 145, 821825.Google Scholar
Sevov, M, Elfineh, L and Cavelier, LB 2006. Resveratrol regulates the expression of LXR-a in human macrophages. Biochemical and Biophysical Research Communications 348, 10471054.Google Scholar
Steibel, JP, Poletto, R, Coussens, PM and Rosa, GJM 2009. A powerful and flexible linear mixed model framework for the analysis of relative quantification RT-PCR data. Genomics 94, 146152.Google Scholar
Torno, C, Staats, S, Pascual-Teresa, S, Rimbach, G and Schulz, C 2017. Fatty acid profile is modulated by dietary resveratrol in rainbow trout (Oncorhynchus mykiss). Marine Drugs 15, 252.Google Scholar
Torstensen, BE, Espe, M, Sanden, M, Stubhaug, I, Waagbø, R, Hemre, GI, Fontanillas, R, Nordgarden, U, Hevrøy, EM, Olsvik, P and Berntssen, MHG 2008. Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 285, 193200.Google Scholar
Trenzado, CE, Morales, AE, Palma, JM and de la Higuera, M 2009. Blood antioxidant defenses and hematological adjustments in crowded/uncrowded rainbow trout (Oncorhynchus mykiss) fed on diets with different levels of antioxidant vitamins and HUFA. Comparative Biochemistry and Physiology C Toxicology and Pharmacology 149, 440447.Google Scholar
Turchini, GM, Torstensen, BE and Ng, WK 2009. Fish oil replacement in finfish nutrition. Reviews in Aquaculture 1, 1057.Google Scholar
Valenzano, DR, Terzibasi, E, Genade, T, Cattaneo, A, Domenici, L and Cellerino, A 2006. Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate. Current Biology 16, 296300.Google Scholar
Wang, L, Harris, SM, Espinoza, HM, McClain, V and Gallagher, EP 2012. Characterization of phospholipid hydroperoxide glutathione metabolizing peroxidase (gpx4) isoforms in Coho salmon olfactory and liver tissues and their modulation by cadmium. Aquatic Toxicology 114–115, 134141.Google Scholar
Zhang, D, Yan, Y, Tian, H, Jiang, G, Li, X and Liu, W 2018. Resveratrol supplementation improves lipid and glucose metabolism in high-fat diet-fed blunt snout bream. Fish Physiology and Biochemistry 44, 163173.Google Scholar