Skip to main content Accessibility help
×
Home

Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.)

  • Bente E. Torstensen (a1), Marit Espe (a1), Ingunn Stubhaug (a1) (a2) and Øyvind Lie (a1)

Abstract

In order to study whether lipid metabolism may be affected by maximum replacement of dietary fish oil and fish meal with vegetable oils (VO) and plant proteins (PP), Atlantic salmon (Salmo salar L.) smolts were fed a control diet containing fish oil and fish meal or one of three plant-based diets through the seawater production phase for 12 months. Diets were formulated to meet all known nutrient requirements. The whole-body lipid storage pattern was measured after 12 months, as well as post-absorptive plasma, VLDL and liver TAG. To further understand the effects on lipid metabolism, expression of genes encoding for proteins involved in VLDL assembly (apoB100), fatty acid uptake (FATP1, cd36, LPL and FABP3, FABP10 and FABP11) were measured in liver and visceral adipose tissue. Maximum dietary VO and PP increased visceral lipid stores, liver TAG, and plasma VLDL and TAG concentrations. Increased plasma TAG correlated with an increased expression of apoB100, indicating increased VLDL assembly in the liver of fish fed the high-plant protein- and VO-based diet. Atlantic salmon fed intermediate replacement levels of VO or PP did not have increased body fat or visceral mass. Overall, the present results demonstrate an interaction between dietary lipids and protein on lipid metabolism, increasing overall adiposity and TAG in the body when fish meal and fish oil are replaced concomitantly at maximised levels of VO and PP.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.)
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.)
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.)
      Available formats
      ×

Copyright

Corresponding author

*Corresponding author: Dr Bente E. Torstensen, fax +47 55905299, email bente.torstensen@nifes.no

References

Hide All
1Tacon, AGJ, Hasan, MR & Subasinghe, RP (2006) Use of Fishery Resources as Feed Inputs for Aquaculture Development: Trends and Policy Implications. FAO Fisheries Circular no. 1018. Rome: FAO.
2Torstensen, BE, Bell, JG, Rosenlund, G, et al. (2005) Tailoring of Atlantic salmon (Salmo salar L.) flesh lipid composition and sensory quality by replacing fish oil with a vegetable oil blend. J Agric Food Chem 53, 1016610178.
3Turchini, GM, Torstensen, BT & Ng, WK (2009) Fish oil replacement in finfish nutrition. Rev Aquacult 1, 1057.
4Hertrampf, JW & Piedad-Pascual, F (2000) Handbook on Ingredients for Aquaculture Feeds. Dordrecht, The Netherlands: Kluwer Academic Publishers.
5Leaver, MJ, Bautista, JM, Bjornsson, BT, et al. (2008) Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev Fish Sci 16, 7394.
6Dias, J, Alvarez, MJ, Arzel, J, et al. (2005) Dietary protein source affects lipid metabolism in the European seabass (Dicentrarchus labrax). Comp Biochem Physiol A 142, 1931.
7Kaushik, SJ & Seiliez, I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquacult Res 41, 322332.
8Messina, M, Tulli, F, Messina, C, et al. (2007) Varying plant protein sources in the diet of sea bass Deicentrarchus labrax differently affects lipid metabolism and deposition. Ital J Anim Sci 6, 806808.
9Jordal, A-EO, Lie, Ø & Torstensen, BE (2007) Complete replacement of dietary fish oil with a vegetable oil blend affect liver lipid and plasma lipoprotein levels in Atlantic salmon (Salmo salar L.). Aquacult Nutr 13, 114130.
10Ruyter, B, Moya-Falcón, C, Rosenlund, G, et al. (2006) Fat content and morphology of liver and intestine of Atlantic salmon (Salmo salar): effects of temperature and dietary soybean oil. Aquaculture 252, 441452.
11Torstensen, BE, Nanton, DA, Olsvik, PA, et al. (2009) Gene expression of fatty acid binding proteins (FABPs), fatty acid transport proteins (cd36 and FATP) and β-oxidation related genes in Atlantic salmon (Salmo salar L.) fed fish oil or vegetable oil. Aquacult Nutr 15, 440445.
12Ranheim, T, Gedde-Dahl, A, Rustan, AC, et al. (1994) Effect of chronic incubation of CaCo-2 cells with eicosapentaenoic acid (20:5n-3) and oleic acid (18:1n-9) on triacylglycerol production. Biochem J 303, 155161.
13Vegusdal, A, Gjøen, T, Berge, RK, et al. (2005) Effect of 18:1n-9, 20:5n-3 and 22:6n-3 on lipid accumulation and secretion by Atlantic salmon hepatocytes. Lipids 40, 477486.
14Halvorsen, B, Rustan, AC, Madsen, L, et al. (2001) Effects of long-chain monounsaturated and n-3 fatty acids on fatty acid oxidation and lipid composition in rats. Ann Nutr Metab 45, 3037.
15Berge, RK, Madsen, L, Vaagenes, H, et al. (1999) In contrast with docosahexaenoic acid, eicosapentaenoic acid and hypolipidaemic derivatives decrease hepatic synthesis and secretion of triacylglycerol acyltransferase activity and stimulation of fatty acid oxidation. Biochem J 343, 191197.
16Madsen, L, Rustan, AC, Vaagenes, H, et al. (1999) Eicosapentaenoic and docosahexaenoic acid affect mitochondrial and peroxisomal fatty acid oxidation in relation to substrate preference. Lipids 34, 951963.
17Nossen, , Rustan, AC, Gloppestad, SH, et al. (1986) Eicosapentaenoic acid inhibits synthesis and secretion of triacylglycerols by cultured rat hepatocytes. Biochim Biophys Acta 879, 5665.
18Willumsen, N, Vaagenes, H, Asiedu, D, et al. (1996) Eicosapentaenoic acid but not docosahexaenoic acid (both as ethyl esters) increases mitochondrial fatty acid oxidation and upregulates 2,4-dienoyl-CoA reductase gene expression. A potential mechanism for the hypolipidemic action of fish oil in rats. Lipids 31, 579592.
19Frøyland, L, Madsen, L, Vaagenes, H, et al. (1997) Mitochondrion is the principal target for nutritional and pharmacological control of triglyceride metabolism. J Lipid Res 38, 18511858.
20Frøyland, L, Vaagenes, H, Asiedu, DK, et al. (1996) Chronic administration of eicosapentaenoic acid and docosahexaenoic acid as ethyl esters reduced plasma cholesterol and changed the fatty acid composition in rat blood and organs. Lipids 31, 169178.
21Lang, CA & Davis, RA (1990) Fish oil fatty acids impair VLDL assembly and/or secretion by cultured rat hepatocytes. J Lipid Res 31, 20792086.
22Brown, AM, Castle, J, Hebbachi, AM, et al. (1999) Administration of n-3 fatty acids in the diets of rats directly to hepatocyte cultures results in different effects on hepatocellular ApoB metabolism and secretion. Arterioscler Thromb Vasc Biol 19, 106114.
23Kendrick, JS & Higgins, JA (1999) Dietary fish oils inhibit early events in the assembly of very low density lipoproteins and target ApoB for degradation within the rough endoplasmatic reticulum of hamster hepatocytes. J Lipid Res 40, 504514.
24Harris, WS, Connor, WE & McMurphy, MP (1983) The comparative reductions of the plasma lipids and lipoproteins by dietary polyunsaturated fats: salmon oil versus vegetable oils. Metabolism 32, 179184.
25Nestel, PJ (1990) Effects of n-3 fatty acids on lipid metabolism. Ann Rev Nutr 10, 149167.
26Bang, HO, Dyerberg, J & Nielsen, AB (1971) Plasma lipid and lipoprotein pattern in Greenlandic west-coast eskimos. Lancet i, 11431145.
27Seierstad, SL, Seljeflot, I, Johansen, O, et al. (2005) Dietary intake of differently fed salmon; the influence on markers of human atherosclerosis. Eur J Clin Invest 35, 5259.
28de Francesco, M, Parisi, G, Medale, F, et al. (2004) Effect of long term feeding with a plant protein mixture based diet on growth and body/fillet quality traits of large rainbow trout, Oncorhynchus mykiss. Aquaculture 263, 413429.
29Espe, M, Lemme, A, Petri, A, et al. (2006) Can Atlantic salmon grow on diets devoid of fish meal? Aquaculture 255, 255262.
30Espe, M, Lemme, A, Petri, A, et al. (2007) Assessment of lysine requirement for maximal protein accretion in Atlantic salmon using plant protein diets. Aquaculture 263, 168178.
31Gomes, EF, Rema, P & Kaushik, SJ (1995) Replacement of fish meal by plant proteins in the diet of rainbow trout (Oncorhynchus mykiss): digestibility and growth performance. Aquaculture 130, 177186.
32Kaushik, SJ, Cravedi, JP, Lalles, JP, et al. (1995) Partial or total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout, Oncorhynchus mykiss. Aquaculture 133, 257274.
33Kaushik, SJ, Covès, D, Dutto, G, et al. (2004) Almost total replacement of fish meal by plant protein sources in the diet of a marine teleost, the European sea bass, Dicentrarchus labrax. Aquaculture 230, 391404.
34Espe, M, Rathore, RM, Du, Z-Y, et al. (2010) Methionine limitation results in increased hepatic FAS activity, higher liver 18:1 to 18:0 fatty acid ratio and hepatic TAG accumulation in Atlantic salmon, Salmo salar. Amino Acids 39, 449460.
35Rathore, RM, Liaset, B, Hevrøy, EM, et al. (2010) Lysine limitation alters the storage pattern of protein, lipid and glycogen in on-growing Atlantic salmon. Aquacult Res 41, e751e759.
36Torstensen, BE, Espe, M, Sanden, M, et al. (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.
37Gaber, MMA (2005) The effect of different levels of krill meal supplementation of soybean-based diets on feed intake, digestibility, and chemical composition of juvenile Nile tilapia Oreochromis niloticus, L. J World Aquacult Soc 36, 346353.
38Olsen, RE, Suontama, J, Langmyhr, E, et al. (2006) The replacement of fish meal with Antarctic krill, Euphausia superba in diets for Atlantic salmon, Salmo salar. Aquacult Nutr 12, 280290.
39National Research Council (1993) Nutrient Requirements of Fish. Washington, DC: National Academy Press.
40Lie, Ø & Lambertsen, G (1991) Fatty acid composition of glycerophospholipids in seven tissues of cod (Gadus morhua), determined by combined high-performance liquid chromatography and gas chromatography. J Chromatogr 565, 119129.
41Torstensen, BE, Frøyland, L & Lie, Ø (2004) Replacing dietary fish oil with increasing levels of rapeseed oil and olive oil – effects on Atlantic salmon (Salmo salar) tissue and lipoprotein composition and lipogenic enzyme activities. Aquacult Nutr 10, 175192.
42Ackman, RG (1980) Fish Lipids. Farnham: Fishing News Books.
43Bell, JG, Dick, JR, McVicar, AH, et al. (1993) Dietary sunflower, linseed and fish oils affect phospholipid fatty acid composition, development of cardiac lesions, phospholipase activity and eicosanoid production in Atlantic salmon. Prostaglandins Leukot Essent Fatty Acids 49, 665673.
44Vitello, F & Zanetta, J-P (1978) Thin-layer chromatography of phospholipids. J Chromatogr 166, 637640.
45Havel, RJ, Eder, HA & Havel, RJ (1955) The distribution and chemical composition of ultra-centrifugally separated lipoproteins in human sera. J Clin Invest 34, 13451353.
46Aviram, A (1983) Plasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med 30, 111118.
47Lie, Ø, Sandvin, A & Waagboe, R (1994) Transport of α-tocopherol in Atlantic salmon (Salmo salar) during vitellogenesis. Fish Physiol Biochem 13, 241247.
48Warnick, GR, Cheung, MC & Albers, JJ (1979) Comparison of current methods for high-density lipoprotein cholesterol quantitation. Clin Chem 25, 596604.
49Simon, P (2003) Q-Gene: processing quantitative real-time RT-PCR data. Bioinformatics 19, 14391440.
50Olsvik, PA, Lie, KK, Jordal, A-EO, et al. (2005) Selection of normalizing genes in quantitative real time RT-PCR: a case study of Atlantic salmon. BMC Mol Biol 6, 21.
51Vandesompele, J, Preter, KD, Pattyn, F, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3, research0034.0031–research0034.0011.
52Zar, JH (1984) Biostatistical Analysis, pp. 253260. Englewood Cliffs, NY: Prentice-Hall.
53Sokal, RR & Rohlf, FJ (1981) Assumptions of analysis of variance. In Biometry, pp. 392450. New York: W.H. Freeman & Co.
54Gudbrandsen, OA, Wergedahl, H, Mork, S, et al. (2006) Dietary soya protein concentrate enriched with isoflavones reduced fatty liver, increased hepatic fatty acid oxidation and decreased the hepatic mRNA level of VLDL receptor in obese Zucker rats. Br J Nutr 96, 249257.
55Liaset, B, Madsen, L, Hao, Q, et al. (2009) Fish protein hydrolysate elevates plasma bile acids and reduces visceral adipose tissue mass in rats. Biochim Biophys Acta 1791, 254262.
56Nagao, K & Yanagita, T (2008) Bioactive lipids in metabolic syndrome. Prog Lipid Res 47, 127146.
57Torres, N, Torre-Villalvazo, I & Tovar, AR (2006) Regulation of lipid metabolism by soy protein and its implication in diseases mediated by lipid disorders. J Nutr Biochem 17, 365373.
58Tovar, AR & Torres, N (2010) The role of dietary protein on lipotoxicity. Biochim Biophys Acta 1801, 367371.
59Wergedahl, H, Gudbrandsen, OA, Røst, TH, et al. (2009) Combination of fish oil and fish protein concentrate reduces the plasma cholesterol level with a concurrent increase in hepatic level in high-fat-fed Wistar rats. Nutr Food Sci 25, 98104.
60Lombardo, YB, Hein, G & Chicco, A (2007) Metabolic syndrome: effects of n-3 PUFAs on a model of dyslipidemia, insulin resistance and adiposity. Lipids 42, 427437.
61Todorcević, M, Vegusdal, A, Gjøen, T, et al. (2008) Changes in fatty acids metabolism during differentiation of Atlantic salmon preadipocytes; effects of n-3 and n-9 fatty acids. Biochim Biophys Acta 1781, 326335.
62Huang, TS, Todorcevic, M, Ruyter, B, et al. (2009) Altered expression of CCAAT/enhancer binding protein and FABP11 genes during adipogenesis in vitro in Atlantic salmon (Salmo salar). Aquacult Nutr 16, 7280.
63Kim, HK, La-Fera, M, Lin, J, et al. (2006) Docosahexaenoic acid inhibits adipocyte differentiation and induces apoptosis in 3T3-L1 preadipocytes. J Nutr 136, 29652969.
64Belzung, F, Raclot, T & Groscolas, R (1993) Fish-oil n-3 fatty-acids selectively limit the hypertrophy of abdominal fat depots in growing rats fed high-fat diets. Am J Physiol 264, R1111R1118.
65Okuno, M, Kajiwara, K, Imai, S, et al. (1997) Perilla oil prevents the excessive growth of visceral adipose tissue in rats by down-regulating adipocyte differentiation. J Nutr 127, 17521757.
66Carlotti, M, Hainault, I, Guichard, C, et al. (1993) Beneficial-effects of a fishoil enriched high lard diet on obesity and hyperlipemia in Zucker rats. Ann N Y Acad Sci 683, 349350.
67Cunnane, SC, Mcadoo, KR & Horrobin, DF (1986) n-3 Essential fatty-acids decrease weight-gain in genetically-obese mice. Br J Nutr 56, 8795.
68Ikemoto, S, Takahashi, M, Tsunoda, N, et al. (1996) High-fat diet-induced hyperglycemia and obesity in mice: differential effects of dietary oils. Metab Clin Exp 45, 15391546.
69Jones, PJH (1989) Effect of fatty-acid composition of dietary-fat on energy-balance and expenditure in hamsters. Can J Physiol Pharm 67, 994998.
70Smith, AJ, Sanders, MA, Juhlmann, BE, et al. (2008) Mapping of the hormone-sensitive lipase binding site on the adipocyte fatty acid-binding protein (AFABP). Identification of the charge quartet on the AFABP/aP2 helix-turn-helix domain. J Biol Chem 283, 3353633543.
71Baar, RA, Dingfelder, CS, Smith, LA, et al. (2005) Investigation of in vivo fatty acid metabolism in AFABP/aP2− / −  mice. Am J Physiol Endocrinol Metab 288, E187E193.
72Agulleiro, MJ, André, M, Morais, S, et al. (2007) High transcript level of fatty acid-binding protein 11 but not of very low-density lipoprotein receptor is correlated to ovarian follicle atresia in a teleost fish (Solea senegalensis). Biol Reprod 77, 504516.
73Espe, M, Hevrøy, EM, Liaset, B, et al. (2008) Methionine intake affects hepatic sulphur metabolism in Atlantic salmon, Salmo salar. Aquaculture 274, 132141.
74Mato, JM, Corrales, FJ, Lu, SC, et al. (2002) S-adenosylmethionine: a control switch that regulates liver function. FASEB J 16, 1526.
75Bogevik, AS, Tocher, DR, Langmyhr, E, et al. (2009) Atlantic salmon (Salmo salar) postsmolts adapt lipid digestion according to elevated dietary wax esters from Calanus finmarchius. Aquacult Nutr 15, 94103.
76Yamamoto, T, Suzuki, N, Furuita, H, et al. (2007) Supplemental effect of bile salts to soybean meal-based diet on growth and feed utilization of rainbow trout Oncorhynchus mykiss. Fish Sci 73, 123131.
77Yokogoshi, H & Oda, H (2002) Dietary taurine enhances cholesterol degradation and reduces serum and liver cholesterol concentrations in rats fed a high cholesterol diet. Amino Acids 23, 433439.
78Chen, W, Matuda, K, Nishimura, N, et al. (2004) The effect of taurine on cholesterol degradation in mice fed a high-cholesterol diet. Life Sci 74, 18891898.
79Watanabe, M, Houten, SM, Wang, L, et al. (2004) Bile acids lower triglyceride levels via a pathway involving FXR, SHP, and SREBP-1C. J Clin Invest 113, 14081418.
80Espe, M, Liaset, B, Hevrøy, EM, et al. (2010) dl-Methionine enrichment in diets fed to Atlantic salmon increases apparent digestibility. Aquacult Res (epublication ahead of print version 11 November 2010).
81Espe, M, Ruohonen, K & El-Mowafi, A (2011) Effect of taurine supplementation on the metabolism and body lipid-to-protein ratio in juvenile Atlantic salmon (Salmo salar). Aquacult Res (In the Press).
82Noga, AA & Vance, DE (2003) Insights into the requirement of phosphatidylcholine synthesis for liver function in mice. J Lipid Res 44, 19982005.
83Vance, DE (2008) Role of phosphatidylcholine biosynthesis in the regulation of lipoprotein homeostasis. Curr Opin Lipidol 19, 229234.
84Anstee, QM & Goldin, RD (2006) Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Path 87, 116.
85Chawla, RK, Watson, WH, Eastin, CE, et al. (1998) S-adenosylmethionine deficiency and TNF-α in lipopolysaccharide-induced hepatic injury. Am J Physiol 275, G125G129.
86Griffin, ME, Wilson, KA, White, MR, et al. (1994) Dietary choline requirement of juvenile hybrid striped bass. J Nutr 124, 16851689.
87Slow, S & Garrow, TA (2006) Liver choline dehydrogenase and kidney betain-homocysteine methyltrasferase expression are not affected by methionine or choline intake in growing rats. J Nutr 136, 22792283.
88Tocher, DR, Bendiksen, EA, Campbell, PJ, et al. (2008) The role of phospholipids in nutrition and metabolism of teleost fish. Aquaculture 280, 2134.
89Kjær, MA, Vegusdal, A, Gjøen, T, et al. (2008) Effect of rapeseed oil and dietary n-3 fatty acids on triacylglycerol synthesis and secretion in Atlantic salmon hepatocytes. Biochim Biophys Acta 1781, 112122.
90Wang, HX, Chen, XL & Fisher, EA (1993) n-3 Fatty-acids stimulate intracellular degradation of apoprotein B in rat hepatocytes. J Clin Invest 91, 13801389.
91Wong, SH, Fisher, EA & Marsh, JB (1989) Effects of eicosapentaenoic and docosahexaenoic acids on apoprotein-B messenger-RNA and secretion of very low-density lipoprotein in HepG2 cells. Arteriosclerosis 9, 836841.
92Sundaram, M & Yao, ZM (2010) Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr Metab 7, 35.
93Caballero, MJ, Izquierdo, MS, Kjørsvik, E, et al. (2003) Morphological aspects of intestinal cells from gilthead seabream (Sparus aurata) fed diets containing different lipid sources. Aquaculture 225, 325340.
94Caballero, MJ, Obach, A, Rosenlund, G, et al. (2002) Impact of different dietary lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Onchorhynchus mykiss. Aquaculture 214, 253271.
95Olsen, RE, Myklebust, R, Kaino, T, et al. (1999) Lipid digestibility and ultrastructural changes in the enterocytes of Arctic char (Salvelinus alpinus L.) fed linseed oil and soyabean lecithin. Fish Physiol Biochem 21, 3544.
96Cheal, KL, Abbasi, F, Lamendola, C, et al. (2004) Relationship to insulin resistance of the adult treatment panel III diagnostic criteria for identification of the metabolic syndrome. Diabetes 53, 11951200.

Keywords

Dietary plant proteins and vegetable oil blends increase adiposity and plasma lipids in Atlantic salmon (Salmo salar L.)

  • Bente E. Torstensen (a1), Marit Espe (a1), Ingunn Stubhaug (a1) (a2) and Øyvind Lie (a1)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed