Substitution of dietary fish oil with plant oils is associated with shortened mid intestinal folds in Atlantic salmon (Salmo salar)

BMC Veterinary Research

Erling Olaf Koppang¹  Magne Kaldhusdal³  Ole Bendik Dale³  Grethe Rosenlund²  Bente E Torstensen⁴  Lars Austbø¹  Jannicke Wiik-Nielsen³  Guro Løkka¹  Torfinn Moldal³ 

[1] Norwegian School of Veterinary Science, Post Box 8146 Dep, 0033 Oslo, Norway;Skretting ARC, Post Box 48, 4001 Stavanger, Norway;Norwegian Veterinary Institute, Post Box 750 Sentrum, 0106 Oslo, Norway;National Institute of Nutrition and Seafood Research, Post Box 2029 Nordnes, 5817 Bergen, Norway

关键词: Real-time PCR;    Plant oils;    Morphometric analyses;    Intestine;    Inflammation;    Fish oil;    Fatty acids;    Atlantic salmon;   

Others  :  1119310
DOI  :  10.1186/1746-6148-10-60

 received in 2013-11-19, accepted in 2014-02-25,  发布年份 2014

【 摘 要 】

Background

Fish meal and fish oil are increasingly replaced by ingredients from terrestrial sources in the feeds for farmed salmonids due to expanding production and reduced availability of marine feed raw material. Fish oil that is rich in n-3 polyunsaturated fatty acids is considered beneficial to human health in general and to prevent intestinal inflammation and carcinogenesis in particular. In contrast, n-6 fatty acids that are present in many vegetable oils have been associated with increased risk of colitis and colon cancer in rodents and humans, as well as lowered transcription levels of certain stress and antioxidant-related genes in Atlantic salmon.

The aim of the present study was to investigate the intestinal health in Atlantic salmon fed with different vegetable oils as partial substitutes of fish oil in the diet. A feed trial lasting for 28 weeks included one reference diet containing fish oil as the sole lipid source and three diets where 80% of the fish oil was replaced by a plant oil blend with either olive oil, rapeseed oil or soybean oil as the main lipid source. These plant oils have intermediate or low n-3/n-6-ratios compared to fish oil having a high n-3/n-6-ratio. The protein and carbohydrate fractions were identical in all the feeds.

Results

Morphometric measurements showed significantly shorter folds in the mid intestine in all groups fed vegetable oils compared to the group fed fish oil. In the distal intestine, the complex folds were significantly shorter in the fish fed soybean oil compared to the fish fed rapeseed oil. Histological and immunohistochemical examination did not show clear difference in the degree of inflammation or proliferation of epithelial cells related to dietary groups, which was further confirmed by real-time RT-PCR which revealed only moderate alterations in the mRNA transcript levels of selected immune-related genes.

Conclusions

Shortened intestinal folds might be associated with reduced intestinal surface and impaired nutrient absorption and growth, but our results suggest that partial substitution of dietary fish oil with vegetable oils does not have any major negative impact on the intestinal health of Atlantic salmon.

【 授权许可】

   
2014 Moldal et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Forster I, Gatlin DM, Goldburg RJ, Hua K, Nichols PD: Feeding aquaculture in an era of finite resources. Proc Natl Acad Sci USA 2009, 106:15103-15110.
• [2]Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbø R, Hemre GI, Fontanillas R, Nordgarden U, Hevrøy EM, Olsvik P, Berntssen MHG: 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 2008, 285:193-200.
• [3]Powell K: Eat your veg. Nature 2003, 426:378-379.
• [4]Obach A: Trends and advances in feed formulation – towards lowest cost fish production. In Practical Developments in Aquafeeds - Feed Advances to Boost Profitability: 2013. Nashville, Tennessee, USA: Nashville Convention Center; 2013.
• [5]Sustainibility report 2012 http://www.skretting.com webcite
• [6]Chapkin RS, McMurray DN, Lupton JR: Colon cancer, fatty acids and anti-inflammatory compounds. Curr Opin Gastroenterol 2007, 23:48-54.
• [7]Calder PC: n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 2006, 83:1505S-1519S.
• [8]Bell JG, Ashton I, Secombes CJ, Weitzel BR, Dick JR, Sargent JR: Dietary lipid affects phospholipid fatty acid compositions, eicosanoid production and immune function in Atlantic salmon (Salmo salar). Prostaglandins Leukot Essent Fatty Acids 1996, 54:173-182.
• [9]Seierstad SL, Haugland Ø, Larsen S, Waagbø R, Evensen Ø: Pro-inflammatory cytokine expression and respiratory burst activity following replacement of fish oil with rapeseed oil in the feed for Atlantic salmon (Salmo salar L.). Aquaculture 2009, 289:212-218.
• [10]Tjønneland A, Overvad K, Bergmann MM, Nagel G, Linseisen J, Hallmans G, Palmqvist R, Sjödin H, Hägglund G, Berglund G, Lindgren S, Grip O, Palli D, Day NE, Khaw KT, Bingham S, Riboli E, Kennedy H, Hart A: Linoleic acid, a dietary n-6 polyunsaturated fatty acid, and the aetiology of ulcerative colitis: a nested case-control study within a European prospective cohort study. Gut 2009, 58:1606-1611.
• [11]Whelan J, McEntee MF: Dietary (n-6) PUFA and intestinal tumorigenesis. J Nutr 2004, 134:3421S-3426S.
• [12]Ghosh S, DeCoffe D, Brown K, Rajendiran E, Estaki M, Dai CB, Yip A, Gibson DL: Fish oil attenuates omega-6 polyunsaturated fatty acid-induced dysbiosis and infectious colitis but impairs LPS dephosphorylation activity causing sepsis. PLoS One 2013, 8(2):e55468. doi:10.1371/journal.pone.0055468
• [13]Calder PC: Mechanisms of action of (n-3) fatty acids. J Nutr 2012, 142:592S-599S.
• [14]Calder PC, Yaqoob P, Thies F, Wallace FA, Miles EA: Fatty acids and lymphocyte functions. Br J Nutr 2002, 87(Suppl 1):31-48.
• [15]Calder PC: Immunomodulation by omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids 2007, 77:327-335.
• [16]Denstadli V, Vegusdal A, Krogdahl Å, Bakke-McKellep AM, Berge GM, Holm H, Hillestad M, Ruyter B: Lipid absorption in different segments of the gastrointestinal tract of Atlantic salmon (Salmo salar L.). Aquaculture 2004, 240:385-398.
• [17]Denstadli V, Bakke AM, Berge GM, Krogdahl Å, Hillestad M, Holm H, Ruyter B: Medium-chain and long-chain fatty acids have different postabsorptive fates in atlantic salmon. J Nutr 2011, 141:1618-1625.
• [18]Torstensen BE, Lie Ø, Frøyland L: Lipid metabolism and tissue composition in Atlantic salmon (Salmo salar L.) - Effects of capelin oil, palm oil, and oleic acid-enriched sunflower oil as dietary lipid sources. Lipids 2000, 35:653-664.
• [19]Torstensen BE, Frøyland L, Lie Ø: Replacing dietary fish oil with increasing levels of rapeseed oil and olive oil - effects on Atlantic salmon (Salmo salar L.) tissue and lipoprotein lipid composition and lipogenic enzyme activities. Aquac Nutr 2004, 10:175-192.
• [20]Torstensen BE, Frøyland L, Ørnsrud R, Lie Ø: Tailoring of a cardioprotective muscle fatty acid composition of Atlantic salmon (Salmo salar) fed vegetable oils. Food Chem 2004, 87:567-580.
• [21]Torstensen BE, Bell JG, Rosenlund G, Henderson RJ, Graff IE, Tocher DR, Lie Ø, Sargent JR: 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 2005, 53:10166-10178.
• [22]Liland NS, Rosenlund G, Berntssen MHG, Brattelid T, Madsen L, Torstensen BE: Net production of Atlantic salmon (FIFO, Fish in Fish out < 1) with dietary plant proteins and vegetable oils. Aquac Nutr 2013, 19:289-300.
• [23]Bæverfjord G, Krogdahl Å: Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J Fish Dis 1996, 19:375-387.
• [24]Penn MH, Bendiksen EA, Campbell P, Krogdahl Å: High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.). Aquaculture 2011, 310:267-273.
• [25]Olsvik PA, Torstensen BE, Berntssen MHG: Effects of complete replacement of fish oil with plant oil on gastrointestinal cell death, proliferation and transcription of eight genes’ encoding proteins responding to cellular stress in Atlantic salmon Salmo salar L. J Fish Bio 2007, 71:550-568.
• [26]Oxley A, Jolly C, Eide T, Jordal AEO, Svardal A, Olsen RE: The combined impact of plant-derived dietary ingredients and acute stress on the intestinal arachidonic acid cascade in Atlantic salmon (Salmo salar). Br J Nutr 2010, 103:851-861.
• [27]Dale OB, Tørud B, Kvellestad A, Koppang HS, Koppang EO: From chronic feed-induced intestinal inflammation to adenocarcinoma with metastases in salmonid fish. Cancer Res 2009, 69:4355-4362.
• [28]Løkka G, Austbø L, Falk K, Bjerkås I, Koppang EO: Intestinal morphology of the wild Atlantic salmon (Salmo salar). J Morphol 2013, 274:859-876.
• [29]Koppang EO, Hordvik I, Bjerkås I, Torvund J, Aune L, Thevarajan J, Endresen C: Production of rabbit antisera against recombinant MHC class II beta chain and identification of immunoreactive cells in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 2003, 14:115-132.
• [30]Koppang EO, Fischer U, Moore L, Tranulis MA, Dijkstra JM, Köllner B, Aune L, Jirillo E, Hordvik I: Salmonid T cells assemble in the thymus, spleen and in novel interbranchial lymphoid tissue. J Anat 2010, 217:728-739.
• [31]Olsvik PA, Lie KK, Jordal AEO, Nilsen TO, Hordvik I: Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Mol Biol 2005., 6doi:10.1186/1471-2199-6-21
• [32]Liu YL, Chen F, Odle J, Lin X, Jacobi SK, Zhu HL, Wu ZF, Hou YQ: Fish oil enhances intestinal integrity and inhibits TLR4 and NOD2 signaling pathways in weaned pigs after LPS challenge. J Nutr 2012, 142:2017-2024.
• [33]Rosa DD, de Sales RL, Moraes LFD, Lourenco FC, Neves CA, Sabarense CM, Ribeiro SMR, Peluzio MDG: Flaxseed, olive and fish oil influence plasmatic lipids, lymphocyte migration and morphometry of the intestinal of Wistar rats. Acta Cir Bras 2010, 25:275-280.
• [34]Van den Ingh TSGA, Krogdahl Å, Olli JJ, Hendriks HGCJ, Koninkx JGJF: Effects of soybean-containing diets on the proximal and distal intestine in atlantic salmon (Salmo salar) - a morphological study. Aquaculture 1991, 94:297-305.
• [35]Oberhuber G: Histopathology of celiac disease. Biomed Pharmacother 2000, 54:368-372.
• [36]Bakke-McKellep AM, Penn MH, Salas PM, Refstie S, Sperstad S, Landsverk T, Ringø E, Krogdahl Å: Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). Br J Nutr 2007, 97:699-713.
• [37]Merrifield DL, Dimitroglou A, Bradley G, Baker RTM, Davies SJ: Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 2009, 32:755-766.
• [38]Ringø E, Lødemel JB, Myklebust R, Jensen L, Lund V, Mayhew TM, Olsen RE: The effects of soybean, linseed and marine oils on aerobic gut microbiota of Arctic charr Salvelinus alpinus L. before and after challenge with Aeromonas salmonicida ssp. salmonicida. Aquac Res 2002, 33:591-606.
• [39]Røsjø C, Nordrum S, Olli JJ, Krogdahl Å, Ruyter B, Holm H: Lipid digestibility and metabolism in Atlantic salmon (Salmo salar) fed medium-chain triglycerides. Aquaculture 2000, 190:65-76.
• [40]Berntssen MHG, Hylland K, Julshamn K, Lundebye AK, Waagbø R: Maximum limits of organic and inorganic mercury in fish feed. Aquac Nutr 2004, 10:83-97.
• [41]Krogdahl Å, Nordrum S, Sørensen M, Brudeseth L, Røsjø C: Effects of diet composition on apparent nutrient absorption along the intestinal tract and of subsequent fasting on mucosal disaccharidase activities and plasma nutrient concentration in Atlantic salmon Salmo salar L. Aquac Nutr 1999, 5:121-133.
• [42]Zhu LY, Nie L, Zhu G, Xiang LX, Shao JZ: Advances in research of fish immune-relevant genes: A comparative overview of innate and adaptive immunity in teleosts. Dev Comp Immunol 2013, 39:39-62.
• [43]Marjara IS, Chikwati EM, Valen EC, Krogdahl Å, Bakke AM: Transcriptional regulation of IL-17A and other inflammatory markers during the development of soybean meal-induced enteropathy in the distal intestine of Atlantic salmon (Salmo salar L.). Cytokine 2012, 60:186-196.
• [44]Rombout J, Abelli L, Picchietti S, Scapigliati G, Kiron V: Teleost intestinal immunology. Fish Shellfish Immunol 2011, 31:616-626.
• [45]Liu Y, Moore L, Koppang EO, Hordvik I: Characterization of the CD3 zeta, CD3 gamma delta and CD3 epsilon subunits of the T cell receptor complex in Atlantic salmon. Dev Comp Immunol 2008, 32:26-35.
• [46]Koppang EO, Lundin M, Press CM, Rønningen K, Lie Ø: Differing levels of Mhc class II beta chain expression in a range of tissues from vaccinated and non-vaccinated Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 1998, 8:183-196.
• [47]Salinas I, Zhang YA, Sunyer JO: Mucosal immunoglobulins and B cells of teleost fish. Dev Comp Immunol 2011, 35:1346-1365.
• [48]Ruyter B, Røsjø C, Einen O, Thomassen MS: Essential fatty acids in Atlantic salmon: effects of increasing dietary doses of n-6 and n-3 fatty acids on growth, survival and fatty acid composition of liver, blood and carcass. Aquac Nutr 2000, 6:119-127.
• [49]Sargent J, Bell G, McEvoy L, Tocher D, Estevez A: Recent developments in the essential fatty acid nutrition of fish. Aquaculture 1999, 177:191-199.