Soybean meal‐induced enteritis in Atlantic salmon (Salmo salar L.) at different temperatures
Paula A. Urán, Aquaculture and Fisheries group, Wageningen University P.O. Box 338, 6700 AH Wageningen, The Netherlands. E‐mail: paula.uran@wur.nl
Abstract
This study evaluates the effect of temperature on the development of intestinal disorders when Atlantic salmon are fed soybean meal (SBM). In this study 20% of the dietary fishmeal was replaced by solvent‐extracted Hipro SBM. Atlantic salmon reared at two different water temperatures (8 °C and 12 °C), were fed a control diet and an experimental diet for 20 days. Samples were taken at days 7 and 20. The extent of the morphological changes was assessed using a semi‐quantitative scoring system developed for this purpose. The study demonstrates that enteritis is affected by temperature. The intestinal disorders were more severe in fish reared at 12 °C compared with those reared at 8 °C. It can be concluded from this study that temperature changes the speed but not the type of SBM‐induced enteritis expressed as a delay on the response when Atlantic salmon are kept at lower temperatures.
Citing Literature
Number of times cited according to CrossRef: 82
- Daniel Matulić, Josip Barišić, Ivica Aničić, Tea Tomljanović, Roman Safner, Tomislav Treer, Jian Gao, Ines Glojnarić, Rozelindra Čož-Rakovac, Growth, health aspects and histopathology of brown bullhead (Ameiurus nebulosus L.): replacing fishmeal with soybean meal and brewer’s yeast, Scientific Reports, 10.1038/s41598-020-57722-3, 10, 1, (2020).
- Stefanie M. Colombo, Zeyu Zhang, David F. Wong, Zhirun Yuan, Hydrolysis lignin as a multifunctional additive in Atlantic salmon feed improves fish growth performance and pellet quality and shifts gut microbiome, Aquaculture Nutrition, 10.1111/anu.13092, 26, 4, (1353-1368), (2020).
- Hung Duc Pham, Muhammad A.B. Siddik, Ravi Fotedar, Md Reaz Chaklader, Md Javed Foysal, Chau Minh Nguyen, Sukham Munilkumar, Substituting fishmeal with lupin Lupinus angustifolius kernel meal in the diets of cobia Rachycentron canadum: Effects on growth performance, nutrient utilization, haemato-physiological response, and intestinal health, Animal Feed Science and Technology, 10.1016/j.anifeedsci.2020.114556, (114556), (2020).
- Shi-Mei Lin, Xing-Mei Zhou, Yue-lang Zhou, Wen-Ming Kuang, Yong-Jun Chen, Li Luo, Fang-Yin Dai, Intestinal morphology, immunity and microbiota response to dietary fibers in largemouth bass, Micropterus salmoide, Fish & Shellfish Immunology, 10.1016/j.fsi.2020.04.070, (2020).
- Benjamin D. Gallo, John M. Farrell, Brian F. Leydet, Fish Gut Microbiome: A Primer to an Emerging Discipline in the Fisheries Sciences, Fisheries, 10.1002/fsh.10379, 45, 5, (271-282), (2020).
- Gary Burr, Brian Peterson, Michael Pietrak, Wendy Sealey, Stephanie Block, John Bowzer, Effect of PROPLEX DY and PROPLEX T on growth performance of Atlantic salmon smolts, Aquaculture Research, 10.1111/are.14814, 51, 11, (4689-4697), (2020).
- Yathish Ramena, Steven D. Rawles, Rebecca Lochmann, T. Gibson Gaylord, Matthew E. McEntire, Bradley D. Farmer, Wes Baumgartner, Carl D. Webster, Benjamin H. Beck, Bartholomew W. Green, Louis M. Barnett, Growth, nutrient retention, innate immune response, and intestinal morphology of juvenile, soy-naïve hybrid striped bass, Morone saxatilis x M. chrysops fed commercial-type, soy-based, ideal protein, fish meal replacement diets, Aquaculture, 10.1016/j.aquaculture.2020.735150, (735150), (2020).
- José Pablo Fuentes‐Quesada, Fernanda Cornejo‐Granados, José A. Mata‐Sotres, Juan Pablo Ochoa‐Romo, Artur N. Rombenso, Yanet Guerrero‐Rentería, Juan Pablo Lazo, Camilo Pohlenz, Adrián Ochoa‐Leyva, María Teresa Viana, Prebiotic agavin in juvenile totoaba, Totoaba macdonaldi diets, to relieve soybean meal‐induced enteritis: Growth performance, gut histology and microbiota, Aquaculture Nutrition, 10.1111/anu.13151, 26, 6, (2115-2134), (2020).
- Karolina Kwasek, Michal Wojno, Federica Iannini, Vance J. McCracken, Giovanni S. Molinari, Genciana Terova, Nutritional programming improves dietary plant protein utilization in zebrafish Danio rerio, PLOS ONE, 10.1371/journal.pone.0225917, 15, 3, (e0225917), (2020).
- Felipe Pinheiro de Souza, Ed Christian Suzuki de Lima, Angela Maria Urrea-Rojas, Suelen Aparecida Suphoronski, César Toshio Facimoto, Jailton da Silva Bezerra Júnior, Thalita Evani Silva de Oliveira, Ulisses de Pádua Pereira, Giovana Wingeter Di Santis, Carlos Antonio Lopes de Oliveira, Nelson Mauricio Lopera-Barrero, Effects of dietary supplementation with a microalga (Schizochytrium sp.) on the hemato-immunological, and intestinal histological parameters and gut microbiota of Nile tilapia in net cages, PLOS ONE, 10.1371/journal.pone.0226977, 15, 1, (e0226977), (2020).
- Christian Caimi, Laura Gasco, Ilaria Biasato, Vanda Malfatto, Katia Varello, Marino Prearo, Paolo Pastorino, Maria Cristina Bona, Danila Raffaella Francese, Achille Schiavone, Antonia Concetta Elia, Ambrosius Josef Martin Dörr, Francesco Gai, Could Dietary Black Soldier Fly Meal Inclusion Affect the Liver and Intestinal Histological Traits and the Oxidative Stress Biomarkers of Siberian Sturgeon (Acipenser baerii) Juveniles?, Animals, 10.3390/ani10010155, 10, 1, (155), (2020).
- Md. Reaz Chaklader, Muhammad A. B. Siddik, Ravi Fotedar, Total replacement of fishmeal with poultry by-product meal affected the growth, muscle quality, histological structure, antioxidant capacity and immune response of juvenile barramundi, Lates calcarifer, PLOS ONE, 10.1371/journal.pone.0242079, 15, 11, (e0242079), (2020).
- Minmin Wei, Derek M. Anderson, Zeyu Zhang, Stefanie M. Colombo, High‐oil residue camelina meal, a viable source of protein at low levels in diets for juvenile salmonids, Aquaculture Nutrition, 10.1111/anu.13017, 26, 2, (558-567), (2019).
- Brett D. Glencross, Johanna Baily, Marc H.G. Berntssen, Ronald Hardy, Simon MacKenzie, Douglas R. Tocher, Risk assessment of the use of alternative animal and plant raw material resources in aquaculture feeds, Reviews in Aquaculture, 10.1111/raq.12347, 12, 2, (703-758), (2019).
- H. Sundh, F. Finne-Fridell, T. Ellis, G.L. Taranger, L. Niklasson, E.F. Pettersen, H.I. Wergeland, K. Sundell, Reduced water quality associated with higher stocking density disturbs the intestinal barrier functions of Atlantic salmon (Salmo salar L.), Aquaculture, 10.1016/j.aquaculture.2019.734356, (734356), (2019).
- David Huyben, Aleksandar Vidakovic, Henrik Sundh, Kristina Sundell, Anders Kiessling, Torbjörn Lundh, Haematological and intestinal health parameters of rainbow trout are influenced by dietary live yeast and increased water temperature, Fish & Shellfish Immunology, 10.1016/j.fsi.2019.04.047, 89, (525-536), (2019).
- Kim T. Tran‐Ngoc, Mahmoud N. Haidar, Arjen J. Roem, João Sendão, Johan A. J. Verreth, Johan W. Schrama, Effects of feed ingredients on nutrient digestibility, nitrogen/energy balance and morphology changes in the intestine of Nile tilapia (Oreochromis niloticus), Aquaculture Research, 10.1111/are.14214, 50, 9, (2577-2590), (2019).
- Vignesh Venkatakrishnan, János T Padra, Henrik Sundh, Kristina Sundell, Chunsheng Jin, Markus Langeland, Hanna Carlberg, Aleksandar Vidakovic, Torbjörn Lundh, Niclas G. Karlsson, Sara K. Lindén, Exploring the Arctic charr intestinal glycome: evidence for increased N-glycolylneuraminic acid levels and changed host-pathogen interactions in response to inflammation, Journal of Proteome Research, 10.1021/acs.jproteome.8b00973, (2019).
- Fotini Kokou, Morgane Henry, Chrisa Nikoloudaki, Christiana Kounna, Antigoni Vasilaki, Eleni Fountoulaki, Optimum protein‐to‐lipid ratio requirement of the juvenile shi drum (Umbrina cirrosa) as estimated by nutritional and histological parameters, Aquaculture Nutrition, 10.1111/anu.12870, 25, 2, (444-455), (2018).
- Julie C. Schroeter, Brian C. Peterson, Jacob Bledsoe, Menghe Li, Brian C. Small, Targeted gene expression panels and microbiota analysis provide insight into the effects of alternative production diet formulations on channel catfish nutritional physiology, Aquaculture, 10.1016/j.aquaculture.2018.02.004, 489, (46-55), (2018).
- José Pablo Fuentes-Quesada, María Teresa Viana, Artur N. Rombenso, Yanet Guerrero-Rentería, Mario Nomura-Solís, Vilma Gomez-Calle, Juan Pablo Lazo, José A. Mata-Sotres, Enteritis induction by soybean meal in Totoaba macdonaldi diets: Effects on growth performance, digestive capacity, immune response and distal intestine integrity, Aquaculture, 10.1016/j.aquaculture.2018.05.025, 495, (78-89), (2018).
- Patrick C. Blaufuss, T. Gibson Gaylord, Wendy M. Sealey, Madison S. Powell, Effects of high-soy diet on S100 gene expression in liver and intestine of rainbow trout (Oncorhynchus mykiss), Fish & Shellfish Immunology, 10.1016/j.fsi.2018.12.025, (2018).
- Arturo Vargas, Basilio Randazzo, Paola Riolo, Cristina Truzzi, Giorgia Gioacchini, Elisabetta Giorgini, Nino Loreto, Sara Ruschioni, Matteo Zarantoniello, Matteo Antonucci, Sara Polverini, Gloriana Cardinaletti, Simona Sabbatini, Francesca Tulli, Ike Olivotto, Rearing Zebrafish on Black Soldier Fly ( Hermetia illucens ): Biometric, Histological, Spectroscopic, Biochemical, and Molecular Implications , Zebrafish, 10.1089/zeb.2017.1559, 15, 4, (404-419), (2018).
- Elisabetta Giorgini, Basilio Randazzo, Giorgia Gioacchini, Gloriana Cardinaletti, Lisa Vaccari, Emilio Tibaldi, Ike Olivotto, New insights on the macromolecular building of rainbow trout (O. mykiss) intestine: FTIR Imaging and histological correlative study, Aquaculture, 10.1016/j.aquaculture.2018.07.032, 497, (1-9), (2018).
- Hans Jákup Jacobsen, Tor Andreas Samuelsen, Albert Girons, Katerina Kousoulaki, Different enzyme incorporation strategies in Atlantic salmon diet containing soybean meal: Effects on feed quality, fish performance, nutrient digestibility and distal intestinal morphology, Aquaculture, 10.1016/j.aquaculture.2018.03.053, 491, (302-309), (2018).
- Sian Egerton, Sarah Culloty, Jason Whooley, Catherine Stanton, R. Paul Ross, The Gut Microbiota of Marine Fish, Frontiers in Microbiology, 10.3389/fmicb.2018.00873, 9, (2018).
- P Mosberian‐Tanha, T Landsverk, C M Press, L T Mydland, J W Schrama, M Øverland, Granulomatous enteritis in rainbow trout (Oncorhynchus mykiss) associated with soya bean meal regardless of water dissolved oxygen level, Journal of Fish Diseases, 10.1111/jfd.12710, 41, 2, (269-280), (2017).
- Z. Zhou, E. Ringø, R.E. Olsen, S.K. Song, Dietary effects of soybean products on gut microbiota and immunity of aquatic animals: A review, Aquaculture Nutrition, 10.1111/anu.12532, 24, 1, (644-665), (2017).
- Li Zhang, Lin Feng, Wei-Dan Jiang, Yang Liu, Pei Wu, Sheng-Yao Kuang, Ling Tang, Wu-Neng Tang, Yong-An Zhang, Xiao-Qiu Zhou, Vitamin A deficiency suppresses fish immune function with differences in different intestinal segments: the role of transcriptional factor NF-κB and p38 mitogen-activated protein kinase signalling pathways , British Journal of Nutrition, 10.1017/S0007114516003342, 117, 1, (67-82), (2017).
- Fotini Kokou, Elena Sarropoulou, Efthimia Cotou, Maroudio Kentouri, Maria Alexis, George Rigos, Effects of graded dietary levels of soy protein concentrate supplemented with methionine and phosphate on the immune and antioxidant responses of gilthead sea bream ( Sparus aurata L.), Fish & Shellfish Immunology, 10.1016/j.fsi.2017.03.017, 64, (111-121), (2017).
- Michael Clarkson, Herve Migaud, Christoforos Metochis, Luisa M. Vera, Daniel Leeming, Douglas R. Tocher, John F. Taylor, Early nutritional intervention can improve utilisation of vegetable-based diets in diploid and triploid Atlantic salmon ( Salmo salar L.) , British Journal of Nutrition, 10.1017/S0007114517001842, 118, 1, (17-29), (2017).
- Kim T. Tran-Ngoc, Johan W. Schrama, Mai T.T. Le, Thinh H. Nguyen, Arjen J. Roem, Johan A.J Verreth, Salinity and diet composition affect digestibility and intestinal morphology in Nile tilapia (Oreochromis niloticus), Aquaculture, 10.1016/j.aquaculture.2016.11.037, 469, (36-43), (2017).
- Wei-Guang Kong, Si-Si Li, Xiao-Xuan Chen, Yu-Qing Huang, Ying Tang, Zhi-Xin Wu, A study of the damage of the intestinal mucosa barrier structure and function of Ctenopharyngodon idella with Aeromonas hydrophila, Fish Physiology and Biochemistry, 10.1007/s10695-017-0366-z, 43, 5, (1223-1235), (2017).
- V. I. Fuchs, J. Schmidt, M. J. Slater, B. H. Buck, D. Steinhagen, Influence of immunostimulant polysaccharides, nucleic acids, and Bacillus strains on the innate immune and acute stress response in turbots (Scophthalmus maximus) fed soy bean- and wheat-based diets, Fish Physiology and Biochemistry, 10.1007/s10695-017-0388-6, 43, 6, (1501-1515), (2017).
- Timothy J. Bruce, Michael L. Brown, A Review of Immune System Components, Cytokines, and Immunostimulants in Cultured Finfish Species, Open Journal of Animal Sciences, 10.4236/ojas.2017.73021, 07, 03, (267-288), (2017).
- David A.J. Stone, Emma J. Bellgrove, Rebecca E.A. Forder, Gordon S. Howarth, Matthew S. Bansemer, Inducing sub-acute enteritis in Yellowtail Kingfish ( Seriola lalandi ): the effect of dietary inclusion of soybean meal and grape seed extract on hind-gut morphology and inflammation , North American Journal of Aquaculture, 10.1080/15222055.2017.1386145, (2017).
- C. De Santis, D.R. Tocher, K. Ruohonen, A. El-Mowafi, S.A.M. Martin, C.E. Dehler, C.J. Secombes, V. Crampton, Air-classified faba bean protein concentrate is efficiently utilized as a dietary protein source by post-smolt Atlantic salmon ( Salmo salar ), Aquaculture, 10.1016/j.aquaculture.2015.10.035, 452, (169-177), (2016).
- Tyler D. Brown, Tiago S. Hori, Xi Xue, Chang Lin Ye, Derek M. Anderson, Matthew L. Rise, Functional Genomic Analysis of the Impact of Camelina (Camelina sativa) Meal on Atlantic Salmon (Salmo salar) Distal Intestine Gene Expression and Physiology, Marine Biotechnology, 10.1007/s10126-016-9704-x, 18, 3, (418-435), (2016).
- Simona Rimoldi, Giovanna Finzi, Chiara Ceccotti, Rossana Girardello, Annalisa Grimaldi, Chiara Ascione, Genciana Terova, Butyrate and taurine exert a mitigating effect on the inflamed distal intestine of European sea bass fed with a high percentage of soybean meal, Fisheries and Aquatic Sciences, 10.1186/s41240-016-0041-9, 19, 1, (2016).
- Armando García-Ortega, Karma R. Kissinger, Jesse T. Trushenski, Evaluation of fish meal and fish oil replacement by soybean protein and algal meal from Schizochytrium limacinum in diets for giant grouper Epinephelus lanceolatus, Aquaculture, 10.1016/j.aquaculture.2015.10.020, 452, (1-8), (2016).
- Enric Gisbert, Mansour Torfi Mozanzadeh, Yannis Kotzamanis, Alicia Estévez, Weaning wild flathead grey mullet (Mugil cephalus) fry with diets with different levels of fish meal substitution, Aquaculture, 10.1016/j.aquaculture.2016.04.035, 462, (92-100), (2016).
- Chang Lin Ye, Derek M. Anderson, Santosh P. Lall, The effects of camelina oil and solvent extracted camelina meal on the growth, carcass composition and hindgut histology of Atlantic salmon ( Salmo salar ) parr in freshwater, Aquaculture, 10.1016/j.aquaculture.2015.08.019, 450, (397-404), (2016).
- Karma R. Kissinger, Armando García-Ortega, Jesse T. Trushenski, Partial fish meal replacement by soy protein concentrate, squid and algal meals in low fish-oil diets containing Schizochytrium limacinum for longfin yellowtail Seriola rivoliana, Aquaculture, 10.1016/j.aquaculture.2015.10.022, 452, (37-44), (2016).
- Kim T. Tran-Ngoc, Ngu T. Dinh, Thinh H. Nguyen, Arjen J. Roem, Johan W. Schrama, Johan A.J. Verreth, Interaction between dissolved oxygen concentration and diet composition on growth, digestibility and intestinal health of Nile tilapia (Oreochromis niloticus), Aquaculture, 10.1016/j.aquaculture.2016.05.005, 462, (101-108), (2016).
- H. Liu, J. Jin, X. Zhu, D. Han, Y. Yang, S. Xie, Effect of substitution of dietary fish meal by soybean meal on different sizes of gibel carp (arassius auratus gibelio): digestive enzyme gene expressions and activities, and intestinal and hepatic histology, Aquaculture Nutrition, 10.1111/anu.12375, 23, 1, (129-147), (2015).
- Aurélia Saraiva, Joana Costa, Joana Serrão, Cristina Cruz, Jorge C. Eiras, A histology-based fish health assessment of farmed seabass (Dicentrarchus labrax L.), Aquaculture, 10.1016/j.aquaculture.2015.06.028, 448, (375-381), (2015).
- Irene Salinas, David Parra, Fish mucosal immunity: intestine, Mucosal Health in Aquaculture, 10.1016/B978-0-12-417186-2.00006-6, (135-170), (2015).
- Christian De Santis, Viv O. Crampton, Beatrix Bicskei, Douglas R. Tocher, Replacement of dietary soy- with air classified faba bean protein concentrate alters the hepatic transcriptome in Atlantic salmon ( Salmo salar ) parr, Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 10.1016/j.cbd.2015.07.005, 16, (48-58), (2015).
- Polyana F. Silva, Charles McGurk, David L. Knudsen, Alexandra Adams, Kim D. Thompson, James E. Bron, Histological evaluation of soya bean-induced enteritis in Atlantic salmon (Salmo salar L.): Quantitative image analysis vs. semi-quantitative visual scoring, Aquaculture, 10.1016/j.aquaculture.2015.04.002, 445, (42-56), (2015).
- Henrik Sundh, Kristina S. Sundell, Environmental impacts on fish mucosa, Mucosal Health in Aquaculture, 10.1016/B978-0-12-417186-2.00007-8, (171-197), (2015).
- Christian De Santis, Kerry L. Bartie, Rolf E. Olsen, John B. Taggart, Douglas R. Tocher, Nutrigenomic profiling of transcriptional processes affected in liver and distal intestine in response to a soybean meal-induced nutritional stress in Atlantic salmon (Salmo salar), Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 10.1016/j.cbd.2015.04.001, 15, (1-11), (2015).
- A. Rodiles, M. Herrera, I. Hachero‐Cruzado, I. Ruiz‐Jarabo, J.M. Mancera, M.L. Cordero, S.P. Lall, F.J. Alarcón, Tissue composition, blood biochemistry and histology of digestive organs in Senegalese sole (olea senegalensis) juveniles fed diets containing different plant protein ingredients, Aquaculture Nutrition, 10.1111/anu.12207, 21, 6, (767-779), (2014).
- M.S. Bansemer, R.E.A. Forder, G.S. Howarth, G.M. Suitor, J. Bowyer, D.A.J. Stone, The effect of dietary soybean meal and soy protein concentrate on the intestinal mucus layer and development of subacute enteritis in Yellowtail Kingfish (eriola lalandi) at suboptimal water temperature, Aquaculture Nutrition, 10.1111/anu.12160, 21, 3, (300-310), (2014).
- M.N. Amin, R. Katersky Barnes, L.R. Adams, Effect of temperature and varying level of carbohydrate and lipid on growth, feed efficiency and nutrient digestibility of brook trout, Salvelinus fontinalis (Mitchill, 1814), Animal Feed Science and Technology, 10.1016/j.anifeedsci.2014.04.016, 193, (111-123), (2014).
- Hans-Christian Ingerslev, Mikael Lenz Strube, Louise von Gersdorff Jørgensen, Inger Dalsgaard, Mette Boye, Lone Madsen, Diet type dictates the gut microbiota and the immune response against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss), Fish & Shellfish Immunology, 10.1016/j.fsi.2014.08.021, 40, 2, (624-633), (2014).
- H.H. Yu, F. Han, M. Xue, J. Wang, P. Tacon, Y.H. Zheng, X.F. Wu, Y.J. Zhang, Efficacy and tolerance of yeast cell wall as an immunostimulant in the diet of Japanese seabass (Lateolabrax japonicus), Aquaculture, 10.1016/j.aquaculture.2014.04.043, 432, (217-224), (2014).
- Elliott C. Kittel, Wendy M. Sealey, Brian C. Small, Preliminary Investigation of Dietary Soy Sensitivity in Shovelnose Sturgeon, Journal of Applied Aquaculture, 10.1080/10454438.2014.965397, 26, 4, (356-369), (2014).
- M. Hartviksen, J.L.G. Vecino, E. Ringø, A.‐M. Bakke, S. Wadsworth, Å. Krogdahl, K. Ruohonen, A. Kettunen, Alternative dietary protein sources for Atlantic salmon (almo salar L.) effect on intestinal microbiota, intestinal and liver histology and growth, Aquaculture Nutrition, 10.1111/anu.12087, 20, 4, (381-398), (2014).
- Jenna N. Bowyer, Jian G. Qin, Richard P. Smullen, Louise R. Adams, Michael J.S. Thomson, David A.J. Stone, The use of a soy product in juvenile yellowtail kingfish (Seriola lalandi) feeds at different water temperatures: 1. Solvent extracted soybean meal, Aquaculture, 10.1016/j.aquaculture.2012.12.005, 384-387, (35-45), (2013).
- E. N. Schaefer, J. O. Harris, G. S. Howarth, M. S. Bansemer, D. A. J. Stone, Comparative Histological Changes in the Greenlip Abalone Haliotis laevigata Gastrointestinal Tract in Response to Water Temperature, Different Dietary Protein Levels, and Animal Age , Journal of Shellfish Research, 10.2983/035.032.0119, 32, 1, (131-141), (2013).
- Steven D. Rawles, S. Adam Fuller, Benjamin H. Beck, T. Gibson Gaylord, Frederic T. Barrows, Matthew E. McEntire, Lysine optimization of a commercial fishmeal-free diet for hybrid striped bass (Morone chrysops×M. saxatilis), Aquaculture, 10.1016/j.aquaculture.2013.02.014, 396-399, (89-101), (2013).
- Timothy J. Green, Richard Smullen, Andrew C. Barnes, Dietary soybean protein concentrate-induced intestinal disorder in marine farmed Atlantic salmon, Salmo salar is associated with alterations in gut microbiota, Veterinary Microbiology, 10.1016/j.vetmic.2013.05.009, 166, 1-2, (286-292), (2013).
- Liang Hu, Biao Yun, Min Xue, Jia Wang, Xiufeng Wu, Yinhua Zheng, Fang Han, Effects of fish meal quality and fish meal substitution by animal protein blend on growth performance, flesh quality and liver histology of Japanese seabass (Lateolabrax japonicus), Aquaculture, 10.1016/j.aquaculture.2012.10.025, 372-375, (52-61), (2013).
- P. Navarrete, P. Fuentes, L. la Fuente, L. Barros, F. Magne, R. Opazo, C. Ibacache, R. Espejo, J. Romero, Short‐term effects of dietary soybean meal and lactic acid bacteria on the intestinal morphology and microbiota of Atlantic salmon (almo salar), Aquaculture Nutrition, 10.1111/anu.12047, 19, 5, (827-836), (2013).
- Manuel I. Hedrera, Jorge A. Galdames, Maria F. Jimenez-Reyes, Ariel E. Reyes, Ruben Avendaño-Herrera, Jaime Romero, Carmen G. Feijóo, Soybean Meal Induces Intestinal Inflammation in Zebrafish Larvae, PLoS ONE, 10.1371/journal.pone.0069983, 8, 7, (e69983), (2013).
- Silvia Martínez-Llorens, Rosa Baeza-Ariño, Silvia Nogales-Mérida, Miguel Jover-Cerdá, Ana Tomás-Vidal, Carob seed germ meal as a partial substitute in gilthead sea bream (Sparus aurata) diets: Amino acid retention, digestibility, gut and liver histology, Aquaculture, 10.1016/j.aquaculture.2012.01.029, 338-341, (124-133), (2012).
- David Roque Hernández, Juan José Santinón, Sebastián Sánchez, Hugo Alberto Domitrovic, Dietary soybean meal on growth and intestinal morphology of South American catfish, Rhamdia quelen, larvae, Ciência Rural, 10.1590/S0103-84782012000900023, 42, 9, (1662-1668), (2012).
- J. Laporte, J. Trushenski, Production performance, stress tolerance and intestinal integrity of sunshine bass fed increasing levels of soybean meal, Journal of Animal Physiology and Animal Nutrition, 10.1111/j.1439-0396.2011.01174.x, 96, 3, (513-526), (2011).
- Michael H. Penn, Eldar Å. Bendiksen, Patrick Campbell, Åshild Krogdahl, High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.), Aquaculture, 10.1016/j.aquaculture.2010.10.040, 310, 3-4, (267-273), (2011).
- Jan H.W.M. Rombout, Luigi Abelli, Simona Picchietti, Giuseppe Scapigliati, Viswanath Kiron, Teleost intestinal immunology, Fish & Shellfish Immunology, 10.1016/j.fsi.2010.09.001, 31, 5, (616-626), (2011).
- K. VECHKLANG, S. BOONANUNTANASARN, S. PONCHUNCHOOVONG, N. PIRARAT, C. WANAPU, The potential for rice wine residual as an alternative protein source in a practical diet for Nile tilapia (Oreochromis niloticus) at the juvenile stage, Aquaculture Nutrition, 10.1111/j.1365-2095.2011.00870.x, 17, 6, (685-694), (2011).
- G.S. BURR, F.T. BARROWS, G. GAYLORD, W.R. WOLTERS, Apparent digestibility of macro‐nutrients and phosphorus in plant‐derived ingredients for Atlantic salmon, Salmo salar and Arctic charr, Salvelinus alpinus, Aquaculture Nutrition, 10.1111/j.1365-2095.2011.00855.x, 17, 5, (570-577), (2011).
- E. MARTÍNEZ‐MONTAÑO, E. PEÑA, M.T. VIANA, In vitro amino acid absorption using hydrolysed sardine muscle or soybean meal at different intestinal regions of the Pacific bluefin tuna (Thunnus orientalis), Aquaculture Nutrition, 10.1111/j.1365-2095.2011.00850.x, 17, 3, (e789-e797), (2011).
- A. ESTÉVEZ, L. TREVIÑO, Y. KOTZAMANIS, I. KARACOSTAS, L. TORT, E. GISBERT, Effects of different levels of plant proteins on the ongrowing of meagre (Argyrosomus regius) juveniles at low temperatures, Aquaculture Nutrition, 10.1111/j.1365-2095.2010.00798.x, 17, 2, (e572-e582), (2010).
- Ana Paula Oeda Rodrigues, Patricia Pauletti, Liris Kindlein, Eduardo Francisquine Delgado, José Eurico Possebon Cyrino, Raul Machado-Neto, Intestinal histomorphology in Pseudoplatystoma fasciatum fed bovine colostrum as source of protein and bioactive peptides, Scientia Agricola, 10.1590/S0103-90162010000500005, 67, 5, (524-530), (2010).
- S. Refstie, T. ÅsgåRd, Advances in aquaculture feeds and feeding: salmonids, New Technologies in Aquaculture, 10.1533/9781845696474.3.498, (498-541), (2009).
- N.H. Sissener, A.M. Bakke, J. Gu, M.H. Penn, E. Eie, Å. Krogdahl, M. Sanden, G.I. Hemre, An assessment of organ and intestinal histomorphology and cellular stress response in Atlantic salmon (Salmo salar L.) fed genetically modified Roundup Ready® soy, Aquaculture, 10.1016/j.aquaculture.2009.10.011, 298, 1-2, (101-110), (2009).
- Koji Murashita, Tadahide Kurokawa, Tom Ole Nilsen, Ivar Rønnestad, Ghrelin, cholecystokinin, and peptide YY in Atlantic salmon (Salmo salar): Molecular cloning and tissue expression, General and Comparative Endocrinology, 10.1016/j.ygcen.2008.11.024, 160, 3, (223-235), (2009).
- P A Urán, J W Schrama, J H W M Rombout, J J Taverne‐Thiele, A Obach, W Koppe, J A J Verreth, Time‐related changes of the intestinal morphology of Atlantic salmon, Salmo salar L., at two different soybean meal inclusion levels, Journal of Fish Diseases, 10.1111/j.1365-2761.2009.01049.x, 32, 9, (733-744), (2009).
- P.A. URÁN, J.W. SCHRAMA, S. JAAFARI, G. BAARDSEN, J.H.W.M. ROMBOUT, W. KOPPE, J.A.J. VERRETH, Variation in commercial sources of soybean meal influences the severity of enteritis in Atlantic salmon (Salmo salar L.), Aquaculture Nutrition, 10.1111/j.1365-2095.2008.00615.x, 15, 5, (492-499), (2009).
- P. A. UrÁn, R. Aydin, J. W. Schrama, J. A. J. Verreth, J. H. W. M. Rombout, Soybean meal‐induced uptake block in Atlantic salmon Salmo salar distal enterocytes, Journal of Fish Biology, 10.1111/j.1095-8649.2008.02091.x, 73, 10, (2571-2579), (2008).
- P.A. Urán, A.A. Gonçalves, J.J. Taverne-Thiele, J.W. Schrama, J.A.J. Verreth, J.H.W.M. Rombout, Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.), Fish & Shellfish Immunology, 10.1016/j.fsi.2008.02.013, 25, 6, (751-760), (2008).
