Pathophysiological and Immunological Characteristics of Soybean Meal-Induced Enteropathy in Salmon: Contribution of Recent Molecular Investigations
Resumen
Full-fat and defatted (hexane-extracted) soybean meal (SBM) in formulated feeds cause an inflammatory response in the distal intestine of all salmonids tested to date. The condition has been described as a non-infectious, subacute enteritis and apparently resolves only when SBM is removed from the diet. The signs include reduced weight gain, nutrient malabsorption, and diarrhea. The afflicted distal intestinal tissue has reduced function, as reflected by decreased brush border digestive enzyme activity and nutrient transport. Histomorhological investigations reveal shortening of the primary and secondary mucosal folds with a widening of the central stroma (lamina propria) and submucosa, shortened microvilli of the brush border membrane, increased formation of microvillar vesicles, and a dramatic decrease or even absence of the normal supranuclear absorptive vacuoles in the enterocytes. The lamina propria is widened with a profound infiltration of a mixed population of inflammatory cells such as T lymphocytes, neutrophilic granulocytes, cells of monocytic lineage including macrophages, eosinophilic granular cells, and diffuse IgM. Recent RNA expression studies indicate that pro-inflammatory cytokines and other signaling and regulatory factors involved in recruitment and activation of T cells and other immune cells, and factors involved in maintenance of normal mucosal integrity, were differentially expressed during the development of the enteropathy. The involvement of saponins, lectins, trypsin inhibitors, soy antigens and/or commensal microorganisms has been suggested. Various processing methods and feed additives may aid in modulation the inflammatory response and show some promise in allowing the use of standard SBM qualities in salmonid feeds without infringing on fish health and welfare.Descargas
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Aalberse, R.C., 1997. Food allergens. Environ. Toxicol. Phar. 4, 55-60.
Alvarez, J.R., Torres-Pinedo, R., 1982. Interactions of soybean lectins, soyasaponins, and glycinin with rabbit jejunal mucosa in vitro. Pediatric Res. 16, 728-731.
Arnesen, P., Brattås, L.E., Olli, J.J., Krogdahl, Å., 1990. Soybean carbohydrates appear to restrict the utilization of nutrients by Atlantic salmon (Salmo salar L.). In: Takeda, M., Watanabe, T. (Eds.) The Current Status of Fish Nutrition in Aquaculture. Tokyo Univ. Fisheries, Tokyo, Japan, pp. 273-280.
Aslaksen, M.A., Kraugerud, O.F., Penn, M., Svihus, B., Denstadli, V., Jørgensen, H.Y., Hillestad, M., Krogdahl, Å., Storebakken, T., 2007. Screening of nutrient digestibilities and intestinal pathologies in Atlantic salmon fed diets with legumes, oilseeds, or cereals. Aquaculture 272, 541-555.
Bach-Knudsen, K.E., 1997. Carbohydrate and lignin contents of plant material used in animal feeding. Anim. Feed Sci. Technol. 67, 319-338.
Baeverfjord, G., Krogdahl, A., 1996. 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. 19, 375-387.
Bakke-McKellep, A.M., 1999. Intestinal nutrient absorption in Atlantic salmon (Salmo salar L.) and pathophysiological response of the intestinal mucosa to dietary soybean meal. Ph.D. thesis, Norwegian School of Veterinary Science, Oslo, Norway.
Bakke-McKellep, A.M., Press, C.M., Krogdahl, A., Landsverk, T., 2000. Changes in immune and enzyme histochemical phenotypes of cells of the intestinal mucosa of Atlantic salmon (Salmo salar L.) with soybean-meal induced enteritis. J. Fish Dis. 23, 115-127.
Bakke-McKellep, A.M., Froystad, M.K., Lilleeng, E., Dapra, F., Refstie, S., Krogdahl, A., Landsverk, T., 2007a. Response to soy: T-cell-like reactivity in the intestine of Atlantic salmon, Salmo salar L. J. Fish Dis. 30, 13-25.
Bakke-McKellep, A.M., Penn, M.H., Salas, P.M., Refstie, S., Sperstad, S., Landsverk, T., Ringo, E., Krogdahl, A., 2007b. Effects of dietary soybean 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. 97, 699-713.
Bakke-McKellep, A.M., Penn, M.H., Chikwati, E., Hage, E., Cai, C., Krogdahl, A., 2008. In vitro effects of various anti-nutritional factors on intestinal glucose absorption and histology in Atlantic salmon. Book of Abstracts from XIII ISFNF - International Symposium on Fish Nutrition and Feeding, June 1-5 2008, Florianopolis, Brazil.
Bauer, E., Williams, B.A., Smidt, H., Mosenthin, R., Verstegen, M.W.A., 2006. Influence of dietary components on development of the microbiota in single-stomached species. Nutr. Res. Rev. 19, 63-78.
Bonaldo, A., Roem, A.J., Pecchini, A., Grilli, E., Gatta, P.P., 2006. Influence of dietary soybean meal levels on growth, feed utilization and gut histology of Egyptian sole (Solea aegyptiaca) juveniles. Aquaculture 261, 580-586.
Bonaldo, A., Roem, A.J., Fagioli, P., Pecchini, A., Cipollini, I., Gatta, P.P., 2008. Influence of dietary levels of soybean meal on the performance and gut histology of gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). Aquacult. Res. 39, 970-978.
Bureau, D.P., Harris, A.M., Cho, C.Y., 1998. The effects of purified alcohol extracts from soy products on feed intake and growth of chinook salmon (Oncorhynchus tshawytscha) and rainbow trout (Oncorhynchus mykiss). Aquaculture 161, 27-43.
Burrells, C., Williams, P.D., Southgate, P.J., Crampton, V.O., 1999. Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentrations of soybean proteins. Vet. Immunol. Immunopathol. 72, 277-288.
Buttle, L.G., Burrells, A.C., Good, J.E., Williams, P.D., Southgate, P.J., Burrells, C., 2001. The binding of soybean agglutinin (SBA) to the intestinal epithelium of Atlantic salmon, Salmo salar and rainbow trout, Oncorhynchus mykiss, fed high levels of soybean meal. Vet. Immunol. Immunopathol. 80, 237-244.
Chehade, M. Mayer, L., 2005. Oral tolerance and its relation to food hypersensitivities. J Allergy Clin. Immunol. 115, 3-12.
Chikwati, E.M., Venold, F.F., Penn, M.H., Rohloff, J., Refstie, S., Guttvik, A., Hillestad, M., Krogdahl, Å., 2011. Interaction of soyasaponins with plant ingredients in diets for Atlantic salmon, Salmo salar L. Brit. J. Nutr., in press, doi:10.1017/S0007114511004892.
Cummings, J.H., Englyst, H.N., Wiggins, H.S., 1986. The role of carbohydrates in lower gut function. Nutr. Rev. 44, 50-54.
Dabrowski, K., Poczyczynski, P., Köck, G., Berger, R., 1989. Effect of partially or totally replacing fishmeal protein by soybean meal protein on growth, feed utilisation and proteolytic enzyme activities in rainbow trout (Salmo gairdneri). New in vivo test for endocrine pancreatic secretion. Aquaculture 77, 29-49.
Dezfuli, B.S., Arrighi, S., Domeneghini, C., Bosi, G., 2000. Immunohistochemical detection of neuromodulators in the intestine of Salmo trutta L. naturally infected with Cyathocephalus truncatus Pallas (Cestoda). J. Fish Dis. 23, 265-273.
D’Mello, F.J.P., 1991. Antigenic proteins. In: D’Mello, F.J.P., Duffus, C.M., Duffus, J.H. (Eds.), Toxic Substances in Crop Plants. The Royal Society of Chemistry, Thomas Graham House, Science Park, Cambridge CB4 4WF, Cambridge, pp. 108-125.
Ellis, A.E., 1995. Recent development in oral vaccine delivery systems. Fish Pathol. 30, 293-300.
Evans, J.J., Pasnik, D.J., Peres, H., Lim, C., Klesius, P.H., 2005. No apparent differences in intestinal histology of channel catfish (Ictalurus punctatus) fed heat-treated and non-heat-treated raw soybean meal. Aquacult. Nutr. 11, 123-129.
Fish, B.C., Thompson, L.U., 1991. Lectin–tannin interactions and their influence on pancreatic amylase activity and starch digestibility. J. Agric. Food Chem. 39, 727–731.
Francis, G., Makkar, H.P.S., Becker, K., 2001. Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199, 197-227.
Francis, G., Kerem, Z., Makkar, H.P.S., Becker, K., 2002. The biological action of saponins in animal systems: a review. Br. J. Nutr. 88, 587-605.
Freeland, W.J., Calcott, P.H., Anderson, L.R., 1985. Tannins and saponin: interaction in herbivore diet. Biochem. Syst. Ecol. 13 Ž2., 189–193.
Gee, J.M., Wortley, G.M., Johnson, I.T., Price, K.R., Rutten, A.A.J.J., Houben, G.F., Penninks, A.H., 1996. Effects of saponins and glycoalkaloids on the permeability and viability of mammalian intestinal cells and on the integrity of tissue preparations in vitro. Toxicol. In Vitro 10, 117-128.
Goldstein, W.S., Spencer, K.C., 1985. Inhibition of cyanogenesis by tannins. J. Chem. Ecol. 11, 847–857.
Grisdale-Helland, B., Helland, S.J., Baeverfjord, G., Berge, G.M., 2002. Full-fat soybean meal in diets for Atlantic halibut: growth, metabolism and intestinal histology. Aquacult. Nutr. 8, 265-270.
Hansen A.C., Rosenlund, G., Karlsen, R., Olsvik, P.A., Hemre, G.I., 2006. The inclusion of plant protein in cod diets, its effects on macronutrient digestibility, gut and liver histology and heat shock protein transcription. Aquacult. Res. 37, 773-784.
Hardy, R.W., 1996. Alternate protein sources for salmon and trout diets. Anim. Feed Sci. Technol. 59, 71-80.
Hendricks, H.G.C.J.M., van den Ingh, T.S.G.A.M., Krogdahl, A., Olli, J., Koninkx, J.F.J.G., 1990. Binding of soybean agglutinin to small intestinal brush border membranes and brush border membrane enzyme activities in Atlantic salmon (Salmo salar). Aquaculture 91, 163-170.
Iwashita, Y., Suzuki, N., Matsunari, H., Sugita, T., Yamamoto, T., 2008. Influence of soya saponins, soya lectin, and cholyltarine supplemented to a casein-based semipurified diet on intestinal morphology and biliary bile status in fingerling rainbow trout Oncorhynchus mykiss. Fish. Sci. 75, 1307-1315.
Johnson, I.T., Gee, J.M., Price, K., Curl, C., Fenwick, G.R., 1986. Influence of Saponins on Gut Permeability and Active Nutrient Transport Invitro. J. Nutr. 116, 2270-2277.
Kaushik, S.J., Cravedi, J.P., Lalles, J.P., Sumpter, J., Fauconneau, B., LaRoche, M., 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, 257-274.
Kitagawa, I., Saito, M., Taniyama, T., Yoshikawa, M., 1985. Saponin and sapogenol . Structure of soyasaponin-A2, a bisdesmoside of soyasapogenol-A, from soybean, the seeds of Glycine max Merrill. Chem. Pharm. Bull. 33, 598-608.
Knudsen, D., Ron, O., Baardsen, G., Smedsgaard, J., Koppe, W., Froklaer, H., 2006. Soyasaponins resist extrusion cooking and are not degraded during gut passage in Atlantic salmon (Salmo salar L.). J. Agric. Food Chem. 54, 6428-6435.
Knudsen, D., Uran, P., Arnous, A., Koppe, W., Frokiaer, H., 2007. Saponin-containing subfractions of soybean molasses induce enteritis in the distal intestine of Atlantic salmon. J. Agric. Food Chem. 55, 2261-2267.
Knudsen, D., Jutfelt, F., Sundh, H., Sundell, K., Koppe, W., Frøkiær, H., 2008. Dietary soya saponins increase gut permeability and play a key role in the onset of soyabean-induced enteritis in Atlantic salmon (Salmo salar L.). Brit. J. Nutr. 100, 120-129.
Krogdahl, A., Roem, A., Baeverfjord, G., 1995. Effects of soybean saponin, raffinose and soybean alcohol extract on nutrient digestibilities, growth and intestinal morphology in Atlantic salmon. Proceedings of the International Conference of Aquaculture '95 and the Satellite Meeting Nutrition and Feeding of Cold Water Species , pp. 118-119. Ghent, Belgium, European Aquaculture Society. European Aquaculture Society Special Publication no. 23.
Krogdahl, A., Bakke-McKellep, A.M., Røed, K.H., Baeverfjord, G., 2000 Feeding Atlantic salmon (Salmo salar L.) soybean products: Effects on disease resistance (furunculosis), and lysozyme and IgM levels in the intestinal mucosa. Aquacult. Nutr. 6, 77-84.
Krogdahl, A., Bakke-McKellep, A.M., Baeverfjord, G., 2003. Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquaculture Nutr. 9, 361-371.
Krogdahl, Å., Bakke-McKellep, A.M., 2005. Fasting and refeeding cause rapid changes in intestinal tissue mass and digestive enzyme capacities of Atlantic salmon (Salmo salar L.). Comp. Biochem. Physiol. 141A, 450-460.
Krogdahl, Å., Penn, M., Thorsen, J., Refstie, S. Bakke, A.M., 2010. Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquacult. Res. 41, 333-344.
Lalles, J.P., Peltre, G., 1996. Biochemical features of grain legume allergens in humans and animals. Nutr. Rev. 54, 101-107.
Lilleeng, E., Froystad, M.K., Ostby, G.C., Valen, E.C., Krogdahl, Å., 2007. Effects of diets containing soybean meal on trypsin mRNA expression and activity in Atlantic salmon (Salmo salar L). Comp. Biochem. Physiol. A-Mol. Integrative Physiol. 147, 23-36.
Lilleeng, E., Penn, M.H., Haugland, O., Xu, C., Bakke, A.M., Krogdahl, Å., Landsverk, T., Froystad-Saugen, M.K., 2009. Decreased expression of TGF-ß, GILT and T-cell markers in the early stages of soybean enteropathy in Atlantic salmon (Salmo salar L.). Fish Shelfish Immunol. 27, 65-72.
McLean, E., Ash, R., 1987. Intact protein (antigen) absorption in fishes: mechanisms and physiological significance. J. Fish Biol. 31 (Suppl A), 219-223.
Mulero, I., Sepulcre, M.P., Meseguer, J., García-Ayala, A., Mulero, V., 2007. Histamine is stored in mast cells of most evolutionarily advanced fish and regulates the fish inflammatory response. PNAS 104, 19434-19439.
Norwegian Veterinary Institute (2010) The health situation in Norwegian aquaculture 2010. http://www.vetinst.no/eng/Research/Publications/Fish-Health-Report/Farmed-Fish-Healt-Report-2010.
Olli, J.J., Krogdahl, Å., 1994. Nutritive value of four soybean products as protein sources in diets for rainbow trout (Oncorhynchus mykiss, Walbaum) reared in fresh water. Acta Agricult. Scand., Sec. A, Anim. Sci. 44, 185-192.
Ostaszewska, T., Dabrowski, K., Palacios, M.E., Olejniczak, M., Wieczorek, M., 2005. Growth and morphological changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) and pacu (Piaractus mesopotamicus) due to casein replacement with soybean proteins. Aquaculture 245, 273-286.
Penn, M.H., Bendiksen, E.Å., Campbell, P., Krogdahl, Å., 2011. High level of dietary pea protein concentrate induces enteropathy in Atlantic salmon (Salmo salar L.). Aquaculture 310, 267-273.
Peres, H., Lim, C., Klesius, P.H., 2003. Nutritional value of heat-treated soybean meal for channel catfish (Ictalurus punctatus). Aquaculture 225, 67-82.
Peumans, W.J., Van Damme, E.J.M., 1995. Lectins as plant defense proteins. Plant Physiol. 109, 347-352.
Pusztai, A., Ewen, S.W.B., Grant, G., Peumans, W.J., Van Damme, E.J.M., Coates, M.E., Bardocz, S., 1995. Lectins and also bacteria modify the glycosylation of gut surface receptors in the rat. Glycoconjugate J. 12, 22-35.
Refstie, S., Helland, S.J., Storebakken, T., 1997. Adaptation to soybean meal in diets for rainbow trout, Oncorhynchus mykiss. Aquaculture 153, 263-272.
Refstie, S., Korsoen, O.J., Storebakken, T., Baeverfjord, G., Lein, I., Roem, A.J., 2000. Differing nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Aquaculture 190, 49-63.
Refstie, S., Sahlström, S., Bråthen, E., Baeverfjord, G., Krogedal, P., 2005. Lactic acid fermentation eliminates indigestible carbohydrates and antinutritional factors in soybean meal for Atlantic salmon (Salmo salar). Aquaculture 246, 331-345.
Refstie, S., Landsverk, T., Bakke-McKellep, A.M., Ringø, E., Sundby, A., Shearer, K.D., Krogdahl, Å., 2006. Digestive capacity, intestinal morphology, and microflora of 1-year and 2-year old Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean meal. Aquaculture 261, 269-284.
Reite, O.B., 1965. A phylogenetical approach to the functional significance of tissue mast cell histamine. Nature 206, 1334-1336.
Reite, O.B., 1972. Comparative physiology of histamine. Physiol. Rev. 52, 778-819.
Romarheim, O.H., Skrede, A., Gao, Y.L., Krogdahl, Å., Denstadli, V., Lilleeng, E., Storebakken, T., 2006. Comparison of white flakes and toasted soybean meal partly replacing fish meal as protein source in extruded feed for rainbow trout (Oncorhynchus mykiss). Aquaculture 256, 354-364.
Romarheim, O.H., Overland, M., Mydland, L.T., Skrede, A., Landsverk, T., 2011. Bacteria grown on natural gas prevent soybean meal-induced enteritis in Atalntic salmon. J. Nutr. 141, 124-130.
Rumsey, G.L., Siwicki, A.K., Anderson, D.P., Bowser, P.R., 1994. Effect of soybean protein on serological response, non-specific defense mechanisms, growth, and protein utilization in rainbow trout. Vet. Immunol. Immunopathol. 41, 323-339.
Saini, H.S., 1989. Legume seed oligosaccharides. In: Huisman, J., Van der Poel, A.F.B., Liener, I.E. (Eds) Recent Advances of Research in Antinutritional Factors in Legume Seeds. Pudoc, Wageningen, pp. 329–341.
Sanden, M., Berntssen, M.H.G., Krogdahl, Å., Hemre, G.-I., Bakke-McKellep, A.M., 2005. An examination of the intestinal tract of Atlantic salmon (Salmo salar L.) parr fed different varieties of soy and maize. J. Fish Dis. 28, 317-330.
Sandholm, M., Smith, R.R., Shih, J.C.H., Scott, M.L., 1976. Determination of antitrypsin activity on agar plates: relationship between antitrypsin and biological value of soybeans for trout. J. Nutr. 106, 761-766.
Sansonetti, P.J., 2004. War and peace at mucosal surfaces. Nat. Rev. Immunol. 4, 953-964.
Sire, M.F., Vernier, J.-M., 1992. Intestinal absorption of protein in teleost fish. Comp. Biochem. Physiol. 103A, 771-781.
Sire, M.-F., Dorin, D., Vernier, J.-M., 1992. Intestinal absorption of macromolecular proteins in rainbow trout. Aquaculture 100, 234-235.
Sorensen, M., Penn, M., El-Mowafi, A., Storebakken, T., Cai, C.F., Overland, M., Krogdahl, A., 2011. Effect of stachyose, raffinose and soya-saponins supplementation on nutrient digestibility, digestive enzymes, gut morphology and growth performance in Atlantic salmon (Salmo salar L.). Aquaculture 314, 145-152.
Tacon, A.G.J., Haastler, J.V., Featherstone, P.B., Kerr, K., Jackson, A.J., 1983. Studies on the utilization of full-fat and solvent extracted soybean meal in a complete diet for rainbow trout. Bull. Jap. Soc. Sci. Fisheries 49, 1437-1443.
Thorsen, J., Lilleeng, E., Valen, E.C., Krogdahl, A., 2008. Proteinase-activated reseptor-2: two potential inflammatory mediators of the gastrointestinal tract in Atlantic salmon. J. Inflamm. 5, 18.
Twibell, R.G., Wilson, R.P., 2004. Preliminary evidence that cholesterol improves growth and feed intake of soybean meal-based diets in aquaria studies with juvenile channel catfish, Ictalurus punctatus. Aquaculture 236, 539-546.
Uran, P.A., Aydin, R., Schrama, J.W.,Verreth, J.A.J., Rombout, J.H.W.M., 2008a. Soybean meal-induced uptake block in Atlantic salmon Salmo salar distal enterocytes. J. Fish Biol. 73, 2571-2579.
Uran, P.A., Goncalves, A.A.,Taverne-Thiele, J.J., Schrama, J.W., Verreth, J.A.J., Rombout, J.H.W.M., 2008b. Soybean meal induces intestinal inflammation in common carp (Cyprinus carpio L.). Fish Shellfish Immunol. 25, 751-760.
Valen, E., Marjara, I.S., Kortner, T.M., Krogdahl, Å., Bakke, A.M., 2010. Time response expression profiles of genes, possibly associated with effects of altered intestinal microbiota in Atlantic salmon (Salmo salar L.) fed soybean meal. Book of Abstracts from XIV ISFNF - International Symposium on Fish Nutrition and Feeding, May 31-June 4 2010, Qingdao, China.
Van den Ingh, T.S.G.A.M., Krogdahl, A., Olli, J., Hendricks, H.G.C.J.M., Koninkx, J.F.J.G., 1991. Effects of soybean-containing diets on the proximal and distal intestine in Atlantic salmon (Salmo salar): a morphological study. Aquaculture 94, 297-305.
Van den Ingh, T.S.G.A.M., Olli, J.J., Krogdahl, A., 1996. Alcohol-soluble components in soybeans cause morphological changes in the distal intestine of Atlantic salmon, Salmo salar L. J. Fish Dis. 19, 47-53.
VKM, 2009. Criteria for the safe use of plant ingredients in diets for aquacultured fish. Norwegian Scientific Committee for Food Safety, Oslo, Norway http://www.vkm.no/dav/aef85c6079.pdf
Yamamoto, T., Suzuki, N., Furuita, H., Sugita, T., Tanaka, N., Goto, T., 2007. Supplemental effect of bile salts to soybean meal-based diet on growth and feed utilization of rainbow trout Oncorhynchus mykiss. Fisheries Sci. 73, 123-131.
Yamamoto, T., Goto, T., Kine, Y., Endo, Y., Kitaoka, Y., Sugita, T., Furuita, H., Iwashita, Y., Suzuki, N., 2008. Effect of an alcohol extract from a defatted soybean meal supplemented with a casein-based semi-purified diet on the biliary bile status and intestinal conditions in rainbow trout Oncorhynchus mykiss (Walbaum). Aquacult. Res. 39, 986-994.
Yamamoto, T., Iwashita, Y., Matsunari, H., Sugita, T., Furuita, H., Akimoto, A., Okamatsu, K., Suzuki, N., 2010. Influence of fermentation conditions for soybean meal in a non-fish meal diet on the growth performance and physiological condition of rainbow trout Oncorhynchus mykiss. Aquaculture 309, 173-180.
