Effect of nutrition and Enteromyxum leei infection on gilthead sea bream Sparus aurata intestinal carbohydrate distribution

Diseases of Aquatic Organisms

Volumn 100, Issue 1, 2012, Pages 29-42

  Estensoro, Itziar ^a   Redondo, María José ^a   Salesa, Beatriz ^a   Kaushik, Savasidam ^b   Pérez Sánchez, Jaume ^a   Sitjà Bobadilla, Ariadna ^a  

^a CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

^b UR1067 Nutrition Metabolism Aquaculture   (France)

Author keywords

Goblet cell; Histochemistry; Lectin; Mucin; Myxosporea; Myxozoa; Parasite; Replacement diet

Indexed keywords

EDIBLE OIL; FISH OIL; MUCIN; VEGETABLE OIL;

CARBOHYDRATE; DIET; INFECTIOUS DISEASE; PARASITE INTENSITY; PARASITIC DISEASE; PERCIFORM; PROTEIN; SAMPLING;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ANIMAL PARASITOSIS; ARTICLE; CARBOHYDRATE METABOLISM; CHEMISTRY; DIET; FISH DISEASE; INTESTINE; METABOLISM; MYXOZOA; NUTRITIONAL STATUS; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; SEA BREAM;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CARBOHYDRATE METABOLISM; DIET; DIETARY FATS, UNSATURATED; FISH DISEASES; FISH OILS; INTESTINES; MUCINS; MYXOZOA; NUTRITIONAL STATUS; PARASITIC DISEASES, ANIMAL; PLANT OILS; SEA BREAM;

ARCHOSARGUS RHOMBOIDALIS; ENTEROMYXUM LEEI; MYXOSPOREA; MYXOZOA; SAMBUCUS NIGRA; SPARUS AURATA;

EID: 84866235151     PISSN: 01775103     EISSN: 16161580     Source Type: Journal    
DOI: 10.3354/dao02486     Document Type: Article

References (77)

1. APROMAR (La Asociación Empresarial de Productores de Cultivos Marinos de España) (2011) La acuicultura mar - ina de peces en España. Accessed 15 Dec 2011 www.apromar.es/Informes/informe%202011/ Informe-APROMAR-2011.pdf
2. Arnold JW, Klimpel GR, Niesel DW (1993) Tumor Necrosis Factor (TNF?) regulates intestinal mucus production during salmonellosis. Cell Immunol 151: 336-344 (Pubitemid 23325456)
3. Benedito-Palos L, Saera-Vila A, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J (2007) Combined replacement of fish meal and oil in practical diets for fast growing juveniles of gilthead sea bream (Sparus aurata L.): networking of systemic and local components of GH/IGF axis. Aquaculture 267: 199-212 (Pubitemid 46899124)
4. Benedito-Palos L, Navarro JC, Sitjà-Bobadilla A, Bell JG, Kaushik S, Pérez-Sánchez J (2008) High levels of vegetable oils in plant protein-rich diets fed to gilthead sea bream (Sparus aurata L.): growth performance, muscle fatty acid profiles and histological alterations of target tissues. Br J Nutr 100: 992-1003
5. Benedito-Palos L, Navarro JC, Bermejo-Nogales A, Saera- Vila A, Kaushik S, Pérez-Sánchez J (2009) The time course of fish oil wash-out follows a simple dilution model in gilthead sea bream (Sparus aurata L.) fed graded levels of vegetable oils. Aquaculture 288: 98-105
6. Bergstrom KSB, Guttman JA, Rumi M, Ma C and others (2008) Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect Immun 76: 796-811 (Pubitemid 351251753)
7. Bermúdez R, Faílde LD, Losada AP, Redondo MJ, Alvarez- Pellitero P, Quiroga MI (2009) Morphopathological and ultrastructural studies on enteromyxosis of turbot (Psetta maxima L.). 14th Int Conf Eur Assoc Fish Path. HA LA - MA, Prague, p 17
8. Bosi G, Arrighi S, Di Giancamillo A, Domeneghini C (2005) Histochemistry of glycoconjugates in mucous cells of Salmo trutta uninfected and naturally parasitized with intestinal helminths. Dis Aquat Org 64: 45-51 (Pubitemid 40641112)
9. Carrassón M, Grau A, Dopazo LR, Crespo S (2006) A histological, histochemical and ultrastructural study of the digestive tract of Dentex dentex (Pisces, Sparidae). Histol Histopathol 21: 579-593
10. Costello MJ (2009) The global economic cost of sea lice to the salmonid farming industry. J Fish Dis 32: 115-118
11. Davey GC, Calduch-Giner JA, Houeix B, Talbot A, Sitjà- Bobadillac A, Prunet P, Pérez-Sánchez J, Cairns MT (2011) Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei. Mol Immunol 48: 2102-2112
12. Dezfuli BS, Manera M, Onestini S, Rossi R (1997) Histo - pathology of the alimentary canal of Anguilla anguilla L. associated with digenetic trematodes: a light and electron microscopic study. J Fish Dis 20: 317-322 (Pubitemid 27307326)
13. Dezfuli BS, Pironi F, Campisi M, Shinn AP, Giari L (2010) The response of intestinal mucous cells to the presence of enteric helminths: their distribution, histochemistry and fine structure. J Fish Dis 33: 481-488
14. Dharmani P, Srivastava V, Kissoon-Singh V, Chadee K (2009) Role of intestinal mucins in innate host defense mechanisms against pathogens. J Innate Immun 1: 123-135
15. Domeneghini C, Pannelli Straini R, Veggetti A (1998) Gut glycoconjugates in Sparus aurata L. (Pisces, Teleostei). A comparative histochemical study in larval and adult ages. Histol Histopathol 13: 359-372 (Pubitemid 28197702)
16. Domeneghini C, Arrighi S, Radaelli G, Bosi G, Veggetti A (2005) Histochemical analysis of glycoconjugate secretion in the alimentary canal of Anguilla anguilla L. Acta Histochem 106: 477-487 (Pubitemid 40221903)
17. Elbal MT, Agulleiro B (1986) A histochemical and ultrastructural study of the gut of Sparus auratus (Teleostei). J Submicrosc Cytol Pathol 18: 335-347 (Pubitemid 16111499)
18. Else KJ (2005) Have gastrointestinal nematodes outwitted the immune system? Parasite Immunol 27: 407-415 (Pubitemid 41413488)
19. Escaffre AM, Kaushik S, Mambrini M (2007) Morphometric evaluation of changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) due to fish meal replacement with soy protein concentrate. Aquaculture 273: 127-138 (Pubitemid 350141649)
20. Estensoro I, Benedito-Palos L, Palenzuela O, Kaushik S, Sitjà-Bobadilla A, Pérez-Sánchez J (2011a) The nutritional background of the host alters the disease course in a fish?myxosporean system. Vet Parasitol 175: 141-150
21. Estensoro I, Jung-Schroers V, Steinhagen D, Sitjà-Bobadilla A (2011b) Glycoprotein changes in the intestinal mucus of gilthead sea bream Sparus aurata parasitized by Enteromyxum leei (Myxozoa). 14th Int Conf Eur Assoc Fish Path. Dalmacijapapir, Split, p 63
22. Estensoro I, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J, Sitjà-Bobadilla A (2011c) Modulation of the gene expression of IgM and distribution of IgM+ cells by nutritional background and infection by Enteromyxum leei (Myxozoa) in gilthead sea bream (Sparus aurata). 14th Int Conf Eur Assoc Fish Path. Dalmacijapapir, Split, p 81
23. Ferguson JA, Koketsu W, Ninomiya I, Rossignol PA, Jacobson KC, Kent ML (2011) Mortality of coho salmon (Oncorhynchus kisutch) associated with burdens of multiple parasite species. Int J Parasitol 41: 1197-1205
24. Fernandez F, Sharma R, Hinton M, Bedford MR (2000) Diet influences the colonisation of Campylobacter jejuni and distribution of mucin carbohydrates in the chick intestinal tract. Cell Mol Life Sci 57: 1793-1801
25. Fiertak A, Kilarski WM (2002) Glycoconjugates of the intestinal goblet cells of four cyprinids. Cell Mol Life Sci 59: 1724-1733 (Pubitemid 35346976)
26. Fleurance R, Sauvegrain C, Marques A, Le Breton A, Guereaud C, Cherel Y, Wyers M (2008) Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis Aquat Org 79: 219-228 (Pubitemid 351806262)
27. Fujino T, Fried B (1993) Echinostoma caproni and E. trivolvis alter the binding of glycoconjugates in the intestinal mucosa of C3H mice as determined by lectin histochemistry. J Helminthol 67: 179-188 (Pubitemid 23335755)
28. Gendler SJ, Spicer AP (1995) Epithelial mucin genes. Annu Rev Physiol 57: 607-634
29. Geurden I, Jutfelt F, Olsen RE, Sundell KS (2009) A vegetable oil feeding history affects digestibility and intestinal fatty acid uptake in juvenile rainbow trout Oncho - rhynchus mykiss. Comp Biochem Physiol A 152: 552-559
30. Harikrishnan R, Balasundaram C, Heo MS (2011) Impact of plant products on innate and adaptive immune system of cultured finfish and shellfish. Aquaculture 317: 1-15
31. Karlsson NG, Olson FJ, Jovall PÅ, Andersch Y, Enerbäck L, Hansson GC (2000) Identification of transient glycosylation alterations of sialylated mucin oligosaccharides during infection by the rat intestinal parasite Nippostrongylus brasiliensis. Biochem J 350: 805-814
32. Kent ML, Margolis L, Whitaker DJ, Hoskins GE, McDonald TE (1994) Review of Myxosporea of importance in salmonid fisheries and aquaculture in British Columbia. Folia Parasitol 41: 27-37 (Pubitemid 2090166)
33. Lambert ME, Schofield PF, Ironside AG, Mandal BK (1979) Campylobacter colitis. BMJ 1: 857-859 (Pubitemid 9140823)
34. Leknes IL (2010) Histochemical study on the intestine goblet cells in cichlid and poecilid species (Teleostei). Tissue Cell 42: 61-64
35. Leknes IL (2011) Mucus cells in the digestive tract in prenatal platyfish larvae (Poeciliidae, Teleostei). Anat Histol Embryol 40: 375-378
36. Lima dos Santos CAM, Howgate P (2011) Fishborne zoonotic parasites and aquaculture: a review. Aquaculture 318: 253-261
37. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckinMA (2008) Mucins in the mucosal barrier to infection. Mucosal Immunol 1: 183-197 (Pubitemid 351541304)
38. Maruyama H, Yabu Y, Yoshida A, Nawa Y, Ohta N (2000) A role of mast cell glycosaminoglycans for the immunological expulsion of intestinal nematode, Strongyloides venezuelensis. J Immunol 164: 3749-3754 (Pubitemid 30169831)
39. Maruyama H, Hirabayashi Y, El-Malky M, Okamura S and others (2002) Strongyloides venezuelensis: longitudinal distribution of adult worms in the host intestine is influenced by mucosal sulfated carbohydrates. Exp Parasitol 100: 179-185 (Pubitemid 36269036)
40. McCracken VJ, Lorenz RG (2001) The gastrointestinal ecosystem: a precarious alliance among epithelium, immunity and microbiota. Cell Microbiol 3: 1-11 (Pubitemid 32107421)
41. Mennerat A, Nilsen F, Ebert D, Skorping A (2010) Intensive farming: evolutionary implications for parasites and pathogens. Evol Biol 37: 59-67
42. Moncada DM, Kammanadiminti SJ, Chadee K (2003) Mucin and toll-like receptors in host defense against intestinal parasites. Trends Parasitol 19: 305-311 (Pubitemid 36833218)
43. Moran JDW, Whitaker DJ, Kent ML (1999) A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172: 163-196 (Pubitemid 29096960)
44. Murray HM, Wright GM, Goff GP (1996) A comparative histological and histochemical study of the post-gastric alimentary canal from three species of pleuronectid, the Atlantic halibut, the yellowtail flounder and the winter flounder. J Fish Biol 48: 187-206 (Pubitemid 126734245)
45. Okamura B, Feist SW (2011) Emerging diseases in fresh - water systems. Freshw Biol 56: 627-637
46. Palenzuela O (2006) Myxozoan infections in Mediterranean mariculture. Parassitologia 48: 27-29
47. Palenzuela O, Bartholomew JL (2002) Molecular tools for the diagnosis of Ceratomyxa shasta (Myxozoa). In: Cunningham CO (ed) Molecular diagnosis of salmonid diseases. Kluwer Academic Publishers, Dordrecht, p 285-298
48. Parillo F, Fagioli O, Ceccarelli P (2002) Glucidic determinants expressed by the digestive apparatus of Umbrina cirrosa (L.) fries as revealed by lectin histochemistry. Acta Histochem 104: 209-215 (Pubitemid 34606367)
49. Park JY, Kim IS, Kim SY (2003) Structure and mucous histochemistry of the intestinal respiratory tract of the mud loach, Misgurnus anguillicaudatus (Cantor). J Appl Ichthyology 19: 215-219 (Pubitemid 37178170)
50. Patel N, Kreider T, Urban JF, Gause WC (2009) Characterisation of effector mechanisms at the host: parasite interface during the immune response to tissue-dwelling intestinal nematode parasites. Int J Parasitol 39: 13-21
51. Pedini V, Scocco P, Radaelli G, Fagioli O, Ceccarelli P (2001) Carbohydrate histochemistry of the alimentary canal of the shi drum, Umbrina cirrosa L. Anat Histol Embryol 30: 345-349
52. Perez-Vilar J, Hill RL (1999) The structure and assembly of secreted mucins. J Biol Chem 274: 31751-31754
53. Piel C, Montagne L, Sève B, Lallès JP (2005) Increasing digesta viscosity using carboxymethylcellulose in weaned piglets stimulates ileal goblet cell numbers and maturation. J Nutr 135: 86-91 (Pubitemid 40094326)
54. Redondo MJ, Alvarez-Pellitero P (2009) Lectinhistochemical detection of terminal carbohydrate residues in the enteric myxozoan Enteromyxum leei parasitizing gilthead seabream Sparus aurata (Pisces: Teleostei): a study using light and transmission electron microscopy. Folia Parasitol 56: 259-267
55. Redondo MJ, Alvarez-Pellitero P (2010a) Carbohydrate patterns in the digestive tract of Sparus aurata L. and Psetta maxima (L.) (Teleostei) parasitized by Enteromyxum leei and E. scophthalmi (Myxozoa). Parasitol Int 59: 445-453
56. Redondo MJ, Alvarez-Pellitero P (2010b) The effect of lectins on the attachment and invasion of Enteromyxum scophthalmi (Myxozoa) in turbot (Psetta maxima L.) intestinal epithelium in vitro. Exp Parasitol 126: 577-581
57. Redondo MJ, Cortadellas N, Palenzuela O, Alvarez-Pellitero P (2008) Detection of carbohydrate terminals in the enteric parasite Enteromyxum scophthalmi (Myxozoa) and possible interactions with its fish host Psetta maxima. Parasitol Res 102: 1257-1267
58. Rombout JHMW, Abelli L, Picchietti S, Scapigliati G, Kiron V (2011) Teleost intestinal immunology. Fish Shellfish Immunol 31: 616-626
59. Sachdev HP, Chadha V, Malhotra V, Verghese A, Puri RK (1993) Rectal histopathology in endemic Shigella and Salmonella diarrhea. J Pediatr Gastroenterol Nutr 16: 33-38 (Pubitemid 23014268)
60. Saera-Vila A, Benedito-Palos L, Sitjà-Bobadilla A, Nácher- Mestre J, Serrano R, Kaushik S, 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: 87-95
61. Santigosa E, Sánchez J, Médale F, Kaushik S, Pérez-Sánchez J, Gallardo MA (2008) Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 282: 68-74
62. Sarasquete C, Gisbert E, Ribeiro L, Vieira L, Dinis MT (2001) Glycoconjugates in epidermal, branchial and digestive mucous cells and gastric glands of gilthead sea bream, Sparus aurata, Senegal sole, Solea senegalensis, and Siberian sturgeon, Acipenser baeri development. Eur J Histochem 45: 267-278 (Pubitemid 33700731)
63. Scocco P, Menghi G, Ceccarelli P (1997) Histochemical differentiation of glycoconjugates occurring in the tilapine intestine. J Fish Biol 51: 848-857 (Pubitemid 27441876)
64. Silva FCP, Nicoli JR, Zambonino-Infante JL, Le Gall MM, Kaushik S, Gatesoupe FJJ (2010) Influence of partial substitution of dietary fish meal on the activity of digestive enzymes in the intestinal brush border membrane of gilthead sea bream, Sparus aurata and goldfish, Carassius auratus. Aquaculture 306: 233-237
65. Sitjà-Bobadilla A, Diamant A, Palenzuela O, Alvarez-Pellitero P (2007) Effect of host factors and experimental conditions on the horizontal transmission of Entero - myxum leei (Myxozoa) to gilthead sea bream, Sparus aurata L., and European sea bass, Dicentrarchus labrax (L.). J Fish Dis 30: 243-250 (Pubitemid 46496670)
66. Sitjà-Bobadilla A, Calduch-Giner J, Saera-Vila A, Palenzuela O, Alvarez-Pellitero P, Pérez-Sánchez J (2008) Chronic exposure to the parasite Enteromyxum leei (Myxo zoa: Myxosporea) modulates the immune re - sponse and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish Shellfish Immunol 24: 610-619
67. Smith LS (1989) Digestive functions in teleost fishes. In: Halver JE (ed) Fish nutrition, 2nd edn. Academic Press, San Diego, CA, p 331-421
68. Soffientino B, Gómez-Chiarri M, Specker J (2006) Developmental changes in stomach, intestine, and skin glycoconjugates in summer flounder (Paralichthys dentatus): a lectin histochemical study. Aquaculture 253: 680-687
69. Steinberg SE, Banwell JG, Yardley JH, Keusch GT, Hendrix TR (1975) Comparison of secretory and histological effects of shigella and cholera enterotoxins in rabbit jejunum. Gastroenterology 68: 309-317
70. Stroband HWJ, van deer Meer H, Timmermans LPM (1979) Regional functional differentiation in the gut of the grasscarp, Ctenopharyngodon idella (Val.). Histochemistry 64: 235-249 (Pubitemid 10218792)
71. Tacchi L, Bickerdike R, Douglas A, Secombes CJ, Martin SAM (2011) Transcriptomic responses to functional feeds in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 31: 704-715
72. Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285: 146-158
73. Torrecillas S, Makol A, Caballero MJ, Montero D and others (2007) Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol 23: 969-981 (Pubitemid 47381424)
74. Torrecillas S, Makol A, Caballero MJ, Montero D, Ginés R, Sweetman J, Izquierdo MS (2011a) Improved feed utilization, intestinal mucus production and immune para - meters in sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS). Aquacult Nutr 17: 223-233
75. Torrecillas S, Makol A, Benítez-Santana T, Caballero MJ, Montero D, Sweetman J, Izquierdo MS (2011b) Reduced gut bacterial translocation in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides (MOS). Fish Shellfish Immunol 30: 674-681
76. Udayamputhoor RS, Hariharan H, Van Lunen TA, Lewis PJ, Heaney S, Price L, Woodward D (2003) Effects of diet formulations containing proteins from different sources on intestinal colonization by Campylobacter jejuni in broiler chickens. Can J Vet Res 67: 204-212 (Pubitemid 37038659)
77. Woo PTK (2003) Cryptobia (Trypanoplasma) salmositica and salmonid crytobiosis. J Fish Dis 26: 627-646 (Pubitemid 38042962)