The nutritional background of the host alters the disease course in a fish-myxosporean system

Veterinary Parasitology

Volumn 175, Issue 1-2, 2011, Pages 141-150

  Estensoro, Itziar ^a   Benedito Palos, Laura ^a   Palenzuela, Oswaldo ^a   Kaushik, Sadasivam ^b   Sitjà Bobadilla, Ariadna ^a   Pérez Sánchez, Jaume ^a  

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

^b IFREMER   (France)

Author keywords

Anorexia; Enteromyxum; Immune response; Myxozoa; Parasites; Sparus aurata; Vegetable oils

Indexed keywords

FISH OIL; GLUTATHIONE; GLUTATHIONE DISULFIDE; LYSOZYME; VEGETABLE OIL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOREXIA; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; EFFLUENT; ENTEROMYXUM LEEI; GROWTH RATE; HEMATOCRIT; HOST PARASITE INTERACTION; IMMUNE RESPONSE; MYXOZOA; NONHUMAN; OXIDATIVE STRESS; PARASITE TRANSMISSION; PARASITE VIRULENCE; SEA BREAM; SPARUS AURATA;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; ANTIOXIDANTS; DIET; DIETARY FATS, UNSATURATED; FISH DISEASES; GLUTATHIONE; HOST-PARASITE INTERACTIONS; MYXOZOA; PLANT OILS; SEA BREAM;

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

EID: 78049480746     PISSN: 03044017     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetpar.2010.09.015     Document Type: Article

References (67)

1. Alvarez-Pellitero P. Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Vet. Immunol. Immunopathol. 2008, 126:171-198.
2. Alvarez-Pellitero P., Palenzuela O., Sitjà-Bobadilla A. Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol. Int. 2008, 57:110-120.
3. APROMAR, 2009. La acuicultura marina de peces en España (). http://www.apromar.es/informes.asp.
4. Argilés J.M., Busquets S., López-Soriano F.J. Cytokines as mediators and targets for cancer cachexia. Cancer Treat. Res. 2006, 130:199-217.
5. Bakke-McKellep A.M., Penn M.H., Salas P.M., Refstie S., Sperstad S., Landsverk T., Ringo E., Krogdahl A. 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.
6. Beecher G.R. Overview of dietary flavonoids: nomenclature, occurrence and intake. J. Nutr. 2003, 133:3248s-3254s.
7. Bell J.G., Ashton I., Secombes C.J., Weitzel B.R., Dick J.R., Sargent J.R. 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.
8. Benedito-Palos L., Saera-Vila A., Calduch-Giner J.A., Kaushik S., Pérez-Sánchez J. 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 2007, 267:199-212.
9. Benedito-Palos L., Navarro J.C., Sitjà-Bobadilla A., Bell J.G., Kaushik S., Pérez-Sánchez J. 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. Brit. J. Nutr. 2008, 100:992-1003.
10. Benedito-Palos L., Navarro J.C., Bermejo-Nogales A., Saera-Vila A., Kaushik S., Pérez-Sánchez J. 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 2009, 288:98-105.
11. Bermúdez R., Vigliano F., Marcaccini A., Sitjà-Bobadilla A., Quiroga M.I., Nieto J.M. Response of Ig-positive cells to Enteromyxum scophthalmi (Myxozoa) experimental infection in turbot, Scophthalmus maximus (L.): a histopathological and immunohistochemical study. Fish Shellfish Immunol. 2006, 21:501-512.
12. Bermúdez R., Losada A.P., Vázquez S., Redondo M.J., Alvarez-Pellitero P., Quiroga M.I. Light and electron microscopic studies on turbot Psetta maxima infected with Enteromyxum scophthalmi: histopathology of turbot enteromyxosis. Dis. Aquat. Org. 2010, 89:209-221.
13. Bransden M.P., Carter C.G., Nichols P.D. Replacement of fish oil with sunflower oil in feeds for Atlantic salmon (Salmo salar L.): effect on growth performance, tissue fatty acid composition and disease resistance. Comp. Biochem. Phys. B 2003, 135:611-625.
14. Calder P.C. Immunomodulation by omega-3 fatty acids. Prostaglandins Leukot. Essent. Fatty Acids 2007, 77:327-335.
15. Cerami A., Beutler B. The role of cachectin/TNF in endotoxic-shock and cachexia. Immunol. Today 1988, 9:28-31.
16. Carroll J.A. Bidirectional communication: growth and immunity in domestic livestock. J. Anim. Sci. 2008, 86:E126-E137.
17. Chapkin R.S., Wang N., Fan Y.Y., Lupton J.R., Prior I.A. Docosahexaenoic acid alters the size and distribution of cell surface microdomains. Biochim. Biophys. Acta 2008, 1778:466-471.
18. Colditz I.G. Six costs of immunity to gastrointestinal nematode infections. Parasite Immunol. 2008, 30:63-70.
19. Costello M.J. The global economic cost of sea lice to the salmonid farming industry. J. Fish Dis. 2009, 32:115-118.
20. Cuesta A., Muñoz P., Rodriguez A., Salinas I., Sitjà-Bobadilla A., Alvarez-Pellitero P., Esteban M.A., Meseguer J. Gilthead sea bream (Sparus aurata L.) innate defence against the parasite Enteromyxum leei (Myxozoa). Parasitology 2006, 132:95-104.
21. De Pablo M.A., De Cienfuegos G.A. Modulatory effects of dietary lipids on immune system functions. Immunol. Cell Biol. 2000, 78:31-39.
22. Dezfuli B.S., Giari L., Arrighi S., Domeneghini C., Bosi G. Influence of enteric helminths on the distribution of intestinal endocrine cells belonging to the diffuse endocrine system in brown trout, Salmo trutta L. J. Fish Dis. 2003, 26:155-166.
23. Emery P.W. Cachexia in experimental models. Nutrition 1999, 15:600-603.
24. Erdal J.I., Evensen O., Kaurstad O.K., Lillehaug A., Solbakken R., Thorud K. Relationship between diet and immune response in Atlantic salmon (Salmo salar L.) after feeding various levels of ascorbic-acid and omega-3-fatty-acids. Aquaculture 1991, 98:363-379.
25. Estensoro I., Bermúdez R., Losada A.P., Quiroga M.I., Pérez-Sánchez J., Alvarez-Pellitero P., Sitjà-Bobadilla A. Effect of Enteromyxum leei (Myxozoa) on gastrointestinal neuromodulators and cell apoptosis of gilthead sea bream (Sparus aurata). Diseases of Fish and Shellfish, Abstract Book, 14th EAFP Int. Conf 2009, 264.
26. Fang Y.Z., Yang S., Wu G.Y. Free radicals, antioxidants and nutrition. Nutrition 2002, 18:872-879.
27. Fekete S.G., Kellems R.O. Interrelationship of feeding with immunity and parasitic infection: a review. Vet. Med. Czech. 2007, 52:131-143.
28. Fisher D.S. Defining the experimental unit in grazing trials. J. Anim. Sci. 2000, 77:1E-5E.
29. Fleurance R., Sauvegrain C., Marques A., Le Breton A., Guereaud C., Cherel Y., Wyers M. Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis. Aquat. Org. 2008, 79:219-228.
30. Fracalossi D.M., Lovell R.T. Dietary lipid sources influence responses of channel catfish (Ictalurus punctatus) to challenge with the pathogen Edwardsiella ictaluri. Aquaculture 1994, 119:287-298.
31. Golomazou E., Athanassopoulou F., Karagouni E., Tsagozis P., Tsantilas H., Vagianou S. Experimental transmission of Enteromyxum leei Diamant, Lom and Dyková, 1994 in sharpsnout sea bream, Diplodus puntazzo C. and the effect on some innate immune parameters. Aquaculture 2006, 260:44-53.
32. Guo F.C., Woo P.T.K. Selected parasitosis in cultured and wild fish. Vet. Parasitol. 2009, 163:207-216.
33. Ishimatsu A., Hayashi M., Nakane M., Sameshima M. Pathophysiology of cultured tiger puffer Takifugu rubripes suffering from the myxosporean emaciation disease. Fish Pathol. 2007, 42:211-217.
34. Karagouni E., Athanassopoulou F., Tsagozis P., Ralli E., Moustakareas T., Lytra K., Dotsika E. The impact of a successful anti-myxosporean treatment on the phagocyte functions of juvenile and adult Sparus aurata L. Int. J. Immunopathol. Pharmacol. 2005, 18:121-132.
35. Kasper L.H., Buzoni-Gatel D. Ups and downs of mucosal cellular immunity against protozoan parasites. Infect. Immun. 2001, 69:1-8.
36. Kim H.P., Son K.H., Chang H.W., Kang S.S. Anti-inflammatory plant flavonoids and cellular action mechanisms. J. Pharmacol. Sci. 2004, 96:229-245.
37. Kiron V., Fukuda H., Takeuchi T., Watanabe T. Essential fatty-acid nutrition and defense mechanisms in rainbow trout Oncorhynchus mykiss. Comp. Biochem. Phys. A 1995, 111:361-367.
38. Kiron V., Puangkaew J., Ishizaka K., Satoh S., Watanabe T. Antioxidant status and nonspecific immune responses in rainbow trout (Oncorhynchus mykiss) fed two levels of vitamin E along with three lipid sources. Aquaculture 2004, 234:361-379.
39. Kurtz J., Wegner K.M., Kalbe M., Reusch T.B.H., Schaschl H., Hasselquist D., Milinski M. MHC genes and oxidative stress in sticklebacks: an immuno-ecological approach. Proc. R. Soc. B 2006, 273:1407-1414.
40. Kyriazakis I., Tolkamp B.J., Hutchings M.R. Towards a functional explanation for the occurrence of anorexia during parasitic infections. Anim. Behav. 1998, 56:265-274.
41. Lightbody J.H., Stevenson L.M., Jackson F., Donaldson K., Jones D.G. Comparative aspects of plasma antioxidant status in sheep and goats, and the influence of experimental abomasal nematode infection. J. Comp. Pathol. 2001, 124:192-199.
42. Lin Y.H., Shiau S.Y. Effects of dietary blend of fish oil with corn oil on growth and non-specific immune responses of grouper, Epinephelus malabaricus. Aquacult. Nutr. 2007, 13:137-144.
43. Mendieta-Zerón H., López M., Diéguez C. Gastrointestinal peptides controlling body weight homeostasis. Gen. Comp. Endocrinol. 2008, 155:481-495.
44. Misra S., Sahu N.P., Pal A.K., Xavier B., Kumar S., Mukherjee S.C. Pre- and post-challenge immuno-haematological changes in Labeo rohita juveniles fed gelatinised or non-gelatinised carbohydrate with n-3 PUFA. Fish Shellfish Immunol. 2006, 21:346-356.
45. Montero D., Kalinowski T., Obach A., Robaina L., Tort L., Caballero M.J., Izquierdo M.S. Vegetable lipid sources for gilthead sea bream (Sparus aurata): effects on fish health. Aquaculture 2003, 225:353-370.
46. 2a, immue function and effectiveness of a fish oil finishing diet. Aquacult. Nutr. 2005, 11:25-40.
47. Olsen R.E., Myklebust R., Ringø E., Mayhew T.M. The influences of dietary linseed oil and saturated fatty acids on caecal enterocytes in Arctic char (Salvelinus alpinus L.): a quantitative ultrastructural study. Fish Physiol. Biochem. 2000, 22:207-216.
48. Ots I., Kerimov A.B., Ivankina E.V., Ilyina T.A., Horak P. Immune challenge affects basal metabolic activity in wintering great tits. Proc. R. Soc. B 2001, 268:1175-1181.
49. Palenzuela O. Myxozoan infections in Mediterranean mariculture. Parassitologia 2006, 48:27-29.
50. Palenzuela O., Bartholomew J.L. Molecular tools for the diagnosis of Ceratomyxa shasta (Myxozoa). Molecular Diagnosis of Salmonid Diseases 2002, 285-298. Kluwer Academic Publishers, The Netherlands. C.O. Cunningham (Ed.).
51. Pergola C., Rossi A., Dugo P., Cuzzocrea S., Sautebin L. Inhibition of nitric oxide biosynthesis by anthocyanin fraction of blackberry extract. Nitric Oxide-Biol. Chem. 2006, 15:30-39.
52. Saera-Vila A., Benedito-Palos L., Sitjà-Bobadilla A., Nácher-Mestre J., Serrano R., Kaushik S., Pérez-Sánchez J. Assessment of the health and antioxidant trade-off in gilthead sea bream (Sparus aurata L.) fed alternative diets with low levels of contaminants. Aquaculture 2009, 296:87-95.
53. Saurabh S., Sahoo P.K. Lysozyme: an important defence molecule of fish innate immune system. Aquacult. Res. 2008, 39:223-239.
54. Sawai T., Drongowski R.A., Lampman R.W., Coran A.G., Harmon C.M. The effect of phospholipids and fatty acids on tight-junction permeability and bacterial translocation. Pediatr. Surg. Int. 2001, 17:269-274.
55. Schroers V., Van der Marel M., Steinhagen D. Influence of carp intestinal mucus molecular size and glycosylation on bacterial adhesion. Dis Aquat. Org. 2008, 81:135-142.
56. Sitjà-Bobadilla A. Parasites in Mediterranean aquacultured fish: current impact and future research directions. Multidisciplinarity for Parasites, Vectors and Parasitic Diseases 2004, 301-311. Medimond, Bologna, Italy. S. Mas-Coma (Ed.).
57. Sitjà-Bobadilla A. Can myxosporean parasites compromise fish and amphibian reproduction?. Proc. R. Soc. B 2009, 276:2861-2870.
58. Sitjà-Bobadilla A., Peña-Llopis S., Gómez-Requeni P., Médale F., Kaushik S., Pérez-Sánchez J. Effect of fish meal replacement by plant protein sources on non-specific defence mechanisms and oxidative stress in gilthead sea bream (Sparus aurata). Aquaculture 2005, 249:387-400.
59. Sitjà-Bobadilla A., Redondo M.J., Bermudez R., Palenzuela O., Ferreiro I., Riaza A., Quiroga I., Nieto J.M., Alvarez-Pellitero P. Innate and adaptive immune responses of turbot, Scophthalmus maximus (L.), following experimental infection with Enteromyxum scophthalmi (Myxosporea: Myxozoa). Fish Shellfish Immunol. 2006, 21:485-500.
60. Sitjà-Bobadilla A., Diamant A., Palenzuela O., Alvarez-Pellitero P. Effect of host factors and experimental conditions on the horizontal transmission of Enteromyxum leei (Myxozoa) to gilthead sea bream, Sparus aurata L. and European sea bass, Dicentrarchus labrax (L.). J. Fish Dis. 2007, 30:243-250.
61. Sitjà-Bobadilla A., Calduch-Giner J., Saera-Vila A., Palenzuela O., Alvarez-Pellitero P., Pérez-Sánchez J. Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish Shellfish Immunol. 2008, 24:610-619.
62. Sundaram U., Hassanain H., Suntres Z., Yu J.G., Cooke H.J., Guzman J., Christofi F.L. Rabbit chronic ileitis leads to up-regulation of adenosine A1/A3 gene products, oxidative stress, and immune modulation. Biochem. Pharmacol. 2003, 65:1529-1538.
63. Tacon A.G.J., Metian M. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 2008, 285:146-158.
64. Thomas P.T., Woo P.T.K. Anorexia in rainbow trout, Oncorhynchus mykiss (Walbaum), infected with Cryptobia salmositica (Sarcomastigophora: Kinetoplastida): its onset and contribution to the immunodepression. J. Fish Dis. 1992, 15:443-447.
65. Thompson K.D., Tatner M.F., Henderson R.J. Effects of dietary (n-3) and (n-6) polyunsaturated fatty acid ratio on the immune response of Atlantic salmon, Salmo salar L. Aquacult. Nutr. 1996, 2:21-31.
66. Vargas R.J., De Souza S.N.G., Mabilia R.G., Carlet F., Baggio S.R. Physiological response of experimental challenge of Ichthyophthirius multifiliis (Fouquet, 1876) in jundia (Rhamdia quelen Quoy and Gaimard, 1824) fingerlings rather fed with different lipid sources. Rev. Bras. Parasitol. Vet. 2008, 17:81-86.
67. Yoshino T.P., Boyle J.P., Humphries J.E. Receptor-ligand interactions and cellular signalling at the host-parasite interface. Parasitology 2001, 123:S143-S157.