Effect of Low Dose of Fumonisins on Pig Health: Immune Status, Intestinal Microbiota and Sensitivity to Salmonella

Toxins

Volumn 5, Issue 4, 2013, Pages 841-864

  Burel, Christine ^a,d   Tanguy, Mael ^a   Guerre, Philippe ^b   Boilletot, Eric ^a   Cariolet, Roland ^a   Queguiner, Marilyne ^a   Postollec, Gilbert ^a   Pinton, Philippe ^c   Salvat, Gilles ^a   Oswald, Isabelle P ^c   Fravalo, Philippe ^a,e  

^a FRENCH AGENCY FOR FOOD   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^d UR1067 Nutrition Metabolism Aquaculture   (France)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Co contamination; Fumonisins; Growth; Health; Immune status; Intestinal microbiota; Mycotoxins; Pig; Salmonella

Indexed keywords

FUMONISIN; SPHINGANINE; SPHINGOSINE;

ANIMAL EXPERIMENT; ANIMAL FOOD; ANIMAL TISSUE; ARTICLE; BACTERIAL TRANSLOCATION; CONTROLLED STUDY; FECES MICROFLORA; FOOD CONTAMINATION; IMMUNE STATUS; INTESTINE FLORA; LONG TERM EXPOSURE; LYMPHOCYTE PROLIFERATION; MIXED INFECTION; MYCOTOXICOSIS; NONHUMAN; SALMONELLA TYPHIMURIUM; SEROCONVERSION; SWINE;

ANIMALS; ANIMALS, INBRED STRAINS; ANTIGENS, BACTERIAL; BIOLOGICAL MARKERS; CELL PROLIFERATION; FECES; FEMALE; FOOD CONTAMINATION; FRANCE; FUMONISINS; IMMUNITY, CELLULAR; INTESTINES; LYMPHOCYTES; MALE; MICROBIAL VIABILITY; MITOGENS; SALMONELLA TYPHIMURIUM; SPECIFIC PATHOGEN-FREE ORGANISMS; SPHINGOSINE; SUS SCROFA; WEIGHT GAIN;

EID: 84877273411     PISSN: 20726651     EISSN: None     Source Type: Journal    
DOI: 10.3390/toxins5040841     Document Type: Article

References (48)

1. o 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. Eur. Union 2006, L364/5, 5-24.
2. The Commission of the European Communities. Commission Recommendation of 17 August 2006 on the prevention and reduction of Fusarium toxins in cereals and cereal products. Off. J. Eur. Union 2006, L234/35, 35-40.
3. Haschek, W.M.; Gumprecht, L.A.; Smith, G.; Tumbleson, M.E.; Constable, P.D. Fumonisin toxicosis in swine: An overview of porcine pulmonary edema and current perspectives. Environ. Health Perspect. 2001, 109, 251-257.
4. Pettersson, H. Mycotoxin Contamination of Animal Feed. In Animal Feed Contamination: Effects on Livestock and Food Safety; Fink-Gremmels, J., Ed.; Woodhead Publishing Series in Food Science, Technology and Nutrition: Cambridge, UK, 2012; pp. 233-285.
5. Bouhet, S.; Oswald, I.P. The intestine as a possible target for fumonisin toxicity. Mol. Nutr. Food Res. 2007, 51, 925-931.
6. Lessard, M.; Boudry, G.; Seve, B.; Oswald, I.P.; Lalles, J.P. Intestinal physiology and peptidase activity in male pigs are modulated by consumption of corn culture extracts containing fumonisins. J. Nutr. 2009, 139, 1303-1307.
7. Lalles, J.P.; Lessard, M.; Boudry, G. Intestinal barrier function is modulated by short-term exposure to fumonisin B-1 in Ussing chambers. Vet. Res. Commun. 2009, 33, 1039-1043.
8. Bracarense, A.P.; Lucioli, J.; Grenier, B.; Drociunas Pacheco, G.; Moll, W.D.; Schatzmayr, G.; Oswald, I.P. Chronic ingestion of deoxynivalenol and fumonisin, alone or in interaction, induces morphological and immunological changes in the intestine of piglets. Br. J. Nutr. 2012, 107, 1776-1786.
9. Riley, R.T.; An, N.H.; Showker, J.L.; Yoo, H.S.; Norred, W.P.; Chamberlain, W.J.; Wang, E.; Merrill, A.H., Jr.; Motelin, G.; Beasley, V.R.; et al. Alteration of tissue and serum sphinganine to sphingosine ratio: An early biomarker of exposure to fumonisin-containing feeds in pigs. Toxicol. Appl. Pharmacol. 1993, 118, 105-112.
10. Zomborszky-Kovacs, M.; Vetesi, F.; Horn, P.; Repa, I.; Kovacs, F. Effects of prolonged exposure to low-dose fumonisin B-1 in pigs. J. Vet. Med. Ser. B 2002, 49, 197-201.
11. Wang, E.; Norred, W.P.; Bacon, C.W.; Riley, R.T.; Merrill, A.H. Inhibition of sphingolipid biosynthesis by fumonisins-Implications for diseases associated with fusarium-moniliforme. J. Biol. Chem. 1991, 266, 14486-14490.
12. AFSSA. Evaluation des Risques Liés à la Présence de Mycotoxines Dans les Chaines Alimentaires Humaine et Animale; AFSSA: Maisons-Alfort, France, 2009; p. 339.
13. Oswald, I.P.; Desautels, C.; Laffitte, J.; Fournout, S.; Peres, S.Y.; Odin, M.; le Bars, P.; le Bars, J.; Fairbrother, J.M. Mycotoxin fumonisin B-1 increases intestinal colonization by pathogenic Escherichia coli in pigs. Appl. Environ. Microbiol. 2003, 69, 5870-5874.
14. Devriendt, B.; Gallois, M.; Verdonck, F.; Wache, Y.; Bimczok, D.; Oswald, I.P.; Goddeeris, B.M.; Cox, E. The food contaminant fumonisin B(1) reduces the maturation of porcine CD11R1(+) intestinal antigen presenting cells and antigen-specific immune responses, leading to a prolonged intestinal ETEC infection. Vet. Res. 2009, 40, 40.
15. Deshmukh, S.; Asrani, R.K.; Jindal, N.; Ledoux, D.R.; Rottinghaus, G.E.; Sharma, M.; Singh, S.P. Effects of Fusarium moniliforme culture material containing known levels of fumonisin B1 on progress of Salmonella Gallinarum infection in Japanese quail: Clinical signs and hematologic studies. Avian Dis. 2005, 49, 274-280.
16. The Commission of the European Communities. Regulation (EC) N2160/2003 of the European Parliament and of the Council of 17 November 2003 on the control of salmonella and other specified food-borne zoonotic agents. Off. J. Eur. Union 2003, L325/1, 1-15.
17. D'Aoust, J.Y. Salmonella and the international food trade. Int. J. Food Microbiol. 1994, 24, 11-31.
18. Patten, R.C. Salmonellosis. Am. Fam. Physician 1981, 23, 113-117.
19. Berends, B.R.; VanKnapen, F.; Snijders, J.M.A.; Mossel, D.A.A. Identification and quantification of risk factors regarding Salmonella spp. On pork carcasses. Int. J. Food Microbiol. 1997, 36, 199-206.
20. Steinbach, G.; Kroell, U. Salmonella infections in swine herds-Epidemiology and importance for human illnesses. Deutsch. Tierarztl. Wochenschr. 1999, 106, 282-288.
21. Mikkelsen, L.L.; Naughton, P.J.; Hedemann, M.S.; Jensen, B.B. Effects of physical properties of feed on microbial ecology and survival of Salmonella enterica serovar Typhimurium in the pig gastrointestinal tract. Appl. Environ. Microbiol. 2004, 70, 3485-3492.
22. Hopwood, D.E.; Pethick, D.W.; Hampson, D.J. Increasing the viscosity of the intestinal contents stimulates proliferation of enterotoxigenic Escherichia coli and Brachyspira pilosicoli in weaner pigs. Br. J. Nutr. 2002, 88, 523-532.
23. Becker, B.; Bresch, H.; Schillinger, U.; Thiel, P.G. The effect of fumonisin B-1 on the growth of bacteria. World J. Microbiol. Biotechnol. 1997, 13, 539-543.
24. Tenk, I.; Fodor, E.; Szathmary, C. The effect of pure fusarium toxin-t-2, toxin-f-2 and toxin-das on the microflora of the gut and on plasma glucocorticoid levels in rat and swine. Zentralblatt Bakteriol. Mikrobiol. Hyg. Ser. A 1982, 252, 384-393.
25. Verbrugghe, E.; Vandenbroucke, V.; Dhaenens, M.; Shearer, N.; Goossens, J.; De Saeger, S.; Eeckhout, M.; D'Herde, K.; Thompson, A.; Deforce, D.; et al. T-2 toxin induced Salmonella typhimurium intoxication results in decreased Salmonella numbers in the cecum contents of pigs, despite marked effects on Salmonella-host cell interactions. Vet. Res. 2012, 43, 22.
26. Wache, Y.J.; Valat, C.; Postollec, G.; Bougeard, S.; Burel, C.; Oswald, I.P.; Fravalo, P. Impact of deoxynivalenol on the intestinal microflora of pigs. Int. J. Mol. Sci. 2009, 10, 1-17.
27. Cariolet, R.; Le Diguerher, G.; Ecobichon, P.; Julou, P.; Jolly, J.-P.; Madec, F. Production of Long Term, Low-Cost Specific Pathogen Free Pigs, In Proceedings of Animal Production in Europe: The Way Forward in a Changing World, International Society for Animal Hygiene: Saint Malo, France, 11-13 October 2004; p. 149.
28. Solfrizzo, M.; Avantaggiato, G.; Visconti, A. Rapid method to determine sphinganine/sphingosine in human and animal urine as a biomarker for fumonisin exposure. J. Chromatogr. B 1997, 692, 87-93.
29. Dilkin, P.; Direito, G.; Simas, M.M.S.; Mallmann, C.A.; Correa, B. Toxicokinetics and toxicological effects of single oral dose of fumonisin B1 containing Fusarium verticillioides culture material in weaned piglets. Chem. Biol. Interact. 2010, 185, 157-162.
30. Zomborszky, M.K.; Vetesi, F.; Repa, I.; Kovacs, F.; Bata, A.; Horn, P.; Toth, A.; Romvari, R. Experiment to determine limits of tolerance for fumonisin B1 in weaned piglets. J. Vet. Med. Ser. B 2000, 47, 277-286.
31. Rotter, B.A.; Thompson, B.K.; Prelusky, D.B.; Trenholm, H.L.; Stewart, B.; Miller, J.D.; Savard, M.E. Response of growing swine to dietary exposure to pure fumonisin B1 during an eight-week period: Growth and clinical parameters. Nat. Toxins 1996, 4, 42-50.
32. Dilkin, P.; Zorzete, P.; Mallmann, C.A.; Gomes, J.D.F.; Utiyama, C.E.; Oetting, L.L.; Correa, B. Toxicological effects of chronic low doses of aflatoxin B-1 and fumonisin B-1-containing Fusarium mondiforme culture material in weaned piglets. Food Chem. Toxicol. 2003, 41, 1345-1353.
33. Grenier, B.; Loureiro-Bracarense, A.P.; Lucioli, J.; Pacheco, G.D.; Cossalter, A.M.; Moll, W.D.; Schatzmayr, G.; Oswald, I.P. Individual and combined effects of subclinical doses of deoxynivalenol and fumonisins in piglets. Mol. Nutr. Food Res. 2011, 55, 761-771.
34. Fravalo, P.; Cariolet, R.; Proux, K.; Salvat, G. Le portage asymptomatique de Salmonella enterica par les porcs: Résultats issus de la constitution d'un modèle en conditions expérimentales. J. Rech. Porcine 2003, 35, 393-400.
35. Oswald, I.P.; Coméra, C. Immunotoxicity of mycotoxins. Rev. Méd. Vét. 1998, 149, 585-590.
36. Halloy, D.J.; Gustin, P.G.; Bouhet, S.; Oswald, I.P. Oral exposure to culture material extract containing fumonisins predisposes swine to the development of pneumonitis caused by Pasteurellamultocida. Toxicology 2005, 213, 34-44.
37. Posa, R.; Donko, T.; Bogner, P.; Kovacs, M.; Repa, I.; Magyar, T. Interaction of Bordetella bronchiseptica, Pasteurella multocida, and fumonisin B1 in the porcine respiratory tract as studied by computed tomography. Can. J. Vet. Res. Rev. Canadienne Rech. Vet. 2011, 75, 176-182.
38. Bouhet, S.; Hourcade, E.; Loiseau, N.; Fikry, A.; Martinez, S.; Roselli, M.; Galtier, P.; Mengheri, E.; Oswald, I.P. The mycotoxin fumonisin B1 alters the proliferation and the barrier function of porcine intestinal epithelial cells. Toxicol. Sci. 2004, 77, 165-171.
39. Loiseau, N.; Debrauwer, L.; Sambou, T.; Bouhet, S.; Miller, J.D.; Martin, P.G.; Viadere, J.L.; Pinton, P.; Puel, O.; Pineau, T.; et al. Fumonisin B1 exposure and its selective effect on porcine jejunal segment: Sphingolipids, glycolipids and trans-epithelial passage disturbance. Biochem. Pharmacol. 2007, 74, 144-152.
40. Bouhet, S.; le Dorze, E.; Peres, S.; Fairbrother, J.M.; Oswald, I.P. Mycotoxin fumonisin B1 selectively down-regulates the basal IL-8 expression in pig intestine: In vivo and in vitro studies. Food Chem. Toxicol. 2006, 44, 1768-1773.
41. Taranu, I.; Marin, D.E.; Bouhet, S.; Pascale, F.; Bailly, J.D.; Miller, J.D.; Pinton, P.; Oswald, I.P. Mycotoxin fumonisin B1 alters the cytokine profile and decreases the vaccinal antibody titer in pigs. Toxicol. Sci. 2005, 84, 301-307.
42. Marteau, P. Factor Controlling the Bacterial Microflora. In Gut Microflora: Digestive Physiology and Pathology; Rambaud, J.C., Buts, J.P., Cortier, G., Flourié, B., Eds.; John Libbey Eurotext, DL: Paris, France, 2006; pp. 37-55.
43. Proux, K.; Houdayer, C.; Humbert, F.; Cariolet, R.; Rose, V.; Eveno, E.; Madec, F. Development of a complete ELISA using Salmonella lipopolysaccharides of various serogronps allowing to detect all infected pigs. Vet. Res. 2000, 31, 481-490.
44. Pinton, P.; Accensi, F.; Beauchamp, E.; Cossalter, A.M.; Callu, P.; Grosjean, F.; Oswald, I.P. Ingestion of deoxynivalenol (DON) contaminated feed alters the pig vaccinal immune responses. Toxicol. Lett. 2008, 177, 215-222.
45. Fravalo, P.; Hascoet, Y.; Le Fellic, M.; Queguiner, S.; Petton, J.; Salvat, G. Convenient method for rapid and quantitative assessment of Salmonella enterica contamination: The mini-MSRV MPN technique. J. Rapid Methods Autom. Microbiol. 2003, 11, 81-88.
46. McOrist, A.L.; Jackson, M.; Bird, A.R. A comparison of five methods for extraction of bacterial DNA from human faecal samples. J. Microbiol. Methods 2002, 50, 131-139.
47. Delbes, C.; Moletta, R.; Godon, J.J. Bacterial and archaeal 16S rDNA and 16S rRNA dynamics during an acetate crisis in an anaerobic digestor ecosystem. FEMS Microbiol. Ecol. 2001, 35, 19-26.
48. Legendre, P.; Legendre, L. Numerical Ecology; Elsevier: Amsterdan, The Netherlands, 1998; Volume 20.