Impact of deoxynivalenol on the intestinal microflora of pigs

International Journal of Molecular Sciences

Volumn 10, Issue 1, 2009, Pages 1-17

  Waché, Yann J ^a,b   Valat, Charlotte ^a   Postollec, Gilbert ^a   Bougeard, Stephanie ^a   Burel, Christine ^a   Oswald, Isabelle P ^b   Fravalo, Philippe ^a  

^a Healthy Pigs Production and Experimentation Section   (France)

^b CEMAGREF   (France)

Author keywords

Anaerobic sulfite reducing bacteria; CE SSCP; Deoxynivalenol; Faeces; Growth performance; Intestinal microflora; Mycotoxin; Pigs

Indexed keywords

VOMITOXIN;

ANIMAL EXPERIMENT; ANIMAL FOOD; ARTICLE; BACTERIUM CULTURE; CAPILLARY ELECTROPHORESIS; CONTROLLED STUDY; EXPOSURE; FEMALE; FOOD CONTAMINATION; INTESTINE FLORA; MALE; MESOPHILIC BACTERIUM; MICROBIAL COMMUNITY; MOLECULAR DYNAMICS; NONHUMAN; SINGLE STRAND CONFORMATION POLYMORPHISM; SWINE; WEANING; WEIGHT GAIN;

ANAEROBIC SULFITE-REDUCING BACTERIA; CE-SSCP; DEOXYNIVALENOL; FAECES; GROWTH PERFORMANCE; INTESTINAL MICROFLORA; MYCOTOXIN; PIGS;

ANIMAL FEED; ANIMALS; ANTIFUNGAL AGENTS; INTESTINES; MICROBIOTA; POLYMORPHISM, GENETIC; SWINE; TRICHOTHECENES;

ANIMALIA; FUSARIUM; SUIDAE;

EID: 59649129460     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms10010001     Document Type: Article

References (58)

1. CAST Report, Council for Agricultural Science and Technology. Mycotoxins: Risks in plant, Animal, and Human Systems. Ames, IA, USA, 2003.
2. Oswald, I.P.; Comera, C. Immunotoxicity of mycotoxins. Rev. Med. Vet. 1998, 149, 585-590.
3. SCOOP Collection of occurence data of Fusarium toxins in food and assessment of dietary intake of the population of EU member states. Directorate-general health and consumer protection. Available at http//europa.eu.int:comm/food:fs:scoop:task3210.pdf, 2003; accessed October 20, 2008.
4. st Ed.; CRC press: Boca Raton, FL, USA, 1991; p. 875.
5. Rotter, B.A.; Prelusky, D.B.; Pestka, J.J. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 1996, 48, 1-34.
6. Pestka, J.J.; Smolinski, A.T. Deoxynivalenol: Toxicology and potential effects on humans. J. Toxicol. Environ. Health B. Crit. Rev. 2005, 8, 39-69.
7. st Ed.; Oswald, I.P., Taranu, I., Eds.; Research Signpost: Kerala, India, 2008; pp. 113-130.
8. 14C-labeled deoxynivalenol in swine. Fundam. Appl. Toxicol. 1988, 10, 276-286.
9. Eriksen, G.S.; Pettersson, H.; Lindberg, J.E. Absorption, metabolism and excretion of 3-acetyl DON in pigs. Arch. Tierernahr. 2003, 57, 335-345.
10. Cote, L.M.; Beasley, V.R.; Bratich, P.M.; Swanson, S.P.; Shivaprasad, H.L.; Buck, W.B. Sex-related reduced weight gains in growing swine fed diets containing deoxynivalenol. J. Anim. Sci. 1985, 61, 942-950.
11. Bouhet, S.; Oswald, I.P. The effects of mycotoxins, fungal food contaminants, on the intestinal epithelial cell-derived innate immune response. Vet. Immunol. Immunopathol. 2005, 105, 199-209.
12. Maresca, M.; Mahfoud, R.; Garmy, N.; Fantini, J. The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J. Nutr. 2002, 132, 2723-2731.
13. Awad, W.A.; Razzazi-Fazeli, E.; Bohm, J.; Zentek, J. Influence of deoxynivalenol on the D-glucose transport across the isolated epithelium of different intestinal segments of laying hens. J. Anim. Physiol. Anim. Nutr. (Berl.) 2007, 91, 175-180.
14. Awad, W.A.; Razzazi-Fazeli, E.; Bohm, J.; Zentek, J. Effects of B-trichothecenes on luminal glucose transport across the isolated jejunal epithelium of broiler chickens. J. Anim. Physiol. Anim. Nutr. (Berl.) 2008, 92, 225-230.
15. Van De Walle, J.; Romier, B.; Larondelle, Y.; Schneider, Y.J. Influence of deoxynivalenol on NF-kappaB activation and IL-8 secretion in human intestinal Caco-2 cells. Toxicol. Lett. 2008, 177, 205-214.
16. 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.
17. Maresca, M.; Yahi, N.; Younes-Sakr, L.; Boyron, M.; Caporiccio, B.; Fantini, J. Both direct and indirect effects account for the pro-inflammatory activity of enteropathogenic mycotoxins on the human intestinal epithelium: Stimulation of interleukin-8 secretion, potentiation of interleukin-1beta effect and increase in the transepithelial passage of commensal bacteria. Toxicol. Appl. Pharmacol. 2008, 225, 84-92.
18. Kollarczik, B.; Gareis, M.; Hanelt, M. In vitro transformation of the Fusarium mycotoxins deoxynivalenol and zearalenone by the normal gut microflora of pigs. Nat. Toxins 1994, 2, 105-110.
19. Eriksen, G.S.; Pettersson, H.; Johnsen, K.; Lindberg, J.E. Transformation of trichothecenes in ileal digesta and faeces from pigs. Arch. Tierernahr. 2002, 56, 263-274.
20. He, P.; Young, L.G.; Forsberg, C. Microbial transformation of deoxynivalenol (vomitoxin). Appl. Environ. Microbiol. 1992, 55, 3857-3863.
21. Niderkorn, V.; Boudra, H.; Morgavi, D.P. Binding of Fusarium mycotoxins by fermentative bacteria in vitro. J. Appl. Microbiol. 2006, 101, 849-856.
22. Young, J.C.; Zhou, T.; Yu, H.; Zhu, H.; Gong, J. Degradation of trichothecene mycotoxins by chicken intestinal microbes. Food Chem. Toxicol. 2007, 45, 136-143.
23. Tenk, I.; Fodor, E.; Szathmary, C. The effect of pure Fusarium toxins (T-2, F-2, DAS) on the microflora of the gut and on plasma glucocorticoid levels in rat and swine. Zentralbl. Bakteriol. Mikrobiol. Hyg. [A] 1982, 252, 384-393.
24. Tanguy, M.; Burel, C.; Pinton, P.; Guerre, P.; Grosjean, F.; Queguiner, M.; Cariolet, R.; Tardieu, D.; Rault, J.C.; Oswald, I.P.; Fravalo, P. Effets des fumonisines sur la santé du porc: sensibilité aux salmonelles et statut immunitaire. Journées Rech. Porcine 2006, 35, 393-398.
25. 1 on the growth of bacteria. World J. Microbiol. Biotechnol. 1997, 13, 539-543.
26. 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.
27. Pluske, J.R.; Kim, J.C.; Hansen, C.F.; Mullan, B.P.; Payne, H.G.; Hampson, D.J.; Callesen, J.; Wilson, R.H. Piglet growth before and after weaning in relation to a qualitative estimate of solid (creep) feed intake during lactation: A pilot study. Arch. Anim. Nutr. 2007, 61, 469-480.
28. Sneath, P.H.; Sokal, R.R. Numerical taxonomy. Nature 1962, 193, 855-860.
29. st Ed.; Rambaud, J.C., Buts, J.P., Cortier, G., Flourié, B., Eds.; J. Libbey Eurotext, DL: Paris, France, 2006; pp. 37-55.
30. Rotter, B.A.; Thompson, B.K.; Lessard, M.; Trenholm, H.L.; Tryphonas, H. Influence of low-level exposure to Fusarium mycotoxins on selected immunological and hematological parameters in young swine. Fundam. Appl. Toxicol. 1994, 23, 117-124.
31. Alm, H.; Brussow, K.P.; Torner, H.; Vanselow, J.; Tomek, W.; Danicke, S.; Tiemann, U. Influence of Fusarium-toxin contaminated feed on initial quality and meiotic competence of gilt oocytes. Reprod. Toxicol. 2006, 22, 44-50.
32. Pollmann, D.S.; Koch, B.A.; Seitz, L.M.; Mohr, H.E.; Kennedy, G.A. Deoxynivalenol-contaminated wheat in swine diets. J. Anim. Sci. 1985, 60, 239-247.
33. Bergsjo, B.; Langseth, W.; Nafstad, I.; Jansen, J.H.; Larsen, H.J. The effects of naturally deoxynivalenol-contaminated oats on the clinical condition, blood parameters, performance and carcass composition of growing pigs. Vet. Res. Commun. 1993, 17, 283-294.
34. Prelusky, D.B.; Gerdes, R.G.; Underhill, K.L.; Rotter, B.A.; Jui, P.Y.; Trenholm, H.L. Effects of low-level dietary deoxynivalenol on haematological and clinical parameters of the pig. Nat. Toxins 1994, 2, 97-104.
35. Swanson, S.P.; Helaszek, C.; Buck, W.B.; Rood, H.D., Jr.; Haschek, W.M. The role of intestinal microflora in the metabolism of trichothecene mycotoxins. Food. Chem. Toxicol. 1988, 26, 823-829.
36. Tzortzis, G.; Goulas, A.K.; Gee, J.M.; Gibson, G.R. A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J. Nutr. 2005, 135, 1726-1731.
37. Mai, V.; Morris, J.G.J. Colonic bacterial flora: changing understandings in the molecular age. J. Nutr. 2003, 134, 459-464.
38. nd Ed.; Sonegate Publishing: Davis, CA, USA, 1990; pp. 224-241.
39. Jensen, T.K.; Boye, M.; Moller, K.; Leser, T.D.; Jorsal, S.E. Association of Serpulina hyodysenteriae with the colonic mucosa in experimental swine dysentery studied by fluorescent in situ hybridization. Apmis 1998, 106, 1061-1068.
40. Zoetendal, E.G.; Akkermans, A.D.; De Vos, W.M. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl. Environ. Microbiol. 1998, 64, 3854-3859.
41. Peu, P.; Brugere, H.; Pourcher, A.M.; Kerouredan, M.; Godon, J.J.; Delgenes, J.P.; Dabert, P. Dynamics of a pig slurry microbial community during anaerobic storage and management. Appl. Environ. Microbiol. 2006, 72, 3578-3585.
42. Tanguy, M.; Pissavin, C.; Queguiner, M.; Cariolet, R.; Le Diguerher, G.; Burel, C.; Fravalo, P. Utilisation de la PCR-SSCP capillaire pour l'etude de la flore digestive de groupes de porcs EOPS. Journées Rech. Porcine 2007, 39, 369-376.
43. nd Ed.; Garnsworthy, P.C., Cole, D.J.A., Eds.; Nottingham University Press: Nottingham, UK, 1994; pp. 57-79.
44. Simpson, J.M.; McCracken, V.J.; Gaskins, H.R.; Mackie, R.I. Denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA amplicons to monitor changes in fecal bacterial populations of weaning pigs after introduction of Lactobacillus reuteri strain MM53. Appl. Environ. Microbiol. 2000, 66, 4705-4714.
45. Gelsomino, A.; Keijzer-Wolters, A.C.; Cacco, G.; van Elsas, J.D. Assessment of bacterial community structure in soil by polymerase chain reaction and denaturing gradient gel electrophoresis. J. Microbiol. Meth. 1999, 38, 1-15.
46. Tiedje, J.M. Opening the black box of soil microbial diversity. Applied Soil Ecology 1999, 13, 109-122.
47. Baker, G.C.; Cowan, D.A. 16 S rDNA primers and the unbiased assessment of thermophile diversity. Biochem. Soc. Trans. 2004, 32, 218-221.
48. Klappenbach, J.A.; Saxman, P.R.; Cole, J.R.; Schmidt, T.M. rrndb: the Ribosomal RNA Operon Copy Number Database. Nucleic Acids Res. 2001, 29, 181-184.
49. Loisel, P.; Harmand, J.; Zemb, O.; Latrille, E.; Lobry, C.; Delgenes, J.P.; Godon, J.J. Denaturing gradient electrophoresis (DGE) and single-strand conformation polymorphism (SSCP) molecular fingerprintings revisited by simulation and used as a tool to measure microbial diversity. Environ. Microbiol. 2006, 8, 720-731.
50. Pryde, S.E.; Richardson, A.J.; Stewart, C.S.; Flint, H.J. Molecular analysis of the microbial diversity present in the colonic wall, colonic lumen, and cecal lumen of a pig. Appl. Environ. Microbiol. 1999, 65, 5372-5377.
51. Hong, H.; Pruden, A.; Reardon, K.F. Comparison of CE-SSCP and DGGE for monitoring a complex microbial community remediating mine drainage. J. Microbiol. Methods 2007, 69, 52-64.
52. INRA, A. Table de composition et de valeur nutritive des matieres premières destinées aux animaux d'elevage; INRA: Paris, France, 2002.
53. Delbes, C.; Moletta, R.; Godon, 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.
54. SAS. SAS OnLineDoc version 9.1. Cary, NC, USA, 2004.
55. Laird, N.M.; Ware, J.H. Random-effects models for longitudinal data. Biometrics 1982, 38, 963-974.
56. Wolfinger, R.D. An example of using mixed models and PROC MIXED for longitudinal data. J. Biopharm. Stat. 1997, 7, 481-500.
57. Littell, R.C.; Henry, P.R.; Ammerman, C.B. Statistical analysis of repeated measures data using SAS procedures. J. Anim. Sci. 1998, 76, 1216-1231.
58. Forno, E.; Onderdonk, A.B.; McCracken, J.; Litonjua, A.A.; Laskey, D.; Delaney, M.L.; Dubois, A.M.; Gold, D.R.; Ryan, L.M.; Weiss, S.T.; Celedon, J.C. Diversity of the gut microbiota and eczema in early life. Clin. Mol. Allergy 2008, 6, 11.