Impacts of the feed contaminant deoxynivalenol on the intestine of monogastric animals: Poultry and swine

Journal of Applied Toxicology

Volumn 35, Issue 4, 2015, Pages 327-337

  Ghareeb, Khaled ^a,b   Awad, Wageha A ^a,b   Böhm, Josef ^a   Zebeli, Qendrim ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b South Valley University   (Egypt)

Author keywords

Deoxynivalenol; Gene expression; Immune function; Intestinal barrier function; Nutrient absorption; Pigs; Poultry

Indexed keywords

CLAUDIN 4; CLAUDIN 5; FREE RADICAL; FRUCTOSE; GLUCOSE; MITOGEN ACTIVATED PROTEIN KINASE; PHLORIZIN; PROLINE; REACTIVE OXYGEN METABOLITE; TIGHT JUNCTION PROTEIN; TOLL LIKE RECEPTOR 4; VOMITOXIN; MYCOTOXIN; TRICHOTHECENE DERIVATIVE;

CELL STIMULATION; CHICKEN; COMMENSAL; CYTOKINE RELEASE; CYTOTOXICITY; DOWN REGULATION; DYSBIOSIS; FEEDING; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOBLOTTING; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; INNATE IMMUNITY; INTESTINE; INTESTINE ABSORPTION; INTESTINE CELL; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE FUNCTION; INTESTINE MUCOSA PERMEABILITY; NONHUMAN; NUTRIENT UPTAKE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR ENTERITIDIS; SALMONELLOSIS; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS INFECTION; SWINE; UPREGULATION; ANIMAL; ANIMAL FOOD; BIRD DISEASE; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYMOLOGY; FOOD CONTAMINATION; FOODBORNE DISEASES; INTESTINE MUCOSA; MALABSORPTION; METABOLISM; PIG; POULTRY; SWINE DISEASE; VETERINARY;

ANIMALIA; GALLUS GALLUS; SUIDAE;

ANIMAL FEED; ANIMALS; FOOD CONTAMINATION; FOODBORNE DISEASES; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; INTESTINES; MALABSORPTION SYNDROMES; MAP KINASE SIGNALING SYSTEM; MYCOTOXINS; POULTRY; POULTRY DISEASES; SUS SCROFA; SWINE; SWINE DISEASES; TRICHOTHECENES;

EID: 84923021530     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.3083     Document Type: Review

References (104)

1. Antonissen G, Van Immerseel F, Pasmans F, Ducatelle R, Haesebrouck F, Timbermont L, Verlinden M, Janssens G, Eeckhout M, De Saeger S, Boeckx P, Delezie E, Hessenberger S, Martel A, Croubels S. 2013. Deoxynivalenol predisposes for necrotic enteritis by affecting the intestinal barrier in broilers. Georgia World Congress Center: Atlanta, Georgia; 9-10.
2. Avantaggiato G, Havenaar R, Visconti A. 2004. Evaluation of the intestinal absorption of deoxynivalenol and nivalenol by an in vitro gastrointestinal model, and the binding efficacy of activated carbon and other adsorbent materials. Food Chem. Toxicol. 42: 817-824.
3. Awad WA, Böhm J, Razzazi-Fazeli E, Hulan HW, Zentek J. 2004. Effects of deoxynivalenol on general performance and electrophysiological properties of intestinal mucosa of broiler chickens. Poult. Sci. 83: 1964-1972.
4. Awad WA, Böhm J, Razzazi-Fazeli E, Zentek J. 2005a. In vitro effects of deoxynivalenol on electrical properties of the intestinal mucosa of laying hens. Poult. Sci. 84: 921-927.
5. Awad WA, Böhm J, Razzazi-Fazeli E, Zentek J. 2006a. Effects of feeding deoxynivalenol contaminated wheat on growth performance, organ weights and histological parameters of the intestine of broiler chickens. J. Anim. Physiol. Anim. Nutr. 90: 32-37.
6. Awad WA, Ghareeb K, Böhm J, Zentek J. 2013a. The toxicological impacts of the fusarium mycotoxin, deoxynivalenol, in poultry flocks with special reference to immunotoxicity. Toxins 5: 912-925.
7. Awad WA, Ghareeb K, Dadak A, Gille L, Staniek K, Hess M, Böhm J. 2012. Genotoxic effects of deoxynivalenol in broiler chickens fed with low protein diets. Poult. Sci. 91: 550-555.
8. Awad WA, Ghareeb K, Dadak A, Hess M, Böhm J. 2014a. Single and combined effects of deoxynivalenol mycotoxin and a microbial feed additive on lymphocyte DNA damage and oxidative stress in broiler chickens. PLoS One 9: e88028.
9. Awad WA, Ghareeb K, Paßlack N, Zentek J. 2013b. Dietary inulin alters the intestinal absorptive and barrier function of piglet intestine after weaning. Res. Vet. Sci. 95: 249-254.
10. Awad WA, Molnár A, Aschenbach JR, Ghareeb K, Khayal B, Hess C, Liebhart D, Dublecz K, Hess M. 2014b. Campylobacter infection in chickens modulates the intestinal epithelial barrier function. Innate Imm. DOI: 10.1177/1753425914521648
11. Awad WA, Razzazi-Fazeli E, Böhm J, Ghareeb K, Zentek J. 2006b. Effect of addition of a probiotic microorganism to broiler diets contaminated with deoxynivalenol on performance and histological alterations of intestinal villi of broiler chickens. Poult. Sci. 85: 974-979.
12. Awad WA, Razzazi-Fazeli E, Böhm J, Zentek J. 2007. Influence of deoxynivalenol on the D-glucose transport across the isolated epithelium of different intestinal segments of laying hens. J. Anim. Physiol. Anim. Nutr. 91: 175-180.
13. Awad WA, Razzazi-Fazeli E, Bohm J, Zentek J. 2008. Effects of B- trichothecenes on luminal glucose transport across the isolated jejunal epithelium of broiler chickens. J. Anim. Physiol. Anim. Nutr. 92: 225-230.
14. Awad WA, Rehman H, Bohm J, Razzazi-Fazeli E, Zentek J. 2005b. Effects of luminal deoxynivalenol and L-proline on electrophysiological parameters in the jejunums of laying hens. Poult. Sci. 84: 928-932.
15. Awad WA, Vahjen W, Aschenbach JR, Zentek J. 2011. A diet naturally contaminated with the Fusarium mycotoxin deoxynivalenol down regulates gene Expression of glucose transporters in the intestine of broiler chickens. Livestock Sci. 140: 72-79.
16. Awad WA, Zentek J. 2014. The feed contaminant deoxynivalenol affects the intestinal barrier permeability through inhibition of protein synthesis. Arch. Toxicol. Doi: 10.1007/s00204-014-1284-1289
17. Becker CM, Reiter M, Pfaffl W, Meyer HHD, Bauer J, Meyer KHD. 2011. Expression of immune relevant genes in pigs under the influence of low doses of deoxynivalenol (DON). Mycotox. Res. 27: 287-293.
18. Binder EM, Binder J, Ellend N, Schaffer E, Krska R, Braun R. 1998. Microbiological degradation of deoxynivalenol and 3-acetyl-deoxynivalenol. In Mycotoxins and Phycotoxins: Developments in Chemistry, Toxicology and Food Safety, Miraglia M, Egmond HP, Brera C, Gilbert J, (eds). Fort Collins: Alaken; 279-285.
19. Binder EM, Heidler D, Schatzmayr G, Thimm N. 2000a. A novel feed additive to counteract trichothecene toxicosis in pig production. In Proceedings of the 16th International Pig Veterinary Society Congress, Melbourne, Australia; 250.
20. Binder EM, Heidler D, Schatzmayr G, Thimm N. 2000b. In: Koe WJ, Samson RA, van Egmond HP, Gilbert J, Sabino M, editors. Mycotoxins and Phycotoxins in perspective at the turn of the Millennium. In Proceedings of the 10th International IUPAC Symposium on Mycotoxins and Phycotoxins, Guaruja, Brazil; 271-277.
21. Borutova R, Faix S, Plachaa I, Gresakovaa L, Cobanovaa K, Lenga L. 2008. Effects of deoxynivalenol and zearalenone on oxidative stress and blood phagocytic activity in broilers. Arch. Anim. Nutr. 62: 303-312.
22. Bracarense AP, Lucioli J, Grenier B, Drociunas Pacheco G, Moll WD, Schatzmayr G, Oswald IP. 2012. Chronic ingestion of deoxynivalenol and fumonisin, alone or in interaction, induces morphological and immunological changes in the intestine of piglets. Br. J. Nutr. 107: 1776-1786.
23. Cano PM, Seeboth J, Meurens F, Cognie J, Abrami R, Oswald IP, Guzylack-Piriou L. 2013. Deoxynivalenol as a new factor in the persistence of intestinal inflammatory diseases: An emerging hypothesis through possible modulation of Th17-mediated response. PLoS One 8: e53647. DOI: 10.1371/journal.pone.0053647
24. Dänicke S, Valenta H, Döll S. 2004. On the toxicokinetics and the metabolism of deoxynivalenol (DON) in the pig. Arch. Anim. Nutr. 58: 169-180.
25. Dicksved J, Halfvarson J, Rosenquist M, Jarnerot G, Tysk C, Apajalahti J, Engstrand L, Jansson JK. 2008. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. ISME J. 2: 716-727.
26. Diesing AK, Nossol C, Dänicke S, Walk N, Post A, Kahlert S, Rothkötter HJ, Kluess J. 2011. Vulnerability of polarised intestinal porcine epithelial cells to mycotoxin deoxynivalenol depends on the route of application. PLoS One 6: e17472.
27. Dietrich B, Neuenschwander S, Bucher B, Wenk C. 2012. Fusarium mycotoxin-contaminated wheat containing deoxynivalenol alters the gene expression in the liver and the jejunum of broilers. Animals 6: 278-291.
28. Drochner W, Schollenberger M, Piepho HP, Götz S, Lauber U, Tafaj M, Klobasa F, Weiler U, Claus R, Steffl M. 2004. Serum IgA-promoting effects induced by feed loads containing isolated deoxynivalenol (DON) in growing piglets. J. Toxicol. Environ. Health A 67: 1051-1067.
29. Eriksen G, Pettersson H. 2004. Toxicological evaluation of trichothecenes in animal feed. Anim. Feed Sci. Technol. 114: 205-239.
30. Eriksen GS. 2003. Metabolism and toxicity of trichothecenes. A doctoral thesis, Swedish University of Agricultural Sciences, Uppsala.
31. Eriksen GS, Pettersson H, Johnsen K, Lindberg JE. 2002. Transformation of trichothecenes in ileal digesta and faeces from pigs. Arch. Anim. Nutr. 56: 263-274.
32. European Food Safety Authority (EFSA). 2004. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to deoxynivalenol (DON) as undesirable substance in animal feed. EFSA J. 73: 1-42.
33. European Food Safety Authority (EFSA). 2013. Deoxynivalenol in food and feed: occurrence and exposure. EFSA J. 10: 3379: 56.
34. Förster C. 2008. Tight junctions and the modulation of barrier function in disease. Histochem. Cell Biol. 130: 55-70.
35. Frankic T, Pajk T, Rezar V, Levart A, Salobir J. 2006. The role of dietary nucleotides in reduction of DNA damage induced by T-2 toxin and deoxynivalenol in chicken leukocytes. Food Chem. Toxicol. 44: 1838-1844.
36. Fuchs E, Binder EM, Heidler D, Krska R. 2002. Structural characterization of metabolites after the microbial degradation of type A trichothecenes by bacterial strain BBSH 797. Food Add. Contam. 4: 379-386.
37. Gauvreau HC. 2000. Toxicokinetic, tissue residue, and metabolic studies of deoxynivalenol (vomitoxin) in turkeys. Master thesis, Simon Fraser University, Vancouver, Canada.
38. Gareau MG, Perdue MH, Sherman PM. 2007. Intestinal defenses-maintenance of intestinal barrier function in host defense. US Gastroenterol. Rev. 11: 57-58.
39. Ghareeb K, Awad WA, Böhm J. 2012. Ameliorative effect of a microbial feed additive on infectious bronchitis vaccination (IB) antibody titer and stress index in broiler chicks fed deoxynivalenol. Poult. Sci. 91: 800-807.
40. Ghareeb K, Awad WA, Sid-Ahmed OE, Böhm J. 2014. Insights on the host stress, fear and growth responses to the deoxynivalenol feed contaminant in broiler chickens. PLoS One 9: e87727. DOI: 10.1371/journal.pone.0087727
41. Ghareeb K, Awad WA, Mohnl M, Böhm J, Schatzmayr G. 2013a. Control strategies for Campylobacter infection in poultry production. World's Poult. Sci. J. 69: 57-76.
42. Ghareeb K, Awad WA, Soodoi C, Sasgary S, Strasser A, Böhm J. 2013b. Effects of feed contaminant deoxynivalenol on plasma cytokines and mRNA expression of immune genes in the intestine of broiler chickens. PLoS One 8: e71492. DOI: 10.1371/journal.pone.0071492
43. Girgis GN, Barta JR, Brash M, Smith TK. 2010. Morphological changes in the intestine of broiler breeder pullets fed diets naturally contaminated with Fusarium mycotoxins with or without coccidial challenge. Avian Dis. 54: 67-73.
44. Girgis GN, Sharif S, Barta JR, Boermans HJ, Smith TK. 2008. Immunomodulatory effects of feed-borne Fusarium mycotoxins in chickens infected with coccidia. Exp. Biol. Med. 233: 1411-1420.
45. Grenier B, Applegate, TJ. 2013. Modulation of intestinal functions following mycotoxin ingestion: Meta-analysis of published experiments in animals. Toxins 5: 396-430.
46. Gratz SW, Duncan G, Richardson AJ. 2013. The human fecal microbiota metabolizes deoxynivalenol and deoxynivalenol-3-glucoside and may be responsible for urinary deepoxy-deoxynivalenol. Appl. Environ. Microbiol. 79: 1821-1825.
47. Groschwitz KR, Hogan SP. 2009. Intestinal barrier function: molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 124: 3-20.
48. Halawa A, Dänicke S, Kersten S, Breves G. 2012. Effects of deoxynivalenol and lipopolysaccharide on electrophysiological parameters in growing pigs. Mycotoxin Res. 28: 243-252.
49. Hara-Kudo Y, Sugita-Konishi Y, Kasuga F, Kumagai S. 1996. Effects of deoxynivalenol on Salmonella enteritidis infection. Mycotoxins 42: 51-55.
50. He P, Young LG, Forsberg C. 1992. Microbial transformation of deoxynivalenol (vomitoxin). Appl. Environ. Microbiol. 58: 3857-3863.
51. King RR, Mcqueen RE, Levesque D, Greenhalgh R. 1984. Transformation of deoxynivalenol (vomitoxin) by rumen microorganisms. J. Agric. Food Chem. 32: 1181-1183.
52. Klunker LR, Kahlert S, Panther P, Diesing AK Reinhardt N, Brosig B, Kersten S, Dänicke S, Rothkötter HJ, Kluess JW. 2012. Deoxynivalenol and E. coli lipopolysaccharide alter epithelial proliferation and spatial distribution of apical junction proteins along the small intestinal axis. J. Anim. Sci. 91: 276-285.
53. Kogut MH., Swaggerty C, He H, Pevzner I, Kaiser P. 2006. Toll-like receptor agonists stimulate differential functional activation and cytokine and chemokine gene expression in heterophils isolated from chickens with differential innate responses. Microbes Infect. 8: 1866-1874.
54. Kolf-Clauw M, Castellote J, Joly B, Bourges-Albellaß N, Raymond-Letron I, Pinton P, Oswald IP. 2009. Development of a pig jejunal explant culture for studying the gastrointestinal toxicity of the mycotoxin deoxynialenol: histopathological analysis. Toxicol. In Vitro 23: 1580-1584.
55. Kollarczik B, Gareis M, Hanelt M. 1994. In vitro transformation of the Fusarium mycotoxins deoxynivalenol and zearalenone by the normal gut microflora of pigs. Nat. Toxins 2: 105-110.
56. Kouadio JH, Mobio TA, Baudrimont I, Moukha S, Dano SD, Creppy EE. 2005. Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology 213: 56-65.
57. Lee JT, Jessen KA, Beltran R, Stark V, Schatzmayr G, Borutova R, Caldwell DJ. 2012a. Effects of mycotoxin-contaminated diets and deactivating compound in laying hens: 1. effects on performance characteristics and relative organ weight. Poult. Sci. 91: 2089-2095.
58. Lee JT, Jessen KA, Beltran R, Stark V, Schatzmayr G, Borutova R, Caldwell DJ. 2012b. Effects of mycotoxin-contaminated diets and deactivating compound in laying hens: 2. effects on white shell egg quality and characteristics. Poult. Sci. 91: 2096-2104.
59. Lawlor PG, Lynch PB. 2001. Mycotoxins in pig feeds 1: Source of toxins, prevention and management of mycotoxicosis. Ir. Vet. J. 54: 117-120.
60. Li M, Cuff CF, Pestka JJ. 2005. Modulation of murine host response to enteric reovirus infection by the trichothecene deoxynivalenol. Toxicol. Sci. 87: 134-145.
61. Mann E, Schmitz-Esser S, Zebeli Q, Wagner M, Ritzmann M, Metzler-Zebeli B. 2014. Mucosa-associated bacterial microbiome of the gastrointestinal tract of weaned pigs and dynamics linked to dietary calcium-phosphorus. PLoS One 9: e86950. DOI: 10.1371/journal.pone.0086950
62. Maresca M. 2013. From the gut to the brain: Journey and pathophysiological effects of the food-associated trichothecene mycotoxin deoxynivalenol. Toxins 5: 784-820.
63. Maresca M, Fantini J. 2010. Some food-associated mycotoxins as potential risk factors in humans predisposed to chronic intestinal inflammatory diseases. Toxicon 56: 282-294.
64. Maresca M, Mahfoud R, Garmy N, Fantini J. 2002. The mycotoxin deoxynivalenol affects nutrient absorption in human intestinal epithelial cells. J. Nutr. 132: 2723-2731.
65. Maresca M, Yahi N, Younes-Sakr L, Boyron M, Caporiccio B, Fantini J. 2008. 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. 228: 84-92.
66. Matter K, Balda MS. 2003. Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol. 4: 225-236.
67. Maynard CL, Elson CO, Hatton RD, Weaver CT. 2012. Reciprocal interactions of the intestinal microbiota and immune system. Nat. Rev. 498: 231-241.
68. Metzler-Zebeli BU, Ratriyanto A, Jezierny D, Sauer N, Eklund M, Mosenthin R. 2009. Effects of betaine, organic acids and inulin as single feed additives or in combination on bacterial populations in the gastrointestinal tract of weaned pigs. Arch. Anim. Nutr. 63: 427-441.
69. Metzler-Zebeli BU, Zijlstra RT, Mosenthin R, Gänzle MG. 2011. Dietary calcium phosphate content and oat β-glucan influence gastrointestinal microbiota, butyrate-producing bacteria and butyrate fermentation in weaned pigs. FEMS Microbiol. Ecol. 75: 402-413.
70. Moon Y, Yang H, Lee SH. 2007. Modulation of early growth response gene 1 and interleukin-8 expression by ribotoxin deoxynivalenol (vomitoxin) via ERK1/2 in human epithelial intestine 407 cells. Biochem. Biophys. Res. Commun. 362: 256-262.
71. Nadal I, Donant E, Ribes-Koninckx C, Calabuig M, Sanz Y. 2007. Imbalance in the composition of the duodenal microbiota of children with coeliac disease. J. Med. Microbiol. 56: 1669-1674.
72. Obremski K, Zielonka L, Gajecka M, Jakimiuk E, Bakula T, Baranowski M, Gajecki M. 2008. Histological estamination of the small intestine wall after administration of feed containing deoxynivalenol, T-2 toxin and zearalenone in the pig. Polish J. Vet. Sci. 11: 339-345.
73. Osselaere A, Santos R, Hautekiet V, De Backer P, Chiers K, Ducatelle R, Croubels S. 2013. Deoxynivalenol impairs hepatic and intestinal gene expression of selected oxidative stress, tight junction and inflammation proteins in broiler chickens, but addition of an adsorbing agent shifts the effects to the distal parts of the small intestine. PLoS One 8: e69014. DOI: 10.1371/journal.pone.0069014
74. Pestka JJ. 2003. Deoxynivalenol-induced IgA production and IgA nephropathy-aberrant mucosal immune response with systemic repercussions. Toxicol. Letters 140-141: 287-295.
75. Pestka JJ. 2007. Deoxynivalenol: toxicity, mechanisms and animal health risks. Anim. Feed Sci. Technol. 137: 283-298.
76. Pestka JJ. 2008. Mechanisms of deoxynivalenol-induced gene expression and apoptosis. Food Add. Contam. 25: 1128-1140.
77. Pestka JJ, Zhou HR, Moon Y, Chung YJ. 2004. Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol. Lett. 153: 61-73.
78. Pinton P, Braicu C, Nougayrede JP, Laffitte J, Taranu I, Oswald IP. 2010. Deoxynivalenol impairs porcine intestinal barrier function and decreases the protein expression of claudin-4 through a mitogen-activated protein kinase-dependent mechanism. J. Nutr. 140: 1956-1962.
79. Pinton P, Nougayrède JP, Del Rio JC, Moreno C, Marin DE, Ferrier L, Bracarense AP, Kolf-Clauw M, Oswald IP. 2009. The food contaminant deoxynivalenol, decreases intestinal barrier permeability and reduces claudin expression. Toxicol. Appl. Pharmacol. 237: 41-48.
80. Pinton P, Tsybulskyy D, Lucioli J, Laffitte J, Callu P, Lyazhri F, Grosjean F, Bracarense AP, Kolf-Clauw M, Oswald IP. 2012. Toxicity of deoxynivalenol and its acetylated derivatives on the intestine: differential effects on morphology, barrier function, tight junctions proteins and MAPKinases. Toxicol. Sci. 130: 180-190.
81. Pinton P. Accensi F, Beauchamp E, Cossalter AM, Callu P, Grosjean F, Oswald IP. 2008. Ingestion of deoxynivalenol (DON) contaminated feed alters the pig vaccinal immune responses. Toxicol. Lett. 177: 215-222.
82. Prelusky DB, Hamilton RM, Trenholm HL, Miller JD. 1986. Tissue distribution and excretion of radioactivity following administration of 14C-labeled deoxynivalenol to White Leghorn hens. Fundam. Appl. Toxicol. 7: 635-645.
83. Rotter BA, Prelusky DB, Pestka JJ. 1996. Toxicology of deoxynivalenol (vomitoxin). J. Toxicol. Environ. Health 48: 1-34.
84. Rotter BA, Thompson BK, Lessard M, Trenholm HL, Tryphonas H. 1994. Influence of Low-Level Exposure to Fusarium Mycotoxins on selected immunological and hematological parameters in young swine. Toxicol. Sci. 23: 117-124.
85. Saint-Cyr MJ, Perrin-Guyomard A, Houée P, Rolland J-G, Laurentie M. 2013. Evaluation of an oral subchronic exposure of deoxynivalenol on the composition of human gut microbiota in a model of human microbiota-sssociated rats. PLoS One 8: e80578. DOI: 10.1371/journal.pone.0080578
86. Schatzmayr G, Täubel M, Vekiru E, Moll M, Schatzmayr D, Binder EM, Krska R, Loibner AP. 2006. Detoxification of mycotoxins by biotransformation. In The Mycotoxin Factbook, Barug D, Bhatnagar D, van Egmond HP, van der Kamp JW, van Osenbruggen WA, Visconti A, (eds). Wageningen Academic Publishers: The Netherlands; 363-375.
87. Smith LE, Stoltzfus J R, Prendergast A. 2012. Food Chain Mycotoxin Exposure, Gut Health, and Impaired Growth: A Conceptual Framework. Adv. Nutr. 3: 526-531.
88. Stadnyk AW. 2002. Intestinal epithelial cells as a source of inflammatory cytokines and chemokines. Can. J. Gastroenterol. 16: 241-246.
89. Stanley D, Geier MS, Denman SE, Haring VR, Crowley TM, Hughes RJ, Moore RJ. 2013. Identification of chicken intestinal microbiota correlated with the efficiency of energy extraction from feed. Vet. Microbiol. 164: 85-92.
90. Streit, E., Naehrer K., Rodrigues I, Schatzmayr G. 2013. Mycotoxin occurrence in feed and feed raw materials worldwide: long-term analysis with special focus on Europe and Asia. J. Sci. Food Agric. 93: 2892-2899.
91. Swanson SP, Nicoletti J, Rood JHD, Buck WB, Cote LM. 1987. Metabolism of three trichothecene mycotoxins, T-2 toxin, diacetoxyscirpenol, and deoxynivalenol, by bovine rumen microorganisms. J. Chromatogr. Biomed. Appl. 414: 335-342.
92. Temperley ND, Berlin S, Paton IR, Griffin DK, Burt DW. 2008. Evolution of the chicken Toll-like receptor gene family: A story of gene gain and gene loss. BMC Genomics 9: 62.
93. Turner JR. 2009. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9: 799-809.
94. Van De Walle J, Romier B, Larondelle Y, Schneider YJ. 2008. Influence of deoxynivalenol on NF-kappa B activation and IL-8 secretion in human intestinal Caco-2 cells. Toxicol. Lett. 177: 205-214.
95. Van De Walle J, Sergent T, Piront N, Toussaint O, Schneider YJ, Larondelle Y. 2010. Deoxynivalenol affects in vitro intestinal epithelial cell barrier integrity through inhibition of protein synthesis. Toxicol. Appl. Pharmacol. 245: 291-298.
96. Vandenbroucke V, Croubels S, Martel A, Verbrugghe E, Goossens J, Van Deun K, Boyen F, Thompson A, Shearer N, De Backer P, Haesebrouck F, Pasmans F. 2011. The mycotoxin deoxynivalenol potentiates intestinal jnflammation by salmonella typhimurium in porcine ileal loops. PLoS One 6: e23871.
97. Waché YJ, Valet C, Postollec G, Bougeard S, Burel C, Oswald IP, Fravalo P. 2009. Impact of deoxynivalenol on the intestinal microflora of pigs. Int. J. Mol. Sci. 10: 1-17.
98. Xu L, Eicher SD, Applegate TJ. 2011. Effects of increasing dietary concentrations of corn naturally contaminated with deoxynivalenol on broiler and turkey poult performance and response to lipopolysaccharide. Poult. Sci. 90: 2766-2774.
99. Wexler HM. 2007. Bacteroides: the good, the bad, and the nitty-gritty. Clin. Microbiol. Rev. 20: 593-621.
100. Young JC, Zhou T, Yu H, Zhu HH, Gong JH. 2007. Degradation of trichothecene mycotoxins by chicken intestinal microbes. Food Chem. Toxicol. 45: 136-143.
101. Yunus AW, Blajet-Kosicka A, Kosicki R, Khan MZ, Rehman H, Bohm J. 2012. Deoxynivalenol as a contaminant of broiler feed: Intestinal development, absorptive functionality, and metabolism of the mycotoxin. Poult. Sci. 91: 852-861.
102. Zebeli Q, Metzler-Zebeli BU. 2012. Interplay between rumen digestive disorders and diet-induced inflammation in dairy cattle. Res. Vet. Sci. 93: 1099-1108.
103. Zhang X, Jiang L, Geng C, Cao J, Zhong L. 2009. The role of oxidative stress in deoxynivalenol-induced DNA damage in HepG2 cells. Toxicon 54: 513-518.
104. Zhou HR, Islam Z, Pestka JJ. 2003. Rapid, sequential activation of mitogen-activated protein kinases and transcription factors precedes proinflammatory cytokine mRNA expression in spleens of mice exposed to the trichothecene vomitoxin. Toxicol. Sci. 72: 130-142.