Prevalence and effects of mycotoxins on poultry health and performance, and recent development in mycotoxin counteracting strategies

Poultry Science

Volumn 94, Issue 6, 2015, Pages 1298-1315

  Murugesan, G R ^a   Ledoux, D R ^b   Naehrer, K ^c   Berthiller, F ^d   Applegate, T J ^e   Grenier, B ^e   Phillips, T D ^f   Schatzmayr, G ^c  

^a Biomin Inc   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c BIOMIN RESEARCH CENTER   (Austria)

^d UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^e PURDUE UNIVERSITY   (United States)

^f TEXAS A AND M UNIVERSITY   (United States)

Author keywords

analysis; detoxification; gut; immune function; mycotoxicosis; occurrence

Indexed keywords

ANIMALIA; AVES;

MYCOTOXIN;

ANALYSIS; ANIMAL; FOOD CONTAMINATION; MICROBIOLOGY; MYCOTOXICOSIS; POULTRY; POULTRY DISEASES; PREVALENCE; VETERINARY;

ANIMALS; FOOD CONTAMINATION; MYCOTOXICOSIS; MYCOTOXINS; POULTRY; POULTRY DISEASES; PREVALENCE;

EID: 84930690898     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps/pev075     Document Type: Conference Paper

References (175)

1. Agence Francaise de S'ecurit'e Sanitaire des Aliments. 2009. 'Evaluation des risques li'es à la presence de mycotoxines dans les chanes alimentaires humaine et animale; Agence Francaise de S'ecurit'e Sanitaire des Aliments. Pages 1-308. Maisons-Alfort, France. Published by AFSSA, Maisons-Alfort, France.
2. Antonissen, G., A. Martel, F. Pasmans, R. Ducatelle, E. Verbrugghe, V. Vandenbroucke, S. Li, F. Haesebrouck, F. Van Immerseel, and S. Croubels. 2014. The impact of Fusarium mycotoxins on human and animal host susceptibility to infectious diseases. Toxins. 6:430-452.
3. Applegate, T. J., G. Schatzmayr, K. Pricket, C. Troche, and Z. Jiang. 2009. Effect of aflatoxin culture on intestinal function and nutrient loss in laying hens. Poult. Sci. 88:1235-1241.
4. Avantaggiato, G., R. Havenaar, and A. Visconti. 2007. Assessment of the multi-mycotoxin-binding efficacy of a carbon/aluminosilicatebased product in an in vitro gastrointestinal model. J. Agric. Food Chem. 55:4810-4819.
5. Awad, W. A., J. Bohm, E. Razzazi-Fazeli, H. W. Hulan, and J. Zentek. 2004. Effects of deoxynivalenol on general performance and electrophysiological properties of intestinal mucosa of broiler chickens. Poult. Sci. 83:1964-1972.
6. Awad,W. A., H. Rehman, J. Bohm, E. Razzazi-Fazeli, and J. Zentek. 2005. Effects of luminal deoxynivalenol and L-proline on electrophysiological parameters in the jejunums of laying hens. Poult. Sci. 84:928-932.
7. Awad, W. A., J. R. Aschenbach, F. M. C. S. Setyabudi, E. Razzazi-Fazeli, J. Bohm, and J. Zentek. 2007. In vitro effects of deoxynivalenol on small intestinal D-glucose uptake and absorption of deoxynivalenol across the isolated jejunal epithelium of laying hens. Poult. Sci. 86:15-20.
8. Awad, W. A., E. Razzai-Fazeli, J. Bohm, and J. Zentek. 2008. Effects of B-trichothecenes on luminal glucose transport across the isolated jejunal epithelium of broiler chicks. J. Anim. Physiol. Anim. Nutr. 92:225-230.
9. Awad, W. A., K. Ghareeb, and J. Bohm. 2009. Animal feed additive and the effect of the fusarium toxin deoxynivalenol on the electrophysiological measurement of transepithelial ion transport of young chickens with ussing chamber technique. Intl. J. Poult. Sci. 8:25-27.
10. Awad, W. A., M. Hess, M. Twaruzek, J. Grajewski, R. Kosicki, J. Bohm, and J. Zentek. 2011. The impact of the Fusarium Mycotoxin deoxynivalenol on the health and performance of broiler chicks. Intl. J. Mol. Sci. 12:7996-8012.
11. Awad, W., K. Ghareeb, J. Bohm, and J. Zentek. 2013. The toxicological impacts of the Fusarium mycotoxin, deoxynivalenol, in poultry flocks with special reference to immunotoxicity. Toxins. 5:912-925.
12. Baptista, A. S., J. Horii, M. A. Calori-Domingues, E. M. da Gl'oria, J. M. Salgado, and M. R. Vizioli. 2002. Thermolysed and active yeast to reduce the toxicity of aflatoxin. Scientia Agricola 59:257-260.
13. Bbosa, G. S., D. Kitya, J. Odda, and J. Ogwal-Okeng. 2013. Aflatoxins metabolism, effects on epigenetic mechanisms and their role in carcinogenesis. Health. 5:14-34.
14. Bermudez, A. J., D. R. Ledoux, and G. E. Rottinghaus. 1995. Effects of Fusarium moniliforme culture material containing known levels of fumonisin B1 in ducklings. Avian Dis. 39:879-886.
15. Berthiller, F., C. Crews, C. Dall'Asta, S. D. Saeger, G. Haesaert, P. Karlovsky, I. P. Oswald, W. Seefelder, G. Speijers, and J. Stroka. 2013. Masked mycotoxins: A review. Mol. Nutr. Food Res. 57:165-186.
16. Bezuidenhout, S. C., W. C. A. Gelderblom, C. P. Gorst-Allman, R. M. Horak, W. F. O. Marasas, G. Spiteller, and R. Vleggaar. 1988. Structure elucidation of the fumonisins, mycotoxins from Fusarium moniliforme. J. Chem. Soc. Chem. Commun. 743-745.
17. Binder, E. M., L. M. Tan, L. J. Chin, J. Handl, and J. Richard. 2007. Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Anim. Feed Sci. Technol. 137:265-282.
18. Bouhet, S., and I. P. Oswald. 2007. The intestine as a possible target for fumonisin toxicity. Mol. Nutr. Food Res. 51:925-931.
19. Bracarense, A.-P. F. L., J. Lucioli, B. Grenier, G. Drociunas Pacheco, W. D. Moll, G. Schatzmayr, and I. P. Oswald. 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.
20. Broomhead, J. N., D. R. Ledoux, A. J. Bermudez, and G. E. Rottinghaus. 2002. Chronic effects of fumonisin B1 in broilers and turkeys fed dietary treatments to market age. Poult. Sci. 81:56-61.
21. Brown, T. P., G. E. Rottinghaus, and M. E. Williams. 1992. Fumonisin mycotoxicosis in broilers: Performance and pathology. Avian Dis. 36:450-454.
22. Bryden, W. L. 2012. Mycotoxin contamination of the feed supply chain: Implications for animal productivity and feed security. Anim. Feed Sci. Technol., 173(1-2):134-158.
23. Busby, W. F., Jr., and G. N. Wogan. 1981. Aflatoxins. Pages 3-27 in Mycotoxins and N-Nitrosocompounds, Environmental Risks. Vol. 2. R. C. Shank ed. CRC Press Inc., Boca Raton, FL.
24. Cabassi, E., F. Miduri, and A. M. Cantoni. 2005. Intoxication with fumonisin B1 (FB1) in piglets and supplementation with granulated activated carbon: Cellular-mediated immunoresponse. Vet. Res. Comm. 29:225-227.
25. Carretero, M. 2002. Clay minerals and their beneficial effects upon human health. Appl. Clay Sci. 21:155-163.
26. CAST. 2003. Mycotoxins: Risks in plant, animal, and human systems, Task Force Report No. 139. Pages 13-85 in Council for Agricultural Science and Technology, Ames, IA.
27. Cawood, M. E., W. C. A. Gelderblom, R. Vleggaar, Y. Behrend, P. G. Thiel, and W. F. O. Marasas. 1991. Isolation of the fumonisin mycotoxins: A quantitative approach. J. Agric. Food Chem. 39:1958-1962.
28. Chen, J., C. J. Mirocha, W. Xie, L. Hogge, and D. Olson. 1992. Production of the mycotoxin fumonisin B1 by Alternaria alternata f. sp. Lycopersici. Appl. Environ. Microbiol. 58:3928-3931.
29. Ciegler, A., B. Lillehoj, E. Peterson, and H. H. Hall. 1966. Microbial detoxification of aflatoxin. Appl. Microbiol. 14:934-939.
30. D'Mello, J., C. Placinta, and A. Macdonald. 1999. Fusarium mycotoxins: A review of global implications for animal health, welfare and productivity. Anim. Feed Sci. Technol. 80:183-205.
31. Dakovi'c, A., S. Matijasevi'c, G. E. Rottinghaus, D. R. Ledoux, P. Butkeraitis, and Z. Sekuli'c. 2008. Aflatoxin B1 adsorption by natural and copper modified montmorillonite. Colloid. Surface. B. 66:20-25.
32. Danicke, S., M. Gareis, and J. Bauer, 2001. Orientation values for critical concentrations of deoxynivalenol and zearalenone in diets for pigs, ruminants and gallinaceous poultry. Proc. Soc. Nutr. Physiol. 10:171-174.
33. Danicke, S., 2002. Prevention and control of mycotoxins in the poultry production chain: A European view. World. Poult. Sci. J. 58:451-474.
34. Danicke, S., K. H. Ueberschar, I. Halle, S. Matthes, H. Valenta, and G. Flachowsky. 2002. Effect of addition of a detoxifying agent to laying hen diets containing uncontaminated or Fusarium toxincontaminated maize on performance of hens and on carryover of zearalenone. Poult. Sci. 81:1671-1680.
35. Danicke, S., S. Matthes, I. Halle, K. H. Ueberschar, S. Doll, and H. Valenta. 2003. Effects of graded levels of Fusarium toxincontaminated wheat and of a detoxifying agent in broiler diets on performance, nutrient digestibility and blood chemical parameters. Brit. Poult. Sci. 44:113-126.
36. Danicke, S., H. Valenta, and S. Matthes. 2007. On the interactions between fusarium toxin-contaminated wheat and nonstarch polysaccharide hydrolyzing enzymes in diets of broilers on performance, intestinal viscosity, and carryover of deoxynivalenol. Poult. Sci. 85:291-298.
37. Deng, Y., A. B. Vel'azquez, F. Billes, and J. Dixon. 2010. Bonding mechanisms between aflatoxin B1 and smectite. Appl. Clay Sci. 50:92-98.
38. Desmarchelier, A., J.-M. Oberson, P. Tella, E. Gremaud, W. Seefelder, and P. Mottier. 2010. Development and comparison of two multiresidue methods for the analysis of 17 mycotoxins in cereals by liquid chromatography electrospray ionization tandem mass spectrometry. J. Agric. Food Chem. 58:7510-7519.
39. Devegowda, G., and T. N. K. Murthy, 2005. Mycotoxins: Their effects in poultry and some practical solutions. Pages 25-56 in The Mycotoxin Blue Book. D. E. Diaz ed. Nottingham University Press, Nottingham, UK.
40. Diamond, J. 1999. Dirty eating for healthy living. Nature. 400:120-121.
41. Diaz, D., W. Hagler, Jr., J. Blackwelder, J. Eve, B. Hopkins, K. Anderson, F. Jones, and L. Whitlow. 2004. Aflatoxin binders II: Reduction of aflatoxin M1 in milk by sequestering agents of cows consuming aflatoxin in feed. Mycopathologia. 157:233-241.
42. Diaz, G. J., E. Calabrese, and R. Blain. 2008. Aflatoxicosis in chickens (Gallus gallus): An example of hormesis? Poult. Sci. 87:727-732.
43. Dietrich, B., S. Neuenschwander, B. Bucher, and C. Wenk. 2012. Fusarium mycotoxin-contaminated wheat containing deoxynivalenol alters the gene expression in the liver and the jejunum of broilers. Animal. 6:278-291.
44. Edds, G. T., and R. R. Bortell. 1983. Biological effects of aflatoxin in poultry. Pages 55-61 in Aflatoxin and Aspergillus flavus in corn. U. L. Diener, R. L. Asquith, and J. W. Dickens eds. Southern Cooperative Services Bulletin. 279. Alabama Agricultural Experiment Station, Auburn University, AL.
45. EFSA. 2010. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP); Statement on the establishment of guidelines for the assessment of additives from the functional group 'substances for reduction of the contamination of feed by mycotoxins'. EFSA Journal 8:8.
46. EFSA. 2013. EFSA FEEDAP Panel: Scientific opinion on the safety and efficacy of micro-organism DSM 11798 when used as a technological feed additive for pigs. EFSA Journal 11:18.
47. EFSA. 2014. EFSA Panel on Additives and Products or Substances used in Animal Feed; Scientific Opinion on the safety and efficacy of fumonisin esterase (FUMzyme R) as a technological feed additive for pigs. EFSA Journal 12:3667.
48. El-Nezami, H. S., H. Mykkanen, P. Kankaanpaa, T. Suomalainen, J. T. Ahokas, and S. Salminen. 2000. The ability of a mixture of Lactobacillus and Propionibacterium to influence the faecal recovery of aflatoxins in healthy Egyptian volunteers: A pilot clinical study. Biosci. Microflora. 19:41-45.
49. El-Nezami, H. S., N. N. Polychronaki, J. Ma, H. Zhu, W. Ling, E. K. Salminen, R. O. Juvonen, S. J. Salminen, T. Poussa, and H. M. Mykkanen. 2006. Probiotic supplementation reduces a biomarker for increased risk of liver cancer in young men from Southern China. Am. J. Clin. Nutr. 83:1199-1203.
50. European Commission (EC). Directive. 2002. 2002/32/EC of the European Parliament and of the Council on undesirable substances in animal feed. Off. J. Eur. Union 140:10-22.
51. European Commission (EC). Commission Recommendation (2006/576/EC) of 17 August 2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding. Off. J. Eur. Union 229:7-9.
52. Ferguson, J., and A. Keaton. 1950. Studies of the diets of pregnant women in Mississippi: I. The ingestion of clay and laundry starch. New Orleans Med. Surg. J. 102:460-463.
53. Fruhauf, S., H. Schwartz, F. Ottner, R. Krska, and E. Vekirua. 2012. Yeast cell based feed additives: Studies on aflatoxin B1 and zearalenone. Food Addit. Contam. Part A. Chem. Anal. Control Expo. Risk. Assess. 29:217-231.
54. Fuchs, E., E. M. Binder, D. Heidler, and R. Krska. 2002. Structural characterization of metabolites after the microbial degradation of type A trichothecenes by the bacterial strain BBSH 797. Food Addit. Contam. 19:379-386.
55. Gelderblom,W. C. A., K. Jaskiewicz, W. F. O. Marasas, P. G. Thiel, R. M. Horak, R. Vleggaar, and N. P. J. Kriek. 1988. Fumonisins: Novel mycotoxins with cancer-promoting activity produced by Fusarium moniliforme. Appl. Environ. Microbiol. 54:1806-1811.
56. Gibson, R. M., C. A. Bailey, L. F. Kubena, W. E. Huff, and R. B. Harvey. 1989. Ochratoxin A and dietary protein. 1. Effects on body weight, feed conversion, relative organ weight, and mortality in three-week-old broilers. Poult. Sci. 68:1658-1663.
57. Girgis, G. N., S. Sharif, J. R. Barta, H. J. Boermans, and T. K. Smith. 2008. Immunomodulatory effects of feed-borne Fusarium mycotoxins in chickens infected with coccidia. Exp. Biol. Med. 233:1411-1420.
58. Girgis, G. N., J. R. Barta, M. Brash, and T. K. Smith. 2010a. Morphologic 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.
59. Girgis, G. N., J. R. Barta, C. K. Girish, N. A. Karrow, H. J. Boermans, and T. K. Smith. 2010b. Effects of feed-borne Fusarium mycotoxins and an organic mycotoxin adsorbent on immune cell dynamics in the jejunum of chickens infected with Eimeria maxima. Vet. Immunol. Immunopathol. 138:218-223.
60. Girish, C. K., and T. Smith. 2008. Impact of feed-borne mycotoxins on avian cell-mediated and humoral immune responses. World Mycotoxin J. 1:105-121.
61. Glahn, R. P., R. S. Shapiro, V. E. Vena, R. F. Wideman, Jr., and W. E. Huff. 1989. Effects of chronic ochratoxin A and citrinin toxicosis on kidney function of single comb white leghorn pullets. Poult. Sci. 68:1205-1212.
62. Glahn, R. P., R. F. Wideman, Jr., J. W. Evangelisti, and W. E. Huff. 1988. Effects of ochratoxin A alone and in combination with citrinin on kidney function of single comb white leghorn pullets. Poult. Sci. 67:1034-1042.
63. Grant, P. G., and T. D. Phillips. 1998. Isothermal adsorption of Aflatoxin B1 on HSCAS clay. J. Agric. Food Chem. 46:599-605.
64. Grenier, B., and I. P. Oswald. 2011. Mycotoxin co-contamination of food and feed: Meta-analysis of publications describing toxicological interactions. World Mycotoxin J. 4:285-313.
65. Grenier, B., A. P. Loureiro-Bracarense, J. Lucioli, G. D. Pacheco, A. M. Cossalter,W. D. Moll, G. Schatzmayr, and I. P. Oswald. 2011. Individual and combined effects of subclinical doses of deoxynivalenol and fumonisins in piglets. Mol. Nutr. Food Res. 55:761-771.
66. Grenier, B., A. P. F. L. Bracarense, H. E. Schwartz, C. Trumel, A. M. Cossalter, G. Schatzmayr, M. Kolf-Clauw, W. D. Moll, and I. P. Oswald. 2012. The low intestinal and hepatic toxicity of hydrolyzed fumonisin B 1 correlates with its inability to alter the metabolism of sphingolipids. Biochem. Pharmacol. 83: 1465-1473.
67. Grenier, B., A. P. F. Bracarense, H. E. Schwartz, J. Lucioli, A.-M. Cossalter, W.-D. Moll, G. Schatzmayr, and I. P. Oswald. 2013. Biotransformation approaches to alleviate the effects induced by fusarium mycotoxins in swine. J. Agric. Food Chem. 61:6711-6719.
68. Grenier, B., and T. J. Applegate. 2013. Invited review-Modulation of intestinal functions upon mycotoxin ingestion: Meta-analysis of published experiments in animals. Toxins. 5:396-430.
69. Griessler, K., I. Rodrigues, J. Handl, and U. Hofstetter, 2010. Occurrence of mycotoxins in Southern Europe. World Mycotoxin J. 3:301-309.
70. Hamilton, P. B., W. E. Huff, J. R. Harris, and R. D. Wyatt. 1982. Natural occurrences of ochratoxicosis in poultry. Poult. Sci. 61:1832-1841.
71. Han, X. Y., Q. C. Huang, W. F. Li, J. F. Jiang, and Z. R. Xu. 2008. Changes in growth performance, digestive enzyme activities and nutrient digestibility of cherry valley ducks in response to aflatoxin B1 levels. Livestock Sci. 119:216-220.
72. Hartinger, D., and W. D. Moll. 2011. Fumonisin elimination and prospects for detoxification by enzymatic transformation. World Mycotoxin J. 4:271-283.
73. Heinl, S., D. Hartinger, M. Thamhesl, E. Vekiru, R. Krska, G. Schatzmayr, W. D. Moll, and R. Grabherr. 2010. Degradation of fumonisin B1 by the consecutive action of two bacterial enzymes. J. Biotechnol. 145:120-129.
74. Huebner, H. J., S. L. Lemke, S. E. Ottinger, K. Mayura, and T. D. Phillips. 1999. Molecular characterization of high affinity, high capacity clays for the equilibrium sorption of ergotamine. Food Addit. Contam. 16:159-171.
75. Huff, W. E., and P. B. Hamilton. 1975. Decreased plasma carotenoids during ochratoxicosis. Poult. Sci. 54:1308-1310.
76. Huff, W. E., and J. Doerr. 1981. Synergism between aflatoxin and ochratoxin A in broiler chickens. Poult. Sci. 60:550-555.
77. Huff, W. E., R. B. Harvey, L. F. Kubena, and G. E. Rottinghaus. 1988a. Toxic synergism between aflatoxin and T-2 toxin in broiler chickens. Poult. Sci. 67:1418-1423.
78. Huff, W. E., L. F. Kubena, and R. B. Harvey. 1988b. Progression of ochratoxicosis in broiler chicks. Poult. Sci. 67:1139-1146.
79. Huff, W. E., L. F. Kubena, R. B. Harvey, W. M. Hagler, Jr., S. P. Swanson, T. D. Phillips, and C. R. Creger, 1986. Individual and combined effects of aflatoxin and deoxynivalenol (DON, vomitoxin) in broiler chickens. Poult. Sci. 65:1291-1298.
80. Huff, W. E., L. F. Kubena, R. B. Harvey, and T. D. Phillips. 1992. Efficacy of hydrated sodium calcium aluminosilicate to reduce the individual and combined toxicity of aflatoxin and ochratoxin A. Poult. Sci. 71:64-69.
81. Jestoi, M. 2008. Emerging fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin: A review. Crit. Rev. Food Sci. Nutr. 48:21-49.
82. Johns, T., and M. Duquette. 1991. Detoxification and mineral supplementation as functions of geophagy. Am. J. Clin. Nutr. 53:448-456.
83. Kannewischer, I., A. Tenorio, G. White, and J. Dixon. 2006. Smectite clays as adsorbents of aflatoxin B1: Initial steps. Clay Sci. 12:199-204.
84. Karlovsky, P. 2011. Biological detoxification of the mycotoxin deoxynivalenol and its use in genetically engineered crops and feed additives. Appl. Microbiol. Biotechnol. 91:491-504.
85. Kensler, T. W., J. D. Groopman, P. A. Egner, A. M͡noz, G. Qian, and J. Chen. 2013. Chemoprevention of Hepatic Cancer in Aflatoxin Endemic Areas in Primary Liver Cancer. in J. Gu ed. Zhejiang University Press, Hangzhou, China, and Springer-Verlag, Berlin Heidelberg, Germany.
86. Kermanshahi, H., M. R. Akbari, M. Maleki, and M. Behgar. 2007. Effect of prolonged low level inclusion of aflatoxin B1 into diet on performance, nutrient digestibility, histopathology and blood enzymes of broiler chickens. J. Anim. Vet. Adv. 6:686-692.
87. Koynarski, V., S. Stoev, N. Grozeva, T. Mirtcheva, H. Daskalov, J. Mitev, and P. Mantle. 2007a. Experimental coccidiosis provoked by Eimeria acervulina in chicks simultaneously fed on ochratoxin A contaminated diet. Res. Vet. Sci. 82:225-231.
88. Koynarsky, V., S. D. Stoev, N. Grozeva, and T. Mirtcheva. 2007b. Experimental coccidiosis provoked by Eimeria adenoeides in turkey poults given ochratoxin A. Veterinarski Archiv. 77:113-128.
89. Kubena, L. F., W. E. Huff, R. B. Harvey, D. E. Corrier, T. D. Phillips, and C. R. Creger, 1988. Influence of ochratoxin A and deoxynivalenol (DON) on growing broiler chicks. Poult. Sci. 67:253-260.
90. Kubena, L. F., W. E. Huff, R. B. Harvey, T. D. Phillips, and G. E. Rottinghaus, 1989. Individual and combined toxicity of deoxynivalenol and T-2 toxin in broiler chicks. Poult. Sci. 68:622-626.
91. Kubena, L. F., R. B. Harvey, T. D. Phillips, and B. A. Clement. 1993. Effect of hydrated sodium calcium aluminosilicates on aflatoxicosis in broiler chicks. Poult. Sci. 72:651-657.
92. Ledoux, D. R., A. J. Bermudez, and G. E. Rottinghaus. 1996. The effects of feeding Fusarium moniliforme culture material, containing known levels of fumonisin B1, in the young turkey poult. Poult. Sci. 75:1472-1478.
93. Ledoux, D. R., T. P. Brown, T. S. Weibking, and G. E. Rottinghaus. 1992. Fumonisin toxicity in broiler chicks. J. Vet. Diagn. Invest. 4:330-333.
94. Leeson, S., G. J. Diaz, and J. D. Summers. 1995. Poultry Metabolic Disorders and Mycotoxins. University Books, Guelph, Ontario, Canada.
95. Lemke, S. L., P. G. Grant, and T. D. Phillips. 1998. Adsorption of zearalenone by organophilic montmorillonite clay. J. Agric. Food Chem. 46:3749-3796.
96. Loggi, D. G., Jr., G. Regenye, and M. Miles. 1992. Pica and irondeficiency anaemia: A case report. J. Oral Maxillofac. Surg. 50:633-635.
97. Magan, N., A. Medina, and D. Aldred. 2011. Possible climatechange effects on mycotoxin contamination of food crops preand postharvest. Plant Pathol. 60:150-163.
98. Magnoli, A., M. Monge, R. Miazzo, L. Cavaglieri, C. Magnoli, C. Merkis, A. Cristofolini, A. Dalcero, and S. Chiacchiera. 2011. Effect of low levels of aflatoxin B1 on performance, biochemical parameters, and aflatoxin B1 in broiler liver tissues in the presence of monensin and sodium bentonite. Poult. Sci. 90:48-58.
99. Malachova, A., M. Sulyok, R. Schuhmacher, F. Berthiller, J. Hajslova, Z. Veprikova, M. Zachariasova, V. M. T. Lattanzio, S. De Saeger, J. D. Di Mavungu, S. V. Malysheva, S. Biselli, O. Winkelmann, A. Breidbach, S. Hird, and R. Krska. 2013. Collaborative investigation of matrix effects in mycotoxin determination by high performance liquid chromatography coupled to mass spectrometry. Qual. Assur. Saf. Crops Foods 5:91-103.
100. Malachova, A., M. Sulyok, E. Beltr'an Iturat, F. Berthiller, and R. Krska. 2014. Optimization and validation of a quantitative 1 liquid chromatography-Tandem mass spectrometric method covering 295 bacterial and fungal metabolites including all relevant mycotoxins in four model food matrices. J. Chrom. A. 1362:145-156.
101. Marroqu'n-Cardona, A., Y. Deng, J. F. Taylor, C. T. Hallmark, N. M. Johnson, and T. D. Phillips. 2009. In vitro and in vivo characterization of mycotoxin binding additives used for animal feeds in Mexico. Food Addit. Contam. (A) 26:733-743.
102. Marquardt, R. R., and A. A. Frohlich. 1992. A review of recent advances in understanding ochratoxicosis. J. Anim. Sci. 70:3968-3988.
103. Masimango, N., J. Remacale, and J. L. Ramaut. 1978. The role of adsorption in the elimination of aflatoxin B1 from contaminated media. European J. Appl. Microbiol. Biotechnol. 6:101-105.
104. Mayura, K., M. Abdel-Wahhab, K. McKensie, A. Sarr, J. Edwards, K. Naguib, and T. Phillips. 1998. Prevention of maternal and developmental toxicity in rats via dietary inclusion of common aflatoxin sorbents: Potential for hidden risks. Toxicol. Sci. 41:175-182.
105. McCormick, S. P. 2013. Microbial detoxification of mycotoxins. J. Chem. Ecol. 39:907-918.
106. Miller, J. D., A. W. Schaafsma, D. Bhatnagar, G. Bondy, I. Carbone, L. J. Harris, G. Harrison, G. P. Munkvold, I. P. Oswald, J. J. Pestka, L. Sharpe, M. W. Sumarah, S. A. Tittlemier, and T. Zhou. 2014. Mycotoxins that affect the North American agrifood sector: State of the art and directions for the future. World Mycotoxin J. 7:63-82.
107. Mitchell, N. J., K. S. Xue, S. Lin, A. Marroquin-Cardona, K. A. Brown, S. E. Elmore, L. Tang, A. Romoser, W. C. Gelderblom, J.-S. Wang, and T. Phillips. 2014. Calcium montmorillonite clay reduces AFB1 and FB1 biomarkers in rats exposed to single and co-exposures of aflatoxin and fumonisin. Toxicol. Appl. Pharmacol. 34(7):795-804.
108. Molnar, O., G. Schatzmayr, E. Fuchs, and H. Prillinger. 2004. Trichosporon mycotoxinivorans sp. nov., a new yeast species useful in biological detoxification of various mycotoxins. Syst. Appl. Microbiol. 27:661-671.
109. Moran, E. T., Jr., B. Hunter, P. Ferket, L. G. Young, and L. G. McGirr, 1982. High tolerance of broilers to vomitoxin from corn infected with Fusarium graminearum. Poult. Sci. 61:1828-1831.
110. Nagl, V., H. Schwartz, R. Krska, W.-D. Moll, S. Knasmuller, M. Ritzmann, G. Adam, and F. Berthiller. 2012. Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in rats. Toxicol. Lett. 213:367-373.
111. Nagl, V., B. Wochtl, H. E. Schwartz-Zimmermann, I. Hennig-Pauka, W.-D. Moll, G. Adam, and F. Berthiller. 2014. Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in pigs. Toxicol. Lett. 229:190-197.
112. Norred, W. P. 1993. Fumonisins-mycotoxins produced by Fusarium moniliforme. J. Toxicol. Environ. Health. 38:309-328.
113. OECD. 1992. Test No. 406: Skin Sensitisation, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, France. doi: 10. 1787/9789264070660-en.
114. OECD. 1997. Test No. 471: Bacterial Reverse Mutation Test, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, France. doi: 10. 1787/9789264071247-en.
115. OECD. 1997. Test No. 473: In vitro Mammalian Chromosome Aberration Test, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, France. doi: 10. 1787/9789264071261-en.
116. OECD. 1997. Test No. 474: Mammalian Erythrocyte Micronucleus Test, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, France. doi: 10. 1787/9789264071285-en.
117. OECD. 1998. Test No. 408: Repeated Dose 90-Day Oral Toxicity Study in Rodents, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, France. doi: 10. 1787/9789264070707-en.
118. OECD. 2002. Test No. 404: Acute Dermal Irritation/Corrosion, OECD Guidelines for the Testing of Chemicals, Section 4, OECD Publishing, Paris, France. doi: 10. 1787/9789264070622-en.
119. Osborne, D. J., R. D. Wyatt, and P. B. Hamilton, 1975. Fat digestion during aflatoxicosis in chickens. Poult. Sci. 54:1802.
120. Osborne, D. J., and P. B. Hamilton. 1981. Decreased pancreatic digestive enzymes during aflatoxicosis. Poult. Sci. 60:1818-1821.
121. Osborne, D. J., W. E. Huff, P. B. Hamilton, and H. R. Burmeister. 1982. Comparison of ochratoxin, aflatoxin, and T-2 toxin for their effects on elected parameters related to digestion and evidence for specific metabolism of carotenoids in chickens. Poult. Sci. 61:1646-1652.
122. Osselaere, A., M. Devreese, J. Goossens, V. Vandenbroucke, S. de Baere, P. de Backer, and S. Croubels. 2013. Toxicokinetic study and absolute oral bioavailability of deoxynivalenol, T-2 toxin and zearalenone in broiler chickens. Food Chem. Toxicol. 51:350-355.
123. Osselaere, A., R. Santos, V. Hautekiet, P. De Backer, K. Chiers, R. Ducatelle, and S. Croubels. 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.
124. doi:10. 1371/journal.pone.0069014.
125. Pastorelli, H., J. van Milegen, P. Lovatto, and L. Montagne. 2012. Meta-analysis of feed intake and growth responses of growing pigs after a sanitary challenge. Animal. 6:952-961.
126. Phillips, T. 1999. Dietary clay in the chemoprevention of aflatoxininduced disease. Toxicol. Sci. 52:118-126.
127. Phillips, T., B. Clement, and D. Park. 1994. Approaches to reduction of aflatoxins in foods and feeds. In: D. L. Eaton and J. D. Groopman, eds. Pages 383-406 in The Toxicology of Aflatoxins. Academic Press, San Diego (CA).
128. Phillips, T., L. Kubena, R. Harvey, D. Taylor, and N. Heidelbaugh. 1988. Hydrated sodium calcium aluminosilicate: A high affinity sorbent for aflatoxin. Poult. Sci. 67:243-247.
129. Phillips, T., S. Lemke, and P. Grant. 2002. Characterization of clay based enterosorbents for the prevention of aflatoxicosis. In: J. W. DeVries, M. W. Trucksess, and L. S. Jackson, eds. Pages 157-171 in Mycotoxins and Food Safety: Advances in Experimental Medicine and Biology. Kluwer Academic/Plenum Publishers, New York (NY).
130. Phillips, T., A. Sarr, and P. Grant. 1995. Selective chemisorption and detoxification of aflatoxins by phyllosilicate clay. Nat. Toxins. 3:204-213.
131. Phillips, T. D., E. Afriyie-Gyawu, J. H. Williams, H. J. Huebner, N.-A. Ankrah, D. Ofori-Adjei, P. E. Jolly, N. Johnson, J. F. Taylor, A. Marroquin-Cardona, L. Xu, L. Tang, and J. S. Wang. 2008. Reducing human exposure to aflatoxin through use of clay. Food Addit. Contam. 25:134-145.
132. Pinton, P., D. Tsybulskyy, J. Lucioli, J. Laffitte, P. Callu, F. Lyazhri, F. Grosjean, A. P. Bracarense, M. Kolf-Clauw, and I. P. Oswald. 2012. Toxicity of deoxynivalenol and its acetylated derivatives on the intestine: Differential effects on morphology, barrier function, tight junction proteins and MAPKinases. Toxicol. Sci. 130:180-190.
133. Piva, A., G. Casadei, G. Pagliuca, E. Cabassi, M. Galvano Solfrizzo, R. T. Riley, and D. E. Diaz. 2005. Activated carbon does not prevent the toxicity of culture material containing fumonisin B1 when fed to weanling piglets. J. Anim. Sci. 83:1939-1947.
134. Plattner, R. D., D. Weisleder, D. D. Shackleford, R. Peterson, and R. G. Powell. 1992. A new fumonisin from solid cultures of Fusarium moniliforme. Mycopathologia. 117:23-28.
135. Politis, I., K. Fegeros, S. Nitsch, G. Schatzmayr, and D. Kantas. 2005. Use of Trichosporon mycotoxinivorans to suppress the effects of ochratoxicosis on the immune system of broiler chicks. Brit. Poult. Sci. 46:58-65.
136. Raju, M., and G. Devegowda. 2000. Influence of esterifiedglucomannan on performance and organ morphology, serum biochemistry and haematology in broilers exposed to individual and combined mycotoxicosis (aflatoxin, ochratoxin and T-2 toxin). Brit. Poult. Sci. 41:640-650.
137. Richard, J. 2000. Romer Labs Guide to Mycotoxins. Vol. 2: Sampling and Sample Preparation for Mycotoxin Analysis. Romer Labs, Union, MO.
138. Richardson, K. E., and P. B. Hamilton. 1987. Enhanced production of pancreatic digestive enzymes during aflatoxicosis in egg-type chickens. Poult. Sci. 66:640-644.
139. Riley, R. T., N. H. An, J. L. Showker, H. S. Yoo, W. P. Norred, W. J. Chamberlain, E. Wang, A. H. Merrill, G. Motelin, V. R. Beasley, and W. M. Haschek. 1993. Alteration of tissue and serum sphinganine to sphingosine ratio: An early biomarker of exposure to fumonisin-containing feeds in pigs. Toxicol. Appl. Pharmacol. 118:105-112.
140. Ramos, A. J., E. Hern'andez, J. M. Pl'a-Delfina, and M. Merino. 1996. Intestinal absorption of zearalenone and in vitro study of non-nutritive sorbent materials. Intl. J. Pharm. 128:129-137.
141. Ringot, D., A. Chango, Y. J. Schneider, and Y. Larondelle. 2006. Toxicokinetics and toxicodynamics of ochratoxin A, an update. Chem. Biol. Interact. 159:18-46.
142. Robinson, A., N. M. Johnson, A. Strey, J. F. Taylor, A. Marroquin-Cardona, N. J. Mitchell, E. Afriyie-Gyawu, N. A. Ankrah, J. H. Williams, J. S. Wang, P. E. Jolly, R. J. Nachman, and T. D. Phillips. 2012. Calcium montmorillonite clay reduces urinary biomarkers of fumonisin B(1) exposure in rats and humans. Food Addit. Contam. A. Chem. Anal. Control Expo. Risk Assess. 29:809. doi: 10. 1080/19440049. 2011. 651628.
143. Rodrigues, I., J. Handl, and E. M. Binder. 2011. Mycotoxin occurrence in commodities, feeds and feed ingredients sourced in the Middle East and Africa. Food. Addit. Contam. B. 4:168-179.
144. Rodrigues, I., and L. J. Chin. 2012. A comprehensive survey on the occurrence of mycotoxins in maize dried distillers' grain and solubles sourced worldwide. World Mycotoxin J. 5:83-88.
145. Rodrigues, I., and K. Naehrer. 2012. A three-year survey on the worldwide occurrence of mycotoxins in feedstuffs and feed. Toxins. 4:663-675.
146. Sergent, T., L. Ribonnet, A. Kolosova, S. Garsou, A. Schaut, S. de Saeger, C. van Peteghem, Y. Larondelle, L. Pussemier, and Y. J. Schneider. 2008. Molecular and cellular effects of food contaminants and secondary plant components and their plausible interactions at the intestinal level. Food Chem. Toxicol. 46:813-841.
147. Schaeffer, J. L., J. J. Tyczkowski, and P. B. Hamilton. 1987. Alterations in carotenoid metabolism during ochratoxicosis in young broiler chickens. Poult. Sci. 66:318-324.
148. Schatzmayr, G., D. Heidler, E. Fuchs, S. Nitsch, M. Mohnl, M. Taiubel, A. P. Loibner, R. Braun, and E. M. Binder. 2003. Investigation of different yeast strains for the detoxification of ochratoxin A. Mycotoxin Res. 19:124-128.
149. Schatzmayr, G., M. Taubel, E. Vekiru, D. Moll, D. Schatzmayr, E. M. Binder, R. Krska, and A. P. Loibner. 2006a. Detoxification of mycotoxins by biotransformation. Pages 363-375 in The Mycotoxin Factbook, Food and Feed Topics. D. Barug, D. Bhatnagar, H. P. van Egmond, J. W. van der Kamp, W. A. van Osenbruggen, and A. Visconti eds. Wageningen Academic Publishers, Wageningen, The Netherlands.
150. Schatzmayr, G., F. Zehner, M. Táubel, D. Schatzmayr, A. Klimitsch, A. P. Loibner, and E. M. Binder. 2006b. Microbiologicals for deactivating mycotoxins. Mol. Nutr. Food Res. 50:543-551.
151. Schatzmayr, G., and E. Streit. 2013. Global occurrence of mycotoxins in the food and feed chain: Facts and figures. World Mycotoxin J. 6(3):213-222.
152. Schiefer, H. 1990. Mycotoxicoses of domestic animals and their diagnosis. Can. J. Physiol. Pharmacol. 68:987-990.
153. Schumacher, R., R. Ksrka, J. Weingaertner, and M. Grasserbauer. 1997. Interlaboratory comparison study for the determination of the Fusarium mycotoxins deoxynivalenol in wheat and zearenone in maize using different methods. Fresenius J Anal. Chem. 359:510-515.
154. Scott, P. M. 1998. Industrial and farm detoxification processes for mycotoxins. Revue de M'edecine V'et'erinaire. 149:543-548.
155. Streit, E., K. Naehrer, I. Rodrigues, and G. Schatzmayr. 2013a. Mycotoxin occurrence in feed and feed raw materials worldwide: Long-term analysis with special focus on Europe and Asia. J. Sci. Food Agri. 93:2892-2899.
156. Streit, E., C. Schwab, M. Sulyok, K. Naehrer, R. Krska, and G. Schatzmayr. 2013b. Multi-mycotoxin screening reveals the occurrence of 139 different secondary metabolites in feed and feed ingredients. Toxins. 5:504-523.
157. Sulyok, M., F. Berthiller, R. Krska, and R. Schuhmacher. 2006. Development and validation of a liquid chromatography/tandem mass spectrometric method for the determination of 39 mycotoxins in wheat and maize. Rapid Commun. Mass Spectrom. 20:2649-2659.
158. Tran, S. T., A. Auvergne, G. Benard, J. D. Bailly, D. Tardieu, R. Babile, and P. Guerre, 2005. Chronic effects of fumonisin B1 on ducks. Poult. Sci. 84:22-28.
159. Varga, E., T. Glauner, R. Kóppen, K. Mayer, M. Sulyok, R. Schuhmacher, R. Krska, and F. Berthiller. 2012. Stable isotope dilution assay for the accurate determination of mycotoxins in maize by UHPLC-MS/MS. Anal. Bioanal. Chem. 402:2675-2686.
160. Varga, E., A. Malachova, H. Schwartz, R. Krska, and F. Berthiller. 2013a. Survey of deoxynivalenol and its conjugates deoxynivalenol-3-glucoside and 3-acetyl-deoxynivalenol in 374 beer samples. Food Addit. Contam. A. 30:137-146.
161. Varga, E., T. Glauner, F. Berthiller, R. Krska, R. Schuhmacher, and M. Sulyok. 2013b. Development and validation of a (semi-)quantitative UHPLC-MS/MS method for the determination of 191 mycotoxins and other fungal metabolites in almonds, hazelnuts, peanuts and pistachios. Anal. Bioanal. Chem. 405:5087-5104.
162. Varga, I., and A. Vanyi. 1992. Interaction of T-2 fusariotoxin with anticoccidial efficacy of lasalocid in chickens. Int. J. Parasit. 22:523-525.
163. Vekiru, E., S. Fruhauf, M. Sahin, F. Ottner, G. Schatzmayr, and R. Krska. 2007. Investigation of various adsorbents for their ability to bind Aflatoxin B1. Mycotoxin Res. 23:27-33.
164. Vekiru, E., C. Hametner, R. Mitterbauer, J. Rechthaler, G. Adam, G. Schatzmayr, R. Krska, and R. Schuhmacher. 2010. Cleavage of zearalenone by Trichosporon mycotoxinivorans to a novel nonestrogenic metabolite. Appl. Env. Microbiol. 76:2353-2359.
165. Verma, J., T. S. Johri, and B. K. Swain. 2007. Effect of aflatoxin, ochratoxin and their combination on protein and energy utilisation in white leghorn laying hens. J. Sci. Food Agric. 87:760-764.
166. Warth, B., M. Sulyok, P. Fruhmann, H. Mikula, F. Berthiller, R. Schuhmacher, C. Hametner, W. A. Abia, G. Adam, J. Fróhlich, and R. Krska. 2012. Development and validation of a rapid multi-biomarker liquid chromatography/tandem mass spectrometry method to assess human exposure to mycotoxins. Rapid Commun. Mass Spectrom. 26:1533-1540.
167. Wang, E., W. P. Norred, C. W. Bacon, R. T. Riley, and A. H. Merrill, Jr. 1991. Inhibition of sphingolipid biosynthesis by fumonisins: Implications for diseases associated with Fusarium moniliforme. J. Biol. Chem. 266:14486-14490.
168. Weibking, T. S., D. R. Ledoux, A. J. Bermudez, J. R. Turk, G. E. Rottinghaus, E. Wang, and A. H. Merrill, Jr. 1993. Effects of feeding Fusarium moniliforme culture material, containing known levels of fumonisin B1, on the young broiler chick. Poult. Sci. 72:456-466.
169. Weibking, T. S., D. R. Ledoux, A. J. Bermudez, J. R. Turk, and G. E. Rottinghaus. 1995. Effects on turkey poults of feeding Fusarium moniliforme M-1325 culture material grown under different environmental conditions. Avian Dis. 39:32-38.
170. Whitaker, T. B. 2006. Sampling foods for mycotoxins. Food Addit. Contam. 23:50-61.
171. Wu, F., D. Bhatnagar, T. Bui-Klimke, I. Carbone, R. Hellmich, G. Munkvold, P. Paul, G. Payne, and E. Takle. 2011. Climate change impacts on mycotoxin risks in US maize. World Mycotoxin J. 4: 79-93.
172. Xu, L., S. Eicher, and T. J. Applegate. 2011. Effect of increasing dietary concentrations of corn naturally-contaminated with deoxynivalenol on broiler and turkey poult performance and response to LPS. Poult. Sci. 90:2766-2774.
173. Yarru, L. P., R. S. Settivari, N. K. S. Gowda, E. Antoniou, D. R. Ledoux, and G. E. Rottinghaus. 2009a. Effects of turmeric (Curcuma longa) on the expression of hepatic genes associated with biotransformation, antioxidant, and immune systems in broiler chicks fed aflatoxin. Poult Sci. 88:12, 2620-2627.
174. Yarru, L. P., R. S. Settivari, E. Antoniou, D. R. Ledoux, and G. E. Rottinghaus. 2009b. Toxicological and gene expression analysis of the impact of aflatoxin B1 on hepatic function of male broiler chicks. Poult Sci. 88:360-371.
175. Yunus, A. W., E. Razzazi-Fazeli, and J. Bohm. 2011. Aflatoxin B1 in affecting broilers performance, immunity, and gastrointestinal tract: A review of history and contemporary issues. Toxins. 3:566-590.