Abstract
The effect of dietary aflatoxin B1 (AFB1) and Salmonella Enteritidis infection on intestinal permeability was investigated. Two hundred 1-day-old male Ross 308 broiler chickens were randomly divided into 4 treatments of 5 replicates each (10 birds per replicate), which were fed ad libitum for 3 weeks with the following treatments: control, chickens fed an AFB1-free diet; AF, chickens fed an AFB1-contaminated diet at 470 ng/g; SE, chickens fed an AFB1-free diet and challenged with 108 cfu of S. Enteritidis per bird at 18 days old; AF + SE, chickens fed an AFB1-contaminated diet and challenged with 108 cfu of S. Enteritidis per bird at 18 days old. At day 21 of age, chicks received an oral gavage dose of fluorescein isothiocyanate dextran (FITC-dextran) to evaluate gastrointestinal leakage. Blood and intestinal samples were collected to evaluate serum biochemistry and total intestinal IgA secretion, respectively. Liver tissues were aseptically collected to assess bacterial invasiveness and for histomorphological studies. The results showed that chickens receiving AFB1 presented a significant increment (up to 2.4-fold) in serum FITC-dextran concentration (p < 0.05). Nevertheless, S. Enteritidis infection had no additional effect on gastrointestinal leakage. Furthermore, the ingestion of AFB1 had no impact on the invasive potential of S. Enteritidis. These results suggest that moderate-dose AFB1 adversely affects intestinal barrier function resulting in increased gut permeability in broiler chickens.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12550-019-00367-7/MediaObjects/12550_2019_367_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs12550-019-00367-7/MediaObjects/12550_2019_367_Fig2_HTML.png)
Similar content being viewed by others
References
Asao T, Buchi G, Abdel-Kader M, Chang S, Wick EL, Wogan G (1963) Aflatoxins B and G. J Am Chem Soc 85:1706–1707
Awad W, Hess C, Hess M (2017) Enteric pathogens and their toxin-induced disruption of the intestinal barrier through alteration of tight junctions in chickens. Toxins 9:60
Baxter MF, Merino-Guzman R, Latorre JD, Mahaffey BD, Yang Y, Teague KD, Graham LE, Wolfenden AD, Hernandez-Velasco X, Bielke LR, Hargis BM, Tellez G (2017) Optimizing fluorescein isothiocyanate dextran measurement as a biomarker in a 24-h feed restriction model to induce gut permeability in broiler chickens. Front Vet Sci 4:56
Burel C, Tanguy M, Guerre P, Boilletot E, Cariolet R, Queguiner M, Postolec G, Pinton P, Salvat G, Oswald IP, Fravalo P (2013) Effect of low dose of fumonisins on pig health: immune status, intestinal microbiota and sensitivity to Salmonella. Toxins 5:841–864
Cesaro C, Tiso A, Del Prete A, Cariello R, Tuccillo C, Cotticelli G, del Vecchio Blanco C, Loguercio C (2011) Gut microbiota and probiotics in chronic liver diseases. Dig Liver Dis 43:431–438
Chen X, Naehrer K, Applegate T (2016) Interactive effects of dietary protein concentration and aflatoxin B1 on performance, nutrient digestibility, and gut health in broiler chicks. Poult Sci 95:1312–1325
Coenen A, Smit A, Zhonghua L, Van Luijtelaar G (2000) Gas mixtures for anaesthesia and euthanasia in broiler chickens. Worlds Poult Sci J 56:226–234
del Pilar Monge M, Magnoli CE, Chiacchiera SM (2012) Survey of Aspergillus and Fusarium species and their mycotoxins in raw materials and poultry feeds from Córdoba, Argentina. Mycotoxin Res 28:111–122
Feibelman TP, Cotty PJ, Doster M, Michailides T (1998) A morphologically distinct strain of Aspergillus nomius. Mycologia 90:618–623
Galarza-Seeber R, Latorre JD, Bielke LR, Kuttappan VA, Wolfenden AD, Hernandez-Velasco X, Merino-Guzman R, Vicente JL, Donoghue A, Cross D, Hargis BM, Tellez G (2016) Leaky gut and mycotoxins: aflatoxin B1 does not increase gut permeability in broiler chickens. Front Vet Sci 3:10
Gratz S, Wu Q, El-Nezami H, Juvonen R, Mykkänen H, Turner P (2007) Lactobacillus rhamnosus strain GG reduces aflatoxin B1 transport, metabolism, and toxicity in Caco-2 cells. Appl Environ Microbiol 73:3958–3964
Grenier B, Applegate T (2013) Modulation of intestinal functions following mycotoxin ingestion: meta-analysis of published experiments in animals. Toxins 5:396–430
Hernández-Meléndez D, Salas-Téllez E, Zavala-Franco A, Téllez G, Méndez-Albores A, Vázquez-Durán A (2018) Inhibitory effect of flower-shaped zinc oxide nanostructures on the growth and aflatoxin production of a highly toxigenic strain of Aspergillus flavus Link. Materials 11:1265
Hernandez-Patlan D, Solis-Cruz B, Adhikari B, Pontin KP, Latorre JD, Baxter MF, Hernandez-Velasco X, Merino-Guzman R, Méndez-Albores A, Kwon YM, Hargis BM, Lopez-Arellano R, Arreguin-Nava MA, Tellez-Isaias G (2019) Evaluation of the antimicrobial and intestinal integrity properties of boric acid in broiler chickens infected with Salmonella enteritidis: proof of concept. Res Vet Sci 123:7–13
Husáková E, Bobíková K, Stašová D (2015) Total IgA in spleen, bursa and intestine of chickens pretreated with E. faecium AL41 and challenged with Salmonella Enteritidis PT4. Food Agric Immunol 26:366–370
Ilan Y (2012) Leaky gut and the liver: a role for bacterial translocation in nonalcoholic steatohepatitis. World J Gastroenterol 18:2609
Jardon-Xicotencatl S, Díaz-Torres R, Marroquín-Cardona A, Villarreal-Barajas T, Méndez-Albores A (2015) Detoxification of aflatoxin-contaminated maize by neutral electrolyzed oxidizing water. Toxins 7:4294–4314
Jiang M, Fang J, Peng X, Cui H, Yu Z (2015) Effect of aflatoxin B1 on IgA+ cell number and immunoglobulin mRNA expression in the intestine of broilers. Immunopharmacol Immunotoxicol 37:450–457
Kasuga F, Hara-Kudo Y, Saito N, Kumagai S, Sugita-Konishi Y (1998) In vitro effect of deoxynivalenol on the differentiation of human colonic cell lines Caco-2 and T84. Mycopathologia 142:161–167
Kubena LF, Huff WE, Harvey RB, Phillips TD, Rottinghaus GE (1989) Individual and combined toxicity of deoxynivalenol and T-2 toxin in broiler chicks. Poult Sci 68:622–626
McLaughlin J, Padfield PJ, Burt JP, O'Neill CA (2004) Ochratoxin A increases permeability through tight junctions by removal of specific claudin isoforms. Am J Phys Cell Physiol 287:C1412–C1417
Méndez-Albores A, Arambula-Villa G, Loarca-Piña M, Castano-Tostado E, Moreno-Martínez E (2005) Safety and efficacy evaluation of aqueous citric acid to degrade B-aflatoxins in maize. Food Chem Toxicol 43:233–238
Merino-Guzmán R, Latorre JD, Delgado R, Hernandez-Velasco X, Wolfenden AD, Teague KD, Graham LE, Mahaffey BD, Baxter MFA, Hargis BM, Tellez G (2017) Comparison of total immunoglobulin A levels in different samples in Leghorn and broiler chickens. Asian Pac J Trop Biomed 7:116–120
Nacional Research Council, (NRC) (1994) Nutrient requirements of chickens. In: Nutrient requirements of poultry. 8th rev. National Academy Press, Washington DC, pp 11–15
Norma Oficial Mexicana NOM-188-SSA1-2002 Productos y Servicios: Control de aflatoxinas en cereales para consumo humano y animal, especificaciones sanitarias. Diario Oficial de la Federacion. 2002:11 de Marzo de 1999.
Ostry V, Malir F, Toman J, Grosse Y (2017) Mycotoxins as human carcinogens—the IARC monographs classification. Mycotoxin Res 33:65–73
Overman EL, Rivier JE, Moeser AJ (2012) CRF induces intestinal epithelial barrier injury via the release of mast cell proteases and TNF-α. PLoS One 7:e39935
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
Raju M, Rao S, Radhika K, Chawak M (2005) Dietary supplementation of Spirulina and its effects on broiler chicken exposed to aflatoxicosis. Indian J Poult Sci 40:36–40
Rawal S, Kim JE, Coulombe R Jr (2010) Aflatoxin B1 in poultry: toxicology, metabolism and prevention. Res Vet Sci 89:325–331
Romero A, Ares I, Ramos E, Castellano V, Martínez M, Martínez-Larrañaga MR, Anadón A, Martínez MA (2016) Mycotoxins modify the barrier function of Caco-2 cells through differential gene expression of specific claudin isoforms: protective effect of illite mineral clay. Toxicology 353:21–33
Sapcota D, Islam R, Upadhyaya T (2006) Dietary supplementation of Emblica officinalis for amelioration of experimental aflatoxicosis in commercial broilers. Anim Nutr Feed Technol 6:65–71
SAS Institute (2002) SAS/STAT User’s guide release 9.0 edition. SAS institute, Cary
Seki E, Schnabl B (2012) Role of innate immunity and the microbiota in liver fibrosis: crosstalk between the liver and gut. J Physiol 590:447–458
Sergent T, Parys M, Garsou S, Pussemier L, Schneider YJ, Larondelle Y (2006) Deoxynivalenol transport across human intestinal Caco-2 cells and its effects on cellular metabolism at realistic intestinal concentrations. Toxicol Lett 164:167–176
Tejada-Castaneda Z, Avila-Gonzalez E, Casaubon-Huguenin M, Cervantes-Olivares R, Vásquez-Peláez C, Hernandez-Baumgarten E, Moreno-Martínez E (2008) Biodetoxification of aflatoxin-contaminated chick feed. Poult Sci 87:1569–1576
Vicuña EA, Kuttappan VA, Tellez G, Hernandez-Velasco X, Seeber-Galarza R, Latorre JD, Faulkner OB, Wolfenden AD, Hargis BM, Bielke LR (2015) Dose titration of FITC-D for optimal measurement of enteric inflammation in broiler chicks. Poult Sci 94:1353–1359
Weibking TS, Ledoux DR, Bermudez AJ, Turk JR, Rottinghaus GE, Wang E, Merrill AH 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
Acknowledgments
J.O. Hernández-Ramírez acknowledges CONACyT for the Ph.D. scholarship (245747).
Funding
This work was partially supported by Programa Interno de Apoyo para Proyectos de Investigacion (PIAPI) Grant number PIAPI-1806.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
None.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hernández-Ramírez, J.O., Nava-Ramírez, M.J., Merino-Guzmán, R. et al. The effect of moderate-dose aflatoxin B1 and Salmonella Enteritidis infection on intestinal permeability in broiler chickens. Mycotoxin Res 36, 31–39 (2020). https://doi.org/10.1007/s12550-019-00367-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12550-019-00367-7