doi: 10.15389/agrobiology.2024.5.847eng
UDC: 619:615.9:636.085.19
PROSPECTS OF ANALYTICAL APPROACH FOR DIAGNOSTICS OF ANIMAL MYCOTOXICOSES (review)
G.P. Kononenko ✉, E.V. Zotova
All-Russian Research Institute of Veterinary Sanitation, Hygiene, and Ecology — Branch of FSC ARRIEV RAS, 5, Zvenigorodskoe sh., Moscow, 123022 Russia, e-mail kononenkogp@mail.ru (✉ corresponding author), zotelena63@gmail.com
ORCID:
Kononenko G.P. orcid.org/0000-0002-9144-615X
Zotova E.V. orcid.org/0000-0002-1479-8602
Final revision received April 02, 2024
Accepted June 05, 2024
Outbreaks of animal intoxication from the consumption of feed containing mycotoxins remain the most important problem of animal husbandry (M.M. Zaki et al., 2012; C. Gruber-Dorninger et al., 2019). At the end of the last century and in the next two decades, world science made significant progress in studying the mechanisms of action of these natural toxicants and obtained convincing evidence of the possibility of using mycotoxins and their metabolites as biochemical markers to confirm the fact of entry into the body of animals (L. Escrivá et al., 2017; A. Vidal et al., 2018). In our country a national database on the occurrence and content of mycotoxins in feed is being actively formed (G.P. Kononenko et al., 2020), however, the problem of differentiation of mycogenic intoxication in animals still remains unresolved. Recommended diagnostic schemes, based on epizootological data, clinical picture, pathoanatomic changes, results of histological, mycotoxicological studies and experimental reproduction of intoxications (MU, 1985, 1986), do not allow unambiguously and timely determination of their cause.This review provides up-to-date information necessary for the development of analytical methods for the diagnosis of toxicosis caused by 4-deoxynivalenol (DON), T-2 toxin (T-2), zearalenone (ZEN), fumonisin B1 (FB1) and ochratoxin A (OA). The main ways of their transformation in vivo in pigs, ruminants, poultry are discussed and information about metabolites in biological fluids and excreta suitable for in vivo diagnostics is summarized. The use of high-performance liquid chromatography in combination with mass spectrometric detection made it possible to identify DON, deepoxy-DON and their glucuronides in the blood and urine of pigs and ruminants (H.E. Schwartz-Zimmermann et al., 2017), DON, deepoxy-DON and DON sulfate in the blood and droppings of poultry (I. Riahi et al., 2021), clarify the nature of multiple metabolism of T-2 (E. Janin et al., 2021) and ZEN (P. Llorens et al., 2022), and confirm the free-form presence of FB1 in faeces of pigs (P. Dilkin et al., 2010), and OA in poultry droppings. An important achievement in recent years has been the experimental evidence of the correlation between the doses of DON and ZEN coming from feed and the content of indicator substances in target matrices in dairy cows (J. Winkler et al., 2014, 2015) and pigs (L. Gambacorta et al., 2013; S. Thanner et al., 2016; T. Van Limbergen et al., 2017). Schemes based on chromatographic and enzyme immunoassay are already used to control biomarkers of these toxins on livestock farms in Japan (M. Tagaki et al., 2011; H. Hasunuma et al., 2012; O.S. Widodo et al., 2022). Priority areas for the development of the analytical approach include the improvement and development of alternative methods, clarification of sample preparation conditions and sampling procedures, synthesis and certification of calibrants necessary for quantitative measurements, as well as exploring the possibility of using other matrices, in particular, hair and feather cover, for diagnostic purposes.
Keywords: 4-deoxynivalenol, T-2 toxin, zearalenone, fumonisin B1, ochratoxin A, biomarkers, mycotoxicoses, diagnostics.
REFERENCES
- Miller J.D. Mycotoxins in food and feed: a challenge for the twenty-first century. In: Biology of microfungi. D.-W. Li (ed.). Springer Link, 2016: 469-493 CrossRef
- Tola M., Kebede B. Occurrence, importance and control of mycotoxins: a review. Cogent Food & Agriculture, 2016, 2(1): 1191103 CrossRef
- Ali S., Freire L.G.D., Rezende V.T., Norman M., Ullah S., Abdullah, Badshah G., Afridi M.S., Tonin F.G., De Oliveira C.A.F. Occurrence of mycotoxins in foods: unraveling the knowledge gaps on their persistence in food production systems. Foods, 2023, 12, 4314 CrossRef
- Escrivá L., Font G., Manyes L., Berrada H. Studies on the presence of mycotoxins in biological samples: An overview. Toxins, 2017, 9(8): 251 CrossRef
- Schelstraete W., Devreese M., Croubels S. Comparative toxicokinetics of Fusarium mycotoxins in pigs and humans. Food and Chemical Toxicology, 2020, 137: 111140 CrossRef
- Sun Y., Jiang J., Mu R., Lin R., Wen J., Deng Y. Toxicokinetics and metabolism of deoxynivalenol in animals and humans. Archives of Toxicology, 2022, 96(10): 2639-2654 CrossRef
- Turner P.C., Flannery B., Isitt C., Ali M., Pestka J. The role of biomarkers in evaluating human health concerns from fungal contaminants in food. Nutrition Research Reviews, 2012, 25(1): 162-179 CrossRef
- Vidal A., Mengelers M., Yang Sh., De Saeger S., De Boerve M. Mycotoxin biomarkers of exposure: A comprehensive review. Comprehensive Reviews in Food Science and Food Safety, 2018, 17(5): 1127-1155 CrossRef
- Marín S., Ramos A.J., Sanchis V., Cano-Sancho G. An overview of mycotoxin biomarker application in exposome-health studies. Current Opinion in Food Science, 2021, 39: 31-35 CrossRef
- Gambacorta L., Pinton P., Avantaggiato G., Oswald I.P., Solfrizzo M. Grape pomace, an agricultural byproduct reducing mycotoxin absorption: in vivo assessment in pig using urinary biomarkers. Journal of Agricultural and Food Chemistry, 2016, 64(35): 6762-6771 CrossRef
- Lauwers M., Croubels S., Letor B., Gougoulias C., Devreese M. Biomarkers of exposure as a tool for efficacy testing of a mycotoxin detoxifier in broiler chicken and pigs. Toxins, 2019, 11(4): 187 CrossRef
- Ji J., Yu J., Ye Y., Sheng L., Fang J., Yang Y., Sun X. Biodegradation methods and product analysis of zearalenone and its future development trend: a review. Food Control, 2023, 145: 109469 CrossRef
- Fushimi Y., Takagi M., Hasunuma H., Uno S., Kokushi E., Watanabe U., Liu J., Marey M.A., Miyamoto A., Otoi T., Deguchi E., Fink-Gremmels J. Application of mycotoxin adsorbent to cattle feed contaminated with zearalenone: urinary zearalenone excretion and association with anti-Müllerian hormone. World Mycotoxin Journal, 2014, 7(3): 367-378 CrossRef
- Winkler J., Kersten S., Meyer U., Stinshoff H., Locher L., Rehage J., Wrenzycki C., Engelhardt U.H., Dänicke S. Diagnostic opportunities for evaluation of the exposure of dairy cows to the mycotoxins deoxynivalenol (DON) and zearalenone (ZEN): reliability of blood plasma, bile and follicular fluid as indicators. Journal of Animal Physiology and Animal Nutrition, 2015, 99(5): 847-855 CrossRef
- Takagi M., Uno S., Kokushi E., Sato F., Wijayagunawardane M.M.P., Fink-Gremmels J. Measurement of urinary concentrations of the mycotoxins zearalenone and sterigmatocystin as biomarkers of exposure in mares. Reproduction in Domestic Animals, 2018, 53(1): 68-73 CrossRef
- Zaki M.M., El-Midani S.A., Shaheen H.M., Rizzi L. Mycotoxins in animals: occurrence, effects, prevention and management. Journal of Toxicology and Environmental Health Sciences, 2012, 4(1): 13-28 CrossRef
- Gruber-Dorninger C., Jenkins T., Schatzmayr G. Global mycotoxin occurrence in feed: a ten year survey. Toxins, 2019, 11: 375 CrossRef
- Kononenko G.P., Burkin A.A., Zotova E.V. Veterinariya segodnya, 2020, 1(32): 60-65 CrossRef (in Russ.).
- Kononenko G.P., Burkin A.A., Zotova E.V. Veterinariya segodnya, 2020, 2(33): 139-145 CrossRef (in Russ.).
- Kononenko G.P., Burkin A.A., Zotova E.V. Veterinariya segodnya, 2020, 3(34): 213-219 CrossRef (in Russ.).
- Rekomendatsii po diagnostike i profilaktike okhratoksikoza u sviney. Utv. GUV MSKh SSSR ot 21.03.1985 g. [Recommendations for the diagnosis and prevention of ochratoxicosis in pigs. Approved by the Main Directorate of the Ministry of Agriculture of the USSR on 03/21/1985] (in Russ.).
- Metodicheskie ukazaniya po diagnostike i profilaktike zearalenontoksikoza sviney i ptits. Utv. GUV MSKh SSSR ot 5.12.1985 g. [Guidelines for the diagnosis and prevention of zearalenone toxicosis in pigs and birds. Approved by the Main Directorate of the Ministry of Agriculture of the USSR on 12/5/1985](in Russ.).
- Metodicheskie ukazaniya po diagnostike i profilaktike patulinotoksikoza u sviney. Utv. GUV MSKh SSSR ot 28.06.1986 g. [Guidelines for the diagnosis and prevention of patulinotoxicosis in pigs. Approved by the Main Directorate of the Ministry of Agriculture of the USSR on 06/28/1986](in Russ.).
- Pestka J.J. Deoxynivalenol: toxicity, mechanisms and animal health risks. Animal Feed Science and Technology, 2007, 137(3-4): 283-298 CrossRef
- Kuca K., Dohnal V., Jezkova A., Jun D. Metabolic pathways of T-2 toxin. Current Drug Metabolism, 2008, 9(1): 77-82 CrossRef
- Zinedine A., Soriano J.M., Moltó J.C., Mañes J. Review on the toxicity, occurrence, metabolism, detoxication, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food and Chemical Toxicology, 2007, 45(1): 1-18 CrossRef
- Shephard G.S., Van Der Westhuizen L., Sewram V. Biomarkers of exposure to fumonisin mycotoxins: a review. Food Additives & Contaminants, 2007, 24(10): 1196-1201 CrossRef
- Ringot D., Chango A., Schneider Y.-J., Larondelle Y. Toxicokinetics and toxicodynamics of ochratoxin A, an update. Chemico-Biological Interactions, 2006, 159(1): 18-46 CrossRef
- Dänicke S., Valenta H., Döll S. On the toxicokinetics and the metabolism of deoxynivalenol (DON) in the pig. Archives of Animal Nutrition, 2004, 58(2): 169-180 CrossRef
- Broekaert N., Devreese M., Van Bergen T., Schauvliege S., De Boevre M., De Saeger S., Vanhaecke L., Berthiller F., Michlmayr H., Malachová A., Adam G., Vermeulen A., Croubels S. In vivo contribution of deoxynivalenol-3-β-D-glucoside to deoxynivalenol exposure in broiler chickens and pigs: oral bioavailability, hydrolysis and toxicokinetics. Archives of Toxicology, 2017, 91: 699-712 CrossRef
- Dänicke S., Goyarts T., Valenta H., Razzazi E., Böhm J. On the effects of deoxynivalenol (DON) in pig feed on growth performance, nutrients utilization and DON metabolism. Journal of Animal and Feed Sciences, 2004, 13(4): 539-556 CrossRef
- Dänicke S., Brüssow K.-P., Valenta H., Ueberschär K.-H., Tiemann U., Schollenberger M. On the effects of graded levels of Fusarium toxin contaminated wheat in diets for gilts on feed intake, growth performance and metabolism of deoxynivalenol and zearalenone. Molecular Nutrition & Food Research, 2005, 49(10): 932-943 CrossRef
- Brezina U., Rempe I., Kersten S., Valenta H., Humpf H.U., Dänicke S. Diagnosis of intoxications of piglets fed with Fusarium toxin contaminated maize by the analysis of mycotoxin residues in serum, liquor and urine with LC-MS/MS. Archives of Animal Nutrition, 2014, 68(6): 425-447 CrossRef
- Van Limbergen T., Devreese M., Croubels S., Broekaert N., Michiels A., De Saeger S., Maes D. Role of mycotoxins in herds with and without problems with tail necrosis in neonatal pigs. Veterinary Record, 2017, 181(20): 539 CrossRef
- Dänicke S., Valenta H., Klobasa F., Döll S., Ganter M., Flachowsky G. Effects of graded levels of Fusarium toxin contaminated wheat in diets for fattening pigs on growth performance, nutrient digestibility, deoxynivalenol balance and clinical serum characteristics. Archives of Animal Nutrition, 2004, 58(1): 1-17 CrossRef
- Nagl V., Woechtl B., Schwartz-Zimmermann H.E., Henning-Pauka I., Moll W.-D., Adam G., Berthiller F. Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in pigs. Toxicology Letters, 2014, 229(1): 190-197 CrossRef
- Schwartz-Zimmermann H.E., Hametner C., Nagl V., Fiby I., Macheiner L., Winkler J., Dänicke S., Clark E., Pestka J.J., Berthiller F. Glucuronidation of deoxynivalenol (DON) by different animal species: identification of iso-DON glucuronides and iso-epoxy-DON glucuronides as novel DON metabolites in pigs, rats, mice, and cows. Archives of Toxicology, 2017, 91(12): 3857-3872 CrossRef
- Valgaeren B., Théron L., Croubels S., Devreese M., De Baere S., Van Pamel E., Daeseleire E., De Boevre M., De Saeger S., Vidal A., Di Mavundu J.D., Fruhmann P., Adam G., Callebaut A., Bayrou C., Frisée V., Rao A.-S., Knapp E., Sartelet A., Pardon B., Deprez P., Antonissen G. The role of roughage provision on the absorption and disposition of the mycotoxin deoxynivalenol and its acetylated derivatives in calves: from field observations to toxicokinetics. Archives of Toxicology, 2019, 93(2): 293-310 CrossRef
- Seeling K., Dänicke S., Valenta H., Van Egmond H.P., Schothorst R.C., Jekel A.A., Lebzien P., Schollenberger M., Razzazi-Fazeli E., Flachowsky G. Effects of Fusarium toxin-contaminated wheat and feed intake level on the biotransformation and carry-over of deoxynivalenol in dairy cows. Food Additives and Contaminants, 2006, 23(10): 1008-1020 CrossRef
- Keese C., Meyer U, Valenta H., Schollenberger M., Starke A., Weber I.-A., Rehage J., Breves G., Dänicke S. No carry over of unmetabolised deoxynivalenol in milk of dairy cows fed high concentrate proportions. Molecular Nutrition & Food Research, 2008, 52(12): 1514-1529 CrossRef
- Winkler J., Kersten S., Meyer U., Engelhardt U., Dänicke S. Residues of zearalenone (ZEN), deoxynivalenol (DON) and their metabolites in plasma of dairy cows fed Fusarium contaminated maize and their relationships to performance parameters. Food and Chemical Toxicology, 2014, 65: 196-204 CrossRef
- Wan D., Huang L., Pan Y., Wu Q., Chen D., Tao Y., Wang X., Liu Z., Li J., Wang L., Yuan Z. Metabolism, distribution, and excretion of deoxynivalenol with combined techniques of radiotracing, high-performance liquid chromatography ion trap time-of-flight mass-spectrometry, and online radiometric detection. Journal of Agricultural and Food Chemistry, 2014, 62(1): 288-296 CrossRef
- Devreese M., Antonissen G., Broekaert N., De Mil T., De Baere S., Vanhaecke I., De Backer P., Croubels S. Toxicokinetic study and oral bioavailability of deoxynivalenol in turkey poults, and comparative biotransformation between broilers and turkeys. World Mycotoxin Journal, 2015, 8(4): 533-539 CrossRef
- Schwartz-Zimmermann H.E., Fruhmann P., Dänicke S., Wiesenberger G., Caha S., Weber J., Berthiller F. Metabolism of deoxynivalenol and deepoxy-deoxynivalenol in broiler chickens, pullets, roosters and turkeys. Toxins, 2015, 7(11): 4706-4729 CrossRef
- Riahi I., Marquis V., Pérez-Vendrell A.M., Brufau J., Esteve-Garcia E., Ramos A.J. Effects of deoxynivalenol-contaminated diets on metabolic and immunological parameters in broiler chickens. Animals, 2021, 11(1): 147 CrossRef
- Dänicke S.,Valenta H., Ueberschär K.-H., Matthes S. On the interactions between Fusarium toxin-contaminated wheat and non-polysaccharide hydrolyzing enzymes in turkey diets on performance, health and carry-over of deoxynivalenol and zearalenone. British Poultry Science, 2007, 48(1): 39-48 CrossRef
- Osselaere A., Devreese M., Goossens J., Vandenbroucke V., Baere S.D., Backer P.D., Croubels S. Toxicokinetic study and absolute oral bioavailability of deoxynivalenol, T-2 toxin and zearalenone in broiler chickens. Food and Chemical Toxicology, 2013, 51(1): 350-355 CrossRef
- Riahi I., Ramos A.J., Pérez-Vendrell A.M., Marquis V. A toxicokinetic study reflecting the absorption, distribution, metabolism and excretion of deoxynivalenol in broiler chickens. Journal of Applied Animal Research, 2021, 49(1): 284-288 CrossRef
- Yunus A.W., Valenta H., Abdel-Raheem S.M., Döll S., Dänicke S., Böhm J. Blood plasma levels of deoxynivalenol and its de-epoxy metabolite in broilers after a single oral dose of the toxin. Mycotoxin Research, 2010, 26: 217-220 CrossRef
- Fruhmann P.,Warth B., Hametner C., Berthiller F., Horkel E., Adam G., Sulyok M., Krska R., Flöhlich J. Synthesis of deoxynivalenol-3-β-DO-glucuronide for its as biomarker for dietary deoxynivalenol exposure. World Mycotoxin Journal, 2012, 5(2): 127-132 CrossRef
- Uhlig S., Ivanova L., Faeste C.K. Enzyme-assisted synthesis and structural characterization of the 3-, 8-, and 15-glucuronides of deoxynivalenol. Journal of Agricultural and Food Chemistry, 2013, 61(8): 2006-2012 CrossRef
- Uhlig S., Ivanova L., Faeste C.K. Correction to enzyme-assisted synthesis and structural characterization of the 3-, 8-, and 15-glucuronides of deoxynivalenol. Journal of Agricultural and Food Chemistry, 2016, 64(18): 3732-3732 CrossRef
- Li Y., Wang Z., Beirer R.C., Shen J., De Smet D., De Saeger S., Zhang S. T-2 toxin, a trichothecene mycotoxin: review of toxicity, metabolism, and analytical methods. Journal of Agricultural abd Food Chemistry, 2011, 59(8): 3441-3453 CrossRef
- Sun Y., Zhang G., Zhao H., Znen J., Hu F., Fang B. Liquid chromatography-tandem mass spectrometry method for toxicokinetics, tissue distribution, and excretion studies of T-2 toxin and its major metabolites in pigs. Journal of Chromatography B, 2014, 958: 75-82 CrossRef
- Wu Q., Dohnal V., Huang L., Kuča K., Yuan Z. Metabolic pathways of trichothecenes. Drug Metabolism Reviews, 2010, 42(2): 250-267 CrossRef
- Sun Y.X., Yao X., Shi S.N., Zhang G.J., Xu L.X., Liu Y.J., Fang B.H. Toxicokinetics of T-2 toxin and its major metabolites in broiler chickens after intravenous and oral administration. Journal of Veterinary Pharmacology and Therapeutics, 2015, 38(1): 80-85 CrossRef
- Yang S., De Boevre M., Zhang H., De Ruyck K., Sun F., Zhang J., Jin Y., Li Y., Wang Z., Zhang S., Zhou J., Li Y., De Saeger S. Metabolism of T-2 toxin in farm animals and human in vitro and in chicken in vivo using ultra high-performance liquid chromatography-quadrupole/time-of-flight hybrid mass-spectrometry along with online hydrogen/deuterium exchange technique. Journal of Agricultural and Food Chemistry, 2017, 65(33): 7217-7227 CrossRef
- Janik E., Niemcewicz M., Podogrocki M., Ceremuga M., Stela M., Bijak M. T-2 toxin — the most toxic trichothecene mycotoxin: metabolism, toxicity, and decontamination strategies. Molecules, 2021, 26(22): 6868 CrossRef
- Liu J., Applegate T. Zearalenone (ZEN) in livestock and poultry: dose, toxicokinetics, toxicity and estrogenicity. Toxins, 2020, 12(6): 377 CrossRef
- Wu K., Ren C., Gong Y., Gao X., Rajput S.A., Qi D., Wand S. The insensitive mechanism of poultry to zearalenone: a review. Animal Nutrition, 2021, 7(3): 587-594 CrossRef
- Llorens P., Herrera M., Juan-García A., Payá J.J., Moltó J.C., Ariño A., Juan C. Biomarkers of exposure to zearalenone in in vivo and in vitro studies. Toxins, 2022, 14(5): 291 CrossRef
- Binder S.B., Schwartz-Zimmermann H.E., Varda E., Bichl G., Michlmayr H., Adam G., Berthiller F. Metabolism of zearalenone and its major modified forms in pigs. Toxins, 2017, 9(2): 56 CrossRef
- Goyarts T., Dänicke S., Valenta H., Ueberschär K.-H. Carry-over of Fusarium toxins (deoxynivalenol and zearalenone) from naturally contaminated wheat for the pig. Food Additives and Contaminants, 2007, 24(4): 369-380 CrossRef
- Brezina U., Valenta H., Rempe I., Kersten S., Humpf H.U., Dänicke S. Development of a liquid chromatography tandem mass spectrometry method for the simultaneous determination of zearalenone, deoxynivalenol and their metabolites in pig serum. Mycotoxin Research, 2014, 30: 171-186 CrossRef
- Fleck S.C., Churchwell M.I., Doerge D.R. Metabolism and pharmacokinetics of zearalenone following oral and intravenous administration in juvenile female pigs. Food and Chemical Toxicology, 2017, 106(part A): 193-201 CrossRef
- Catteuw A., Broekaert N., De Baere S., Lauwers M., Gasthuys E., Huybrechts B., Callebaut A., Ivanova L., Uhlig S., De Boevre M., De Saeger S., Gehring R., Devreese M., Croubels S. Insights into in vivo absolute oral bioavailability, biotransformation, and toxicokinetics of zearalenone, a-zearalenol, b-zearalenol, zearalenone-14-glucoside, and zearalenone-14-sulfate in pigs. Journal of Agricultural and Food Chemistry, 2019, 67(12): 3448-3458 CrossRef
- Catteuw A., Devreese M., De Baere S., Antonissen G., Huybrechts B., Ivanova L., Uhlig S., Martens A., De Saeger S., De Boevre M., Croubels S. Toxicokinetic studies in piglets reveal age-related differences in systemic exposure to zearalenone, zearalenone-14-glucoside, and zearalenone-14-sulfate. Journal of Agricultural and Food Chemistry, 2020, 68(29): 7757-7764 CrossRef
- Zöllner P., Jodlbauer J., Kleinova M., Kahlbacher H., Kuhn T., Hochsteiner W., Linder W. Concentration levels of zearalenone and its metabolites in urine, muscle tissue, and liver samples of pigs fed with mycotoxin-contaminated oats. Journal of Agricultural and Food Chemistry, 2002, 50(9): 2494-2501 CrossRef
- Döll S., Dänicke S., Ueberschär K.H., Valenta H., Schnurrbusch U., Ganter M., Klobasa F., Flachowsky G. Effects of graded levels of Fusarium toxin contaminated maize in diets for female weaned piglets. Archives of Animal Nutrition, 2003, 57(5): 311-334 CrossRef
- Seeling K., Dänicke S., Ueberschä K.H., Lebzien P., Flachowsky G. On the effects of Fusarium toxin-contaminated wheat and the feed intake level on the metabolism and carry over of zearalenone in dairy cows. Food Additives and Contaminants, 2005, 22(9): 847-855 CrossRef
- Dänicke S., Keese C., Meyer U., Starke A., Konoshita A., Rehage J. Zearalenone (ZEN) metabolism and residue concentrations in physiological specimens of dairy cows exposed long-term to ZEN-contaminated diets differing in concentrate feed proportions. Archives of Animal Nutrition, 2014, 68(6): 492-506 CrossRef
- Falkauskas R., Bakutis B, Jovaišiené J., Vaičiuliené G., Gerulis G., Kerziené S., Jacevičiené I., Jacevičius E., Baliukoniené V. Zearalenone and its metabolites in blood serum, urine, and milk of dairy cows. Animals, 2022, 12(13): 1651 CrossRef
- Kleinova M., Zöllner P., Kahlbacher H., Hochsteiner W., Lindner W. Metabolic profiles of the mycotoxin zearalenone and of the growth promoter zeranol in urine, liver, and muscle of heifers. Journal of Agricultural and Food Chemistry, 2002, 50(17): 4769-4776 CrossRef
- Winkler J., Kersten S., Valenta H., Hüther L., Meyer U., Engelhardt U., Dänicke S. Simultaneous determination of zearalenone, deoxynivalenol and their metabolites in bovine urine as biomarkers of exposure. World Mycotoxin Journal, 2015, 8(1): 63-74 CrossRef
- Mikula H., Hametner C., Berthiller F., Warth B., Krska R., Adam G., Fröhlich J. Fast and reproducible chemical synthesis of zearalenone-14-β,D-glucuronide. World Mycotoxin Journal, 2012, 5(3): 289-296 CrossRef
- De Andrés F., Zougagh M., Castañeda G., Ríos A. Determination of zearalenone and its metabolites in urine samples by liquid chromatography with electrochemical detection using a carbon nanotube-modified electrode. Journal of Chromatography A, 2008, 1212(1-2): 54-60 CrossRef
- Gutzwiller A., Gafner J.L., Silacci P. Urinary zearalenone measured with ELISA as biomarker of zearalenone exposure in pigs. Mycotoxin Research, 2014, 30(4): 187-190 CrossRef
- Takagi M., Uno S., Kokushi E., Shiga S., Mukai S., Kuriyagawa T., Takagaki K., Hasunuma H., Matsumoto D., Okamoto K., Shahada F., Chenga T., Deguchi E., Fink-Gremmels J. Measurement of urinary zearalenone concentrations for monitoring natural feed contamination in cattle herds: on-farm trials. Journal of Animal Sciences, 2011, 89(1): 287-296 CrossRef
- Hasunuma H., Takagi M., Kawamura O., Taniguchi C., Nakamura M., Chuma T., Uno S., Kokushi E., Matsumoto D., Tshering C., Deguchi E., Fink-Gremmels J. Natural contamination of dietary rice straw with zearalenone and urinary zearalenone concentrations in cattle herd. Journal of Animal Sciences, 2012, 90(5): 1610-1616 CrossRef
- Widodo O.S., Etoh M., Kokushi E., Uno S., Yamato O., Pambudi D., Okawa H., Taniguchi M., Lamid M., Takagi M. Practical application of urinary zearalenone monitoring system for feed hygiene management of a Japanese black cattle breeding herd – The relationship between monthly anti-Müllerian hormone and serum amyloid A concentrations. Toxins, 2022, 14(2): 143 CrossRef
- Devreese M., Antonissen G., Broekaert N., De Baere S., Vanhaecke I., De Backer P., Croubels S. Comparative toxicokinetics, absolute oral bioavailability, and biotransformation of zearalenone in different poultry species. Journal of Agricultural and Food Chemistry, 2015, 63(20): 5092-5098 CrossRef
- Buranatragool K., Poapolathep S., Isariyodom S., Imsilp K., Klangkaew N., Poapolathep A. Dispositions and tissue residue of zearalenone and its metabolites a-zearalenol and β-zearalenol in broilers. Toxicology Reports, 2015, 2: 351-356 CrossRef
- Yang S., Zhang H., Sun F., De Ruyck K., Zhang J., Jin Y., Li Y., Wang Z., Zhang S., De Saeger S., Zhou J., Li Y., De Boevre M. Metabolic profile of zearalenone in liver microsomes from different species and its in vivo metabolism in rats and chickens using ultra-performance liquid chromatography-quadrupole/time-of-flight hybrid mass-spectrometry. Journal of Agricultural and Food Chemistry, 2017, 65(51): 11292-11303 CrossRef
- Gambacorta L., Solfrizzo M., Visconti A., Powers S., Cossalter A.M., Pinton P., Oswald I.P. Validation study on urinary biomarkers of exposure for aflatoxin B1, ochratoxin A, fumonisin B1, deoxynivalenol and zearalenone in piglets. World Mycotoxin Journal, 2013, 6(3): 299-308 CrossRef
- Dilkin P., Zorzete P., Mallmann C.A., Gomes J.D.F., Utiyama C.E., Oetting L.L., Corrêa B. Toxicological effects of chronic low doses of aflatoxin B1 and fumonisin B1-contaminating Fusarium moniliforme culture material in weaned piglets. Food and Chemical Toxicology, 2003, 41(10): 1345-1353 CrossRef
- Dilkin P., Direito G., Simas M.M.S., Mallmann C.A., Corrêa B. Toxicokinetics and toxicological effects of single oral dose of fumonisin B1 containing Fusarium verticilliodes culture material in weaned piglets. Chemico-Biological Interactions, 2010, 185(3): 157-162 CrossRef
- Souto P.C.M.C., Jager A.V., Tonin F.G., Petta T., Di Gregório M., Cossalter A.-M., Pinton P., Oswald I.P., Rottinghaus G.E., Oliveira C.A.F. Determination of fumonisin B1 levels in body fluids and hair from piglets fed fumonisin B1-contaminated diets. Food and Chemical Toxicology, 2017, 108(part A): 1-9 CrossRef
- Guere P. Fusariotoxins in avian species: toxicokinetics, metabolism and persistence in tissues. Toxins, 2015, 7(6): 2289-2305 CrossRef
- Fodor J., Balogh K., Weber M., Mézes M., Kametler L., Pósa R., Mamet R., Bauer J.M., Horn P., Kovács F., Kovács M. Absorption, distribution and elimination of fumonisin B1 metabolites in weaned piglets. Food Additives and Contaminants, 2008, 25(1): 88-96 CrossRef
- Schertz H., Dänicke S., Frahm J., Schatzmayr D., Dohnal I., Bichl G., Schwartz-Zimmermann H.E., Colicchia S., Breves G., Teifke J.P., Kluess J. Biomarker evaluation and toxic effects of an acute oral and systemic fumonisin exposure of pigs with a special focus on dietary fumonisin esterase supplementation. Toxins, 2018, 10(7): 296 CrossRef
- Antonissen G., De Baere S., Novak B., Schatzmayr D., den Hollander D., Devreese M., Croubels S. Toxicokinetics of hydrolyzed fumonisin B1 after single oral or intravenous bolus to broiler chickens fed a control or a fumonisins-contaminated diet. Toxins, 2020, 12(6): 413 CrossRef
- Ominski K.H., Frohlich A.A., Marquardt R.R., Crow G.H., Abramson D. The incidence and distribution of ochratoxin A in western Canadian swine. Food Additives and Contaminants, 1996, 13(2): 185-198 CrossRef
- Höhler D., Südekum K.-H., Wolffram S., Frohlich A.A., Marquardt R.R. Metabolism and excretion of ochratoxin A fed to sheep. Journal of Animal Science, 1999, 77(5): 1217-1223 CrossRef
- Yang S., Zhang H., De Saeger S., De Boevre M., Sun F., Zhang S., Wang Z. In vitro and in vivo metabolism of ochratoxin A: A comparative study of using ultra-performance liquid chromatography-quadrupole/time-of-flight hybrid mass-spectrometry. Analytical and Bioanalytical Chemistry, 2015, 407(13): 3579-3589 CrossRef
- Dekant R., Langer M., Lupp M., Chilaka C.A., Mally A. In vitro and in vivo analysis of ochratoxin A-derived glucuronides and mercapturic acids as biomarkers of exposure. Toxins, 2021, 13(8): 587 CrossRef
- Solfizzo M., Gambacorta L., Lattanzio V.M.T., Powers S., Visconti A. Simultaneous LS-MS/MS determination of aflatoxin M1, ochratoxin A, deoxynivalenol, de-epoxydeoxynivalenol, a and β-zearalenols and fumonisin B1 in urine as multi-biomarker method to assess exposure to mycotoxins. Analytical and Bioanalytical Chemistry, 2011, 401(9): 2831-2841 CrossRef
- Tkaczyk A., Jedziniak P., Zielonka Ł., Dąbrowski M., Ochodzki P., Rudawska A. Biomarkers of deoxynivalenol, citrinin, ochratoxin A and zearalenone in pigs after exposure to naturally contaminated feed close to guidance values. Toxins, 2021, 13(11): 750 CrossRef
- Thanner S., Czeglédi L., Schwartz-Zimmermann H.E., Bertthiller F., Gutzwiller A. Urinary deoxynivalenol (DON) and zearalenone (ZEA) as biomarkers of DON and ZEA exposure of pigs. Mycotoxin Research, 2016, 32(2): 69-75 CrossRef
- Schulz A.-K., Kersten S., Dänicke S., Coenen M., Vervuert I. Effects of deoxynivalenol in natural contaminated wheat on feed intake and health status of horses. Mycotoxin Research, 2015, 31(4): 209-216 CrossRef
- Gambacorta L., Olsen M., Solfrizzo M. Pig urinary concentration of mycotoxins and metabolites reflects regional differences, mycotoxin intake and feed contaminations. Toxins, 2019, 11(7): 378 CrossRef
- Valenta H. Chromatographic methods for the determination of ochratoxin A in animal and human tissues and fluids. Journal of Chromatography A, 1998, 815(1): 75-92 CrossRef
- Razzazi-Fazeli E., Böhm J., Jarukamjorn K., Zentek J. Simultaneous determination of major B-trichothecenes and the de-epoxy-metabolite of deoxynivalenol in pig urine and maize using high-performance liquid chromatography—mass spectrometry. Journal of Chromatography B, 2003, 796(1): 21-33 CrossRef
- Thieu N.Q., Pettersson H. Zearalenone, deoxynivalenol and aflatoxin B1 and their metabolites in pig urine as biomarkers for mycotoxin exposure. Mycotoxin Research, 2009, 25(2): 59-66 CrossRef
- Song S., Ediage E.N., Wu A., De Saeger S. Development and application of salting-out assisted liquid/liquid extraction for multi-mycotoxin biomarkers analysis in pig urine with high performance liquid chromatography/tandem mass spectrometry. Journal of Chromatography A, 2013, 1292: 111-120 CrossRef
- Guo W.R., Ou S.X., Long W.P., Wei Z., Yan X., Yu L. Simultaneous detection method for mycotoxins and their metabolites in animal urine by using impurity absorption purification followed by liquid chromatography-tandem mass detection. Journal of Chromatography & Separation Techniques, 2015, 6(7): 1 CrossRef
- De Baere S., Goossens J., Osselaere A., Devreese M., Vandenbroucke V., De Backer P., Croubels S. Quantitative determination of T-2 toxin, HT-2 toxin, deoxynivalenol and deepoxy-deoxynivalenol in animal body fluids using LC-MS/MS detection. Journal of Chromatography B,2011, 879(24): 2403-2415 CrossRef
- De Baere S., Osselaere A., Devreese M., Vanhaecke L., De Backer P., Croubels S. Development of a liquid-chromatography tandem mass spectrometry and ultra-high-performance liquid chromatography high-resolution mass spectrometry method for the quantitative determination of zearalenone and its major metabolites in chicken and pig plasma. Analytica Chimica Acta,2012, 756: 37-48 CrossRef
- Devreese M., De Baere S., De Backer P., Croubels S. Quantitative determination of several toxicological important mycotoxins in pig plasma using multi-mycotoxin and analyte-specific high performance liquid chromatography-tandem mass spectrometric methods. Journal of Chromatography A, 2012, 1257: 74-80 CrossRef
- Lauwers M., De Baere S., Letor B., Rychlik M., Croubels S., Devreese M. Multi LC-MS/MS and LC-HRMS methods for determination of 24 mycotoxins including major phase I and II biomarker metabolites in biological matrices from pigs and broiler chickens. Toxins, 2019, 11(3): 171 CrossRef
- Hermanson G.T. Bioconjugate techniques. Academic Press, San Diego-New York-Boston-London-Sydney-Tokyo-Toronto, 1996.
- Tkaczyk A., Jedziniak P. Dilute-and-shoot HPLC-UV method for determination of urinary creatinine as a normalization tool in mycotoxin biomonitoring in pigs. Molecules, 2020, 25(10), 2445 CrossRef
- Shvab K. Zhivotnovodstvo Rossii, 2015, 1: 50-52 (in Russ.).
- Burkin A.A., Kononenko G.P., Soboleva N.A. Baltic Journal of Laboratory Animal Science, 2001, 11(4): 160-167 (in Russ.).
- Burkin A.A., Kononenko G.P. Uspekhi meditsinskoy mikologii, 2003, 1: 124-127 (in Russ.).
- Kononenko G.P., Burkin A.A., Zotova E.V., Soboleva N.A. Prikladnaya biokhimiya i mikrobiologiya, 1999, 35(2): 206-211 (in Russ.).
- Burkin A.A., Kononenko G.P. Immunopatologiya, allergologiya, infektologiya, 2010, 1: 187 (in Russ.).
- Burkin A.A., Kononenko G.P., Soboleva N.A. Prikladnaya biokhimiya i mikrobiologiya, 2002, 38(2): 194-202 (in Russ.).
- TR TS 015/2011 Tekhnicheskiy reglament Tamozhennogo soyuza «O bezopasnosti zerna» (s izmeneniyami na 15 sentyabrya 2017 goda): utv. resheniem Komissii Tamozhennogo soyuza ot 09.12.2011. № 874 [TR CU 015/2011 Technical Regulations of the Customs Union "On Grain Safety" (as amended on September 15, 2017): approved by the decision of the Customs Union Commission dated December 9, 2011. № 874]. Available: http://docs.cntd.ru/document/902320395. No date (in Russ.).
- Tkaczyk A., Jedziniak P. Development of a multi-mycotoxin LC-MS/MS method for the determination of biomarkers in pig urine. Mycotoxin Research, 2021, 37(2): 169-181 CrossRef
- Vertiprakhov V.G., Grozina A.A., Yildirim E.A., Gogina N.N., Kislova I.V., Ovchinnikova N.V., Koshcheyeva M.V. Efficacy of a complex preparation to correct digestion in broiler chickens (Gallus gallus L.) in experimental mycotoxicosis. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2022, 57(4): 730-742 CrossRef
- Yildirim E.A., Grozina A.A., Vertiprakhov V.G., Ilina L.A., Filippova V.A., Laptev G.Y., Ponomareva E.S., Dubrovin A.V., Kalitkina K.A., Molotkov V.V., Ahmatchin D.A., Brazhnik E.A., Novikova N.I., Tyurina D.G. Composition and metabolic potential of the intestinal microbiome of Gallus gallus L. broilers under experimental T-2 toxicosis as influenced by feed additives. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2022, 57(4): 743-761 CrossRef
- Charmley E., Trenholm H.L., Thompson B.K., Vudathala D., Nicholson J.W.G., Prelusky D.B., Charmley L.L. Influence of level of deoxynivalenol in the diet of dairy cows on feed intake, milk production, and its composition. Journal of Dairy Science, 1993, 76(11): 3580-3587 CrossRef
- Sayyari A., Uhlig S., Fæste C.K., Framstad T., Sivertsen T. Transfer of deoxynivalenol (DON) through placenta, colostrum and milk sows to their offspring during late gestation and lactation. Toxins, 2018, 10(12): 517 CrossRef
- Flores-Flores M.E., Lizarraga E., López de Cerain A., González-Peñas E. Presence of mycotoxins in animal milk: a review. Food Control, 2015, 53: 163-176 CrossRef
- Winkler J., Kersten S., Valenta H., Meyer U., Engelhardt U.H., Dänicke S. Development of a multi-toxin method for investigating the carryover of zearalenone, deoxynivalenol and their metabolites into milk of dairy cows. Food Additives & Contaminants: Part A, 2015, 32(3): 371-380.
- Fink-Gremmels J. Mycotoxins in cattle feeds and carry-over to dairy milk: a review. Food Additives & Contaminants: Part A, 2008, 25(2): 172-180 CrossRef
- Jurisic N., Schwartz-Zimmermann H.E., Kunz-Vekiru E., Reisinger N., Klein S., Caldwell D., Fruhmann P., Schatzmayr D., Berthiller F. Deoxynivalenol-3-sulphate is the major metabolite of dietary deoxynivalenol in eggs of laying hens. World Mycotoxin Journal, 2019, 12(3): 245-255 CrossRef
- Dänicke S., Ueberschär K.-H., Halle I., Matthes S., Valenta H., Flachowsky G. Effect of addition of a detoxing agent to laying hen diets containing uncontaminated or Fusarium toxin-contaminated maize on performance of hens and on carryover of zearalenone. Poultry Science, 2002, 81(11): 1671-1680 CrossRef
- Armorini S., Al-Qudah K.M., Altafini A., Zaghini A., Roncada P. Biliary ochratoxin A as a biomarker of ochratoxin exposure in laying hens: an experimental study after administration of contaminated diets. Research in Veterinary Science, 2015, 100: 265-270 CrossRef
- Gulyushin S.Yu., Kononenko G.P., Burkin A.A. Rossiyskiy zhurnal Problemy veterinarnoy sanitarii, gigieny i ekologii, 2011, 1(5): 73-76 (in Russ.).
- Ueberschär K.-H., Brezina U., Dänicke S. Zearalenone (ZEN) and ZEN metabolites in feed, urine and bile of sows: analysis, determination of the metabolic profile and evaluation of the binding forms. Applied Agricultural and Forestry Research, 2016, 66(1): 21-28 CrossRef
- Dänicke S., Brezina U. Kinetics and metabolism of the Fusarium toxin deoxynivalenol in farm animals: Consequences for diagnosis of exposure and intoxication and carry over. Food and Chemical Toxicology, 2013, 60: 58-75 CrossRef