Fumonisin mycotoxins: the effect of digestion on the different forms. Toxic effects and biological detoxification
Review
DOI:
https://doi.org/10.31914/aak.5167Keywords:
fumonisin, gastrointestinal tract, food matrix, digestion, bioaccessibilityAbstract
Mycotoxin contamination can occur at almost all levels of food production, processing, storage and distribution, and causes significant economic damage in animal husbandry, animal and crop production. Ingestion of foodborne mycotoxins can cause numerous diseases and health impairments. This review presents the different forms of fumonisin that can occur in foods and feeds, as well as the possible effects of digestion on these forms. The description of the toxicity of fumonisins includes the biochemical background, the different degree of toxicity of individual fumonisin metabolites, and the caused detrimental health effects on different species. The biological detoxification of mycotoxins has an advantage over physical and chemical methods with respect to nutrient losses, therefore this review focuses on the biological processes that can lead to the elimination of fumonisins. The presented methods involve bacterial binding and degradation that can promote the detoxification of fumonisins consumed with food or feed.
References
Andrade P.D. (2023): Dietary risk assessment for fumonisins: challenges and prospects, Current Opinion in Food Science, 54:101080, 11. DOI: https://doi.org/10.1016/j.cofs.2023.101080
Bartók T., Tölgyesi L., Mesterházy Á., Bartók M., Szécsi Á. (2010): Identification of the first fumonisin mycotoxins with three acyl groups by ESI-ITMS and ESI-TOFMS following RP-HPLC separation, palmitoyl, linoleoyl and oleoyl EFB1 fumonisin isomers from a solid culture of Fusarium verti-cillioides. Food Additives and Contaminants 27: 1714-1723. DOI: https://doi.org/10.1080/19440049.2010.521958
Bartók T., Szécsi Á., Juhász K., Bartók M., Mesterházy Á. (2013): ESI-MS and MS/MS identification of the first ceramide analogues of fumonisin B1 mycotoxin from a Fusarium verticillioides culture following RP-HPLC separation. Food Additives and Contaminants, 30: 1651-1659. DOI: https://doi.org/10.1080/19440049.2013.809626
Bouhet S., Oswald I. (2007): The intestine as a possible target for fumonisin toxicity – a review, Molecular Nutrition and Food Research, 51 925-931. DOI: https://doi.org/10.1002/mnfr.200600266
Braun M.S., Wink M. (2017): Exposure, Occurrence, and Chemistry of Fumonisins and their Cryptic Derivatives, Comprehensive Reviews in Food Science and Food Safety, 23. DOI: https://doi.org/10.1111/1541-4337.12334
Csenki Z., Bartók T., Bock I., Horváth L., Lemli B., Zsidó B.Z., Angeli C., Csaba Heté-nyi C., Szabó I, Urbányi B., Kovács M., Poór M. (2023): Interaction of Fumonisin B1, N-Palmitoyl-Fumonisin B1, 5- O-Palmitoyl-Fumonisin B1, and Fumonisin B4 Mycotoxins with Human Serum Albumin and Their Toxic Impacts on Zebrafish Embryos, Biomolecules, 13:755. DOI: https://doi.org/10.3390/biom13050755
Dall’Asta, C., Mangia, M., Berthiller, F., Molinelli, A., Sulyok, M., Schuhmacher, R., Krska, R., Galaverna, G., Dossena, A. and Marchelli R. (2009): Difficulties in fumonisin determination: the issue of hidden fumonisins, Analytical and Bioanalytical Chemistry 395: 1335-1345. DOI: https://doi.org/10.1007/s00216-009-2933-3
Dawlal P., Brabet C., Thantsha M.S., Buys E.M. (2019): Visualisation and quantification of fumonisins bound by lactic acid bacteria isolates from traditional African maize-based fermented cereals, ogi and mahewu, Food Additives & Contaminants: Part A 296-307. DOI: https://doi.org/10.1080/19440049.2018.1562234
Ding S., Cheng Y., Kalam Azad Md. A., Zhu Q., Huang P., Kong X. (2023): Development of small intestinal barrier function and underlying mechanism in Chinese indigenous and Duroc piglets during suckling and weaning periods, Animal Nutrition Journal, 46. DOI: https://doi.org/10.1016/j.aninu.2023.09.005
Domijan A.-M., Abramov A. Y. (2011): Fumonisin B1 inhibits mitochondrial respiration and deregu-lates calcium homeostasis-Implication to mechanism of cell toxicity. The International Journal of Biochemistry & Cell Biology. 897–904. DOI: https://doi.org/10.1016/j.biocel.2011.03.003
Du K., Liu P., Li Y., X. Ma X. (2017): Effects of dietary mycotoxins on gut microbiome, Protein and Peptide Letters, 24, 999. DOI: https://doi.org/10.2174/0929866524666170223095207
Dutton M.F. (2009): The African Fusarium/maize disease. Mycotoxin Research, 25: 29-39. DOI: https://doi.org/10.1007/s12550-008-0005-8
European Food Safety Authority (EFSA) (2018). Appropriateness to set a group health-based gu-idance value for fumonisins and their modified forms. EFSA Journal DOI: https://doi.org/10.2903/j.efsa.2018.5172
Enongene E.N., Sharma R.P., Bhandari N., Voss K.A., Riley R.T. (2000): Disruption of sphingolipid metabolism in small intestines, liver and kidney of mice dosed subcutaneously with fumonisin B1, Food Chem. Toxicol. 38, 793–799. DOI: https://doi.org/10.1016/s0278-6915(00)00065-x
Ezdini K., Salah-Abbés J.B., Belgacem H., Mannai M., Abbés S. (2020): Lactobacillus paracasei allaviates genotoxicity, oxidative stress status and histopatological damage induced by Fumonisin B1 in BALB/c mice, Toxicon 185:46-56. p. DOI: https://doi.org/10.1016/j.toxicon.2020.06.024
Falavigna C., Cirlini M., Galaverna G., C. Dall’Astra (2012): Masked fumonisins in processed food: Co-occurrence of hidden and bound, World Mycotoxin Journal, 5 (3): 325-334. DOI: https://doi.org/10.3920/wmj2012.1403
Ferrara M., Haidukowski M., D’Imperio M., Parente A., De Angelis E., Monaci L., Logrieco A.F., Mulè G. (2021): New insight into microbial degradation of mycotoxins during anaerobic digestion, Was-te Management, 119 215-225. DOI: https://doi.org/10.1016/j.wasman.2020.09.048
Fodor J., Meyer K., Gottschalk C., Mamet R., Kametler L., Bauer J., Horn P., Kovács F., Kovács M. (2007): In vitro microbial metabolism of fumonisin B1, Food Additives and Contaminants, 24 (4) 416-420. DOI: https://doi.org/10.1080/02652030701216461
Freire L., Sant’Ana A.S. (2017): Modified mycotoxins: An updated review on their formation, de-tection, occurrence, and toxic effects, Food and Chemical Toxicology, 111:189-205. DOI: https://doi.org/10.1016/j.fct.2017.11.021
Frisvad J.C., Smedsgaard J., Samson R.A., Larsen T.O., Thrane U. (2007): Fumonisin B2 Production by Aspergillus niger, Journal of Agriculture and Food Chemistry, 55 (23): 9727-9732. DOI: https://doi.org/10.1021/jf0718906
González-Arias C.A., Marín S., Sanchis V., Ramos A.J. (2013): Mycotoxin bioaccessibility/absorption assessment using in vitro digestion models: a review, World Mycotoxin Journal, 6 (2): 167-184. DOI: https://doi.org/10.3920/wmj2012.1521
Gu M.J., Han S.E., Hwang K., Mayer E., Reisinger N., Schatzmayr D., Park B-C., Han S.H., Yun C-H. (2019): Hydrolyzed fumonisin B1 induces less inflammatory responses than fumonisin B1 in the co-culture model of porcine intestinal epithelial and immune cells, Toxicology Letters, 305 110-116. DOI: https://doi.org/10.1016/j.toxlet.2019.01.013
Grenier B., Bracarense A-P. F.L., Schwartz H.E., Trumel C., Cossalter A-M., Schatzmayr G., Kolf-Clauw M., Moll W-D., Oswald I.P. (2012): The low intestinal and hepatic toxicity of hydrolyzed fumo-nisin B1 correlates with its inability to alter the metabolism of sphingolipids, Biochemical Pharmacology, 83 1465-1473. DOI: https://doi.org/10.1016/j.bcp.2012.02.007
Hahn I., Nagl V., Schwartz-Zimmermann H.E., Varga E., Schwartz C., Slavik V., Reisinger N., Malachová A., Cirlini M., Generotti S., Dall’Asta C., Krska R., Moll W-D., Berthiller F. (2014): Effects of orally administered fumonisin B1 (FB1), partially hydrolysed FB1, hydrolysed FB1 and N-(1-deoxy-D-fructos-1-yl) FB1 on the sphingolipid metabolism in rats, Food and Chemical Toxicology, 76: 11-18. DOI: https://doi.org/10.1016/j.fct.2014.11.020
Haschek W.M., Voss K.A., Beasley V.R. (2002): Selected Mycotoxins Affecting Animal and Human Health, Handbook of Toxicologic Pathology (Second Edition), 645-699. DOI: https://doi.org/10.1016/b978-012330215-1/50026-0
Heinl S., Hartinger D., Thamhesl M., Vekiru E., Krska R., Schatzmayr G., Moll W-D., Grabherr R. (2010): Degradation of Fumonisin B1 by the consecutive action of two bacterial enzymes, Journal of Biotechnology 145 (2): 120-129. DOI: https://doi.org/10.1016/j.jbiotec.2009.11.004
Hopmans E.C., Hauck C.C., Hendrich, S., Murphy, P.A. (1997): Excretion of fumonisin B1, hydrolyzed fumonisin B1, and the fumonisin B1-fructose adduct in rats. Journal of Agricultural and Food Chemistry 45: 2618-2625. DOI: https://doi.org/10.1021/jf960886j
Humpf H.U., Voss K.A. (2004): Effects of thermal food processing on the chemical structure and toxicity of fumonisin mycotoxins. Mol Nutr Food Res 48:255–269. DOI: https://doi.org/10.1002/mnfr.200400033
IARC Monographs on the evaluation of carcinogenic risk to humans (2002)
Iqbal N., Czékus Z., Poór P., Ördög A. (2021): Plant defence mechanisms against mycotoxin Fumonisin B1, Chemico-Biological Interactions 343: 1-12. DOI: https://doi.org/10.1016/j.cbi.2021.109494
Jin J., Breekmann K., Ringo E., Rietjens I. M.C.M., Xing F. (2021): Interaction between food-borne mycotoxins and gut microbiota: A review, Food Control 126:1-13. DOI: https://doi.org/10.1016/j.foodcont.2021.107998
Khalil A.A., Abou-Gabal A.E., Abdellatef A.A., Khalid A.E. (2015): Protective role of probiotic lactic acid bacteria against dietary fumonisin B1-induced toxicity and DNA fragmentation in sprague-dawley rats, Preparative Biochemistry and Biotechnology 45: 530-550. DOI: https://doi.org/10.1080/10826068.2014.940969
Kovács M. (2019): Mikotoxinok a takarmány- és élelmiszerláncban, in: Babinszky L., Halas V. (szerk.), Innovatív takarmányozás, Akadémiai Kiadó 18: 750-796. DOI: https://doi.org/10.1556/9789634540571
Kovács M., Horn P., Magyar T., Tornyos G., Pósa R., Mézes M., Cseh S., Szabó A., Szabó-Fodor J. (2016): A fumonizin B1 mikotoxin a táplálékláncban és egészségkárosító hatásai, In Memoriam Kovács Ferenc Nemzetközi Állatorvos és Állattenyésztő Kongresszus 38-43. p.
Kostic A., Milincic D., Petrovic T., Krnjaja V., Stanojevic C., Barac M.B., Tesic Z. Lj., Pesic M.B: (2019): Mycotoxins and mycotoxin producing fungi in pollen: a review, Toxins, 11,64. DOI: https://doi.org/10.3390/toxins11020064
Lallé J-P., Lessard M., P. Oswald I., David J-C. (2009): Consumption of fumonisin B1 for 9 days induces stress proteins along the gastrointestinal tract of pigs, Toxicon, 55: 244-249. DOI: https://doi.org/10.1016/j.toxicon.2009.07.027
Li X., Li J., Feng Y., Liu L., Kuang H., Xu C., Guo L. (2024): Fluorescent microsphere immunochromato-graphic sensor for the detection of total fumonisins B1, B2, and B3 in grain samples, Journal of Food Composition and Analysis, 29. DOI: https://doi.org/10.1016/j.jfca.2024.106018
Liu L., Xie M., Wei D. (2022): Biological Detoxification of Mycotoxins: Current status and future ad-vances, International Journal of Molecular Sciences 23 (1064): 1-19. DOI: https://doi.org/10.3390/ijms23031064
Lu Q., Qin J-A., Yan-Wei Fu Y-W., Luo J-Y., Lu J-H., Logrieco A.F., Yang M-H. (2020): Modified mycoto-xins in foodstuffs, animal feed, and herbal medicine: A systematic review on global occurrence, transformation mechanism and analysis methods, Trends in Analythical Chemistry, 133:28. DOI: https://doi.org/10.1016/j.trac.2020.116088
Manyes L., Ruiz M.J., Luciano F.B., Meca G. (2013): Bioaccessibility and bioavailability of fumonisin B2 and its reaction products with isothiocyanates through a simulated gastrointestinal digestion system, Food Control 37. (2014) 326-335. DOI: https://doi.org/10.1016/j.foodcont.2013.09.056
Massarolo K.C., Ferreira C.FJ., Collazzo C.C., Bianchini A., Kupski L., Badiale-Furlong E. (2020): Re-sistant starch and hydrothermal treatment of cornmeal: Factors in aflatoxins and fumonisin B1 reduction and bioaccessibility, Food Contol (114) DOI: https://doi.org/10.1016/j.foodcont.2020.107274
Merrill A. Jr. Sullard M.C., Wang E., Voss K.A., Riley R.T. (2001): Sphingolipid Metabolism: Roles in Signal Transduction and Disruption by Fumonisins, Environmental Health Perspectives, 283-289. DOI: https://doi.org/10.2307/3435020
Mogensen J.M., Moller K.A., Freiesleben P., Labuda R., Varga E., Sulyok M., Kubatova A., Thrane U., Andersen B., Nielsen K.F. (2010): Production of fumnisins in B2 and B4 in Tolypocladium speci-es, J ind Microbiol Biotechnol (2011) 38: 1329-1335. DOI: https://doi.org/10.1007/s10295-010-0916-1
Musker M., Licinio J., Wong M-L. (2018): Inflammation Genetics of Depression, Inflammation and Immunity in Depression, 411-425. DOI: https://doi.org/10.1016/b978-0-12-811073-7.00023-4
Niderkorn V., Morgavi D.P., Aboab D.P., Lemaire M., Boudra H. (2009): Cell wall component and mycotoxin moietiesinvolved in the binding of fumonosin B1 and B2 by lactic acid bacteria, Jour-nal of Applied Microbiology, 106,3,977-985. DOI: https://doi.org/10.1111/j.1365-2672.2008.04065.x
Pizzolitto R.P., Salvano M.A., Dalcero A.M. (2012): Analysis of fumonisin B1 removal by microor-ganisms in co-occurrence with aflatoxin B1 and the nature of the binding process, International journal of food microbiology 156: 214-221. DOI: https://doi.org/10.1016/j.ijfoodmicro.2012.03.024
Prelusky D.B., Savard M.E., Trenholm H.L., (1994): Pharmacokinetic fate of 14C-labelled fumonisin B1 in swine. Natural Toxins 2: 73-80. DOI: https://doi.org/10.1002/nt.2620020205
Prelusky D.B., Trenholm H.L., Savard, M.E. (1995): Pilot study on the plasma pharmacokinetics of fumonisin B1 in cows following a single dose by oral gavage or intravenous administration. Na-tural Toxins 3: 389-394. DOI: https://doi.org/10.1002/nt.2620030511
Ridley C.P., Khosla C. (2009): Polyketides, Encyclopedia of Microbiology (Third Edition) 472-481. DOI: https://doi.org/10.1016/B978-012373944-5.00158-9
Riley R.T., Alfred H. M. Jr. (2019): Ceramide synthase inhibition by fumonisins: a perfect storm of perturbed sphingolipid metabolism, signaling, and disease, Journal of Lipid Research, 1183-1189. DOI: https://doi.org/10.1194/jlr.s093815
Rychlik M., Humpf H-U., Marko D., Danicke S., Mally A., Berthiller F., Klaffke H., Lorenz N. (2014): Proposal of a comprehensive definition of modified and other forms of mycotoxins including “masked” mycotoxins, Mycotoxin Research, 9. DOI: https://doi.org/10.1007/s12550-014-0203-5
Seefelder W., Hartl M., Humpf H.U. (2001): Determination of N- (Carboxymethyl)fumonisin B1 in corn products by liquid chromatography/electrospray ionization- mass spectrometry. J Agric Food Chem 49:2146–2151. DOI: https://doi.org/10.1021/jf001429c
Shier W.T. (2000): The fumonisin paradox: a review of research on oral bioavailability of fumonisin B1, a mycotoxin produced by Fusarium moniliforme. J Toxicol Toxin Rev 19:161–187. DOI: https://doi.org/10.1081/txr-100100319
Soriano J.M., Gonzales L., Catalá A.I. (2005): Mechanism of action of sphingolipids and their metaboli-tes in the toxicity of fumonisin B1, Progress in Lipid Research 44: 345-356. DOI: https://doi.org/10.1016/j.plipres.2005.09.001
Tan H., Zhou H., Guo T., Zhou Y., Wang S., Liu X., Zhang Y., Ma L. (2022): Matrix-associated mycotoxins in foods, cereals and feedstuffs: A review on occurrence, detection, transformation and future challenges, Critical Reviews in Food Science and Nutrition, 15. DOI: https://doi.org/10.1080/10408398.2022.2131724
Vanhoutte I., Audenaert K., De Gelder L. (2016): Biodegradation of Mycotoxins: Tales from Known and Unexplored Worlds, Frontiers in Microbiology, 7, 561. DOI: https://doi.org/10.3389/fmicb.2016.00561
Versantvoort C., van de Kamp E., Rompelberg C. (2004): Developement and applicability of an in vitro digestion model in assessing the bioaccessibility of contaminants from food, Food and Chemical Toxicology 43 (1) 31-40. DOI: https://doi.org/10.1016/j.fct.2004.08.007
Vudathala D.K., Prelusky D.B., Ayroud M., Trenholm, H.L., Miller, J.D., (1994.): Pharmacokinetic fate and pathological effects of 14C-fumonisin B1 in laying hens. Natural Toxins, 2: 81-88. DOI: https://doi.org/10.1002/nt.2620020206
Wen D., Han W., Chen Q., Qi G., Gao M., Guo P., Liu Y., Wu Z., Fu S., Lu Q., Qiu Y. (2024): Integrating net-work pharmacology and experimental validation to explore the mechanisms of luteolin in allevi-ating fumonisin B1–induced intestinal inflammatory injury, Toxicon (237) DOI: https://doi.org/10.1016/j.toxicon.2023.107531
Yang L., Yang L., Cai Y., Luo Y., Wang H., Wang L., Chen J. (2023): Natural mycotoxin contamination in dog food: A review on toxicity and detoxification methods, Ecotoxicology and Environmental Safety, 257:11. DOI: https://doi.org/10.1016/j.ecoenv.2023.114948
Zeebone Y.Y. (2023): Evaluation of Fumonisins exposure through structural and funcional changes in the gastrointestinal tract of pigs, Doctoral Dissertation, Kaposvár
Zeebone Y.Y., Kovács M., Halas V. (2020): Effects of Fumonisin B1 on the gastrointestinal trackt functionality – a review, Állattenyésztés és Takarmányozás 69 (1): 53-66.
Zhao H., Wang X., Zhang J., Zhang J., Zhang B. (2016): The mechanism of Lactobacillus strains for their ability to remove fumonisin B1 and B2, Food and Chemical Toxicology 97: 40–46. DOI: https://doi.org/10.1016/j.fct.2016.08.028
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Varga-Szatmári Viktória, Vargáné Visi Éva
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
How to Cite
