In Vitro Detoxification of Aflatoxin B1, Deoxynivalenol, Fumonisins, T-2 Toxin and Zearalenone by Probiotic Bacteria from Genus Lactobacillus and Saccharomyces cerevisiae Yeast

Smith MC, Madec S, Coton E, Hymery N (2016) Natural co-occurrence of mycotoxins in foods and feeds and their in vitro combined toxicological effects. Toxins 8(4):94. https://doi.org/10.3390/toxins8040094

Alshannaq A, Yu JH (2017) Occurrence, toxicity, and analysis of major mycotoxins in food. Int J Environ Res Public Health 14(6):632. https://doi.org/10.3390/ijerph14060632

Liew WPP, Mohd-Redzwan S (2018) Mycotoxin: its impact on gut health and microbiota. Front Cell Infect Microbiol 8(60). https://doi.org/10.3389/fcimb.2018.00060

Gallo A, Giuberti G, Frisvad JC, Bertuzzi T, Nielsen KF (2015) Review on mycotoxin issues in ruminants: occurrence in forages, effects of mycotoxin ingestion on health status and animal performance and practical strategies to counteract their negative effects. Toxins 7(8):3057–3111. https://doi.org/10.3390/toxins7083057

Pinotti L, Ottoboni M, Giromini C, Dell’Orto V, Cheli F (2016) Mycotoxin contamination in the EU feed supply chain: a focus on cereal byproducts. Toxins 8(2):45. https://doi.org/10.3390/toxins8020045

Freire L, Sant’Ana AS (2018) Modified mycotoxins: an updated review on their formation, detection, occurrence, and toxic effects. Food Chem Toxicol 111:189–205. https://doi.org/10.1016/j.fct.2017.11.021

Streit E, Schatzmayr G, Tassis P, Tzika E, Marin D, Taranu I, Tabacu C, Nicolau A, Aprodu I, Puel O, Oswald IP (2012) Current situation of mycotoxin contamination and co-occurrence in animal feed-focus on Europe. Toxins 4(10):788–809. https://doi.org/10.3390/toxins4100788

Ji C, Fan Y, Zhao L (2016) Review on biological degradation of mycotoxins. Animal Nutr 2(3):127–133. https://doi.org/10.1016/j.aninu.2016.07.003

Zacharisova M, Dzuman Z, Veprikova Z, Hajkova K, Jiru M, Vaclavikova M, Zacharisaova A, Pospichalova M, Florian M, Hajslova J (2014) Occurrence of multiple mycotoxins in European feedingstuffs, assessment of dietary intake by farm animals. Anim Feed Sci Technol 193:124–140. https://doi.org/10.1016/j.anifeedsci.2014.02.007

Neme K, Mohammed A (2017) Mycotoxin occurrence in grains and the role of postharvest management as a mitigation strategies. A review. Food Control 78:412–425. https://doi.org/10.1016/j.foodcont.2017.03.012

Kosicki R, Błajet-Kosicka A, Grajewski J, Twarużek M (2016) Multiannual mycotoxin survey in feed materials and feedingstuffs. Anim Feed Sci Technol 215:165–180. https://doi.org/10.1016/j.anifeedsci.2016.03.012

European Parliament and the Council (2002) Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on undesirable substances in animal feed - Council statement. https://eur-lex.europa.eu/resource.html?uri=cellar:aca28b8c-bf9d-444f-b470-268f71df28fb.0004.02/DOC_1&format=PDF . Accessed 06 April 2018

The Commission Of The European Communities (2006) Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32006R1881&from=en . Accessed 06 April 2018

The Commission Of The European Communities (2006) 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. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32006H0576&from=EN . Accessed 06 April 2018

Medina A, Magan N (2011) Temperature and water activity effects on production of T-2 and HT-2 by Fusarium langsethiae strains from north European countries. Food Microbiol 28:392–398. https://doi.org/10.1016/j.fm.2010.09.012

Milani JM (2013) Ecological conditions affecting mycotoxin production in cereals: a review. Vet Med (Praha) 58(8):405–411. https://doi.org/10.17221/6979-VETMED

The Commission Of The European Communities (2013) Commission Recommendation 2013/165/EU of 27 March 2013 on the presence of t-2 and ht-2 toxin in cereals and cereal products. http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32013H0165&from=EN . Accessed 06 April 2018

Nugmanov A, Beishova I, Kokanov S, Lozowicka B, Kaczynski P, Konecki R, Snarska K, Wołejko E, Sarsembayeva N, Abdigaliyeva T (2018) Systems to reduce mycotoxin contamination of cereals in the agricultural region of Poland and Kazakhstan. Crop Prot 106:64–71. https://doi.org/10.1016/j.cropro.2017.12.014

The European Parliament And The Council Of The European Union (2017) Regulation (EU) 2017/625 of the European Parliament and of the Council of 15 March 2017 on official controls and other official activities performed to ensure the application of food and feed law, rules on animal health and welfare, plant health and plant protection products. https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32017R0625&from=EN . Accessed 06 April 2018

Aiko V, Mehta L (2015) Occurrence, detection and detoxification of mycotoxins. J Biosci 45(5):943–954. https://doi.org/10.1007/s12038-015-9569-6

Loi M, Fanelli F, Liuzzi VC, Logrieco AF, Mulè G (2017) Mycotoxin biotransformation by native and commercial enzymes: present and future perspectives. Toxins 9(4):111. https://doi.org/10.3390/toxins9040111

Zhu Y, Hassan YI, Lepp D, Shao S, Zhou T (2017) Strategies and methodologies for developing microbial detoxification systems to mitigate mycotoxins. Toxins 9(4):130. https://doi.org/10.3390/toxins9040130

Juodeikiene G, Bartkiene E, Cernauskas D, Cizeikiene D, Zadeike D, Lele V, Bartkevics V (2018) Antifungal activity of lactic acid bacteria and their application for Fusarium mycotoxin reduction in malting wheat grains. LWT-Food Sci Technol 89:307–314. https://doi.org/10.1016/j.lwt.2017.10.061

El-Nezami H, Kankaanpaa P, Salminen S, Ahokas J (1998) Ability of dairy strains of lactic acid bacteria to bind a common food carcinogen, aflatoxin B1. Food Chem Toxicol 36:321–326

FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report. http://www.fao.org/3/a-a0512e.pdf . Accessed 24 March 2018

Vinderola G, Ritieni A (2015) Role of probiotics against mycotoxins and their deleterious effects. J Food Res 4(1):10–21. https://doi.org/10.5539/jfr.v4n1p10

Śliżewska K, Chlebicz A (2017) Strains of lactic acid bacteria from the genus Lactobacillus. Patent Application no 422603

Aflatoxin B1 from Aspergillus flavus, Sigma-Aldrich. https://www.sigmaaldrich.com/catalog/product/sigma/a6636?lang=pl&region=PL . Accessed 21 March 2018

Deoxynivalenol, Sigma-Aldrich. https://www.sigmaaldrich.com/catalog/product/sial/32943?lang=pl&region=PL . Accessed 21 March 2018

Fumonisin B1, Sigma-Aldrich. https://www.sigmaaldrich.com/catalog/product/sial/34139?lang=pl&region=PL&cm_sp=Insite-_-prodRecCold_xorders-_-prodRecCold2-1 . Accessed 21 March 2018

Fumonisin B2, Sigma-Aldrich. https://www.sigmaaldrich.com/catalog/product/sial/34142?lang=pl&region=PL&cm_sp=Insite-_-prodRecCold_xorders-_-prodRecCold2-2 . Accessed 21 March 2018

T-2 toxin, Sigma-Aldrich. https://www.sigmaaldrich.com/catalog/product/sigma/t4887?lang=pl&region=PL . Accessed 21 March 2018

Zearalenone, Sigma-Aldrich. https://www.sigmaaldrich.com/catalog/product/sigma/z2125?lang=pl&region=PL . Accessed 21 March 2018

Devreese M, De Backer P, Croubels S (2013) Different methods to counteract mycotoxin production and its impact on animal health. Vlaams Diergeneeskd Tijdschr 82(4):181–190

Karlovsky P, Suman M, Berthiller F, De Meester J, Eisenbrand G, Perrin I, Oswald IPm Speijers G, Chiodini A, Recker T, Dussort P (2016) Impact of food processing and detoxification treatments on mycotoxin contamination. Mycotoxin Res 32(4):179–205. https://doi.org/10.1007/s12550-016-0257-7

Moslehi-Jenabian S, Pedersen LL, Jespesen L (2010) Beneficial effects of probiotic and food borne yeasts on human health. Nutrients 2(4):449–473. https://doi.org/10.3390/nu2040449

Śliżewska K, Smulikowska S (2011) Detoxification of aflatoxin B1 and change in microflora pattern by probiotic in vitro fermentation of broiler feed. Anim Feed Sci Technol 20:300–309. https://doi.org/10.22358/jafs/66187/2011

Vila-Donat P, Marin S, Sachis V, Ramos AJ (2018) A review of the mycotoxin adsorbing agents, with an emphasis on their multi-binding capacity, for animal feed decontamination. Anim Feed Sci Technol 114:246–259. https://doi.org/10.1016/j.fct.2018.02.044

Haskard CA, El-Nezmi HS, Kankaanpää PE, Salminen S, Ahokas JT (2001) Surface binding of aflatoxin B1 by lactic acid bacteria. Appl Environ Microbiol 67(7):3086–3091. https://doi.org/10.1128/AEM.67.7.3086-3091.2001

Liew WPP, Nurul-Adilah Z, Than LTL, Mohd-Redzwan S (2018) The binding efficiency and interaction of Lactobacillus casei Shirota toward aflatoxin B1. Front Microbiol 9(1503). https://doi.org/10.3389/fmicb.2018.01503

Hernandez-Mendoza A, Garcia HS, Steele JL (2009) Screening of Lactobacillus casei strains for their ability to bind aflatoxin B1. Food Chem Toxicol 47:1064–1068. https://doi.org/10.1016/j.fct.2009.01.042

Huang L, Duan C, Zhao Y, Gao L, Niu C, Xu J, Li S (2017) Reduction of aflatoxin b1 toxicity by lactobacillus plantarum c88: a potential probiotic strain isolated from Chinese traditional fermented food “tofu”. PLoS One 12(1):e0170109. https://doi.org/10.1371/journal.pone.0170109

Kumar SS, Bashisht A, Venkateswaran G, Hariprasad P, Gayathri D (2018) Characterization of novel Lactobacillus fermentum from curd samples of indigenous cows from Malnad region, Karnataka, for their aflatoxin B1 binding and probiotic properties. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-018-9479-7

Hernandez-Mendoza A, Guzman-de-Peña D, Garcia HS (2009) Key role of 383 teichoic acids on aflatoxin B1 384 binding by probiotic bacteria. J Appl Microbiol 107:395–403. https://doi.org/10.1111/j.1365-3852672.2009.04217.x

Gratz S, Mykkänen H, El-Nezami H (2005) Aflatoxin B1 binding by a mixture of Lactobacillus and Propionibacterium: in vitro versus ex vivo. J Food Prot 68(11):2470–2474. https://doi.org/10.4315/0362-028X-68.11.2470

Pizzolitto RP, Armando MR, Combina M, Cavaglieri LR, Dalcero AM, Salvano MA (2012) Evaluation of Saccharomyces cerevisiae strains as probiotic agent with aflatoxin B1 adsorption ability for use in poultry feedstuffs. J Environ Sci Health B 47(10):933–941. https://doi.org/10.1080/03601234.2012.706558

Poloni V, Salvato L, Pereyra L, Oliveira A, Rosa C, Cavaglieri L, Keller KM (2017) Bakery by-products based feeds borne-Saccharomyces cerevisiae strains with probiotic and antimycotoxin effects plus antibiotic resistance properties for use in animal production. Food Chem Toxicol 107:630–636. https://doi.org/10.1016/j.fct.2017.02.040

Pizzolitto RP, Bueno DJ, Armando MR, Cavaglieri L, Dalcero AM, Salvano MA (2011) Binding of aflatoxin B1 to lactic acid bacteria and Saccharomyces cerevisiae in vitro: a useful model to determine the most efficient microorganism. In: Guevara-Gonzalez RG (ed) Aflatoxins. Biochemistry and molecular biology, InTech. https://doi.org/10.5772/23717 . https://www.intechopen.com/books/aflatoxins-biochemistry-and-molecular-biology/binding-of-aflatoxin-b1-to-lactic-acid-bacteria-and-saccharomyces-cerevisiae-in-vitro-a-useful-model . Accessed 28 March 2018

Niderkorn V, Morgavi DP, Pujos E, Tissandier A, Boudra H (2007) Screening of fermentative bacteria for their ability to bind and biotransform deoxynivalenol, zearalenone and fumonisins in an in vitro simulated corn silage model. Food Addit Contam 24(4):406–415. https://doi.org/10.1080/02652030601101110

Franco TS, Garcia S, Hirooka EY, Ono YS, Santos JS (2011) Lactic acid bacteria in the inhibition of Fusarium graminearum and deoxynivalenol detoxification. J Appl Microbiol 111:739–748. https://doi.org/10.1111/j.1365-2672.2011.05074.x

Zou ZY, He ZF, Li HJ, Han PF, Meng X, Zhang Y, Zhou F, Ouyang KP, Chen XY, Tang J (2012) In vitro removal of deoxynivalenol and T-2 toxin by lactic acid bacteria. Food Sci Biotechnol 21(6):1677–1683. https://doi.org/10.1007/s10068-012-0223-x

García GR, Payros D, Pinton P, Dogi CA, Laffitte J, Neves M, González Pereyra ML, Cavaglieri LR, Oswald IP (2018) Intestinal toxicity of deoxynivalenol is limited by Lactobacillus rhamnosus RC007 in pig jejunum explants. Arch Toxicol 92:983–993. https://doi.org/10.1007/s00204-017-2083-x

Campagnollo FB, Franco LT, Rottinghaus GE, Kobashigawa E, Ledoux DR, Daković A, Oliveira CAF (2015) In vitro evaluation of the ability of beer fermentation residue containing Saccharomyces cerevisiae to bind mycotoxins. Food Res Int 77:643–648. https://doi.org/10.1016/j.foodres.2015.08.032

Abbès S, Salah-Abbès JB, Jebali R, Younes RB, Oueslati R (2016) Interaction of aflatoxin B1 and fumonisin B1 in mice causes immunotoxicity and oxidative stress: possible protective role using lactic acid bacteria. J Immunotoxicol 13(1):46–54. https://doi.org/10.3109/1547691X.2014.997905

Zhao H, Wang X, Zhang J, Zhang J, Zhang B (2016) The mechanism of Lactobacillus strains for their ability to remove fumonisins B1 and B2. Food Chem Toxicol 97:40–46. https://doi.org/10.1016/j.fct.2016.08.028

Pizzolitto RP, Salvano MA, Dalcero AM (2012) Analysis of fumonisin B1 removal by microorganisms in co-occurrence with aflatoxin B1 and the nature of the binding process. Int J Food Microbiol 156:214–221. https://doi.org/10.1016/j.ijfoodmicro.2012.03.024

Deepthi BV, Poornachandra Rao K, Chennapa G, Naik MK, Chandrashekara KT, Sreenivasa MY (2016) Antifungal attributes of Lactobacillus plantarum MYS6 against fumonisin producing Fusarium proliferatum associated with poultry feeds. PLoS One 11(6):e0155122. https://doi.org/10.1371/journal.pone.0155122

Martinez Tuppia C, Atanasova-Penichon V, Chéreau S, Ferrer N, Marchegay G, Savoie J, Richard-Forget F (2017) Yeast and bacteria from ensiled high moisture maize grains as potential mitigation agents of fumonisin B1. J Sci Food Agric 97:2443–2452. https://doi.org/10.1002/jsfa.8058

Armando M, Galvagno M, Dogi C, Cerrutti P, Dalcero A, Cavaglieri L (2013) Statistical optimization of culture conditions for biomass production of probiotic gut-borne Saccharomyces cerevisiae strain able to reduce fumonisin B1. J Appl Microbiol 114:1338–1346. https://doi.org/10.1111/jam.12144

Zou Z, Sun J, Huang F, Feng Z, Li M, Shi R, Ding J, Li H (2015) In vitro removal of T-2 toxin by yeasts. J Food Safety 35:544–550. https://doi.org/10.1111/jfs.12204

Zhao L, Jin H, Zhang R, Ren H, Zhang X, Yu G (2015) Detoxification of zearalenone by three strains of Lactobacillus plantarum from fermented food in vitro. Food Control 54:158–164. https://doi.org/10.1016/j.foodcont.2015.02.003

Niderkorn V, Boudra H, Morgavi DP (2006) Binding of Fusarium mycotoxins by fermentative bacteria in vitro. J Appl Microbiol 101:849–856. https://doi.org/10.1111/j.1365-2672.2006.02958.x

Čvek D, Markov K, Frece J, Friganović M, Duraković L, Delaš F (2012) Adhesion of zearalenone to the surface of lactic acid bacteria cells. Croat J Food Tech Biotech Nutr 7:49–52

Sangsila A, Faucet-Marquis V, Pfohl-Leszkowicz A, Itsaranuwat P (2016) Detoxification of zearalenone by Lactobacillus pentosus strains. Food Control 62:187–192. https://doi.org/10.1016/j.foodcont.2015.10.031

Vega MF, Dieguez SN, Riccio B, Aranguren S, Giordano A, Denzoin L, Soraci AL, Tapia MO, Ross R, Apás A, González SN (2017) Zearalenone adsorption capacity of lactic acid bacteria isolated from pigs. Braz J Microbiol 48(4):715–723. https://doi.org/10.1016/j.bjm.2017.05.001

Keller L, Abrunhosa L, Keller K, Rosa CA, Cavaglieri L, Venâncio A (2015) Zearalenone and its derivatives α-zearalenol and β-zearalenol decontamination by Saccharomyces cerevisiae strains isolated from bovine forage. Toxins 7(8):3297–3308. https://doi.org/10.3390/toxins7083297

Armando MR, Pizzolitto RP, Dogi CA, Cristofolini A, Merkis C, Poloni V, Dalcero AM, Cavaglieri LR (2012) Adsorption of ochratoxin A and zearalenone by potential probiotic Saccharomyces cerevisiae strains and its relations with cell wall thickness. J Appl Microbiol 113:256–264. https://doi.org/10.1111/j.1365-2672.2012.05331.x