Recent advances in detoxification strategies for zearalenone contamination in food and feed

doi:10.1016/j.cjche.2020.11.011

Abstract

Abstract: Zearalenone (ZEN) is a widely distributed mycotoxin that frequently contaminates crops and animal feed. ZEN can cause serious health problems in livestock and humans alike, leading to great economic losses in the food industry and livestock farming. Therefore, approaches for efficient ZEN decontamination in food and feed are urgently needed. Traditional physical and chemical methods may decrease the nutritional quality of food and palatability of feed, or leading to residues and safety concerns. By contrast, biological methods for the removal or degradation of ZEN overcome these problems, especially for biological degradation by microorganisms and specific enzymes extracted from strains that can convert ZEN to less toxic or even completely harmless products. In this review, we comprehensively describe methods for ZEN degradation, focusing especially on biological strategies. Finally, emerging strategies and advice on remaining challenges in biodegradation research are also briefly discussed.

Key words: Mycotoxin, Removal, Degradation, Zearalenone, Food safety

摘要： Zearalenone (ZEN) is a widely distributed mycotoxin that frequently contaminates crops and animal feed. ZEN can cause serious health problems in livestock and humans alike, leading to great economic losses in the food industry and livestock farming. Therefore, approaches for efficient ZEN decontamination in food and feed are urgently needed. Traditional physical and chemical methods may decrease the nutritional quality of food and palatability of feed, or leading to residues and safety concerns. By contrast, biological methods for the removal or degradation of ZEN overcome these problems, especially for biological degradation by microorganisms and specific enzymes extracted from strains that can convert ZEN to less toxic or even completely harmless products. In this review, we comprehensively describe methods for ZEN degradation, focusing especially on biological strategies. Finally, emerging strategies and advice on remaining challenges in biodegradation research are also briefly discussed.

关键词: Mycotoxin, Removal, Degradation, Zearalenone, Food safety

Na Wu, Wen Ou, Zhidong Zhang, Yuwen Wang, Qing Xu, He Huang. Recent advances in detoxification strategies for zearalenone contamination in food and feed[J]. Chinese Journal of Chemical Engineering, 2021, 29(2): 168-177.

Na Wu, Wen Ou, Zhidong Zhang, Yuwen Wang, Qing Xu, He Huang. Recent advances in detoxification strategies for zearalenone contamination in food and feed[J]. 中国化学工程学报, 2021, 29(2): 168-177.

References

[1] C. Hansub, K. Woori, P. Ju-Hee, et al., The occurrence of zearalenone in South Korean feedstuffs between 2009 and 2016, Toxins 9 (7) (2017) 223–238.
[2] N.K. Kalagatur, K. Kumarvel, J.A. Allen, et al., Application of activated carbon derived from seed shells of Jatropha curcas for decontamination of zearalenone mycotoxin, Front. Pharmacol. 8 (2017) 760–773.
[3] W.T. Shier, A.C. Shier, W. Xie, C.J. Mirocha, Structure-activity relationships for human estrogenic activity in zearalenone mycotoxins, Toxicon 39 (9) (2001) 1435–1438.
[4] F. Minervini, A. Giannoccaro, A. Cavallini, A. Visconti, Investigations on cellular proliferation induced by zearalenone and its derivatives in relation to the estrogenic parameters, Toxicol. Lett. 159 (3) (2005) 272–283.
[5] Z. Yu, L. Zhang, D. Wu, F. Liu, Anti-apoptotic action of zearalenone in MCF-7 cells, Ecotoxicol. Environ. Saf. 62 (3) (2005) 441–446.
[6] M.E.B.D. Rocha, F.D.C.O. Freire, Fábio Erlan Feitosa Maia, et al., Mycotoxins and their effects on human and animal health, Food Control 36(1) (2014) 159–165.
[7] W. Zheng, B. Wang, X. Li, et al., Zearalenone promotes cell proliferation or causes cell death? Toxins 10 (5) (2018) 184.
[8] K. Gromadzka, A. Waskiewicz, P. Golinski, J. Swietlik, Occurrence of estrogenic mycotoxin-Zearalenone in aqueous environmental samples with various NOM content, Water Res. 43 (4) (2009) 1051–1059.
[9] G.E. Wood, Mycotoxins in foods and feeds in the United States, J. Anim. Sci. 70 (12) (1992) 3941–3949.
[10] L. Pallaroni, C.V. Holst, C. Eskilsson, et al., Microwave-assisted extraction of zearalenone from wheat and corn, Anal. Bioanal. Chem. 374 (1) (2002) 161–166.
[11] A. Zinedine, J.M. Soriano, Juan Carlos Moltó, et al., Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin, Food Chem. Toxicol. 45 (1) (2007) 1–18.
[12] D. Ryu, M.A. Hanna, K.M. Eskridge, et al., Heat stability of zearalenone in an aqueous buffered model system, J. Agric. Food Chem. 51 (6) (2003) 1746–1748.
[13] M. Miraglia, H.J.P. Marvin, G.A. Kleter, et al., Climate change and food safety: An emerging issue with special focus on Europe, Food Chem. Toxicol. 47 (5) (2009) 1009–1021.
[14] Y. Zheng, S.M. Hossen, Y. Sago, M. Yoshida, H. Nakagawa, H. Nagashima, H. Okadome, T. Nakajima, M. Kushiro, Effect of milling on the content of deoxynivalenol, nivalenol, and zearalenone in Japanese wheat, Food Control 40 (2014) 193–197.
[15] Y. Cetin, L.B. Bullerman, Evaluation of reduced toxicity of zearalenone by extrusion processing as measured by the MTT cell proliferation assay, J. Agric. FoodChem. 53 (16) (2005) 6558–6563.
[16] L.B. Bullerman, A. Bianchini, Stability of mycotoxins during food processing, Int. J. Food Microbiol. 119 (1–2) (2007) 140–146.
[17] H.L. Trenholm, L.L. Charmley, D.B. Prelusky, et al., Two physical methods for the decontamination of four cereals contaminated with deoxynivalenol and zearalenone, J. Agric. Food. Chem. 39 (2) (1991) 356–360.
[18] A. Ismail, B.L. Goncalves, D.V. De Neeff, et al., Aflatoxin in foodstuffs: Occurrence and recent advances in decontamination, Food Res. Int. 113 (11) (2018) 74–85.
[19] L. Pallaroni, E. Bjrklund, C.V. Holst, Alternative extraction methods for Zearalenone: microwave assisted extraction and accelerated solvent extraction, Mycotoxin Res. 18 Suppl 1(s1) (2002) 74–77.
[20] M. Denli, J.C. Blandon, M.E. Guynot, et al., Efficacy of activated diatomaceous clay in reducing the toxicity of zearalenone in rats and piglets, J. Anim. Sci. 93 (2) (2015) 637–645.
[21] G.F. Wang, Y.F. Xi, C. Lian, et al., Simultaneous detoxification of polar aflatoxin B1 and weak polar zearalenone from simulated gastrointestinal tract by zwitterionic montmorillonites, J. Hazard. Mater. 364 (2019) 227–237.
[22] Z.L. Sun, C. Lian, C.Q. Li, et al., Investigations on organo-montmorillonites modified by binary nonionic/zwitterionic surfactant mixtures for simultaneous adsorption of aflatoxin B and zearalenone, J. Colloid Interface Sci. 565 (2020) 11–22.
[23] X. Bai, C. Sun, J. Xu, D. Liu, Y. Han, S. Wu, X. Luo, Detoxification of zearalenone from corn oil by adsorption of functionalized GO systems, Appl. Surf. Sci. 430 (2018) 198–207.
[24] A.A. Pirouz, J. Selamat, S.Z. Iqbal, H. Mirhosseini, R.A. Karjiban, F.A. Bakar, The use of innovative and efficient nanocomposite (magnetic graphene oxide) for the reduction on of Fusarium mycotoxins in palm kernel cake, Sci. Rep. 7 (1) (2017) 12453.
[25] Z. Huang, J. He, H. Li, M. Zhang, S. Zhang, Synthesis and application of magnetic-surfaced pseudo molecularly imprinted polymers for zearalenone pretreatment in cereal samples, Food Chem. 308 (2020) 125696.
[26] S. Gbashi, N.E. Madala, S. De Saeger, M. De Boevre, P.B. Njobeh, Numerical optimization of temperature-time degradation of multiple mycotoxins, Food Chem. Toxicol. 125 (2019) 289–304.
[27] E. Numanoglu, S. Yener, V. Gokmen, U. Uygun, H. Koksel, Modelling thermal degradation of zearalenone in maize bread during baking, Food Addit. Contam. Part A Chem. Anal. Control Expo Risk Assess. 30 (3) (2013) 528–533.
[28] A.S. Sebaei, H.M. Sobhy, A.S.M. Fouzy, et al., Occurrence of zearalenone in grains and its reduction by gamma radiation, Water Res. 43 (2009) 1051–1059.
[29] V. Popovic, N. Fairbanks, J. Pierscianowski, M. Biancaniello, T. Zhou, T. Koutchma, Feasibility of 3D UV-C treatment to reduce fungal growth and mycotoxin loads on maize and wheat kernels, Mycotoxin Res. 34 (3) (2018) 211–221.
[30] N. Hojnik, M. Modic, G. Tavcar-Kalcher, J. Babic, J.L. Walsh, U. Cvelbar, Mycotoxin decontamination efficacy of atmospheric pressure air plasma, Toxins 11 (4) (2019) 219–230.
[31] L. Ten Bosch, K. Pfohl, G. Avramidis, S. Wieneke, W. Vioel, P. Karlovsky, Plasma-based degradation of mycotoxins produced by Fusarium, Aspergillus and Alternaria species, Toxins 9 (3) (2017) 97–108.
[32] E. Wielogorska, Y. Ahmed, J. Meneely, W.G. Graham, C.T. Elliott, B.F. Gilmore, A holistic study to understand the detoxification of mycotoxins in maize and impact on its molecular integrity using cold atmospheric plasma treatment, Food Chem. 301 (2019) 125281.
[33] I.Y.S. Rustom, Aflatoxin in food and feed: occurrence, legislation and inactivation by physical methods, Food Chem. 59 (1) (1997) 57–67.
[34] J. Milani, G. Maleki, Effects of processing on mycotoxin stability in cereals, J. Sci. Food Agric. 94 (12) (2014) 2372–2375.
[35] S. Yener, H. Koksel, Effects of washing and drying applications on deoxynivalenol and zearalenone levels in wheat, World Mycotoxin J. 6 (3) (2013) 335–341.
[36] B.M. Mustapha, B. Mehrez, T. Jerbi, et al., Gamma radiation effects on microbiological, physico-chemical and antioxidant properties of Tunisian millet (Pennisetum Glaucum L.R.Br.), Food Chem. 154 (2014) 230–237.
[37] H. Hooshmand, C.F. Klopfenstein, Effects of gamma irradiation on mycotoxin disappearance and amino acid contents of corn, wheat, and soybeans with different moisture contents, Plant Foods Hum. Nutr. 47 (3) (1995) 227–238.
[38] Y. Hidaka, K. Kubota, Study on the sterilization of grain surface using UV radiation-Development and evaluation of UV irradiation equipment, Jpn. Agric. Res. Quart. 40 (2) (2006) 157–161.
[39] H. Murata, M. Mitsumatsu, N. Shimada, Reduction of feed-contaminating mycotoxins by ultraviolet irradiation: an in vitro study, Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 25 (9) (2008) 1107–1110.
[40] J. Ehlbeck, U. Schnabel, M. Polak, J. Winter, T. Von Woedtke, R. Brandenburg, T. Von Dem Hagen, K.D. Weltmann, Low temperature atmospheric pressure plasma sources for microbial decontamination, J. Phys. D-Appl. Phys. 44 (1) (2011) 013002.
[41] G.Y. Park, S.J. Park, M.Y. Choi, I.G. Koo, J.H. Byun, J.W. Hong, J.Y. Sim, G.J. Collins, J.K. Lee, Atmospheric-pressure plasma sources for biomedical applications, Plasma Sources Sci. Technol. 21 (2012) 043001.
[42] G. Fabio, P. Andrea, R. Alberto, et al., Dietary strategies to counteract the effects of mycotoxins: a review, J. Food Prot. 64 (1) (2001) 120–131.
[43] A.P. Santos Alexandre, R.S. Vela-Paredes, A.S. Santos, N.S. Costa, S.G. CanniattiBrazaca, M.A. Calori-Domingues, P.E. Duarte Augusto, Ozone treatment to reduce deoxynivalenol (DON) and zearalenone (ZEN) contamination in wheat bran and its impact on nutritional quality, Food Addit. Contam. Part A-Chem. Anal. Control Expo. Risk Assess. 35 (6) (2018) 1189–1199.
[44] A.P. Santos Alexandre, N. Castanha, N.S. Costa, A.S. Santos, E. Badiale-Furlong, P.E. Duarte Augusto, M.A. Calori-Domingues, Ozone technology to reduce zearalenone contamination in whole maize flour: degradation kinetics and impact on quality, J. Sci. Food Agric. 99 (15) (2019) 6814–6821.
[45] I. Reinholds, G. Juodeikiene, E. Bartkiene, D. Zadeike, V. Bartkevics, V. Krungleviciute, D. Cernauskas, D. Cižeikiene, Evaluation of ozonation as a method for mycotoxins degradation in malting wheat grains, World Mycotoxin J. 9 (3) (2016) 409–417.
[46] Y. Xu, Y. Wang, J. Ji, H. Wu, F. Pi, Y. Zhang, X. Sun, Chemical and toxicological alterations of zearalenone under ozone treatment, Food Addit. Contam. Part AChem. Anal. Control Expo. Risk Assess. 36 (1) (2019) 163–174.
[47] L. Qi, Y. Li, X. Luo, R. Wang, R. Zheng, L. Wang, Y. Li, D. Yang, W. Fang, Z. Chen, Detoxification of zearalenone and ochratoxin A by ozone and quality evaluation of ozonised corn, Food Addit. Contam. Part A-Chem. Anal. Control Expo. Risk Assess. 33 (11) (2016) 1700–1710.
[48] A.T. Tran, J. Kluess, A. Berk, M. Paulick, J. Frahm, D. Schatzmayr, J. Winkler, S. Kersten, S. Daenicke, Detoxification of Fusarium-contaminated maize with sodium sulphite-in vivo efficacy with special emphasis on mycotoxin residues and piglet health, Arch. Anim. Nutr. 72 (1) (2018) 58–75.
[49] I. Rempe, S. Kersten, H. Valenta, S. Daenicke, Hydrothermal treatment of naturally contaminated maize in the presence of sodium metabisulfite, methylamine and calcium hydroxide; effects on the concentration of zearalenone and deoxynivalenol, Mycotoxin Res. 29 (3) (2013) 169–175.
[50] M. Poor, Z. Faisal, A. Zand, T. Bencsik, B. Lemli, S. Kunsagi-Mate, L. Szente, Removal of zearalenone and zearalenols from aqueous solutions using insoluble beta-cyclodextrin bead polymer, Toxins 10 (6) (2018) 216–228.
[51] D. Greco, V. D’Ascanio, E. Santovito, A.F. Logrieco, G. Avantaggiato, Comparative efficacy of agricultural by-products in sequestering mycotoxins, J. Sci. Food Agric. 99 (4) (2019) 1623–1634.
[52] G. Avantaggiato, D. Greco, A. Damascelli, M. Solfrizzo, A. Visconti, Assessment of multi-mycotoxin adsorption efficacy of grape pomace, J. Agric. Food. Chem. 62 (2) (2014) 497–507.
[53] L. Gambacorta, P. Pinton, G. Avantaggiato, I.P. Oswald, M. Solfrizzo, Grape pomace, an agricultural byproduct reducing mycotoxin absorption: in vivo assessment in pig using urinary biomarkers, J. Agric. Food Chem. 64 (35) (2016) 6762–6771.
[54] J.M. Fernandes, T. Calado, A. Guimaraes, M.A.M. Rodrigues, L. Abrunhosa, In vitro adsorption of aflatoxin B1, ochratoxin A, and zearalenone by micronized grape stems and olive pomace in buffer solutions, Mycotoxin Res. 35 (3) (2019) 243–252.
[55] N.J. Althali, A.M. Hassan, M.A. Abdel-Wahhab, Effect of grape seed extract on maternal toxicity and in utero development in mice treated with zearalenone, Environ. Sci. Pollut. Res. 26 (6) (2019) 5990–5999.
[56] M. Long, S.H. Yang, J.X. Han, P. Li, Y. Zhang, S. Dong, X. Chen, J. Guo, J. Wang, J. B. He, The protective effect of grape-seed proanthocyanidin extract on oxidative damage induced by Zearalenone in Kunming Mice Liver, Int. J. Mol. Sci. 17 (6) (2016) 808–819.
[57] K.S. Mckenzie, A.B. Sarr, K. Mayura, et al., Oxidative degradation and detoxification of mycotoxins using a novel source of ozone, Food Chem. Toxicol. 35 (8) (1997) 807–820.
[58] N. Wang, W. Wu, J. Pan, et al., Detoxification strategies for zearalenone using microorganisms: a review, Microorganisms 7 (8) (2019) 208–221.
[59] Q. Shang, S. Jiang, Z. Yang, et al., Toxicity of mycotoxins from contaminated corn with or without yeast cell wall adsorbent on broiler chickens, AsianAustral. J. Anim. Sci. 29 (5) (2016) 674–680.
[60] H.A. Wall-Martinez, X. Pascari, A. Bigorda, A.J. Ramos, S. Marin, V. Sanchis, The fate of Fusarium mycotoxins (deoxynivalenol and zearalenone) through wort fermenting by Saccharomyces yeasts (S. cerevisiae and S. pastorianus), Food Res. Int. 126 (2019) 108587.
[61] F.B. Campagnollo, L.T. Franco, G.E. Rottinghaus, E. Kobashigawa, D.R. Ledoux, A. Dakovic, C.A.F. Oliveira, In vitro evaluation of the ability of beer fermentation residue containing Saccharomyces cerevisiae to bind mycotoxins, Food Res. Int. 77 (2015) 643–648.
[62] A. Rogowska, P. Pomastowski, J. Walczak, V. Railean-Plugaru, J. Rudnicka, B. Buszewski, Investigation of zearalenone adsorption and biotransformation by microorganisms cultured under cellular stress conditions, Toxins 11 (8) (2019) 463–480.
[63] A. Sangsila, V. Faucet-Marquis, A. Pfohl-Leszkowicz, P. Itsaranuwat, Detoxification of zearalenone by Lactobacillus pentosus strains, Food Control 62 (2016) 187–192.
[64] A. Krol, P. Pomastowski, K. Rafinska, V. Railean-Plugaru, J. Walczak, B. Buszewski, Microbiology neutralization of zearalenone using Lactococcus lactis and Bifidobacterium sp, Anal. Bioanal. Chem. 410 (3) (2018) 943–952.
[65] M.F. Vega, S.N. Dieguez, B. Riccio, S. Aranguren, A. Giordano, L. Denzoin, A.L. Soraci, M.O. Tapia, R. Ross, A. Apas, S.N. Gonzalez, Zearalenone adsorption capacity of lactic acid bacteria isolated from pigs, Braz. J. Microbiol. 48 (4) (2017) 715–723.
[66] M.R. Armando, R.P. Pizzolitto, C.A. Dogi, et al., Adsorption of ochratoxin A and zearalenone by potential probiotic Saccharomyces cerevisiae strains and its relation with cell wall thickness, J. Appl. Microbiol. 113 (2) (2012) 256–264.
[67] A. Yiannikouris, J. François, L. Poughon, Alkali extraction of beta-d-glucans from Saccharomyces cerevisiae cell wall and study of their adsorptive properties toward zearalenone, J. Agric. Food. Chem. 52 (11) (2004) 3666–3673.
[68] C.A. Haskard, H.S. El-Nezami, P.E. Kankaanpaa, et al., Surface binding of Aflatoxin B1 by lactic acid bacteria, Appl. Environ. Microbiol. 67 (7) (2001) 3086–3091.
[69] H. El-Nezami, N. Polychronaki, S. Salminen, et al., Binding rather than metabolism may explain the interaction of two food-grade lactobacillus strains with zearalenone and its derivative α-zearalenol, Appl. Environ. Microbiol. 68 (7) (2002) 3545.
[70] F.B. Taheur, K. Fedhila, K. Chaieb, et al., Adsorption of aflatoxin B1, zearalenone and ochratoxin A by microorganisms isolated from Kefir grains, Int. J. Food Microbiol. 251 (2017) 1–7.
[71] G. Juodeikiene, E. Bartkiene, D. Cernauskas, et al., Antifungal activity of lactic acid bacteria and their application for Fusarium mycotoxin reduction in malting wheat grains, LWT- Food Sci. Technol. 89 (2017) 307–314.
[72] G. Fu, J. Ma, L. Wang, X. Yang, J. Liu, X. Zhao, Effect of degradation of zearalenone-contaminated feed by bacillus licheniformis CK1 on postweaning female piglets, Toxins 8 (10) (2016) 300–310.
[73] J. Ju, S.E. Tinyiro, W. Yao, H. Yu, Y. Guo, H. Qian, Y. Xie, The ability of Bacillus subtilis and Bacillus natto to degrade zearalenone and its application in food, J. Food Process. Preserv. 43 (10) (2019) 001–009.
[74] Y. Wang, J. Zhang, Y. Wang, K. Wang, H. Wei, L. Shen, Isolation and characterization of the Bacillus cereus BC7 strain, which is capable of zearalenone removal and intestinal flora modulation in mice, Toxicon 155 (2018) 9–20.
[75] M.L. Gonzalez Pereyra, A.L. Di Giacomo, A.L. Lara, M.P. Martinez, L. Cavaglieri, Aflatoxin-degrading Bacillus sp. strains degrade zearalenone and produce proteases, amylases and cellulases of agro-industrial interest, Toxicon: Off. J. Int. Soc. Toxinol. 180 (2020) 43–48.
[76] S.W. Chen, H.T. Wang, W.Y. Shih, et al., Application of Zearalenone (ZEN)- detoxifying bacillus in animal feed decontamination through fermentation, Toxins 11 (6) (2019) 330–340.
[77] S.-W. Chen, J.-T. Hsu, Y.-A. Chou, H.-T. Wang, The application of digestive tract lactic acid bacteria with high esterase activity for zearalenone detoxification, J. Sci. Food Agric. 98 (10) (2018) 3870–3879.
[78] M. Zloch, A. Rogowska, P. Pomastowski, V. Railean-Plugaru, J. WalczakSkierska, J. Rudnicka, B. Buszewski, Use of Lactobacillus paracasei strain for zearalenone binding and metabolization, Toxicon: Off. J. Int. Soc. Toxinol. 181 (2020) 9–18.
[79] G. Wang, M. Yu, F. Dong, J. Shi, J. Xu, Esterase activity inspired selection and characterization of zearalenone degrading bacteria Bacillus pumilus ES-21, Food Control 77 (2017) 57–64.
[80] H. Zhang, M. Dong, Q. Yang, M.T. Apaliya, J. Li, X. Zhang, Biodegradation of zearalenone by Saccharomyces cerevisiae: Possible involvement of ZEN responsive proteins of the yeast, J. Proteomics 143 (2016) 416–423.
[81] L. Keller, L. Abrunhosa, K. Keller, C.A. Rosa, L. Cavaglieri, A. Venancio, Zearalenone and its derivatives alpha-zearalenol and beta-zearalenol decontamination by saccharomyces cerevisiae strains isolated from bovine forage, Toxins 7 (8) (2015) 3297–3308.
[82] C. Liu, J. Chang, P. Wang, Q. Yin, W. Huang, X. Dang, F. Lu, T. Gao, Zearalenone biodegradation by the combination of probiotics with cell-free extracts of aspergillus oryzae and its mycotoxin-alleviating effect on pig production performance, Toxins 11 (10) (2019) 552–565.
[83] H. Kamimura, Conversion of zearalenone to zearalenone glycoside by Rhizopus sp, Appl. Environ. Microbiol. 52 (3) (1986) 515–519.
[84] J. Plasencia, C.J. Mirocha, Isolation and characterization of zearalenone sulfate produced by Fusarium spp, Appl. Environ. Microbiol. 57 (1) (1991) 146.
[85] S.H. El-Sharkaway, M.I. Selim, M.S. Afifi, et al., Microbial transformation of zearalenone to a zearalenone sulfate, Appl. Environ. Microbiol. 57 (2) (1991) 549–552.
[86] B. Antje, D. Tatjana, K. Julia, et al., Biosynthesis and characterization of zearalenone-14-sulfate, zearalenone-14-glucoside and zearalenone-16- glucoside using common fungal strains, Toxins 10 (3) (2018) 104.
[87] X. Sun, X. He, K.S. Xue, et al., Biological detoxification of zearalenone by Aspergillus niger strain FS10, Food Chem. Toxicol. 72 (2014) 76–82.
[88] P. Li, W. Lin, X. Liu, X. Wang, L. Luo, Environmental factors affecting microbiota dynamics during traditional solid-state fermentation of Chinese Daqu starter, Front. Microbiol 7 (2016) 1237.
[89] Y. Wang, C.X. Zhao, D.D. Zhang, M.M. Zhao, M.M. Peng, P. Guo, Z.J. Cui, Microbial degradation of zearalenone by a novel microbial consortium, NZDC-6, and its application on contaminated corncob by semisolid fermentation, J Agric. Food Chem. 68 (6) (2020) 1634–1644.
[90] R. Kriszt, C. Krifaton, S. Szoboszlay, M. Cserhati, B. Kriszt, J. Kukolya, A. Czeh, S. Feher-Toth, L. Toeroek, Z. Szoke, K.J. Kovacs, T. Barna, S. Ferenczi, A new zearalenone biodegradation strategy using non-pathogenic rhodococcus pyridinivorans K408 strain, PLoS ONE 7 (9) (2012) 001–009.
[91] N. Takahashi-Ando, M. Kimura, H. Kakeya, H. Osada, I. Yamaguchi, A novel lactonohydrolase responsible for the detoxification of zearalenone: enzyme purification and gene cloning, Biochem. J 365 (2002) 1–6.
[92] S. El-Sharkawy, Y.J. Abul-Hajj, Microbial cleavage of zearalenone, Xenobiotica 18 (4) (1988) 365–371.
[93] J. Utermark, P. Karlovsky, Role of zearalenone lactonase in protection of Gliocladium roseum from fungitoxic effects of the mycotoxin zearalenone, Appl. Environ. Microbiol. 73 (2) (2007) 637–642.
[94] K. Bi, W. Zhang, Z. Xiao, D. Zhang, Characterization, expression and application of a zearalenone degrading enzyme from Neurospora crassa, Amb Express 8 (2018) 194–203.
[95] W. Peng, T.P. Ko, Y. Yang, et al., Crystal structure and substrate-binding mode of the mycoestrogen-detoxifying lactonase ZHD from Clonostachys rosea, RSC Adv. 4 (107) (2014) 62321–62325.
[96] Z. Xu, W. Liu, C.C. Chen, et al., Enhanced α-zearalenol hydrolyzing activity of a mycoestrogen-detoxifying lactonase by structure-based engineering, ACS Catal. 6 (2016) 7657–7663.
[97] I. Banu, A. Lupu, I. Aprodu, Degradation of zearalenone by laccase enzyme, Sci. Study Res. 14 (2) (2014) 079–084.
[98] X. Wang, Y. Bai, H. Huang, T. Tu, Y. Wang, Y. Wang, H. Luo, B. Yao, X. Su, Degradation of Aflatoxin B-1 and zearalenone by bacterial and fungal laccases in presence of structurally defined chemicals and complex natural mediators, Toxins 11 (10) (2019) 609–625.
[99] M. Loi, F. Fanelli, M.T. Cimmarusti, V. Mirabelli, M. Haidukowski, A.F. Logrieco, R. Caliandro, G. Mule, In vitro single and combined mycotoxins degradation by Ery4 laccase from Pleurotus eryngii and redox mediators, Food Control 90 (2018) 401–406.
[100] Y. Yu, L. Qiu, H. Wu, et al., Degradation of zearalenone by the extracellular extracts of Acinetobacter sp. SM04 liquid cultures, Biodegradation 22 (3) (2011) 613–622.
[101] Y. Yu, L. Qiu, H. Wu, Y. Tang, F. Lai, Y. Yu, Oxidation of zearalenone by extracellular enzymes from Acinetobacter sp SM04 into smaller estrogenic products, World J. Microbiol. Biotechnol. 27 (11) (2011) 2675–2681.
[102] X. Wang, X. Qin, Z. Hao, H. Luo, B. Yao, X. Su, Degradation of four major mycotoxins by eight manganese peroxidases in presence of a dicarboxylic acid, Toxins 11 (10) (2019) 566–581.
[103] M.S. Azam, D. Yu, N. Liu, A. Wu, Degrading ochratoxin A and zearalenone mycotoxins using a multifunctional recombinant enzyme, Toxins 11 (5) (2019) 301–322.
[104] Y. Yu, H. Wu, Y. Tang, L. Qiu, Cloning, expression of a peroxiredoxin gene from Acinetobacter sp SM04 and characterization of its recombinant protein for zearalenone detoxification, Microbiol. Res. 167 (3) (2012) 121–126.