Fungal mycotoxins
An overview
Svetlana V. Malysheva
Laboratory of Food Analysis, Department of Bio-analysis, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
Search for more papers by this authorJosé Diana Di Mavungu
Laboratory of Food Analysis, Department of Bio-analysis, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
Search for more papers by this authorSarah De Saeger
Laboratory of Food Analysis, Department of Bio-analysis, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
Search for more papers by this authorSvetlana V. Malysheva
Laboratory of Food Analysis, Department of Bio-analysis, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
Search for more papers by this authorJosé Diana Di Mavungu
Laboratory of Food Analysis, Department of Bio-analysis, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
Search for more papers by this authorSarah De Saeger
Laboratory of Food Analysis, Department of Bio-analysis, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium
Search for more papers by this authorDr. Vijai Kumar Gupta
Molecular Glycobiotechnology Group, Discipline of Biochemistry, School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
Search for more papers by this authorProf. Robert L. Mach
Institute of Chemical Engineering and Technical Biosciences, Vienna University of Technology, Vienna, Austria
Search for more papers by this authorProf. S. Sreenivasaprasad
Department of Life Sciences and Institute of Biomedical and Environmental Science and Technology, University of Bedfordshire, Bedfordshire, UK
Search for more papers by this authorSummary
Fungi are distributed worldwide, as they can grow on a wide range of substrates and under various conditions. Fungi not only play an important role in most ecosystems, but they have a direct impact on society due to production of secondary metabolites. From a big array of fungal secondary metabolites, some compounds are beneficial for the society (e.g. antibiotics), and others (e.g. mycotoxins) represent a threat to human and animal health and cause economic losses.
This chapter provides an overview of fungal secondary metabolites with emphasis on one of the most important groups, mycotoxins. The different classes of these metabolites are discussed. Due to an enormous diversity in chemical structures, biosynthetic origins and biological effects, only exemplary classifications are provided, which, however, form a complete and clear picture of similarities and differences between the metabolites. Furthermore, their impact on human and animal health is described. The different routes of human and animal exposure (ingestion, inhalation, dermal route) to mycotoxins are also presented and supported by occurrence data.
References
- Abarca, M.L., M.R. Bragulat, G. Castellá, F.J. Cabańes. 1994. Ochratoxin A production by strains of Aspergillus niger var. niger. Appl. Environ. Microbiol. 60: 2650–2652.
- Abnet, C.C., C.B. Borkowf, Y.L. Qiao, P.S. Albert, E. Wang, A.H. Merrill Jr., S.D. Mark, Z.W. Dong, P.R. Taylor, S.M. Dawsey. 2001. Sphingolipids as biomarkers of fumonisin exposure and risk of esophageal squamous cell carcinoma in China. Cancer Causes Control 12: 821–828.
- Adetayo, A.Q. 2011. Presence of aflatoxins in smoked-dried fish sold in Abeokuta, Ogun state, Southwestern Nigeria. A project report submitted to the Department of Agriculture and Fisheries Management, University of Agriculture, Abeokuta.
- Altomare, C., G. Perrone, M.C. Zonno, A. Evidente, R. Pengue, F. Fanti, L. Polonelli. 2000. Biological characterization of fusapyrone and deoxyfusapyrone, two bioactive secondary metabolites of Fusarium semitectum . J. Nat. Prod. 63: 1131–1135.
- Andersen, B., J. Smedsgaard, J.C. Frisvad. 2004. Penicillium expansum: Consistent production of patulin, chaetoglobosins, and other secondary metabolites in culture and their natural occurrence in fruit products. J. Agric. Food Chem. 52: 2421–2428.
- Ando, K., S. Suzuki, T. Seaki, G. Tamura, K. Arima. 1969. Funiculosin, a new antibiotic. Isolation, biological and chemical properties. J. Antibiot. 22: 189–194.
- Anfossi, L., C. Baggiani, C. Giovannoli, G. D'Arco, C. Passini, G. Giraudi. 2012. Occurrence of aflatoxin M1 in Italian cheese: Results of a survey conducted in 2010 and correlation with manufacturing, production season, milking animals, and maturation of cheese. Food Control 25: 125–130.
- Arroyo-Manzanares, N., A.M. García-Campana, L. Gámiz-Gracia. 2013. Multiclass mycotoxin analysis in Silybum marianum by ultra high performance liquid chromatography–tandem mass spectrometry using a procedure based on QuEChERS and dispersive liquid–liquid microextraction. J. Chromatogr. A 1282: 11–19.
- Arroyo-Manzanares, N., S.V. Malysheva, J. Vanden Bussche, L. Vanhaecke, J. Diana Di Mavungu, S. De Saeger. 2014. Holistic approach based on high resolution and multiple stage mass spectrometry to investigate ergot alkaloids in cereals. Talanta 118: 359–367.
- Ballio, A., E.B. Chain, P. De Leo, B.F. Erlanger, M. Mauri, A. Tonolo. 1964. Fusicoccin: A new wilting toxin produced by Fusicoccum amygdali Del. Nature 203: 297.
- Bennett, J.W., M. Klich. 2003. Mycotoxins. Clin. Microbiol. Rev. 16: 497–516.
- Berg, J.M., J.L. Tymoczko, L. Stryer. 2002. Biochemistry. 5th edition. W.H. Freeman, New York, USA, pp. 1050.
- Berthiller, F., C. Crews, C. Dall'Asta, S. De Saeger, G. Haesaert, P. Karlovsky, I.P. Oswald, W. Seefelder, G. Speijers, J. Stroka. 2013. Masked mycotoxins: A review. Mol. Nutr. Food Res. 57: 165–186.
- Berthiller, F., C. Dall'Asta, R. Schuhmacher, M. Lemmens, G. Adam, R. Krska. 2005a. Masked mycotoxins: Determination of a deoxynivalenol glucoside in artificially and naturally contaminated wheat by liquid chromatography-tandem mass spectrometry. J. Agric. Food Chem. 53: 3421–3425.
- Berthiller, F., R. Schuhmacher, G. Buttinger, R. Krska. 2005b. Rapid simultaneous determination of major type A- and B-trichothecenes as well as zearalenone in maize by high performance liquid chromatography-tandem mass spectrometry. J. Chromatogr. A 1062: 209–216.
- Berthiller, F., M. Sulyok, R. Krska, R. Schuhmacher. 2007. Chromatographic methods for the simultaneous determination of mycotoxins and their conjugates in cereals. Int. J. Food Microbiol. 119: 33–37.
- Berthiller, F., U. Werner, M. Sulyok, R. Krska, M.-T. Hauser, R. Schuhmacher. 2006. Liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) determination of phase II metabolites of the mycotoxin zearalenone in the model plant Arabidopsis thaliana . Food Addit. Contam. 23: 1194–1200.
- Betina, V. 1989. Structure-activity relationships among mycotoxins. Chem. Biol. Interact. 71: 105–146.
- Bezuidenhout, S.C., W.C.A. Gelderblom, C.P. Gorst-Allman, R.M. Horak, W.F.O. Marasas, G. Spiteller, R. Vleggaar. 1988. Structure elucidation of the fumonisins, mycotoxins from Fusarium moniliforme . J. Chem. Soc. Chem. Commun. 11: 743–745.
- Bhat, R.V., P.H. Shetty, R.P. Amruth, R.V. Sudershan. 1997. A foodborne disease outbreak due to the consumption of moldy sorghum and maize containing fumonisin mycotoxins. J. Toxicol. Clin. Toxicol. 35: 249–255.
- Bhatnagar, D., J. Yu, K. Ehrlich. 2002. Toxins of filamentous fungi. In: Fungal Allergy and Pathogenicity. Chemical Immunology. Eds. by M. Breitenbach, R. Crameri, S.B. Lehner Basel, Karger, Vol. 81, 167–206.
- Binder, E.M., L.M. Tan, L.J. Chin, J. Handl, J. Richard. 2007. Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Anim. Feed Sci. Technol. 137: 265–282.
- Bloom, E., K. Bal, E. Nyman, A. Must, L. Larsson. 2007. Mass spectrometry-based strategy for direct detection and quantification of some mycotoxins produced by Stachybotrys and Aspergillus spp. in indoor environments. Appl. Environ. Microbiol. 73: 4211–4217.
- Bloom, E., E. Nyman, A. Must, C. Pehrson, L. Larsson. 2009. Molds and mycotoxins in indoor environments – A survey in water-damaged buildings. J. Occup. Environ. Hyg. 6: 671–678.
- Blount, W.P. 1961. Turkey ‘X’ disease. Turkeys 9: 55–58, 61, 77.
- Bokhari, F.M. 2007. Mycotoxins and toxigenic fungi in Arabic coffee beans in Saudi Arabia. Adv. Biol. Res. 1: 56–66.
- Boonen, J., S.V. Malysheva, L. Taevernier, J. Diana Di Mavungu, S. De Saeger, B. De Spiegeleer. 2012. Human skin penetration of selected model mycotoxins. Toxicology 301: 21–32.
- Brakhage, A.A. 2013. Regulation of fungal secondary metabolism. Nat. Rev. Microbiol. 11: 21–32.
- Brakhage, A.A., V. Schroeckh. 2011. Fungal secondary metabolites – Strategies to activate silent gene clusters. Fungal Genet. Biol. 48: 15–22.
- Briones-Reyes, D., L. Gómez-Martinez, R. Cueva-Rolón. 2007. Zearalenone contamination in corn for human consumption in the state of Tlaxcala, Mexico. Food Chem. 100: 693–698.
- Bud, R. 2007. Penicillin. Oxford University Press, New York, p. 330.
- Burge, P.S. 2004. Sick building syndrome. Occup. Environ. Med. 61: 185–190.
- Cai, Q., L. Tang, J.-S. Wang. 2007. Validation of fumonisin biomarkers in F344 rats. Toxicol. Appl. Pharm. 225: 28–39.
- Cano-Sancho, G., S. Marin, A.J. Ramos, V. Sanchis. 2012. Occurrence of zearalenone, an oestrogenic mycotoxin, in Catalonia (Spain) and exposure assessment. Food Chem. Toxicol. 50: 835–839.
- Cavaliere, C., P. Foglia, C. Guarino, M. Nazzari, R. Samperi, A. Laganà. 2007. Determination of aflatoxins in olive oil by liquid chromatography-tandem mass spectrometry. Anal. Chim. Acta 596: 141–148.
- Cho, M.S., K. Kim, E. Seo, N. Kassim, A.B. Mtenga, W.-B. Shim, S.-H. Lee, D.-H. Chung. 2010. Occurrence of patulin in various fruit juices from South Korea: An exposure assessment. Food Sci. Biotechnol. 19: 1–5.
- Ciegler, A., R.W. Detroy, E.B. Lillehoj. 1971. Patulin, penicillic acid, and other carcinogenic lactones. In: Microbial Toxins, Vol. 6: Fungal Toxins. Eds. by S.J. Ajl, S. Kadis, A. Ciegler, G. Weinbaum, T.C Montie. Academic Press, New York, pp. 409–434.
- Copetti, M.V., B.T. Iamanaka, J.L. Pereira, M.H. Fungaro, M.H. Taniwaki. 2011. Aflatoxigenic fungi and aflatoxin in cocoa. Int. J. Food Microbiol. 148: 141–144.
- Crews, C., W.A.C. Anderson, G. Rees, R. Krska. 2009. Ergot alkaloids in some rye-based UK cereal products. Food Addit. Contam. Part B 2: 79–85.
- Croft, W.A., B.B. Jams, C.S. Yatawaxa. 1986. Airborne outbreak of trichothecene toxicosis. Atmos. Environ. 20: 549–552.
- Daradimos, E., P. Marcaki, M. Koupparis. 2000. Evaluation and validation of two fluorometric HPLC methods for the determination of aflatoxin B1 in olive oil. Food Addit. Contam. 17: 65–73.
- De Boevre, M., J. Diana Di Mavungu, S. Landschoot, K. Audenaert, M. Eeckhout, P. Maene, G. Haesaert, S. De Saeger. 2012. Natural occurrence of mycotoxins and their masked forms in food and feed products. World Mycotoxin J. 5: 207–219.
- De Zotti, M., F. Damato, F. Formaggio, M. Crisma, E. Schievano, S. Mammi, B. Kaptein, Q.B. Broxterman, P.J. Felock, D.J. Hazuda, S.B. Singh, J. Kirschbaum, H. Brückner, C. Toniolo. 2010. Total synthesis, characterization, and conformational analysis of the naturally occurring hexadecapeptide integramide A and a diastereomer. Chem. Eur. J. 16: 316–327.
- Deacon, J. 2006. Fungal Biology. 4th edition. Blackwell Publishing Ltd., Oxford, p. 371.
- Diana Di Mavungu, J., S. Monbaliu, M.-L. Scippo, G. Maghuin-Rogister, Y.-J. Schneider, Y. Larondelle, A. Callebaut, J. Robbens, C. Van Peteghem, S. De Saeger. 2009. LC-MS/MS multi-analyte method for mycotoxin determination in food supplements. Food Addit. Contam. 26: 885–895.
- Directive 2002/32/EC. 2002. Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on undesirable substances in animal feed. Off. J. Eur. Comm. L140: 10–21.
- D'Mello, J.P.F., A.M.C. Macdonald. 1997. Mycotoxins. Anim. Sci. Technol. 69: 155–166.
- Dragusel, R. 2011. Biomarkers of Mycotoxin Exposure in Humans. PhD dissertation, Utrecht University, p. 28. Available from: http://igitur-archive.library.uu.nl/student-theses/2011-0707-200339/Biomarkers%20of%20Mycotoxin%20Exposure%20in%20Humans.pdf (accessed 6 September 2013).
- Driehuis, F., M.C. Spanjer, J.M. Scholten, M.C. te Giffel. 2008. Occurrence of mycotoxins in feedstuffs of dairy cows and estimation of total dietary intakes. J. Dairy Sci. 91: 4261–4271.
- Ediage, E.N., J. Diana Di Mavungu, S. Monbaliu, C. Van Peteghem, S. De Saeger. 2011. A validated multianalyte LC-MS/MS method for quantification of 25 mycotoxins in cassava flour, peanut cake and maize samples. J. Agric. Food Chem. 59: 5173–5180.
- Eisfeld, C. 2009. Nonribosomal peptide synthetases of fungi. In: The Mycota. Physiology and Genetics: Selected Basic and Applied Aspects. Eds. by T. Anke, D. Weber Springer-Verlag, Berlin, Vol. 15, pp. 305–330.
-
European Food Safety Authority (EFSA). 2004. Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission related to aflatoxin B1 as undesirable substance in animal feed. EFSA J. 39: 1–27.
10.2903/j.efsa.2004.1 Google Scholar
- European Food Safety Authority (EFSA). 2005. Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission related to ergot as undesirable substance in animal feed. EFSA J. 225: 1–27.
- European Food Safety Authority (EFSA). 2011. Scientific opinion on the risks for animal and public health related to the presence of T-2 and HT-2 toxin in food and feed. EFSA J. 9, pp. 187.
-
Fernández-Cruz, M.L., M.L. Mansilla, J.L. Tadeo. 2010. Mycotoxins in fruits and their processed products: Analysis, occurrence and health implications. J. Adv. Res. 1: 113–122.
10.1016/j.jare.2010.03.002 Google Scholar
- Fink-Gremmels, J. 1999. Mycotoxins: Their implications for human and animal health. Vet. Q. 21: 115–120.
- Fox, E.M., B.J. Howlett. 2008. Secondary metabolism: Regulation and role in fungal biology. Curr. Opin. Microbiol. 11: 481–487.
- Ge, H.M., Z.G. Yu, J. Zhang, J.H. Wu, R.X. Tan. 2009. Bioactive alkaloids from endophytic Aspergillus fumigatus . J. Nat. Prod. 72: 753–755.
- Ghitakou, S., K. Koutras, E. Kanellou, P. Markaki. 2006. Study of aflatoxin B1 and ochratoxin A production by natural microflora and Aspergillus parasiticus in black and green olives of Greek origin. Food Microbiol. 23: 612–621.
- Goliński, P., K. Hult, J. Grabarkiewicz-Szczesna, J. Chelkowski, P. Kneblewski, K. Szebiotko. 1984. Mycotoxic porcine nephropathy and spontaneous occurrence of ochratoxin A residues in kidneys and blood of polish swine. Appl. Environ. Microbiol. 47: 1210–1212.
- Griffin, D.H. 1994. Fungal Physiology. 2nd edition. Wiley-Liss, Inc., New York, p. 458.
- Groopman, J.D., J.A. Hasler, L.J. Trudel, A. Pikul, P.R. Donahue, G.N. Wogan. 1992. Molecular dosimetry in rat urine of aflatoxin-N7-guanine and other aflatoxin metabolites by multiple monoclonal antibody affinity chromatography and immunoaffinity/high performance liquid chromatography. Cancer Res. 52: 267–274.
- Groopman, J.D., T.W. Kensler. 2005. Role of metabolism and viruses in aflatoxin-induced liver cancer. Toxicol. Appl. Pharm. 206: 131–137.
- Hanson, J.R. 2008. The Chemistry of Fungi. The Royal Society of Chemistry, Cambridge, p. 204.
-
Herbert, R.B. 1989. The Biosynthesis of Secondary Metabolites. Springer, New York, p. 231.
10.1007/978-94-010-9132-9 Google Scholar
- Hewitt, T.C., C.L. Flack, J.K. Kolodziejczyk, A.M. Chacon, K.L. D'Ovidio. 2012. Occurrence of zearalenone in fresh corn and corn products collected from local Hispanic markets in San Diego County, CA. Food Control 26: 300–304.
- Humpf, H.U., E.M. Schmelz, F.I. Filmore, H. Vesper, T.R. Vales, E. Wang, D.S. Menaldino, D.C. Liotta, A.H. Merrill. 1998. Acylation of naturally occurring and synthetic 1-deoxysphinganines by ceramide synthase. J. Biol. Chem. 273: 19060–19064.
- Humpf, H.-U., K.A. Voss. 2004. Effects of thermal food processing on the chemical structure and toxicity of fumonisin mycotoxins. Mol. Nutr. Food Res. 48: 255–269.
- International Agency for Research on Cancer (IARC). 1987. Overall evaluations of carcinogenicity: An updating of IARC Monographs, volumes 1 to 42. Report of an IARC Expert Committee. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Supplement 7, Lyon, France.
- International Agency for Research on Cancer (IARC). 1993. Some naturally occurring substances: Food, items and constituents, heterocyclic aromatic amines and mycotoxins, volume 56. Report of an IARC Expert Committee. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Lyon, France, p. 397.
- Jarvis, B.B., J.D. Miller. 2005. Mycotoxins as harmful indoor air contaminants. Appl. Microbiol. Biotechnol. 66: 367–372.
- Joffe, A.Z., H. Ungar. 1969. Cutaneous lesions produced by topical application of aflatoxin to rabbit skin. J. Invest. Dermatol. 52: 504–507.
- Jonsyn-Ellis, F.E. 2000. Seasonal variation in exposure frequency and concentration levels of aflatoxins and ochratoxins in urine samples of boys and girls. Mycopathologia 152: 35–40.
- Kemppainen, B.W., R.T. Riley, J.G. Pace. 1984. Penetration of [3H]T-2 toxin through excised human and guinea-pig skin during exposure to [3H]T-2 toxin adsorbed to corn dust. Food Chem. Toxicol. 22: 893–896.
- Kemppainen, B.W., R.T. Riley, J.G. Pace. 1988–1989. Skin absorption as a route of exposure for aflatoxin and trichothecenes. J. Toxicol. Toxin Rev. 7: 95–120.
- Kensler, T.W., B.D. Roebuck, G.N. Wogan, J.D. Groopman. 2011. Aflatoxins: A 50-year odyssey of mechanistic and translational toxicology. Toxicol. Sci. 120: S28–S48.
- Kim, D.-H., H.-S. Yoo, Y.-M. Lee, J.-H. Kie, S. Jang, S. Oh. 2006. Elevation of sphinganine 1-phosphate as a predictive biomarker for fumonisin exposure and toxicity in mice. J. Toxicol. Environ. Health A 69: 2071–2082.
- King, B. 1979. Outbreak of ergotism in Wollo, Ethiopia. Lancet 1: 1411.
- Kostelanska, M., M. Zachariasova, O. Lacina, M. Fenclova, A.-L. Kollos, J. Hajslova. 2011. The study of deoxynivalenol and its masked metabolites fate during the brewing process realised by UPLC–TOFMS method. Food Chem. 4: 1870–1876.
- Kozlovskii, A.G., N.G. Vinokurova, V.P. Zhelifonova. 2000. Mycotoxin production profiles of Penicillium vulpinum (Cooke & Massee) Seifert & Samson strains. Microbiology 69: 36–39.
- Krska, R., G. Stubbings, R. Macarthur, C. Crews. 2008. Simultaneous determination of six major ergot alkaloids and their epimers in cereals and foodstuffs by LC-MS-MS. Anal. Bioanal. Chem. 391: 563–576.
- Kuiper-Goodman, T., P.M. Scott, H. Watanabe. 1987. Risk assessment of the mycotoxin zearalenone. Regul. Toxicol. Pharmacol. 7: 253–306.
- Kurobane, I., R. Hutchinson, L. Vining. 1981. The biosynthesis of fulvic acid, a fungal metabolite of heptaketide origin. Tetrahedron Lett. 22: 493–496.
- Lasztity, R. 2009. Micro-organisms important in food microbiology. In: Food Quality and Standards, Ed.: R. Lasztity, EOLSS Publishers Co. Ltd, Oxford, UK, Vol. III, pp. 26–40.
- Lattanzio, V.M.T., M. Pascale, A. Visconti. 2009. Current analytical methods for trichothecene mycotoxins in cereals. Trends Anal. Chem. 28: 758–768.
- Lattanzio, V.M.T., A. Visconti, M. Haidukowski, M. Pascale. 2012. Identification and characterization of new Fusarium masked mycotoxins, T2 and HT2 glycosyl derivatives, in naturally contaminated wheat and oats by liquid chromatography-high-resolution mass spectrometry. J. Mass Spectrom. 47: 466–475.
- Lau, B.P., P.M. Scott, D.A. Lewis, S.R. Kanhere, C. Cleroux, V.A. Roscoe. 2003. Liquid chromatography-mass spectrometry and liquid chromatography-tandem mass spectrometry of the Alternaria mycotoxins alternariol and alternariol monomethyl ether in fruit juices and beverages. J. Chromatogr. A 998: 119–131.
- Leszczynska, J., U. Kucharska, H. Żegota. 2000. Aflatoxins in nuts assayed by immunological methods. Eur. Food Res. Technol. 2010: 213–215.
- Li, F.-Q., T. Yoshizawa, O. Kawamura, X.-Y. Luo, Y.-W. Li. 2001. Aflatoxins and fumonisins in corn from the high-incidence area for human hepatocellular carcinoma in Guangxi, China. J. Agric. Food Chem. 49: 4122–4126.
- Magan, N., M. Olsen. 2004. Mycotoxins in food. Woodhead Publishing Ltd, Cambridge, p. 471.
- Mahmood, Z.A., S.W. Ahmed, I. Azhar, M. Sualeh, M.T. Baig, S. Zoha. 2010. Bioactive alkaloids produced by fungi. I. Updates on alkaloids from the species of the genera Boletus, Fusarium and Psilocybe . Pak. J. Pharm. Sci. 23: 349–357.
- Mahnine, N., G. Meca, M. Fernández-Franzón, J. Mañes, A. Zinedine. 2012. Occurrence of fumonisins B1, B2 and B3 in breakfast and infant cereals from Morocco. Phytopathol. Mediterr. 51: 193–197.
- Malysheva, S.V., D.A. Larionova, J. Diana Di Mavungu, S. De Saeger. 2014a. Pattern and distribution of ergot alkaloids in cereals and cereal products from European countries. World Mycotoxin J. 7: 217–230.
- Malysheva, S.V., V. Polizzi, A. Moretti, C. Van Peteghem, N. De Kimpe, J. Van Bocxlaer, J. Diana Di Mavungu, S. De Saeger. 2014b. Untargeted screening of secondary metabolites in fungal cultures and samples from mouldy indoor environments by time-of-flight mass spectrometry. World Mycotoxin J. 7: 35–44.
- Martins, M.L., H.M. Martins, F. Bernardo. 2001. Fumonisins B-1 and B-2 in black tea and medicinal plants. J. Food Prot. 64: 1268–1270.
- Maskey, R.P., I. Grun-Wollny, H. Laatsch. 2003. Isolation, structure elucidation and biological activity of 8-O-methylaverufin and 1, 8-O-dimethylaverantin as new antifungal agents from Penicillium chrysogenum . J. Antibiot. 56: 488–491.
- Metzler, M. 2011. Proposal for a uniform designation of zearalenone and its metabolites. Mycotoxin Res. 27: 1–3.
-
Milićević, D.R., V.B. Jurić, D.Z. Vuković, M.M. Mandić, T.M. Baltić. 2009. Residue of ochratoxin A in swine tissues – Risk assessment. Arch. Oncol. 17: 56–60.
10.2298/AOO0904056M Google Scholar
- Miraglia, M., H.J.P. Marvin, G.A. Kleter, P. Battilani, C. Brera, E. Coni, F. Cubadda, L. Croci, B. De Santis, S. Dekkers, L. Filippi, R.W.A. Hutjes, M.Y. Noordam, M. Pisante, G. Piva, A. Prandini, L. Toti, G.J. van den Born, A. Vespermann. 2009. Climate change and food safety: An emerging issue with special focus on Europe. Food Chem. Toxicol. 47: 1009–1021.
- Mirocha, C.J., R.A. Pawlosky, K. Chatterjee, S. Watson, W. Hayes. 1983. Analysis for Fusarium toxins in various samples implicated in biological warfare in Southeast Asia. J. Assoc. Off. Anal. Chem. 66: 1485–1499.
- Mngadi, P.T., R. Govinden, B. Odhav. 2008. Co-occurring mycotoxins in animal feeds. Afr. J. Biotechnol. 7: 2239–2243.
- Monbaliu, S., C. Van Poucke, C. Detavernier, F. Dumoulin, M. Van De Velde, E. Schoeters, S. Van Dyck, O. Averkieva, C. Van Peteghem, S. De Saeger. 2010a. Occurrence of mycotoxins in feed as analyzed by a multi-mycotoxin LC-MS/MS method. J. Agric. Food Chem. 58: 66–71.
- Monbaliu, S., A. Wu, D. Zhang, C. Van Peteghem, S. De Saeger. 2010b. Multimycotoxin UPLC-MS/MS for tea, herbal infusions and the derived drinkable products. J. Agric. Food Chem. 58: 12664–12671.
-
Moore, D. 1998. Fungal Morphogenesis. Developmental and Cell Biology Series. Cambridge University Press, New York, p. 469.
10.1017/CBO9780511529887 Google Scholar
- Mulac, D., H.-U. Humpf. 2011. Cytotoxicity and accumulation of ergot alkaloids in human primary cells. Toxicology 282: 112–121.
- Mulder, P.P.J., L.W.D. van Raamsdonk, H.J. van Egmond, J. Voogt, M.W. van Brakel, G.M. van der Horst, J. de Jong. 2012. Dutch Survey Ergot Alkaloids and Sclerotia in Animal Feeds. RIKILT Report 2012.005. RIKILT – Institute of Food Safety, the Netherlands, p. 54.
- Muñoz, K., M. Blaszkewicz, G.H. Degen. 2010. Simultaneous analysis of ochratoxin A and its major metabolite ochratoxin alpha in plasma and urine for an advanced biomonitoring of the mycotoxin. J. Chromatogr. B 878: 2623–2629.
-
Murphy, M. 2006. Sick Building Syndrome and the Problem of Uncertainty: Environmental Politics, Technoscience, and Women Workers. Duke University Press, Durham, NC, p 253.
10.1215/9780822387831 Google Scholar
- Musser, S.M., M.L. Gay, E.P. Mazzola. 1996. Identification of a new series of fumonisins containing 3-hydroxypyridine. J. Nat. Prod. 59: 970–972.
- Musser, S.M., R.D. Plattner. 1997. Fumonisin composition in cultures of Fusarium moniliforme, Fusarium proliferatum, and Fusarium nygami . J. Agric. Food Chem. 45: 1169–1173.
- Nikièma, P.N., L. Worrillow, A.S. Traoré, C.P. Wild, P.C. Turner. 2004. Fumonisin contamination of maize in Burkina Faso, West Africa. Food Addit. Contam. 21: 865–870.
- Nikiema, P.A., L. Worrilow, A.S. Traore, C.P. Wild, P.C. Turner. 2008. Fumonisin exposure and the sphinganine/sphingosine ratio in urine, serum and buccal cells in adults from Burkina Faso, West Africa. World Mycotoxin J. 1: 483–491.
- Njobeh, P.B., M.F. Dutton, A.T. Åberg, P. Haggblom. 2012. Estimation of multi-mycotoxin contamination in South African compound feeds. Toxins 4: 836–848.
- Odhav, B., V. Naicker. 2002. Mycotoxins in South African traditionally brewed beers. Food Addit. Contam. 19: 55–61.
- Oh, H., D.C. Swenson, J.B. Gloer, D.T. Wicklow, P.E. Dowd. 1998. Chaetochalasin A: A new bioactive metabolite from Chaetomium brasiliense . Tetrahedron Lett. 39: 7633–7636.
- Omurtag, G.Z., D. Yazicioglu. 2004. Determination of fumonisins B-1 and B-2 in herbal tea and medicinal plants in Turkey by high performance liquid chromatography. J. Food Prot. 67: 1782–1786.
- O'Riordan, M.J., M.G. Wilkinson. 2008. A survey of the incidence and level of aflatoxin contamination in a range of imported spice preparations on the Irish retail market. Food Chem. 107: 1429–1435.
- Ostry, V. 2008. Alternaria mycotoxins: An overview of chemical characterization, producers, toxicity, analysis and occurrence in foodstuffs. World Mycotoxin J. 1: 175–188.
- Peers, F.G., C.A. Linsell. 1973. Dietary aflatoxins and liver cancer – A population based study in Kenya. Br. J. Cancer 27: 473–484.
- Peraica, M., B. Radić, A. Lucić, M. Pavlović. 1999. Toxic effects of mycotoxins in humans. Bull. World Health Organ. 77: 754–766.
- Polizzi, V., B. Delmulle, A. Adams, A. Moretti, A. Susca, A.M. Picco, Y. Rosseel, R. ’tKindt, J. Van Bocxlaer, N. De Kimpe, C. Van Peteghem, S. De Saeger. 2009. JEM spotlight: Fungi, mycotoxins and microbial volatile organic compounds in mouldy interiors from water-damaged buildings. J. Environ. Monitor. 11: 1849–1858.
- Polonsky, J., M.A. Merrien, P.M. Scott. 1977. Roquefortine and isofumigaclavine A, alkaloids from Penicillium roqueforti . Ann. Nutr. Aliment. 31: 963–968.
- Proctor, R.H., A.E. Desjardins, R.D. Plattner, T.M. Hohn. 1999. A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet. Biol. 27: 100–112.
- Quiroga, N., S. Resnik, A. Pacin, E. Martinez, A. Pagano, I. Riccobene, S. Neira. 1995. Natural occurrence of trichothecenes and zearalenone in Argentine wheat. Food Control 6: 201–204.
- Rapid Alert System for Food and Feed (RASFF). n.d. Available from: http://ec.europa.eu/food/ (accessed 1 September 2013).
- Rodrigues, I., J. Handl, E.M. Binder. 2011. Mycotoxin occurrence in commodities, feeds and feed ingredients sourced in the Middle East and Africa. Food Addit. Contam. B 4: 168–179.
- Rohlfs, M., M. Trienens, U. Fohgrub, F. Kempken. 2009. Evolutionary and ecological interactions of moulds and insects. In: The Mycota. Physiology and Genetics: Selected Basic and Applied Aspects. Eds. by T. Anke, D. Weber Springer-Verlag, Berlin, Vol. 15, pp. 133–152.
- Ruhland, M., G. Engelhardt, W. Schäfer, P.R. Wallnöfer. 1996. Transformation of the mycotoxin ochratoxin A in plants: 1. Isolation and identification of metabolites formed in cell suspension cultures of wheat and maize. Nat. Toxins 4: 254–260.
- Ruhland, M., J. Tischler. 2008. Determination of ergot alkaloids in feed by HPLC. Mycotoxin Res. 24: 73–79.
- Schardl, C.I., D.G. Panaccione, P. Tudzynski. 2006. Ergot alkaloids – Biology and molecular biology. In: The Ergot Alkaloids. Elsevier Inc., Amsterdam, Vol. 63, pp. 45–86.
- Schiff, P.L. 2006. Ergot and its alkaloids. Am. J. Pharm. Educ. 70: 98.
- Schollenberger, M., H.-M. Müller, K. Ernst, S. Sondermann, M. Liebscher, C. Schlecker, G. Wischer, W. Drochner, K. Hartung, H.-P. Piepho. 2012. Occurrence and distribution of 13 trichothecene toxins in naturally contaminated maize plants in Germany. Toxins 4: 778–787.
- Schroeder, H.W., W.H. Kelton. 1975. Production of sterigmatocystin by some species of the genus Aspergillus and its toxicity to chicken embryos. Appl. Microbiol. 30: 589–591.
- Scott, P.M. 2001. Analysis of agricultural commodities and foods for Alternaria mycotoxins. J. AOAC Int. 84: 1809–1817.
- Scott, P.M., G.A. Lawrence, B.P.-Y. Lau. 2006. Analysis of wines, grape juices and cranberry juices for Alternaria toxins. Mycotoxin Res. 22: 142–147.
- Scudamore, K.A., S. Nawaz, M.T. Hetmanski. 1998. Mycotoxins in ingredients of animal feeding stuffs: II. Determination of mycotoxins in maize and maize products. Food Addit. Contam. 15: 30–55.
- Seefelder, W., A. Knecht, H.-U. Humpf. 2003. Bound fumonisin B1: Analysis of fumonisin-B1 glyco and amino acid conjugates by liquid chromatography-electrospray ionization-tandem mass spectrometry. J. Agric. Food Chem. 51: 5567–5573.
- Seydametova, E., R.B.H. Kambol, N.B. Zainol. 2010. Morphological characterization of soil Penicillium sp. strains – Potential producers of statins. Biotechnology Symposium IV, 1–3 December 2010, Universiti Malaysia Sabah, Sabah, Malaysia.
- Shen, B. 2000. Biosynthesis of aromatic polyketides. Biosynthesis. Aromatic polyketides, isoprenoids, alkaloids. In: Topics in Current Chemistry. Eds. by F.J. Leeper, J.C Vederas. Springer, New York, Vol. 209, p. 247.
- Singh, S.B., K. Herath, Z. Guan, D.L. Zink, A.W. Dombrowski, J.D. Polishook, K.C. Silverman, R.B. Lingham, P.J. Felock, D.J. Hazuda. 2002. Integramides A and B, two novel non-ribosomal linear peptides containing nine Cα-methyl amino acids produced by fungal fermentations that are inhibitors of HIV-1 integrase. Org. Lett. 4: 1431–1434.
- Singh, S.B., D.L. Zink, G.F. Bills, A. Teran, K.C. Silverman, R.B. Lingham, P. Felock, D.J. Hazuda. 2003. Four novel bis-(naphtho-γ-pyrones) isolated from Fusarium species as inhibitors of HIV-1 integrase. Bioorg. Med. Chem. Lett. 13: 713–717.
- Smoragiewicz, W., B. Cossette, A. Boutard, K. Krzystyniak. 1993. Trichothecene mycotoxins in the dust of ventilation systems in office buildings. Int. Arch. Occup. Environ. Health 65: 113–117.
- Solfrizzo, M., S.N. Chulze, C. Mallmann, A. Visconti, A. De Girolamo, F. Rojo, A. Torres. 2004a. Comparison of urinary sphingolipids in human populations with high and low maize consumption as a possible biomarker of fumonisin dietary exposure. Food Addit. Contam. 21: 1090–1095.
- Solfrizzo, M., A. De Girolamo, C. Vitti, A. Visconti, R. Van den Bulk. 2004b. Liquid chromatographic determination of Alternaria toxins in carrots. J. AOAC Int. 87: 101–106.
- Sommer, N.F., J.R. Buchanan, R.J. Fortlage. 1976. Aflatoxin and sterigmatocystin contamination of pistachio nuts in orchards. Appl. Environ. Microbiol. 32: 64–67.
- Streit, E., G. Schatzmayr, P. Tassis, E. Tzika, D. Marin, I. Taranu, C. Tabuc, A. Nicolau, J. Aprodu, O. Puel, E.P. Oswald. 2012. Current situation of mycotoxin contamination and co-occurrence in animal feed-focus on Europe. Toxins 4: 788–809.
- Sweeney, M.J., A.D. Dobson. 1998. Mycotoxin production by Aspergillus, Fusarium and Penicillium species. Int. J. Food Microbiol. 43: 141–158.
- Tam, J., M. Mankotia, M. Mably, P. Pantazopoulos, R.J. Neil, P. Calway, P.M. Scott. 2006. Survey of breakfast and infant cereals for aflatoxins B1, B2, G1 and G2. Food Addit. Contam. 23: 693–699.
- Täubel, M., M. Sulyok, V. Vishwanath, E. Bloom, M. Turunen, K. Järvi, E. Kauhanen, R. Krska, A. Hyvärinen, L. Larsson, A. Nevalainen. 2011. Co-occurrence of toxic bacterial and fungal secondary metabolites in moisture-damaged indoor environments. Indoor Air 21: 368–375.
- Tiwary, A.K., B. Puschner, R.H. Poppenga. 2009. Using roquefortine C as a biomarker for penitrem A intoxication. J. Vet. Diagn. Invest. 21: 237–239.
- Torres, M., R. Canela, M. Riba, V. Sanchis. 1987. Production of patulin and griseofulvin by a strain of Penicillium griseofulvum in three different media. Mycopathologia 99: 85–89.
- Tran, S.T., D. Tardieu, A. Auvergne, J.D. Bailly, R. Babilé, S. Durand, G. Benard, P. Guerre. 2006. Serum sphinganine and the sphinganine to sphingosine ratio as a biomarker of dietary fumonisins during chronic exposure in ducks. Chem. Biol. Interact. 160: 41–50.
- Tuomi, T., K. Reijula, T. Johnsson, K. Hemminki, E.-L. Hintikka, O. Lindroos, S. Kalso, P. Koukila-Kähko¨︁lä, H. Mussalo-Rauhamaa, T. Haahtela. 2000. Mycotoxins in crude building materials from water-damaged buildings. Appl. Environ. Microbiol. 66: 1899–1904.
- Turner, P.C., V.J. Burley, J.A. Rothwell, K.L.M. White, J.E. Cade, C.P. Wild. 2008. Dietary wheat reduction decreases the level of urinary deoxynivalenol in UK adults. J. Expo. Sci. Environ. Epidemiol. 18: 392–399.
- Vaclavik, L., M. Vaclavikova, T.H. Begley, A.J. Krynitsky, J.I. Rader. 2013. Determination of multiple mycotoxins in dietary supplements containing green coffee bean extracts using ultra high-performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS). J. Agric. Food Chem. 61: 4822–4830.
- Van Dongen, P.W.J., A.N.J.A. De Groot. 1995. History of ergot alkaloids from ergotism to ergometrine. Eur. J. Obstet. Gynecol. Reprod. Biol. 60: 109–116.
- Van Rensburg, S.J., P. Cook-Mozaffari, D.J. Van Schalkwyk, J.J. Van Der Watt, T.J. Vincent, I.F. Purchase. 1985. Hepatocellular carcinoma and dietary aflatoxin in Mozambique and Transkei. Br. J. Cancer 51: 713–726.
- Ventura, M., A. Gómez, I. Anaya, J. Díaz, F. Broto, M. Agut, L. Comellas. 2004. Determination of aflatoxins B1, G1, B2 and G2 in medicinal herbs by liquid chromatography-tandem mass spectrometry. J. Chromatogr. A 1048: 25–29.
- Ventura, M., D. Guillén, I. Anaya, F. Broto-Puig, J.L. Lliberia, M. Agut, L. Comellas. 2006. Ultra-performance liquid chromatography/tandem mass spectrometry for the simultaneous analysis of aflatoxins B1, G1, B2, G2 and ochratoxin A in beer. Rapid Commun. Mass Spectrom. 20: 3199–3204.
- Völkel, I., E. Schröer-Merker, C.-P. Czerny. 2011. The carry-over of mycotoxins in products of animal origin with special regard to its implications for the European Food Safety Legislation. Food Nutr. Sci. 2: 852–867.
- Wang, H., Y. Wang, W. Wang, P. Fu, P. Liu, W. Zhu. 2011. Anti-influenza virus polyketides from the acid-tolerant fungus Penicillium purpurogenum JS03-21. J. Nat. Prod. 74: 2014–2018.
- Wannemacher, R.W., S.L. Wiener. 1997. Trichothecene mycotoxins. In: Medical Aspects of Chemical and Biological Warfare. Walter Reed Army Medical Center, Washington, DC, pp. 655–676.
- Warth, B., M. Sulyok, P. Fruhmann, F. Berthiller, R. Schuhmacher, C. Hametner, G. Adam, J. Fröhlich, R. Krska. 2012. Assessment of human deoxynivalenol exposure using an LC-MS/MS based biomarker method. Toxicol. Lett. 211: 85–90.
- Wild, C.P., Y.Z. Jiang, S.J. Allen, L.A. Jansen, A.J. Hall, R. Montesano. 1990. Aflatoxin-albumin adducts in human sera from different regions of the world. Carcinogenesis 11: 2271–2274.
- Wilke, M.S., A.L. Lovering, N.C.J. Strynadka. 2005. β-Lactam antibiotic resistance: A current structural perspective. Curr. Opin. Microbiol. 8: 525–533.
- Williams, P.L., R.C. James, S.M. Roberts. 2003. Principles of Toxicology: Environmental and Industrial Applications. 2nd edition. John Wiley and Sons, Inc., New York, p. 624.
- Xiao, H., S. Madhyastha, R.R. Marquardt, S. Li, J.K. Vodela, A.A. Frohlich, B.W. Kemppainen. 1996. Toxicity of ochratoxin A, its opened lactone form and several of its analogs: Structure-activity relationships. Toxicol. Appl. Pharm. 137: 182–192.
- Yamamoto, T., N. Izumi, H. Ui, A. Sueki, R. Masuma, K. Nonaka, T. Hirose, T. Sunazuka, T. Nagai, H. Yamada, S. Omura, K. Shiomi. 2012. Wickerols A and B: Novel anti-influenza virus diterpenes produced by Trichoderma atroviride FKI-3849. Tetrahedron 68: 9267–9271.
- Yaroglu, T., H.H. Oruc, M. Tayar. 2005. Aflatoxin M1 levels in cheese samples from some provinces of Turkey. Food Control 16: 883–885.
- Yim, G., H.H. Wang, J.F.R.S. Davies. 2007. Antibiotics as signalling molecules. Phil. Trans. R. Soc. B 362: 1195–1200.
- Yogendrarajah, P., C. Van Poucke, B. De Meulenaer, S. De Saeger. 2013. Development and validation of a QuEChERS based liquid chromatography tandem mass spectrometry method for the determination of multiple mycotoxins in spices. J. Chromatogr. A 1297: 1–11.
- Zain, M.E. 2011. Impact of mycotoxins on humans and animals. J. Saudi Chem. Soc. 15: 129–144.
- Zhong, J.J., J.-H. Xiao. 2009. Secondary metabolites from higher fungi: Discovery, bioactivity, and bioproduction. Adv. Biochem. Eng. Biotechnol. 113: 79–150.
- Zinedine, A., J.M. Soriano, J.C. Moltó, J. Mañes. 2007. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: An oestrogenic mycotoxin. Food Chem. Toxicol. 45: 1–18.
- Zough, H., L. Yanran, Y. Tang. 2010. Cyclization of aromatic polyketides from bacteria and fungi. Nat. Prod. Rep. 27: 839–868.