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Does fungicide application in vineyards induce resistance to medical azoles in Aspergillus species?

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Abstract

This study assessed if the use of sterol demethylase inhibitor fungicides in vineyard production can induce resistance to azoles in Aspergillus strains and if it can induce selection of resistant species. We also tried to identify the Aspergillus species most prevalent in the vineyards. Two vineyards from northern Portugal were selected from “Vinhos Verdes and “Douro” regions. The vineyards were divided into plots that were treated or not with penconazole (PEN). In each vineyard, air, soil, and plant samples were collected at three different times. The strains of Aspergillus spp. were isolated and identified by morphological and molecular techniques. We identified 46 Aspergillus section Nigri, eight Aspergillus fumigatus, seven Aspergillus lentulus, four Aspergillus wentii, two Aspergillus flavus, two Aspergillus terreus, one Aspergillus calidoustus, one Aspergillus westerdijkiae, one Aspergillus tamarii, and one Eurotium amstelodami. Aspergillus strains were evaluated for their susceptibility to medical azoles used in human therapy (itraconazole, posaconazole, and voriconazole) and to agricultural azoles (PEN) used in the prevention and treatment of plant diseases. The isolates showed moderate susceptibility to voriconazole. We did not observe any decrease of susceptibility to the medical azoles tested throughout the testing period in any of the treated plots, although some of the resistant species were isolated from there.

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References

  • Alanio, A., Sitterlé, E., Liance, M., Farrugia, C., Foulet, F., Botterel, F., et al. (2011). Low prevalence of resistance to azoles in Aspergillus fumigatus in a French cohort of patients treated for haematological malignancies. Journal of Antimicrobial Chemotherapy, 66, 371–374.

    Article  CAS  Google Scholar 

  • Amaro, P. (2001). A protecção integrada da vinha na região norte. Lisboa: ISA/Press.

    Google Scholar 

  • BASF. (2013). http://www.agro.basf.com Accessed 26 July 2013.

  • Bayer CropScience. (2013). http://www.cropscience.bayer.com Accessed 26 July 2013.

  • Brent, K. J. & Hollomon, D. W. (1998). Fungicide resistance: the assessment of risk. Brussels: FRAC Monograph No 2, Global Crop Protection Federation.

  • Bueid, A., Howard, S. J., Moore, C. B., Richardson, M. D., Harrison, E., Bowyer, P., et al. (2010). Azole antifungal resistance in Aspergillus fumigatus: 2008 and 2009. Journal of Antimicrobial Chemotherapy, 65, 2116–2118.

    Article  CAS  Google Scholar 

  • Chiotta, M. L., Ponsone, M. L., Combina, M., Torres, A. M., & Chulze, S. N. (2009). Aspergillus section Nigri species isolated from different wine-grape growing regions in Argentina. International Journal of Food Microbiology, 136, 137–141.

    Article  CAS  Google Scholar 

  • CLSI (Clinical and Laboratory Standards Institute). (2008). Reference method for broth dilution antifungal susceptibility testing of filamentous fungi (Approved standard, 2nd ed. M38-A2). Wayne: Clinical and Laboratory Standards Institute.

    Google Scholar 

  • Coelho, D., Silva, S., Vale-Silva, L., Gomes, H., Pinto, E., Sarmento, A., et al. (2011). Aspergillus viridinutans: an agent of adult chronic invasive aspergillosis. Medical Mycology, 49, 755–759.

    Google Scholar 

  • Copping, L. (2003). The evolution of crop protection companies. Pesticide Outlook, 14, 276–278.

    Article  Google Scholar 

  • Crous, P. W., Gams, W., Stalpers, J. A., Robert, V., & Stegehuis, G. (2004). MycoBank: an online initiative to launch mycology into the 21st century. Studies in Mycology, 50, 19–22.

    Google Scholar 

  • DGADR (Direção Geral de Agricultura e Desenvolvimento Rural). (2013). www.dgadr.pt Accessed 26 July 2013.

  • European Commission. (1991). Council Directive 91/414/EEC of 15 July 1991 concerning the placing of plant protection products on the market.

  • European Commission. (2012). Sustainable use of pesticides. http://ec.europa.eu/environment/ppps/home.htm Accessed 26 July 2013.

  • European Commission - Scientific Steering Committee. (2002). SSC Report: Opinion on azole antimycotic resistance.

  • FRAC (Fungicide Resistance Action Committee). (2013). FRAC Code List 2013: Fungicides sorted by mode of action. http://www.frac.info/publication/anhang/FRAC%20Code%20List%202013-final.pdf Accessed 26 July 2013.

  • Glass, N. L., & Donaldson, G. C. (1995). Development of primer sets designed for use with the PCR to amplify conserved genes for filamentous ascomycetes. Applied and Environmental Microbiology, 61, 1323–1330.

    CAS  Google Scholar 

  • Hedayati, M. T., Mayahi, S., & Denning, D. W. (2010). A study on Aspergillus species in houses of asthmatic patients from Sari City, Iran and a brief review of the health effects of exposure to indoor Aspergillus. Environmental Monitoring and Assessment, 168, 481–487.

    Article  Google Scholar 

  • Hof, H. (2001). Critical annotations to the use of azole antifungal for plant protection. Antimicrobial Agents and Chemotherapy, 45, 2987–2990.

    Article  CAS  Google Scholar 

  • Hof, H. (2008). Is there a serious risk of resistance development to azoles among fungi due to the widespread use and long-term application of azole antifungals in medicine? Drug Resistance Updates, 11, 25–31.

    Article  CAS  Google Scholar 

  • Howard, S. J., Cerar, D., Anderson, M. J., Albarrag, A., Fisher, M. C., Pasqualotto, A. C., et al. (2009). Frequency and evolution of azole resistance in Aspergillus fumigatus associated with treatment failure. Emerging Infectious Diseases, 15, 1068–1076.

    Article  CAS  Google Scholar 

  • Lamb, D. C., Cannieux, M., Warrilow, A. G., Bak, S., Kahn, R. A., Manning, N. J., et al. (2001). Plant sterol 14 alpha-demethylase affinity for azole fungicides. Biochemical and Biophysical Research Communications, 284, 845–849.

    Article  CAS  Google Scholar 

  • Lass-Flörl, C., & Perkhofer, S. (2008). In vitro susceptibility-testing in Aspergillus species. Mycoses, 51, 437–446.

    Article  Google Scholar 

  • Lass-Flörl, C., Alastruey-Izquierdo, A., Cuenca-Estrella, M., Perkhofer, S., & Rodriguez-Tudela, J. L. (2009). In vitro activities of various antifungal drugs against Aspergillus terreus: global assessment using the methodology of the European Committee on antimicrobial susceptibility testing. Antimicrobial Agents and Chemotherapy, 53, 794–795.

    Article  Google Scholar 

  • Lucas, J. (2003). Resistance to QoI fungicides: Implications for cereal disease management in Europe. Pesticide Outlook, 14, 268–270.

    Article  CAS  Google Scholar 

  • Malani, A. N., & Kauffman, C. A. (2007). Changing epidemiology of rare mould infections: Implications for therapy. Drugs, 67, 1803–1812.

    Article  CAS  Google Scholar 

  • Matthews, G. A. (2000). Pesticide application methods (3rd ed.). Oxford: Blackwell Science.

    Book  Google Scholar 

  • Mayr, A., & Lass-Flörl, C. (2011). Epidemiology and antifungal resistance in invasive aspergillosis according to primary disease: Review of the literature. European Journal of Medical Research, 16, 153–157.

    Article  CAS  Google Scholar 

  • Miceli, M. H., & Lee, S. A. (2011). Emerging moulds: Epidemiological trends and antifungal resistance. Mycoses, 54, e666–e678.

    Article  Google Scholar 

  • Ministério da Agricultura. (2013). http://www.dgv.min-agricultura.pt Accessed 26 July 2013.

  • Mortensen, K. L., Mellado, E., Lass-Flörl, C., Rodriguez-Tudela, J. L., Johansen, H. K., & Arendrup, M. C. (2010). Environmental study of azole-resistant Aspergillus fumigatus and other aspergilli in Austria, Denmark, and Spain. Antimicrobial Agents and Chemotherapy, 54, 4545–4549.

    Article  CAS  Google Scholar 

  • Moslem, M. A., Bahkali, A. H., Abd-Elsalam, K. A., & Wit, P. J. (2010). An efficient method for DNA extraction from Cladosporioid fungi. Genetics and Molecular Research, 9, 2283–2291.

    Article  CAS  Google Scholar 

  • Noon, R. (2004). New developments in fungicides: 2004 edition. PJB Publications.

  • Odds, F. C., Brown, A. J., & Gow, N. A. (2003). Antifungal agents: Mechanisms of action. Trends in Microbiology, 11, 272–279.

    Article  CAS  Google Scholar 

  • O’Donnell, K., Nirenberg, H. I., Aoki, T., & Cigelnik, E. (2000). A multigene phylogeny of the Gibberella fujikuroi species complex: Detection of additional phylogenetically distinct species. Mycoscience, 41, 61–78.

    Article  Google Scholar 

  • Pfaller, M. A., & Diekema, D. J. (2007). Epidemiology of invasive candidiasis: a persistent public health problem. Clinical Microbiology Reviews, 20, 133–163.

    Article  CAS  Google Scholar 

  • Pfaller, M. A., Messer, S. A., Boyken, L., Rice, C., Tendolkar, S., Hollis, R. J., et al. (2008). In vitro survey of triazole cross-resistance among more than 700 clinical isolates of Aspergillus species. Journal of Clinical Microbiology, 46, 2568–2572.

    Article  CAS  Google Scholar 

  • Pfaller, M. A., Diekema, D. J., Ghannoum, M. A., Rex, J. H., Alexander, B. D., Andes, D., et al. (2009). Wild-type MIC distribution and epidemiological cutoff values for Aspergillus fumigatus and three triazoles as determined by the Clinical and Laboratory Standards Institute broth microdilution methods. Journal of Clinical Microbiology, 47, 3142–3146.

    Article  CAS  Google Scholar 

  • Pfaller, M. A., Boyken, L., Hollis, R. J., Kroeger, J., Messer, S. A., Tendolkar, S., et al. (2011). Comparison of the broth microdilution methods of the European Committee on antimicrobial susceptibility testing and the Clinical and Laboratory Standards Institute for testing itraconazole, posaconazole, and voriconazole against Aspergillus isolates. Journal of Clinical Microbiology, 49, 1110–1112.

    Article  CAS  Google Scholar 

  • PPDB (Pesticides Properties DataBase). (2012). http://sitem.herts.ac.uk/aeru/footprint/en/ Accessed 26 July 2013.

  • Samson, R. A., Houbraken, J., Thrane, U., Frisvad, J. C., & Andersen, B. (2010). Food and Indoor Fungi. Utretch: CBS Laboratory Manual Series.

  • Sapec. (2013). Sapec Agro Portugal. www.sapecagro.pt Accessed 26 July 2013.

  • Serra, R., Lourenço, A., Alípio, P., & Venâncio, A. (2006). Influence of the region of origin on the mycobiota of grapes with emphasis on Aspergillus and Penicillium species. Mycological Research, 110, 971–978.

    Article  Google Scholar 

  • Shelton, B. G., Kirkland, K. H., Flanders, W. D., & Morris, G. K. (2002). Profiles of airborne fungi in buildings and outdoor environments in the United States. Applied and Environmental Microbiology, 68, 1743–1753.

    Article  CAS  Google Scholar 

  • Snelders, E., Huis In’t Veld, R. A., Rijs, A. J., Kema, G. H., Melchers, W. J., & Verweij, P. E. (2009). Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles. Applied and Environmental Microbiology, 75, 4053–4057.

    Article  CAS  Google Scholar 

  • Snelders, E., Camps, S. M., Karawajczyk, A., Schaftenaar, G., Kema, G. H., Van der Lee, H. A., et al. (2012). Triazoles fungicides can induce cross-resistance to medical triazoles in Aspergillus fumigatus. PLoS ONE, 7, e31801.

    Article  CAS  Google Scholar 

  • Steinkellner, S., & Redl, H. (2001). Sensitivity of Uncinula necator populations following DMI-fungicide usage in Austrian vineyards. Die Bodenkultur, 52, 293–299.

    Google Scholar 

  • Steva, H., Cartolaro, P., Clearjeau, M., Lafon, R., & Gomes da Silva, M. T. (1988). A resistance of grape powdery mildew to triadimenol in Portugal? Phtythoma, 402, 49–50.

    Google Scholar 

  • Syngenta. (2013). http://www.syngenta.com Accessed 26 July 2013.

  • Varga, J., Houbraken, J., Van der Lee, H. A., Verweij, P. E., & Samson, R. A. (2008). Aspergillus calidoustus sp. nov., causative agent of human infections previously assigned to Aspergillus ustus. Eukaryotic Cell, 7, 630–638.

    Article  CAS  Google Scholar 

  • Vermeulen, E., Maertens, J., Schoemans, H., & Lagrou, K. (2012). Azole-resistant Aspergillus fumigatus due to TR46/Y121F/T289A mutation emerging in Belgium, July 2012. Eurosurveillance, 17, pii=20326.

  • Verweij, P. E., Snelders, E., Kema, G. H., Mellado, E., & Melchers, W. J. (2009). Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use? Lancet Infectious Diseases, 9, 789–795.

    Article  CAS  Google Scholar 

  • Verweij, P. E., Camps, S. M., Kema, G. H., & Melchers, W. J. (2011). Comment on: Low prevalence of resistance to azoles in Aspergillus fumigatus in a French cohort of patients treated for haematological malignancies. Journal of Antimicrobial Chemotherapy, 66, 954–955.

    Article  CAS  Google Scholar 

  • Walsh, T. J., Anaissie, E. J., Denning, D. W., Herbrecht, R., Kontoyiannis, D. P., Marr, K. A., et al. (2008). Treatment of aspergillosis: Clinical practice guidelines of the Infectious Diseases Society of America. Clinical Infectious Diseases, 46, 327–360.

    Article  CAS  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innes, D. H. Gelfand, J. S. Sinsky, & T. J. White (Eds.), PCR protocols (pp. 315–322). London: Academic.

    Google Scholar 

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Acknowledgments

The authors are grateful to Fundação para a Ciência e a Tecnologia (FCT) through grants: CEQUIMED-PEst-OE/SAU/UI4040/2011; Reitoria da Universidade do Porto-PP-IJUP2010. The authors would also like to acknowledge the technical association ADVID and the viticulture companies Quinta da Aveleda and Symington Family Estates for the facilities in fields experiments. M. A. Faria thanks financial support from the European Union (FEDER funds through COMPETE) and National Funds (FCT, Fundação para a Ciência e Tecnologia) through project Pest-C/EQB/LA0006/2013. The work also received financial support from the European Union (FEDER funds) under the framework of QREN through Project NORTE-07-0124-FEDER-000069. To all financing sources, the authors are greatly indebted.

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Correspondence to Eugénia Pinto.

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Lago, M., Aguiar, A., Natário, A. et al. Does fungicide application in vineyards induce resistance to medical azoles in Aspergillus species?. Environ Monit Assess 186, 5581–5593 (2014). https://doi.org/10.1007/s10661-014-3804-8

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