Fungicides induced triazole-resistance in Aspergillus fumigatus associated with mutations of TR46/Y121F/T289A and its appearance in agricultural fields

Journal of Hazardous Materials

Volumn 326, Issue , 2017, Pages 54-60

  Ren, Jingbei ^a   Jin, Xiangxiang ^a   Zhang, Qian ^a   Zheng, Yuan ^a   Lin, Dunli ^a   Yu, Yunlong ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Aspergillus fumigatus; Fungicide; Resistance; Triazole

Indexed keywords

AGRICULTURE; ELECTRIC RESISTANCE; FUNGICIDES; GREENHOUSES; STRAIN;

AGRICULTURAL FIELDS; AGRICULTURAL USE; ASPERGILLUS FUMIGATUS; AZOLE RESISTANCES; RESISTANT STRAINS; TRIAZOLE; TRIAZOLE FUNGICIDES; VEGETABLES AND FRUITS;

ASPERGILLUS;

ALANINE; CYP51A; CYTOCHROME; FUNGICIDE; HEXACONAZOLE; HISTIDINE; ISOLEUCINE; ITRACONAZOLE; LEUCINE; METCONAZOLE; PHENYLALANINE; PROPICONAZOLE; TEBUCONAZOLE; THREONINE; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG; VORICONAZOLE; AGRICULTURAL CHEMICAL; CYTOCHROME P-450 CYP51A, ASPERGILLUS; CYTOCHROME P450; FUNGAL PROTEIN;

AGRICULTURAL LAND; FUNGICIDE; FUNGUS; MUTATION; PESTICIDE RESISTANCE; PUBLIC HEALTH; SOIL ANALYSIS;

AGRICULTURE; ANTIFUNGAL RESISTANCE; ARTICLE; ASCOSPORE; ASPERGILLUS FUMIGATUS; CHINA; CODON; CONIDIOPHORE; CONTROLLED STUDY; FRUIT; FUNGAL STRAIN; FUNGUS ISOLATION; GENE MUTATION; GREENHOUSE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; POINT MUTATION; PROMOTER REGION; SEQUENCE ANALYSIS; SOIL; TANDEM REPEAT; VEGETABLE; WILD TYPE; DRUG EFFECT; GENETICS; MICROBIOLOGY; MUTATION;

CHINA; ZHEJIANG;

ASPERGILLUS FUMIGATUS;

AGRICULTURE; AGROCHEMICALS; ASPERGILLUS FUMIGATUS; CYTOCHROME P-450 ENZYME SYSTEM; DRUG RESISTANCE, FUNGAL; FUNGAL PROTEINS; FUNGICIDES, INDUSTRIAL; MUTATION; SOIL MICROBIOLOGY; TRIAZOLES;

EID: 85006511895     PISSN: 03043894     EISSN: 18733336     Source Type: Journal    
DOI: 10.1016/j.jhazmat.2016.12.013     Document Type: Article

References (46)

1. [1] Lockhart, S.R., Frade, J.P., Etienne, K.A., Pfaller, M.A., Diekema, D.J., Balajee, S.A., Azole resistance in Aspergillus fumigatus isolates from the ARTEMIS global surveillance study is primarily due to the TR/L98H mutation in the cyp51A gene. Antimicrob. Agents Chemother. 55 (2011), 4465–4468.
2. [2] Denning, D.W., Venkateswarlu, K., Oakley, K.L., Anderson, M.J., Manning, N.J., Stevens, D.A., Warnock, D.W., Kelly, S.L., Itraconazole resistance in Aspergillus fumigates. Antimicrob. Agents Chemother. 41 (1997), 1364–1368.
3. [3] Snelders, E., Melchers, W.J.G., Verweij, P.E., Azole resistance in Aspergillus fumigatus: a new challenge in the management of invasive aspergillosis. Future Microbiol. 6 (2011), 335–347.
4. [4] Lelièvre, L., Groh, M., Angebault, C., Maherault, A.-C., Didier, E., Bougnoux, M.-E., Azole resistant Aspergillus fumigatus: an emerging problem. Médecine et Maladies Infectieuses 43 (2013), 139–145.
5. [5] Verweij, P.E., Chowdhary, A., Melchers, W.J.G., Meis, J.F., Azole resistance in Aspergillus fumigatus: can we retain the clinical use of mold-Active antifungal azoles. Clin. Infect. Dis. 62 (2016), 362–368.
6. [6] Snelders, E., Karawajczyk, A., Schaftenaar, G., Verweij, P.E., Melchers, W.J.G., Azole resistance profile of amino acid changes in Aspergillus fumigatus CYP51A based on protein homology modeling. Antimicrob. Agents Chemother. 54 (2010), 2425–2430.
7. [7] Natesan, S.K., Wu, W., Cutright, J.L., Chandrasekar, P.H., In vitro-in vivo correlation of voriconazole resistance due to G448S mutation (cyp51A gene) in Aspergillus fumigates. Diagn. Microbiol. Infect. Dis. 74 (2012), 272–277.
8. [8] Howard, S.J., Webster, I., Moore, C.B., Gardiner, R.E., Park, S., Perlin, D.S., Denning, D.W., Multi-azole resistance in Aspergillus fumigates. Int. J. Antimicrob. Agents 28 (2006), 450–453.
9. [9] Hagiwara, D., Takahashi, H., Watanabe, A., Takahashi-Nakaguchi, A., Kawamoto, S., Kamei, K., Gonoia, T., Whole-Genome comparison of Aspergillus fumigatus strains serially isolated from patients with aspergillosis. J. Clin. Microbiol. 52 (2014), 4202–4209.
10. [10] Manavathu, E.K., Vazquez, J.A., Chandrasekar, P.H., Reduced susceptibility in laboratory-selected mutants of Aspergillus fumigatus to itraconazole due to decreased intracellular accumulation of the antifungal agent. Int. J. Antimicrob. Agents 12 (1999), 213–219.
11. [11] Cannon, R.D., Lamping, E., Holmes, A.R., Niimi, K., Baret, P.V., Keniya, M.V., Tanabe, K., Niimi, M., Goffeau, A., Monk, B.C., Efflux-mediated antifungal resistance. Clin. Microbiol. Rev. 22 (2009), 291–321.
12. [12] Camps, S.M., van der Linden, J.W., Li, Y., Kuijper, E.J., van Dissel, J.T., Verweij, P.E., Melchersa, W.J.G., Rapid Induction of multiple resistance mechanisms in Aspergillus fumigatus during azole therapy: a case study and review of the literature. Antimicrob. Agents Chemother. 56 (2012), 10–16.
13. [13] Howard, S.J., Cerar, D., Anderson, M.J., Albarrag, A., Fisher, M.C., Pasqualotto, A.C., Laverdiere, M., Arendrup, M.C., Perlin, D.S., Denning, D.W., Frequency and evolution of azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg. Infect. Dis. 15 (2009), 1068–1076.
14. [14] Tashiro, M., Izumikawa, K., Minematusu, A., Hirano, K., Iwanaga, N., Ide, S., Mihara, T., Hosogaya, N., Takazono, T., Morinaga, Y., Nakamura, S., Kurihara, S., Imamura, Y., Miyazaki, T., Nishino, T., Tsukamoto, M., Kakeya, H., Yamamoto, Y., Yanagihara, K., Yasuoka, A., Tashiro, T., Kohno, S., Antifungal susceptibilities of Aspergillus fumigatus clinical isolates obtained in Nagasaki Japan. Antimicrob. A Chemother. 56 (2012), 584–587.
15. [15] Arendrup, M.C., Mavridou, E., Mortensen, K.L., Snelders, E., Frimodt-Møller, N., Khan, H., Melchers, W.J.G., Verweij, P.E., Development of azole resistance in Aspergillus fumigatus during azole therapy associated with change in virulence. PLoS One, 5, 2010, e10080.
16. [16] van der Linden, J.W.M., Snelders, E., Kampinga, G.A., Rijnders, B.J.A., Mattsson, E., Debets-Ossenkopp, Y.J., Kuijper, E.J., Tiel, F.H.V., Melchers, W.J.G., Verweij, P.E., Clinical implications of azole resistance in Aspergillus fumigatus the Netherlands, 2007–2009. Emerg. Infect. Dis. 17 (2011), 1846–1854.
17. [17] Chowdhary, A., Kathuria, S., Randhawa, H.S., Gaur, S.N., Klaassen, C.H., Meis, J.F., Isolation of multiple-triazole-resistant Aspergillus fumigatus strains carrying the TR/L98H mutations in the cyp51A gene in India. J. Antimicrob. Chemother. 67 (2012), 362–366.
18. [18] Snelders, E., van der Lee, H.A.L., Kuijpers, J., Rijs, A.J.M.M., Varga, J., Samson, R.A., Mellado, E., Donders, A.R.T., Melchers, W.J.G., Verweij, P.E., Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism. PLoS Med., 5, 2008, e219.
19. [19] Kano, R., Kohata, E., Tateishi, A., Murayama, S.Y., Hirose, D., Shibata, Y., Kosuge, Y., Inoue, H., Kamata, H., Hasegawa, A., Does farm fungicide use induce azole resistance in Aspergillus fumigates. Med. Mycol. 53 (2015), 174–177.
20. [20] Price, C.L., Parker, J.E., Warrilow, A.G.S., Kelly, D.E., Kelly, S.L., Azole fungicides-understanding resistance mechanisms in agricultural fungal pathogens. Pest Manag. Sci. 71 (2015), 1054–1058.
21. [21] Astvad, K.M.T., Jensen, R.H., Hassan, T.M., Mathiasen, E.G., Thomsen, G.M., Pedersen, U.G., Christensen, M., Hilberg, O., Arendrupa, M.C., First detection of TR46/Y121F/T289A and TR34/L98H alterations in Aspergillus fumigatus isolates from azole-naive patients in Denmark despite negative findings in the environment. Antimicrob. Agents Chemother. 58 (2014), 5096–5101.
22. [22] Clinical Laboratory Standards Institute (CLSI), Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi; Approved Standard-Second Edition, CLSI document M38- A2. Second Edition ed, 2008, Clinical Laboratory Standards Institute, Wayne Pennsylvania, USA.
23. [23] Bader, O., Weig, M., Reichard, U., Lugert, R., Kuhns, M., Christner, M., Held, J., Peter, S., Schumacher, U., Buchheidt, D., Tintelnot, K., Groß, U., Partners, M.D., cyp51A-based mechanisms of Aspergillus fumigatus azole drug resistance present in clinical samples from Germany. Antimicrob. Agents Chemother. 57 (2013), 3513–3517.
24. [24] EUCAST, Antifungal-breakpoints Table for Interpretation of MICs. 2013 (Accessed 13.01.09) http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/Antifungal_breakpoints_v_5.0.pdf.
25. [25] Mellado, E., Garcia-Effron, G., Alcazar-Fuoli, L., Melchers, W.J.G., Verweij, P.E., Cuenca-Estrella, M., Rodríguez-Tudela, J.L., A new Aspergillus fumigatus resistance mechanism conferring in vitro cross-resistance to azole antifungals involves a combination of cyp51A alternations. Antimicrob. Agents Chemother. 51 (2007), 1897–1904.
26. [26] de Valk, H.A., Meis, J.F.G.M., Curfs, I.M., Muehlethaler, K., Use of a novel panel of nine short tandem repeats for exact and high-resolution fingerprinting of Aspergillus fumigatus isolates. J. Clin. Microbiol. 43 (2005), 4112–4120.
27. [27] Yao, T.T., Wang, Z.X., Preparation, regeneration and transformation of Aspergillus niger protoplasts. J. Food Sci. Biotechnol. 25:4 (2006), 116–120.
28. [28] Spiess, P., Postina, M., Reinwald, O.A., Cornely, A., Hamprecht, M., Lass-Florl, P.M., Rath, J., Steinmann, T., Miethke, M., Lauten, S., Will, N., Merker, W.K., Buchheidt, D., Incidence of cyp51 A key mutations in Aspergillus fumigatus – a study on primary clinical samples of immunocompromised patients in the period of 1995–2013. PLoS One, 9, 2014, e103113.
29. [29] Snelders, S.M.T., Camps, A., Karawajczyk, A.J.M.M., Rijs, J., Zoll, P.E., Genotype–phenotype complexity of the TR46/Y121F/T289A cyp51A azole resistance mechanism in Aspergillus fumigatus. Fungal Genet. Biol. 82 (2015), 129–135.
30. [30] Zhang, J.H., Debets, A.J.M., Verweij, P.E., Melchers, W.J.G., Zwaan, B.J., Schoustra, S.E., Asexual sporulation facilitates adaptation: the emergence of azole resistance in Aspergillus fumigates. Evolution 69 (2015), 2573–2586.
31. [31] Bader, O., Tunnermann, J., Dudakova, A., Tangwattanachuleeporn, M., Weig, M., Gross, U., Environmental isolates of azole-resistant Aspergillus fumigatus in Germany. Antimicrob. Agents Chemother. 59 (2015), 4356–4359.
32. [32] Faria-Ramos, S., Farinha, S., Neves-Maia, J., Tavares, P.R., Miranda, I.M., Estevinho, L.M., Pina-Vaz, C., Rodrigues, A.G., Development of cross-resistance by Aspergillus fumigatus to clinical azoles following exposure to prochloraz an agricultural azole. BMC Microbiol. 14 (2014), 155–159.
33. [33] Sharma, C., Hagen, F., Moroti, R., Meis, J.F., Chowdhary, A., Triazole-resistant Aspergillus fumigatus harbouring G54 mutation: is it de novo or environmentally acquired. J. Glob. Antimicrob. Resist. 3 (2015), 69–74.
34. [34] Verweij, P.E., Mellado, E., Melchers, W.J., Multiple-triazole-resistant aspergillosis. N. Engl. J. Med. 356 (2007), 1481–1483.
35. [35] Leroux, P., Gredt, M., Leroch, M., Walker, A.S., Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agent of gray mold. Appl. Environ. Microbiol. 76 (2010), 6615–6630.
36. [36] Petit, A.N., Vaillant-Gaveau, N., Walker, A.N., Leroux, P., Baillieul, F., Panon, M.L., Clément, C., Fontaine, F., Determinants of fenhexamid effectiveness against grey mould on grapevine: respective role of spray timing, fungicide resistance and plant defences. Crop Prot. 29 (2010), 1162–1167.
37. [37] Escribano, P., Recio, S., Peláez, T., González-Rivera, M., Bouza, E., Guineaa, J., In vitro acquisition of secondary azole resistance in Aspergillus fumigatus isolates after prolonged exposure to itraconazole: presence of heteroresistant populations. Antimicrob. Agents Chemother. 56 (2012), 174–178.
38. [38] Snelders, E., Camps, S.M.T., Karawajczyk, A., Schaftenaar, G., Kema5, G.H.J., van der Lee, H.A., Klaassen, C.H., Melchers, W.J.G., Verweij, P.E., Triazole fungicides can induce cross-resistance to medical triazoles in Aspergillus fumigatus. PLoS One, 7, 2012, e31801.
39. [39] Bueid, A., Howard, S.J., Moore, C.B., Richardson, M.D., Harrison, E., Bowyer, P., Denning, D.W., Azole antifungal resistance in Aspergillus fumigatus: 2008 and 2009. J. Antimicrob. Chemother. 65 (2010), 2116–2118.
40. [40] Fenner, K., Canonica, S., Wackett, L.P., Elsner, M., Evaluating pesticide degradation in the environment: blind spots and emerging opportunities. Science 341 (2013), 752–758.
41. [41] Storck, V., Lucini, L., Mamy, L., Ferrari, F., Papadopoulou, E.S., Nikolaki, S., Karas, P.A., Servien, R., Karpouzas, D.G., Trevisan, M., Benoit, P., Martin-Laurent, F., Identification and characterization of tebuconazole transformation products in soil by combining suspect screening and molecular typology. Environ. Pollut. 208 (2016), 537–545.
42. [42] Snelders, E., Huis in ’t Veld, R.A.G., Rijs, A.J.M.M., Kema, G.H.J., Melchers, W.J.G., Verweij, P.E., Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles. Appl. Environ. Microbiol. 75 (2009), 4053–4057.
43. [43] Verweij, P.E., Snelders, E., Kema, G.H.J., Mellado, E., Melchers, W.J.G., Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use. Lancet Infect. Dis. 9 (2009), 789–795.
44. [44] Chowdhary, A., Sharma, C., Kathuria, S., Hagen, F., Meis, J.F., Azole-resistant Aspergillus fumigatus with the environmental TR46/Y121F/T289A mutation in India. J. Antimicrob. Chemother. 69 (2014), 555–571.
45. [45] van der Linden, J.W.M., Camps, S.M.T., Kampinga, G.A., Arends, J.P.A., Debets-Ossenkopp, Y.J., Haas, P.J.A., Rijnders, B.J.A., Kuijper, E.J., van Tiel, F.H., Varga, J., Aspergillosis due to voriconazole highly resistant Aspergillus fumigatus and recovery of genetically related resistant isolates from domiciles. Clin. Infect. Dis. 57 (2013), 513–520.
46. [46] Fischer, J., van Koningsbruggen-Rietschel, S., Rietschel, E., Vehreschild, M.J.G.T., Wisplinghoff, H., Kronke, M., Hamprecht, A., Prevalence and molecular characterization of azole resistance in Aspergillus spp. isolates from German cystic fibrosis patients. J. Antimicrob. Chemother. 69 (2014), 1533–1536.