Emergence of Azole-Resistant Aspergillus fumigatus Strains due to Agricultural Azole Use Creates an Increasing Threat to Human Health

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  Chowdhary, Anuradha ^a   Kathuria, Shallu ^a   Xu, Jianping ^b   Meis, Jacques F ^c,d  

^a UNIVERSITY OF DELHI   (India)

^b MCMASTER UNIVERSITY   (Canada)

^c CANISIUS WILHELMINA HOSPITAL   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; ANTIFUNGAL AGENT; BROMUCONAZOLE; CYTOCHROME P450; DIFENOCONAZOLE; ECHINOCANDIN; EPOXICONAZOLE; FUNGICIDE; ITRACONAZOLE; POSACONAZOLE; PYRROLE; TEBUCONAZOLE; TRIAZOLE; UNCLASSIFIED DRUG; VORICONAZOLE;

AGRICULTURE; ANTIFUNGAL RESISTANCE; ARTICLE; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; DISEASE SURVEILLANCE; GENETIC VARIABILITY; GENOTYPE; HUMAN; IMMUNITY; INCIDENCE; LUNG ASPERGILLOSIS; LUNG INFECTION; PHYLOGENY; POINT MUTATION; POLYMERASE CHAIN REACTION; PREVALENCE;

AGRICULTURE; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; AZOLES; DRUG RESISTANCE, FUNGAL; FUNGICIDES, INDUSTRIAL; HUMANS;

EID: 84885930731     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003633     Document Type: Article

References (33)

1. Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, et al. (2012) Hidden killers: human fungal infections. Sci Transl Med 4: 165rv13.
2. Denning D, Pleuvry A, Cole D, (2013) Global burden of ABPA in adults with asthma and its complication chronic pulmonary aspergillosis in adults. Med Mycol 51: 361-370.
3. Lass-Flörl C, (2011) Triazole antifungal agents in invasive fungal infections: a comparative review. Drugs 71: 2405-2419.
4. Van der Linden JWM, Arendrup MC, Verweij PE, SCARE network (2011) Prospective international surveillance of azole resistance in Aspergillus fumigatus: SCARE-Network. In: 51st Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC); Sep 17-20; Chicago, IL. Abstract M-490. (SCARE-NETWORK).
5. Pfaller MA, Boyken L, Hollis R, Kroeger J, Messer S, et al. (2011) Use of epidemiological cutoff values to examine 9-year trends in susceptibility of Aspergillus species to the triazoles. J Clin Microbiol 49: 586-590.
6. Krishnan-Natesan S, Swaminathan S, Cutright J, et al. (2010) Antifungal susceptibility pattern of Aspergillus fumigatus isolated from clinical specimens in Detroit Medical Center (DMC): rising frequency of high MIC of azoles (2003-2006). In: The 50th Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC); Sep 12-15; Boston, MA, USA.
7. Chowdhary A, Kathuria S, Randhawa HS, Gaur SN, Klaassen CH, et al. (2012) Isolation of multiple-triazole-resistant Aspergillus fumigatus strains carrying the TR/L98H mutations in the cyp51A gene in India. J Antimicrob Chemother 67: 362-366.
8. Seyedmousavi S, Hashemi SJ, Zibafar E, Zoll J, Hedayati MT, et al. (2013) Azole-resistant Aspergillus fumigatus, Iran. Emerg Infect Dis 19: 832-834.
9. Lockhart SR, Frade JP, Etienne KA, Pfaller MA, Diekema DJ, et al. (2011) 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: 4465-4468.
10. Bowyer P, Moore CB, Rautemaa R, Denning DW, Richardson MD, (2011) Azole antifungal resistance today: focus on Aspergillus. Curr Infect Dis Rep 13: 485-491.
11. Snelders E, van der Lee HAL, Kuijpers J, Rijs AJMM, Varga J, et al. (2008) Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism. PLoS Med 5: e219 doi:10.1371/journal.pmed.0050219.
12. Van der Linden JWM, Snelders E, Kampinga GA, Rijnders BJA, Mattsson E, et al. (2011) Clinical implications of azole resistance in Aspergillus fumigatus, the Netherlands, 2007-2009. Emerg Infect Dis 17: 1846-1852.
13. Howard SJ, Cerar D, Anderson MJ, Albarrag A, Fisher MC, et al. (2009) Frequency and evolution of azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg Infect Dis 15: 1068-1076.
14. Arendrup MC, Mavridou E, Mortensen KL, Snelders E, Frimodt-Møller N, et al. (2010) Development of azole resistance in Aspergillus fumigatus during azole therapy associated with change in virulence. PLoS ONE 5: e10080 doi:10.1371/journal.pone.0010080.
15. Snelders E, Karawajczyk A, Verhoeven RJA, Venselaar H, Schaftenaar G, et al. (2011) The structure-function relationship of the Aspergillus fumigatus cyp51A L98H conversion by site-directed mutagenesis: the mechanism of L98H azole resistance. Fungal Genet Biol 48: 1062-1070.
16. Fraczek MG, Bromley M, Buied A, Moore CB, Rajendran R, et al. (2013) The cdr1B efflux transporter is associated with non-cyp51A mediated itraconazole resistance in Aspergillus fumigatus. J Antimicrob Chemother 68: 1486-1496.
17. Mellado E, Garcia-Effron G, Alcazar-Fuoli L, Melchers WJ, Verweij PE, et al. (2007) A new Aspergillus fumigatus resistance mechanism conferring in vitro cross-resistance to azole antifungals involves a combination of cyp51A alterations. Antimicrob Agents Chemother 51: 1897-904.
18. Snelders E, Karawajczyk, Schaftenaar G, Verweij PE, Melchers WJ, (2010) Azole resistance profile of amino acid changes in Aspergillus fumigatus cyp51A based on protein homology modeling. Antimicrob Agents Chemother 54: 2425-2430.
19. Snelders E, Huis In 't Veld RA, Rijs AJJM, Kema GHJ, Melchers WJ, et al. (2009) Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles. Appl Environ Microbiol 75: 4053-4057.
20. Denning DW, Park S, Lass-Flörl C, Fraczek MG, Kirwan M, et al. (2011) High-frequency triazole resistance found in nonculturable Aspergillus fumigatus from lungs of patients with chronic fungal disease. Clin Infect Dis 52: 1123-1129.
21. Chowdhary A, Kathuria S, Xu J, Sharma C, Sundar G, et al. (2012) Clonal expansion and emergence of environmental multiple-triazole-resistant Aspergillus fumigatus strains carrying the TR34/L98H mutations in the cyp51A gene in India. PLoS ONE 7: e52871 doi:10.1371/journal.pone.0052871.
22. Mortensen KL, Mellado E, Lass-Flörl C, Rodriguez-Tudela JL, Johansen HK, et al. (2010) Environmental study of azole-resistant Aspergillus fumigatus and other aspergilli in Austria, Denmark, and Spain. Antimicrob Agents Chemother 54: 4545-4549.
23. Badali H, Vaezi A, Haghani I, Yazdanparast SA, Hedayati MT, et al. (2013) Environmental study of azole-resistant Aspergillus fumigatus with TR34/L98H mutations in the cyp51A gene in Iran. Mycoses doi:10.1111/myc.12089. In press.
24. van der Linden JW, Camps SM, Kampinga GA, Arends JP, Debets-Ossenkopp YJ, et al. (2013) Aspergillosis due to voriconazole highly resistant Aspergillus fumigatus and recovery of genetically related resistant isolates from domestic homes. Clin Infect Dis 57: 513-520.
25. Vermeulen E, Maertens J, Schoemans H, Lagrou K, (2012) Azole-resistant Aspergillus fumigatus due to TR46/Y121F/T289A mutation emerging in Belgium, July 2012. Euro Surveill 17. pii: 20326.
26. Chowdhary A, Sharma C, Kathuria S, Hagen F, Meis JF, (2013) Azole-resistant Aspergillus fumigatus with the environmental TR46/Y121F/T289A mutation in India. J Antimicrob Chemother doi:10.1093/jac/dkt397. In press.
27. Verweij PE, Kema GH, Zwaan B, Melchers WJ, (2013) Triazole fungicides and the selection of resistance to medical triazoles in the opportunistic mould Aspergillus fumigatus. Pest Manag Sci 69: 165-170.
28. Serfling A, Wohlrab J, Deising HB, (2007) Treatment of a clinically relevant plant-pathogenic fungus with an agricultural azole causes cross-resistance to medical azoles and potentiates caspofungin efficacy. Antimicrob Agents Chemother 51: 3672-3676.
29. Snelders E, Camps SMT, Karawajczyk A, Schaftenaar G, Kema GHJ, et al. (2012) Triazole fungicides can induce cross-resistance to medical triazoles in Aspergillus fumigatus. PLoS ONE 7: e31801 doi:10.1371/journal.pone.0031801.
30. Klaassen CH, Gibbons JG, Fedorova ND, Meis JF, Rokas A, (2012) Evidence for genetic differentiation and variable recombination rates among Dutch populations of the opportunistic human pathogen Aspergillus fumigatus. Mol Ecol 21: 57-70.
31. Mavridou E, Meletiadis J, Jancura P, Abbas S, Arendrup MC, et al. (2013) Composite survival index to compare virulence changes in azole-resistant Aspergillus fumigatus clinical isolates. PLoS ONE 8: e72280 doi:10.1371/journal.pone.0072280.
32. Vale-Silva, Coste AT, Ischer F, Parker JE, Kelly SL, et al. (2012) Azole resistance by loss of function of the sterol Δ5,6- desaturase gene (ERG3) in Candida albicans does not necessarily decrease virulence. Antimicrob Agents Chemother 56: 1960-1968.
33. Camps SMT, Dutilh BE, Arendrup MC, Rijs AJMM, Snelders E, et al. (2012) Discovery of a hapE mutation that causes azole resistance in Aspergillus fumigatus through whole genome sequencing and sexual crossing. PLoS ONE 7: e50034 doi:10.1371/journal.pone.0050034.