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

Volumn 7, Issue 12, 2012, Pages

  Chowdhary, Anuradha ^a   Kathuria, Shallu ^a   Xu, Jianping ^b   Sharma, Cheshta ^a   Sundar, Gandhi ^a   Singh, Pradeep Kumar ^a   Gaur, Shailendra N ^a   Hagen, Ferry ^c   Klaassen, Corné H ^c   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

BROMUCONAZOLE; CYPROCONAZOLE; CYTOCHROME P450; CYTOCHROME P450 51A; DIFENOCONAZOLE; EPOXICONAZOLE; FUNGICIDE; HEXACONAZOLE; ITRACONAZOLE; METCONAZOLE; PENCONAZOLE; POSACONAZOLE; TEBUCONAZOLE; TRIADIMEFON; TRICYCLAZOLE; UNCLASSIFIED DRUG; VORICONAZOLE;

AGRICULTURE; AIR SAMPLING; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; ASPERGILLUS FUMIGATUS; CHINA; CLONAL VARIATION; CONTROLLED STUDY; COTTON; CROSS RESISTANCE; CYP51 GENE; ENVIRONMENT; FLOWER; FRANCE; FUNGAL STRAIN; FUNGUS ISOLATION; GENETIC SUSCEPTIBILITY; GERMANY; INDIA; MICROSATELLITE MARKER; MINIMUM INHIBITORY CONCENTRATION; MUTATIONAL ANALYSIS; NETHERLANDS; NONHUMAN; POPULATION GENETICS; PROGENY; RICE; SOIL ANALYSIS; TEA; WARD;

AMINO ACID SUBSTITUTION; ANTIFUNGAL AGENTS; ASPERGILLUS FUMIGATUS; CLONE CELLS; COLONY COUNT, MICROBIAL; CYTOCHROME P-450 ENZYME SYSTEM; DRUG RESISTANCE, MULTIPLE, FUNGAL; ENVIRONMENT; FUNGAL PROTEINS; FUNGICIDES, INDUSTRIAL; HISTIDINE; HUMANS; INDIA; LEUCINE; MUTATION, MISSENSE; TANDEM REPEAT SEQUENCES; TRIAZOLES;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; AVES; GOSSYPIUM HIRSUTUM;

EID: 84871677613     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052871     Document Type: Article

References (42)

1. Chakrabarti A, Chatterjee SS, Das A, Shivaprakash MR, (2011) Invasive aspergillosis in developing countries. Med Mycol 49(Suppl 1): S35-47.
2. Verweij PE, Denning DW, (1997) The challenge of invasive aspergillosis: increasing numbers in diverse patient groups. Int J Infect Dis 2: 61-63.
3. Denning DW, Perlin DS, (2011) Azole resistance in Aspergillus: a growing public health menace. Future Microbiol 6: 1229-1232.
4. Herbrecht R, Denning DW, Patterson TF, Bennett JE, Greene RE, et al. (2002) Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N Engl J Med 347: 408-415.
5. Cornely OA, Maertens J, Winston DJ, Perfect J, Ullmann AJ, et al. (2007) Posaconazole vs. fluconazole or itraconazole prophylaxis in patients with neutropenia. N Engl J Med 356: 348-359.
6. 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.
7. 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.
8. 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.
9. Howard SJ, Arendrup MC, (2011) Acquired antifungal drug resistance in Aspergillus fumigatus: epidemiology and detection. Med Mycol 49(Suppl 1): S90-S95.
10. Snelders E, Melchers WJ, Verweij PE, (2011) Azole resistance in Aspergillus fumigatus: a new challenge in the management of invasive aspergillosis. Future Microbiol 6: 335-347.
11. Camps SM, van der Linden JW, Li Y, Kuijper EJ, van Dissel JT, et al. (2012) Rapid induction of multiple resistance mechanisms in Aspergillus fumigatus during azole therapy: a case study and review of the literature. Antimicrob Agents Chemother 56: 10-16.
12. Stensvold CR, Jorgensen LN, Arendrup MC, (2012) Azole-resistant invasive Aspergillus: relationship to agriculture. Curr Fungal Infect Rep 6: 178-191.
13. Verweij PE, Snelders E, Kema GH, Mellado E, Melchers WJ, (2009) Azole resistance in Aspergillus fumigatus: a side effect of environmental fungicide use? Lancet Infect Dis 9: 789-795.
14. Rodriguez-Tudela JL, Alcazar-Fuoli L, Mellado E, Alastruey-Izquierdo A, Monzon A, et al. (2008) Epidemiological cutoffs and cross-resistance to azole drugs in Aspergillus fumigatus. Antimicrob Agents Chemother 52: 2468-2472.
15. 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.
16. Howard SJ, Pasqualotto AC, Denning DW, (2010) Azole resistance in allergic bronchopulmonary aspergillosis and Aspergillus bronchitis. Clin Microbiol Infect 16: 683-688.
17. 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.
18. Burgel PR, Baixench MT, Amsellem M, Audureau E, Chapron J, et al. (2012) High prevalence of azole-resistant Aspergillus fumigatus in adults with cystic fibrosis exposed to itraconazole. Antimicrob Agents Chemother 56: 869-874.
19. Rath PM, Buchheidt D, Spiess B, Arfanis E, Buer J, et al. (2012) First reported case of azole-resistant Aspergillus fumigatus due to TR/L98H mutation in Germany. Antimicrob Agents Chemother 56: 6060-6061.
20. Snelders E, van der Lee HA, 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.
21. 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 ONEe 7(3): e31801.
22. 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.
23. Hof H, (2001) Critical annotations to the use of azole antifungals for plant protection. Antimicrob Agents Chemother 45: 2987-2990.
24. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, et al. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484: 186-194.
25. 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.
26. Thind TS, (2007) Changing cover of fungicide umbrella in crop protection. Indian Phytopath 60: 421-433.
27. Singh N, Dureja P, (2000) Persistence of hexaconazole, a triazole fungicide in soils. J Environ Sci Health B 35: 549-558.
28. Kuipers S, Brüggemann RJ, de Sévaux RG, Heesakkers JP, Melchers WJ, et al. (2011) Failure of posaconazole therapy in a renal transplant patient with invasive aspergillosis due to Aspergillus fumigatus with attenuated susceptibility to posaconazole. Antimicrob Agents Chemother 55: 3564-3566.
29. NETHMAP (2012) Consumption of antimicrobial agents and antimicrobial resistance among medically important bacteria in the Netherlands 59-60. Available: http://www.rivm.nl/dsresource?objectid=rivmp:181194&type=org&disposition=inline. Accessed 2012 Sep 4.
30. 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.
31. Müller FM, Staudigel A, Salvenmoser S, Tredup A, Miltenberger R, et al. (2007) Cross-resistance to medical and agricultural azole drugs in yeasts from the oropharynx of human immunodeficiency virus patients and from environmental Bavarian vine grapes. Antimicrob Agents Chemother 51: 3014-3016.
32. zur Wiesch PA, Kouyos R, Engelstädter J, Regoes RR, Bonhoeffer S, (2011) Population biological principles of drug-resistance evolution in infectious diseases. Lancet Infect Dis 11: 236-247.
33. Fisher MC, Henk DA, (2012) Sex, drugs and recombination: the wild life of Aspergillus. Mol Ecol 21: 1305-1306.
34. Glass NL, Donaldson GC, (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61: 1323-1330.
35. Hong SB, Cho HS, Shin HD, Frisvad JC, Samson RA, (2006) Novel Neosartorya species isolated from soil in Korea. Int J Syst Evol Microbiol 56: 477-486.
36. Clinical and Laboratory Standards Institute (2008) Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard, 2nd ed. CLSI document M38-A2. Wayne (PA.
37. Verweij PE, Howard SJ, Melchers WJ, Denning DW, (2009) Azole-resistance in Aspergillus: proposed nomenclature and breakpoints. Drug Resist Updat 12: 141-147.
38. Klaassen CH, de Valk HA, Curfs-Breuker IM, Meis JF, (2010) Novel mixed-format real-time PCR assay to detect mutations conferring resistance to triazoles in Aspergillus fumigatus and prevalence of multi-triazole resistance among clinical isolates in the Netherlands. J Antimicrob Chemother 65: 901-905.
39. de Valk HA, Meis JF, Curfs-Breuker IM, Muehlethaler K, Mouton JW, et al. (2005) Use of a novel panel of nine short tandem repeats for exact and high-resolution fingerprinting of Aspergillus fumigatus isolates. J Clin Microbiol 43: 4112-4120.
40. 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.
41. Peakall R, Smouse PE, (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
42. Agapow PM, Burt A, (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1: 101-102.