Rapid detection of triazole antifungal resistance in Aspergillus fumigatus

Journal of Clinical Microbiology

Volumn 46, Issue 4, 2008, Pages 1200-1206

  Garcia Effron, Guillermo ^a   Dilger, Amanda ^a   Alcazar Fuoli, Laura ^b   Park, Steven ^a   Mellado, Emilia ^b   Perlin, David S ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; CYTOCHROME P450 51A; GLYCINE; ITRACONAZOLE; LEUCINE; METHIONINE; POSACONAZOLE; RAVUCONAZOLE; STEROL 14ALPHA DEMETHYLASE; TRIAZOLE DERIVATIVE; UNCLASSIFIED DRUG; VORICONAZOLE; CYTOCHROME P 450 CYP51A, ASPERGILLUS; CYTOCHROME P-450 CYP51A, ASPERGILLUS; CYTOCHROME P450; FUNGAL PROTEIN;

AMINO ACID SUBSTITUTION; ANTIFUNGAL RESISTANCE; ARTICLE; ASPERGILLUS FUMIGATUS; CONTROLLED STUDY; FUNGAL STRAIN; FUNGUS ISOLATION; GENE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; DNA PROBE; DRUG EFFECT; EVALUATION; GENETICS; HUMAN; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; POLYMERASE CHAIN REACTION; TIME;

ASPERGILLUS FUMIGATUS;

AMINO ACID SUBSTITUTION; ANTIFUNGAL AGENTS; ASPERGILLUS FUMIGATUS; CYTOCHROME P-450 ENZYME SYSTEM; DNA PROBES; DRUG RESISTANCE, FUNGAL; FUNGAL PROTEINS; HUMANS; MICROBIAL SENSITIVITY TESTS; POLYMERASE CHAIN REACTION; TIME FACTORS; TRIAZOLES;

EID: 42449149580     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.02330-07     Document Type: Article

References (46)

1. Balashov, S. V., R. Gardiner, S. Park, and D. S. Perlin. 2005. Rapid, high-throughput, multiplex, real-time PCR for identification of mutations in the cyp51A gene of Aspergillus fumigatus that confer resistance to itraconazole. J. Clin. Microbiol. 43:214-222.
2. Balashov, S. V., S. Park, and D. S. Perlin. 2006. Assessing resistance to the echinocandin antifungal drug caspofungin in Candida albicans by profiling mutations in FKS1. Antimicrob. Agents Chemother. 50:2058-2063.
3. Chen, J., H. Li, R. Li, D. Bu, and Z. Wan. 2005. Mutations in the cyp51A gene and susceptibility to itraconazole in Aspergillus fumigatus serially isolated from a patient with lung aspergilloma. J. Antimicrob. Chemother. 55:31-37.
4. Clark, T. A., and R. A. Hajjeh. 2002. Recent trends in the epidemiology of invasive mycoses. Curr. Opin. Infect. Dis. 15:569-574.
5. Cuenca-Estrella, M., T. M. Diaz-Guerra, E. Mellado, and J. L. Rodriguez-Tudela. 2001. Influence of glucose supplementation and inoculum size on growth kinetics and antifungal susceptibility testing of Candida spp. J. Clin. Microbiol. 39:525-532.
6. Dannaoui, E., E. Borel, M. F. Monier, M. A. Piens, S. Picot, and F. Persat. 2001. Acquired itraconazole resistance in Aspergillus fumigatus. J. Antimicrob. Chemother. 47:333-340.
7. Denning, D. W. 1998. Invasive aspergillosis. Clin. Infect. Dis. 26:781-803.
8. Denning, D. W., S. A. Radford, K. L. Oakley, L. Hall, E. M. Johnson, and D. W. Warnock. 1997. Correlation between in-vitro susceptibility testing to itraconazole and in-vivo outcome of Aspergillus fumigatus infection. J. Antimicrob. Chemother. 40:401-414.
9. Diaz-Guerra, T. M., E. Mellado, M. Cuenca-Estrella, and J. L. Rodriguez-Tudela. 2003. A point mutation in the 14alpha-sterol demethylase gene cyp51A contributes to itraconazole resistance in Aspergillus fumigatus. Antimicrob. Agents Chemother. 47:1120-1124.
10. Diekema, D. J., S. A. Messer, R. J. Hollis, R. N. Jones, and M. A. Pfaller. 2003. Activities of caspofungin, itraconazole, posaconazole, ravuconazole, voriconazole, and amphotericin B against 448 recent clinical isolates of filamentous fungi. J. Clin. Microbiol. 41:3623-3626. 337.
11. Fortun, J., P. Martin-Davila, M. A. Sanchez, V. Pintado, M. E. Alvarez, A. Sanchez-Sousa, and S. Moreno. 2003. Voriconazole in the treatment of invasive mold infections in transplant recipients. Eur. J. Clin. Microbiol. Infect. Dis. 22:408-413.
12. Ghannoum, M. A., and L. B. Rice. 1999. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12:501-517.
13. Gomez-Lopez, A., G. Garcia-Effron, E. Mellado, A. Monzon, J. L. Rodriguez-Tudela, and M. Cuenca-Estrella. 2003. In vitro activities of three licensed antifungal agents against Spanish clinical isolates of Aspergillus spp. Antimicrob. Agents Chemother. 47:3085-3088.
14. Gothard, P., and T. R. Rogers. 2004. Voriconazole for serious fungal infections. Int. J. Clin. Pract. 58:74-80.
15. Greene, R. 2005. The radiological spectrum of pulmonary aspergillosis. Med. Mycol. 43(Suppl. 1):S147-S154.
16. Herbrecht, R., D. W. Denning, T. F. Patterson, J. E. Bennett, R. E. Greene, J. W. Oestmann, W. V. Kern, K. A. Marr, P. Ribaud, O. Lortholary, R. Sylvester, R. H. Rubin, J. R. Wingard, P. Stark, C. Durand, D. Caillot, E. Thiel, P. H. Chandrasekar, M. R. Hodges, H. T. Schlamm, P. F. Troke, and B. de Pauw. 2002. Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N. Engl. J. Med. 347:408-415.
17. Holden, D. W. 1994. DNA miniprep method for Aspergillus fumigatus (and other filamentous fungi), p. 3-9. In B. Maresca and G. S. Kobayashi (ed.), Molecular biology of pathogenic fungi: a laboratory manual. Telos Press, New York, NY.
18. Howard, S. J., I. Webster, C. B. Moore, R. E. Gardiner, S. Park, D. S. Perlin, and D. W. Denning. 2006. Multi-azole resistance in Aspergillus fumigatus. Int. J. Antimicrob. Agents 28:450-453.
19. Imai, J. K., G. Singh, K. V. Clemons, and D. A. Stevens. 2004. Efficacy of posaconazole in a murine model of central nervous system aspergillosis. Antimicrob. Agents Chemother. 48:4063-4066.
20. Kontoyiannis, D. P., and G. P. Bodey. 2002. Invasive aspergillosis in 2002: an update. Eur. J. Clin. Microbiol. Infect. Dis. 21:161-172.
21. Latge, J. P. 1999. Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12:310-350.
22. Maertens, J. A., R. Klont, C. Massen, K. Theunissen, W. Meersseman, K. Lagrou, C. Heinen, B. Crepin, J. Van Eldere, M. Tabouret, J. P. Donnelly, and P. E. Verweij. 2007. Optimization of the cutoff value for the Aspergillus double-sandwich enzyme immunoassay. Clin. Infect. Dis. 44:1329-1336.
23. Mann, P. A., R. M. Parmegiani, S. Q. Wei, C. A. Mendrick, X. Li, D. Loebenberg, B. DiDomenico, R. S. Hare, S. S. Walker, and P. M. McNicholas. 2003. Mutations in Aspergillus fumigatus resulting in reduced susceptibility to posaconazole appear to be restricted to a single amino acid in the cytochrome P450 14α-demethylase. Antimicrob. Agents Chemother. 47:577-581.
24. Marr, K. A., R. A. Carter, F. Crippa, A. Wald, and L. Corey. 2002. Epidemiology and outcome of mould infections in hematopoietic stem cell transplant recipients. Clin. Infect. Dis. 34:909-917.
25. Maschmeyer, G., A. Haas, and O. A. Cornely. 2007. Invasive aspergillosis: epidemiology, diagnosis, and management in immunocompromised patients. Drugs 67:1567-1601.
26. Mellado, E., L. Alcazar-Fuoli, G. Garcia-Effron, A. Alastruey-Izquierdo, M. Cuenca-Estrella, and J. L. Rodriguez-Tudela. 2006. New resistance mechanisms to azole drugs in Aspergillus fumigatus and emergence of antifungal drugs-resistant A. fumigatus atypical strains. Med. Mycol. 44(Suppl.):367-371.
27. Mellado, E., T. M. Diaz-Guerra, M. Cuenca-Estrella, and J. L. Rodriguez-Tudela. 2001. Identification of two different 14-alpha sterol demethylase-related genes (cyp51A and cyp51B) in Aspergillus fumigatus and other Aspergillus species. J. Clin. Microbiol. 39:2431-2438.
28. Mellado, E., G. Garcia-Effron, L. Alcazar-Fuoli, M. Cuenca-Estrella, and J. L. Rodriguez-Tudela. 2004. Substitutions at methionine 220 in the 14α-sterol demethylase (Cyp51A) of Aspergillus fumigatus are responsible for resistance in vitro to azole antifungal drugs. Antimicrob. Agents Chemother. 48:2747-2750.
29. Mellado, E., G. Garcia-Effron, L. Alcazar-Fuoli, W. J. Melchers, P. E. Verweij, M. Cuenca-Estrella, and J. L. Rodriguez-Tudela. 2007. A new Aspergillus fumigatus resistance mechanism conferring in vitro cross-resistance to azole antifungals involves a combination of cyp51A alterations. Antimicrob. Agents Chemother. 51:1897-1904.
30. Mihu, C. N., E. King, O. Yossepovitch, Y. Taur, A. Jakubowski, E. Pamer, and G. A. Papanicolaou. Risk factors and attributable mortality of late aspergillosis after T-cell-depleted hematopoietic stem cell transplantation. Transpl. Infect. Dis., in press.
31. Mosquera, J., and D. W. Denning. 2002. Azole cross-resistance in Aspergillus fumigatus. Antimicrob. Agents Chemother. 46:556-557.
32. Munayyer, H. K., P. A. Mann, A. S. Chau, T. Yarosh-Tomaine, J. R. Greene, R. S. Hare, L. Heimark, R. E. Palermo, D. Loebenberg, and P. M. McNicholas. 2004. Posaconazole is a potent inhibitor of sterol 14α-demethylation in yeasts and molds. Antimicrob. Agents Chemother. 48:3690-3696.
33. Nascimento, A. M., G. H. Goldman, S. Park, S. A. Marras, G. Delmas, U. Oza, K. Lolans, M. N. Dudley, P. A. Mann, and D. S. Perlin. 2003. Multiple resistance mechanisms among Aspergillus fumigatus mutants with high-level resistance to itraconazole. Antimicrob. Agents Chemother. 47:1719-1726.
34. National Committee for Clinical Laboratory Standards. 2002. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard. Document M38-A. NCCLS, Wayne, PA.
35. Petraitiene, R., V. Petraitis, C. A. Lyman, A. H. Groll, D. Mickiene, J. Peter, J. Bacher, K. Roussillon, M. Hemmings, D. Armstrong, N. A. Avila, and T. J. Walsh. 2004. Efficacy, safety, and plasma pharmacokinetics of escalating dosages of intravenously administered ravuconazole lysine phosphoester for treatment of experimental pulmonary aspergillosis in persistently neutropenic rabbits. Antimicrob. Agents Chemother. 48:1188-1196.
36. Petrikkou, E., J. L. Rodriguez-Tudela, M. Cuenca-Estrella, A. Gomez, A. Molleja, and E. Mellado. 2001. Inoculum standardization for antifungal susceptibility testing of filamentous fungi pathogenic for humans. J. Clin. Microbiol. 39:1345-1347.
37. Rodriguez-Tudela, J. L., L. Alcazar-Fuoli, A. Alastruey-Izquierdo, A. Monzon, E. Mellado, and M. Cuenca-Estrella. 2007. Time of incubation for antifungal susceptibility testing of Aspergillus fumigatus: can MIC values be obtained at 24 hours? Antimicrob. Agents Chemother. 51:4502-4504.
38. Rodriguez-Tudela, J. L., E. Chryssanthou, E. Petrikkou, J. Mosquera, D. W. Denning, and M. Cuenca-Estrella. 2003. Interlaboratory evaluation of hematocytometer method of inoculum preparation for testing antifungal susceptibilities of filamentous fungi. J. Clin. Microbiol. 41:5236-5237.
39. Silva Ferreira, M. E., J. L. Capellaro, M. E. dos Reis, I. Malavazi, D. Perlin, S. Park, J. B. Anderson, A. L. Colombo, B. A. Arthington-Skaggs, M. H. Goldman, and G. H. Goldman. 2004. In vitro evolution of itraconazole resistance in Aspergillus fumigatus involves multiple mechanisms of resistance. Antimicrob. Agents Chemother. 48:4405-4413.
40. Slaven, J. W., M. J. Anderson, D. Sanglard, G. K. Dixon, J. Bille, I. S. Roberts, and D. W. Denning. 2002. Increased expression of a novel Aspergillus fumigatus ABC transporter gene, atrF, in the presence of itraconazole in an itraconazole resistant clinical isolate. Fungal Genet. Biol. 36:199-206.
41. Trama, J. P., E. Mordechai, and M. E. Adelson. 2005. Detection of Aspergillus fumigatus and a mutation that confers reduced susceptibility to itraconazole and posaconazole by real-time PCR and pyrosequencing. J. Clin. Microbiol. 43:906-908.
42. Tyagi, S., D. P. Bratu, and F. R. Kramer. 1998. Multicolor molecular beacons for allele discrimination. Nat. Biotechnol. 16:49-53.
43. Upton, A., K. A. Kirby, P. Carpenter, M. Boeckh, and K. A. Marr. 2007. Invasive aspergillosis following hematopoietic cell transplantation: outcomes and prognostic factors associated with mortality. Clin. Infect. Dis. 44:531-540.
44. Verweij, P. E., E. Mellado, and W. J. Melchers. 2007. Multiple-triazole-resistant aspergillosis. N. Engl. J. Med. 356:1481- 1483.
45. Verweij P. E., H. A. L. Van Der Lee, J. Kuijpers, E. Snelders, A. J. M. M. Rijs, and W. J. G. Melchers. 2007. Epidemiology of multiple-triazole-resistant Aspergillus fumigatus. Abstr. 47th Intersci. Conf. Antimicrob. Agents Chemother., abstr. M-2018.
46. Xiao, L., V. Madison, A. S. Chau, D. Loebenberg, R. E. Palermo, and P. M. McNicholas. 2004. Three-dimensional models of wild-type and mutated forms of cytochrome P450 14α-sterol demethylases from Aspergillus fumigatus and Candida albicans provide insights into posaconazole binding. Antimicrob. Agents Chemother. 48:568-574.