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

Volumn 11, Issue 1-2, 2008, Pages 25-31

  Hof, Herbert ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

14 Demethylase; Azoles; Efflux pumps; Horizontal gene transfer; Moulds; Selection; Yeasts

Indexed keywords

ANTIFUNGAL AGENT; FLUCONAZOLE; FUNGAL ENZYME; ITRACONAZOLE; KETOCONAZOLE; POSACONAZOLE; PYRROLE DERIVATIVE; STEROL 14ALPHA DEMETHYLASE; VORICONAZOLE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANTIBIOTIC RESISTANCE; ANTIFUNGAL RESISTANCE; ARTICLE; DRUG MECHANISM; FUNGICIDAL ACTIVITY; FUNGUS ISOLATION; FUNGUS MUTATION; GENETIC CODE; GENETIC SELECTION; GENETIC TRAIT; HORIZONTAL GENE TRANSFER; HUMAN; LONG TERM CARE; LOW DRUG DOSE; MYCOSIS; NONHUMAN; OROPHARYNX CANDIDIASIS; PHENOTYPE; PRIORITY JOURNAL; PROPHYLAXIS; VAGINA CANDIDIASIS; YEAST;

ANIMALS; ANTIFUNGAL AGENTS; AZOLES; DRUG RESISTANCE, FUNGAL; FUNGI; HUMANS; MOLECULAR STRUCTURE; MYCOSES;

EID: 42749086776     PISSN: 13687646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.drup.2008.01.001     Document Type: Article

References (60)

1. Akins R.A. An update on antifungal targets and mechanisms of resistance in Candida albicans. Med. Mycol. 43 (2005) 285-318
2. Anderson J.B. Evolution of antifungal drug resistance: mechanisms and pathogen fitness. Nat. Rev. Microbiol. 3 (2005) 547-556
3. Araujo R., Pina-Vaz C., and Rodrigues A.G. Susceptibility of environmental versus clinical strains of pathogenic Aspergillus. Int. J. Antimicrob. Agents 29 (2007) 108-111
4. Balajee S.A., Weaver M., Imhof A., Gribskov J., and Marr K.A. Aspergillus fumigatus variant with decreased susceptibility to multiple antifungals. Antimicrob. Agents Chemother. 48 (2004) 1197-1203
5. Barchiesi F., Arzeni D., Fothergill A.W., Di Francesco L.F., Caselli F., Rinaldi M.G., and Scalise G. In vitro activities of the new antifungal triazole SCH 56592 against common and emerging yeast pathogens. Antimicrob. Agents Chemother. 44 (2000) 226-229
6. Bedini A., Venturelli C., Mussini C., Guaraldi G., Codeluppi M., Borghi V., Rumpianesi F., Barchiesi F., and Esposito R. Epidemiology of candidaemia and antifungal susceptibility patterns in an Italian tertiary-care hospital. Clin. Microbiol. Infect. 12 (2006) 75-80
7. Brion L.P., Uko S.E., and Goldman D.L. Risk of resistance associated with fluconazole prophylaxis: systematic review. J. Infect. 54 (2007) 521-529
8. Brun S., Dalle F., Saulnier P., Renier G., Bonnin A., Chabasse D., and Bouchara J.P. Biological consequences of petite mutations in Candida glabrata. J. Antimicrob. Chemother. 56 (2005) 307-314
9. Carrillo-Munoz A.J., Quindos G., Ruesga M., Alonso R., del Valle O., Hernandez-Molina J.M., McNicholas P., Loebenberg D., and Santos P. Antifungal activity of posaconazole compared with fluconazole and amphotericin B against yeasts from oropharyngeal candidiasis and other infections. J. Antimicrob. Chemother. 55 (2005) 317-319
10. Chamilos G., and Kontoyiannis D.P. Update on antifungal drug resistance mechanisms of Aspergillus fumigatus. Drug Res. Updates 8 (2005) 344-358
11. Chau A.S., Mendrick C.A., Sabatelli F.J., Loebenberg D., and McNicholas P.M. Application of real-time quantitative PCR to molecular analysis of Candida albicans strains exhibiting reduced susceptibility to azoles. Antimicrob. Agents Chemother. 48 (2004) 2124-2131
12. Cornely O.A., Maertens J., Winston D.J., Perfect J., Ullmann A.J., Walsh T.J., Helfgott D., Holowiecki J., Stockelberg D., Goh Y.T., Petrini M., Hardalo C., Suresh R., and Angulo-Gonzalez D. Posaconazole vs. fluconazole or itraconazole prophylaxis in patients with neutropenia. N. Engl. J. Med. 356 (2007) 348-359
13. Coste A., Turner V., Ischer F., Morschhauser J., Forche A., Selmecki A., Berman J., Bille J., and Sanglard D. A mutation in Tac1p, a transcription factor regulating CDR1 and CDR2, is coupled with loss of heterozygosity at chromosome 5 to mediate antifungal resistance in Candida albicans. Genetics 172 (2006) 2139-2156
14. Cowen L.E. Predicting the emergence of resistance to antifungal drugs. FEMS Microbiol. Lett. 204 (2001) 1-7
15. Cowen L.E., and Lindquist L. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309 (2005) 2185-2189
16. Cowen L.E., Nantel A., Whiteway M.S., Thomas D.Y., Tessier D.C., Kohn L.M., and Anderson J.B. Population genomics of drug resistance in Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 9284-9289
17. Franz R., Ruhnke M., and Morschhäuser J. Molecular aspects of fluconazole resistance development in Candida albicans. Mycoses 42 (1999) 453-458
18. Ghannoum M.A., and Rice L.B. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12 (1999) 501-517
19. Goldman M., et al. A randomized study of the use of fluconazole in continuous versus episodic therapy in patients with advanced HIV infection and a history of oropharyngeal candidiasis: AIDS Clinical Trials Group Study 323/Mycoses Study Group Study 40. Clin. Infect. Dis. 41 (2005) 1473-1480
20. Groll A.H., and Walsh T.J. Posaconazole: clinical pharmacology and potential for management of fingal infections. Expert Rev. Infect. Ther. 3 (2005) 467-487
21. Guinea J., Peláez T., Alcalá L., Ruiz-Serrano M.J., and Bouza E. Antifungal susceptibility of 596 Aspergillus fumigatus strains isolated from outdoor air, hospital air, and clinical samples: analysis by site of isolation. Antimicrob. Agents Chemother. 49 (2005) 3495-3497
22. Guinea J., Sánchez-Somolinos M., Cuevas O., Peláez T., and Bouza E. Fluconazole resistance mechanisms in Candida krusei: the contribution of efflux-pumps. Med. Mycol. 44 (2006) 575-578
23. Hof H. Critical annotations to the use of azole antifungals for plant protection. Antimicrob. Agents Chemother. 45 (2001) 2897-2990
24. Hof H. A new, broad-spectrum azole antifungal: posaconazole-mechanisms of action and resistance, spectrum of activity. Mycoses 49 Suppl. 1 (2006) 1-5
25. Howard S.J., Webster I., Moore C.B., Gardiner R.E., Park S., Perlin D.S., and Denning D.W. Multi-azole resistance in Aspergillus fumigatus. Int. J. Antimicrob. Agents 28 (2006) 450-453
26. Kaya A.D., and Kiraz N. In vitro susceptibilities of Aspergillus spp. causing otomycosis to amphotericin B, voriconazole and itraconazole. Mycoses 50 (2007) 447-450
27. Knoke M. Gastrointestinal microecology of humans and Candida. Mycoses 42 Suppl. 1 (1999) 30-34
28. Levy S.B. The challenge of antibiotic resistance. Sci. Am. 278 (1998) 46-53
29. Li X., Brown N., Chau A.S., López-Ribot J.L., Ruesga M.T., Quindos G., Mendrick C.A., Hare R.S., Loebenberg D., DiDomenico B., and McNicholas P.M. Changes in susceptibility to posaconazole in clinical isolates of Candida albicans. J. Antimicrob. Chemother. 53 (2004) 74-80
30. Lopez J., Pernot C., Aho S., Caillot D., Vagner O., Dalle F., Durnet-Archeray M.J., Chavanet P., and Bonnin A. Decrease in Candida albicans strains with reduced susceptibility to fluconazole following changes in prescribing policies. J. Hosp. Infect. 48 (2001) 122-128
31. Lunel F.M.V., Meis J.F.G.M., and Voss A. Nosocomial fungal infections: candidemia. Diagn. Microbiol. Infect. Dis. 34 (1999) 213-220
32. Lyon B.R., and Skurray R. Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol. Rev. 51 (1987) 88-134
33. Manavathu E.K., Cutright J.L., Loebenberg D., and Chadrasekar P.H. A comparative study of the in vitro susceptibilities of clinical and laboratory-selected resistant isolates of Aspergillus spp. to amphotericin B, itraconazole, voriconazole and posaconazole (SCH 56592). J. Antimicrob. Chemother. 46 (2000) 229-234
34. Mann P.A., Parmegiani R.M., Wei S.Q., Mendrick C.A., Li X., Loebenberg D., DiDomenico B., Hare R.S., Walker S.S., and McNicholas P.M. Mutations in Aspergillus fumigatus resulting in reduced susceptibility to posaconazole appear to be restricted to a single amino acid in the cytochrome P450 14alpha-demethylase. Antimicrob. Agents Chemother. 47 (2003) 577-581
35. Marichal P., Koymans L., Willemsens S., Bellens D., Verhasselt P., Luyten W., Borgers M., Ramaekers F.C., Odds F.C., and Bossche H.V. Contribution of mutations in the cytochrome P450 14alpha-demethylase (Erg11p; Cyp51) to azole resistance in Candida albicans. Microbiology 145 (1999) 2701-2713
36. Marr K.A., White T.C., van Burik J.A., and Bowden R.A. Development of fluconazole resistance in Candida albicans causing disseminated infection in a patient undergoing marrow transplantation. Clin. Infect. Dis. 25 (1997) 908-910
37. Marr K.A., Lyons C.N., Rustad T.R., Bowden R.A., and White T.C. Rapid, transient fluconazole resistance in Candida albicans is associated with increased mRNA levels of CDR. Antimicrob. Agents Chemother. 42 (1998) 2584-2589
38. Martins M.D., Lozano-Chiu M., and Rex J.H. Declining rates of oropharyngeal candidiasis and carriage of Candida albicans associated with trends towards reduced rates of carriage of fluconazole-resistant Candida albicans in human immunodeficiency virus-infected patients. Clin. Inf. Dis. 27 (1998) 1291-1294
39. Meis J., et al. A global evaluation of the susceptibility of Candida species to fluconazole by disk diffusion. Diagn. Microbiol. Infect. Dis 36 (2000) 215-223
40. Mellado E., Garcia-Effron G., Alcázar-Fuoli L., Melchers W.J., Verweij P.E., Cuenca-Estrella M., and Rodríguez-Tudela J.L. A new Aspergillus fumigatus resistance mechanism conferring in vitro cross-resistance to azole antifungals involves a combination of cyp51A alterations. Antimicrob. Agents Chemother. 51 (2007) 1897-1904
41. Meneau I., and Sanglard D. Azole and fungicide resistance in clinical and environmental Aspergillus fumigatus isolates. Med. Mycol. 43 Suppl 1 (2005) S307-S311
42. Munayyer H.K., Mann P.A., Chau A.S., Yarosh-Tomaine T., Greene J.R., Hare R.S., Heimark L., Palermo R.E., Loebenberg D., and McNicholas P.M. Posaconazole is a potent inhibitor of sterol 14alpha-demethylation in yeasts and molds. Antimicrob. Agents Chemother. 48 (2004) 3690-3696
43. Neuhauser M.M., Weinstein R.A., Rydman R., Danziger L.H., Karam G., and Quinn J.P. Antibiotic resistance among gram-negative bacilli in US intensive care units: implications for fluoroquinolone use. JAMA 289 (2003) 885-888
44. Pfaller M.A., Messer A.A., Houston A., Rangel-Frausto M.S., Wiblin T., Blumberg H.M., Edwards J.E., Jarvis W., Martin M.A., Neu H.C., Saiman L., Patterson J.E., Dibb J.C., Roldan C.M., Rinaldi M.G., and Wenzel R.P. National epidemiology of mycoses survey: a multicenter study of strain variation and antifungal susceptibilty among isolates of Candida species. Diagn. Microbiol. Infect. Dis. 31 (1998) 289-296
45. Pfaller M.A., Boyken L., Hollis R.J., Messer S.A., Tendolkar S., and Diekema D.J. In vitro susceptibilities of Candida spp. to caspofungin: four years of global surveillance. J. Clin. Microbiol. 44 (2006) 760-763
46. Raad I.I., Graybill J.R., Bustamante A.B., Cornely O.A., Gaona-Flores V., Afif C., Graham D.R., Greenberg R.N., Hadley S., Langston A., Negroni R., Perfect J.R., Pitisuttithum P., Restrepo A., Schiller G., Pedicone L., and Ullmann A.J. Safety of long-term oral posaconazole use in the treatment of refractory invasive fungal infections. Clin. Infect. Dis. 42 (2006) 1726-1734
47. Redding S., Smith J., Farinacci G., Rinaldi M., Fothergill A., Rhine-Chalberg J., and Pfaller M. Resistance of Candida albicans to fluconazole during treatment of oropharyngeal candidiasis in a patient with AIDS: documentation by in vitro susceptibility testing and DNA subtype analysis. Clin. Infect. Dis. 18 (1994) 240-242
48. Rex J.H., Rinaldi M.G., and Pfaller M.A. Resistance of Candida species to fluconazole. Antimicrob. Agents Chemother. 39 (1995) 1-8
49. Richardson M.D. Changing patterns and trends in systemic fungal infections. J. Antimicrob. Chemother. 56 Suppl. 1 (2005) i5-i11
50. Richter S.S., Galask R.P., Messer S.A., Hollis R.J., Diekema D.J., and Pfaller M.A. Antifungal susceptibilities of Candida species causing vulvovaginitis and epidemiology of recurrent cases. J. Clin. Microbiol. 43 (2005) 2155-2162
51. Sabatelli F., Patel R., Mann P.A., Mendrick C.A., Norris C.C., Hare R., Loebenberg D., Black T.A., and McNicholas P.M. In vitro activities of posaconazole, fluconazole, itraconazole, voriconazole, and amphotericin B against a large collection of clinically important molds and yeasts. Antimicrob. Agents Chemother. 50 (2006) 2009-2015
52. Schauer F., and Hanschke R. Taxonomy and ecology of the genus Candida. Mycoses 42 Suppl. (1999) 12-21
53. In: Schmid H. (Ed). Do azole fungicides endanger the medicinal efficacy of antimycotics? (2001), Industrieverband Agrar, Frankfurt a.M. Germany
54. Sipos G., and Kuchler K. Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Curr. Drug Targets 7 (2006) 471-481
55. Skiest D.J., Vazquez J.A., Anstead G.M., Graybill J.R., Reynes J., Ward D., Hare R., Boparai N., and Isaacs R. Posaconazole for the treatment of azole-refractory oropharyngeal and esophageal candidiasis in subjects with HIV infection. Clin. Infect. Dis. 44 (2007) 607-614
56. Ullmann A.J., Lipton J.H., Vesole D.H., Chandrasekar P., Langston A., Taratolo S.R., Greinix H., Morais de Azevedo W., Reddy V., Boparai N., Pedicone L., Patinho H., and Durrant S. Posaconazole or fluconazole for prophylaxis in severe graft-versus-host disease. N. Engl. J. Med. 356 (2007) 335-347
57. Waard de M., Andrade A.C., Hayashi K., Schoonbeck H.-J., Stergiopoulos I., and Zwiers L.-H. Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manage. Sci. 62 (2006) 195-207
58. Wingard J.R., Merz W.G., Rinaldi M.G., Johnson R.T., Karp J.E., and Saral R. Increase in Candida krusei infections among patients with bone marrow transplantation and neutropenia treated prophylactically with fluconazole. N. Engl. J. Med. 325 (1991) 1274-1277
59. Xiao L., Madison V., Chau A.S., Loebenberg D., Palermo R.E., and McNicholas P.M. Three-dimensional models of wild-type and mutated forms of cytochrome P450 14alpha-sterol demethylases from Aspergillus fumigatus and Candida albicans provide insights into posaconazole binding. Antimicrob. Agents Chemother. 48 (2004) 568-574
60. Zervos M.J., Hershberger E., Nicolau D.P., Ritchie D.J., Blackner L.K., Coyle E.A., Donnelly A.J., Eckel S.F., Eng R.H., Hiltz A., Kuyumjian A.G., Krebs W., McDaniel A., Hogan P., and Lubowski T.J. Relationship between fluoroquinolone use and changes in susceptibility to fluoroquinolones of selected pathogens in 10 United States teaching hospitals, 1991-2000. Clin. Infect. Dis. 37 (2003) 1643-1648