Fluconazole and echinocandin resistance of Candida glabrata correlates better with antifungal drug exposure rather than with MSH2 mutator genotype in a french cohort of patients harboring low rates of resistance

Frontiers in Microbiology

Volumn 7, Issue DEC, 2016, Pages

  Dellière, Sarah ^a   Healey, Kelley ^b   Gits Muselli, Maud ^a,c   Carrara, Bastien ^a   Barbaro, Alessandro ^a   Guigue, Nicolas ^a   Lecefel, Christophe ^a   Touratier, Sophie ^a   Desnos Ollivier, Marie ^d   Perlin, David S ^b   Bretagne, Stéphane ^a,c,d   Alanio, Alexandre ^a,c,d  

^a SAINT LOUIS HOSPITAL   (France)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d CNRS   (France)

Author keywords

Antifungal resistance; Candida glabrata; Echinocandin; Fluconazole; Genotyping; MSH2; Mutator genotype; Short tandem repeat

Indexed keywords

CASPOFUNGIN; ECHINOCANDIN; FLUCONAZOLE; PROTEIN MSH2;

ADULT; AGED; ANTIFUNGAL RESISTANCE; ARTICLE; CANDIDA GLABRATA; CONTROLLED STUDY; DNA POLYMORPHISM; DRUG EXPOSURE; EPSILOMETER TEST; FEMALE; FRANCE; GENE SEQUENCE; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MINIMUM INHIBITORY CONCENTRATION; MSH2 GENE; MUTATOR GENE; NONHUMAN; POLYMERASE CHAIN REACTION; PREVALENCE; SHORT TANDEM REPEAT;

EID: 85009431555     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.02038     Document Type: Article

References (40)

1. Abbes, S., Sellami, H., Sellami, A., Hadrich, I., Amouri, I., Mahfoudh, N., et al. (2012). Candida glabrata strain relatedness by new microsatellite markers. Eur. J. Clin. Microbiol. Infect. Dis. 31, 83-91. doi: 10.1007/s10096-011-1280-4
2. Alexander, B. D., Johnson, M. D., Pfeiffer, C. D., Jiménez-Ortigosa, C., Catania, J., Booker, R., et al. (2013). Increasing echinocandin resistance in Candida glabrata: clinical failure correlates with presence of FKS mutations and elevated minimum inhibitory concentrations. Clin. Infect. Dis. 56, 1724-1732. doi: 10.1093/cid/cit136
3. Arendrup, M. C., Cuenca-Estrella, M., Lass-Flörl, C., Hope, W., and EUCAST-AFST (2012). EUCAST technical note on the EUCAST definitive document EDef 7.2: method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts EDef 7.2 (EUCAST-AFST). Clin. Microbiol. Infect. 18, E246-E247. doi: 10.1111/j.1469-0691.2012.03880.x
4. Arendrup, M. C., Cuenca-Estrella, M., Lass-Flörl, C., and Hope, W. W. (2013). Breakpoints for antifungal agents: an update from EUCAST focussing on echinocandins against Candida spp. and triazoles against Aspergillus spp. Drug Resist. Updat. 16, 81-95. doi: 10.1016/j.drup.2014.01.001
5. Bassetti, M., Merelli, M., Righi, E., Diaz-Martin, A., Rosello, E. M., Luzzati, R., et al. (2013). Epidemiology, species distribution, antifungal susceptibility, and outcome of candidemia across five sites in Italy and Spain. J. Clin. Microbiol. 51, 4167-4172. doi: 10.1128/JCM.01998-13
6. Beyda, N. D., John, J., Kilic, A., Alam, M. J., Lasco, T. M., and Garey, K. W. (2014). FKS mutant Candida glabrata: risk factors and outcomes in patients with candidemia. Clin. Infect. Dis. 59, 819-825. doi: 10.1093/cid/ciu407
7. Bougnoux, M.-E., Dannaoui, E., Accoceberry, I., Angoulvant, A., Bailly, E., Botterel, F., et al. (2016). Multicenter comparison of the etest and EUCAST methods for antifungal susceptibility testing of Candida isolates to micafungin. Antimicrob. Agents Chemother. 60, 5088-5091. doi: 10.1128/AAC.00630-16
8. Bourgeois, N., Laurens, C., Bertout, S., Balard, Y., Krasteva, D., Rispail, P., et al. (2014). Assessment of caspofungin susceptibility of Candida glabrata by the Etest®, CLSI, and EUCAST methods, and detection of FKS1 and FKS2 mutations. Eur. J. Clin. Microbiol. Infect. Dis. 33, 1247-1252. doi: 10.1007/s10096-014-2069-z
9. Brisse, S., Pannier, C., Angoulvant, A., de Meeus, T., Diancourt, L., Faure, O., et al. (2009). Uneven distribution of mating types among genotypes of Candida glabrata isolates from clinical samples. Eukaryot. Cell 8, 287-295. doi: 10.1128/EC.00215-08
10. Castanheira, M., Messer, S. A., Rhomberg, P. R., and Pfaller, M. A. (2016). Antifungal susceptibility patterns of a global collection of fungal isolates: results of the SENTRY antifungal surveillance program (2013). Diagn. Microbiol. Infect. Dis. 85, 200-204. doi: 10.1016/j.diagmicrobio.2016.02.009
11. Cleveland, A. A., Farley, M. M., Harrison, L. H., Stein, B., Hollick, R., Lockhart, S. R., et al. (2012). Changes in incidence and antifungal drug resistance in candidemia: results from population-based laboratory surveillance in Atlanta and Baltimore, 2008-2011. Clin. Infect. Dis. 55, 1352-1361. doi: 10.1093/cid/cis697
12. Dannaoui, E., Desnos-Ollivier, M., Garcia-Hermoso, D., Grenouillet, F., Cassaing, S., Baixench, M.-T., et al. (2012). Candida spp. with acquired echinocandin resistance, France, 2004-2010. Emerg. Infect. Dis. 18, 86-90. doi: 10.3201/eid1801.110556
13. Desnos-Ollivier, M., Bretagne, S., Raoux, D., Hoinard, D., Dromer, F., Dannaoui, E., et al. (2008). Mutations in the fks1 gene in Candida albicans, C. tropicalis, and C. krusei correlate with elevated caspofungin MICs uncovered in AM3 medium using the method of the European Committee on antibiotic susceptibility testing. Antimicrob. Agents Chemother. 52, 3092-3098. doi: 10.1128/AAC.00088-08
14. Espinel-Ingroff, A., Arendrup, M., Cantón, E., Cordoba, S., Dannaoui, E., García-Rodríguez, J., et al. (2016). A multi-center study of method-dependent epidemiological cutoffvalues (ECVs) for resistance detection in Candida spp. and Aspergillus spp. to amphotericin B and echinocandins for the Etest agar diffusion method. Antimicrob. Agents Chemother. doi: 10.1128/AAC.01792-16. [Epub ahead of print].
15. Espinel-Ingroff, A., Arendrup, M. C., Pfaller, M. A., Bonfietti, L. X., Bustamante, B., Canton, E., et al. (2013). Interlaboratory variability of Caspofungin MICs for Candida spp. Using CLSI and EUCAST methods: should the clinical laboratory be testing this agent? Antimicrob. Agents Chemother. 57, 5836-5842. doi: 10.1128/AAC.01519-13
16. European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2015). Antifungal Agents: Brekpoint Tables for Interpretation of MICs, Version 8.0.
17. Farmakiotis, D., Tarrand, J. J., and Kontoyiannis, D. P. (2014). Drug-resistant Candida glabrata infection in cancer patients. Emerg. Infect. Dis. 20, 1833-1840. doi: 10.3201/eid2011.140685
18. Fekkar, A., Dannaoui, E., Meyer, I., Imbert, S., Brossas, J. Y., Uzunov, M., et al. (2014). Emergence of echinocandin-resistant Candida spp. in a hospital setting: a consequence of 10 years of increasing use of antifungal therapy? Eur. J. Clin. Microbiol. Infect. Dis. 33, 1489-1496. doi: 10.1007/s10096-014-2096-9
19. Grenouillet, F., Millon, L., Bart, J.-M., Roussel, S., Biot, I., Didier, E., et al. (2007). Multiple-locus variable-number tandem-repeat analysis for rapid typing of Candida glabrata. J. Clin. Microbiol. 45, 3781-3784. doi: 10.1128/JCM.01603-07
20. Healey, K. R., Zhao, Y., Perez, W. B., Lockhart, S. R., Sobel, J. D., Farmakiotis, D., et al. (2016). Prevalent mutator genotype identified in fungal pathogen Candida glabrata promotes multi-drug resistance. Nat. Commun. 7:11128. doi: 10.1038/ncomms11128
21. Jensen, R. H., Johansen, H. K., Søes, L. M., Lemming, L. E., Rosenvinge, F. S., Nielsen, L., et al. (2015). Posttreatment antifungal resistance among colonizing Candida isolates in candidemia patients: results from a systematic multicenter study. Antimicrob. Agents Chemother. 60, 1500-1508. doi: 10.1128/AAC.01763-15
22. Klotz, U., Schmidt, D., Willinger, B., Steinmann, E., Buer, J., Rath, P.-M., et al. (2016). Echinocandin resistance and population structure of invasive Candida glabrata isolates from two university hospitals in Germany and Austria. Mycoses 59, 312-318. doi: 10.1111/myc.12472
23. Lass-Flörl, C. (2009). The changing face of epidemiology of invasive fungal disease in Europe. Mycoses 52, 197-205. doi: 10.1111/j.1439-0507.2009.01691.x
24. Legrand, M., Chan, C. L., Jauert, P. A., and Kirkpatrick, D. T. (2007). Role of DNA mismatch repair and double-strand break repair in genome stability and antifungal drug resistance in Candida albicans. Eukaryotic Cell 6, 2194-2205. doi: 10.1128/EC.00299-07
25. Lewis, J. S., Wiederhold, N. P., Wickes, B. L., Patterson, T. F., and Jorgensen, J. H. (2013). Rapid emergence of echinocandin resistance in Candida glabrata resulting in clinical and microbiologic failure. Antimicrob. Agents Chemother. 57, 4559-4561. doi: 10.1128/AAC.01144-13
26. Lortholary, O., Renaudat, C., Sitbon, K., Madec, Y., Denoeud-Ndam, L., Wolff, M., et al. (2014). Worrisome trends in incidence and mortality of candidemia in intensive care units (Paris area, 2002-2010). Intensive Care Med. 40, 1303-1312. doi: 10.1007/s00134-014-3408-3
27. Lott, T. J., Frade, J. P., and Lockhart, S. R. (2010). Multilocus sequence type analysis reveals both clonality and recombination in populations of Candida glabrata bloodstream isolates from U.S. Surveillance Studies. Eukaryot. Cell 9, 619-625. doi: 10.1128/EC.00002-10
28. Perlin, D. S. (2015). Echinocandin resistance in Candida. Clin. Infect. Dis. 61(Suppl. 6), S612-S617. doi: 10.1093/cid/civ791
29. Pfaller, M. A., and Diekema, D. J. (2007). Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20, 133-163. doi: 10.1128/CMR.00029-06
30. Pfaller, M. A., Diekema, D. J., Gibbs, D. L., Newell, V. A., Meis, J. F., Gould, I. M., et al. (2007). Results from the ARTEMIS DISK global antifungal surveillance study, 1997 to 2005: an 8.5-year analysis of susceptibilities of Candida species and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J. Clin. Microbiol. 45, 1735-1745. doi: 10.1128/JCM.00409-07
31. Pfaller, M. A., Diekema, D. J., Jones, R. N., and Castanheira, M. (2014a). Use of anidulafungin as a surrogate marker to predict susceptibility and resistance to caspofungin among 4, 290 clinical isolates of Candida by using CLSI methods and interpretive criteria. J. Clin. Microbiol. 52, 3223-3229. doi: 10.1128/JCM.00782-14
32. Pfaller, M. A., Espinel-Ingroff, A., Bustamante, B., Canton, E., Diekema, D. J., Fothergill, A., et al. (2014b). Multicenter study of anidulafungin and micafungin MIC distributions and epidemiological cutoffvalues for eight Candida species and the CLSI M27-A3 broth microdilution method. Antimicrob. Agents Chemother. 58, 916-922. doi: 10.1128/AAC.02020-13
33. Pham, C. D., Iqbal, N., Bolden, C. B., Kuykendall, R. J., Harrison, L. H., Farley, M. M., et al. (2014). Role of FKS mutations in Candida glabrata: MIC values, echinocandin resistance, and multidrug resistance. Antimicrob. Agents Chemother. 58, 4690-4696. doi: 10.1128/AAC.03255-14
34. Shields, R. K., Nguyen, M. H., Press, E. G., Cumbie, R., Driscoll, E., Pasculle, A. W., et al. (2015). Rate of FKS Mutations among consecutive Candida isolates causing bloodstream infection. Antimicrob. Agents Chemother. 59, 7465-7470. doi: 10.1128/AAC.01973-15
35. Thompson, G. R., Wiederhold, N. P., Vallor, A. C., Villareal, N. C., Lewis, J. S., and Patterson, T. F. (2008). Development of caspofungin resistance following prolonged therapy for invasive candidiasis secondary to Candida glabrata infection. Antimicrob. Agents Chemother. 52, 3783-3785. doi: 10.1128/AAC.00473-08
36. Tortorano, A. M., Prigitano, A., Lazzarini, C., Passera, M., Deiana, M. L., Cavinato, S., et al. (2013). A 1-year prospective survey of candidemia in Italy and changing epidemiology over one decade. Infection 41, 655-662. doi: 10.1007/s15010-013-0455-6
37. Vale-Silva, L. A., and Sanglard, D. (2015). Tipping the balance both ways: drug resistance and virulence in Candida glabrata. FEMS Yeast Res. 15:fov025. doi: 10.1093/femsyr/fov025
38. Vallabhaneni, S., Cleveland, A. A., Farley, M. M., Harrison, L. H., Schaffner, W., Beldavs, Z. G., et al. (2015). Epidemiology and risk factors for echinocandin nonsusceptible Candida glabrata bloodstream infections: data from a large multisite population-based candidemia surveillance program, 2008-2014. Open Forum Infect. Dis. 2:ofv163. doi: 10.1093/ofid/ofv163
39. Wisplinghoff, H., Ebbers, J., Geurtz, L., Stefanik, D., Major, Y., Edmond, M. B., et al. (2014). Nosocomial bloodstream infections due to Candida spp. in the USA: species distribution, clinical features and antifungal susceptibilities Int. J. Antimicrob. Agents 43, 78-81. doi: 10.1016/j.ijantimicag.2013.09.005
40. Zimbeck, A. J., Iqbal, N., Ahlquist, A. M., Farley, M. M., Harrison, L. H., Chiller, T., et al. (2010). FKS mutations and elevated echinocandin MIC values among Candida glabrata isolates from U.S. population-based surveillance. Antimicrob. Agents Chemother. 54, 5042-5047. doi: 10.1128/AAC.00836-10