Resistance of Candida spp. to antifungal drugs in the ICU: Where are we now?

Intensive Care Medicine

Volumn 40, Issue 9, 2014, Pages 1241-1255

  Maubon, Danièle ^a,b   Garnaud, Cécile ^a,b   Calandra, Thierry ^c   Sanglard, Dominique ^c   Cornet, Muriel ^a,b  

^a GRENOBLE UNIVERSITY HOSPITAL   (France)

^b UNIV GRENOBLE ALPES   (France)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Antifungal resistance; Candida resistance; Clinical resistance; Intensive care unit; Microbial resistance; Resistance mechanisms

Indexed keywords

ANTIFUNGAL AGENT; ECHINOCANDIN; FLUCYTOSINE; POLYENE; TRIAZOLE DERIVATIVE;

ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; BIOFILM; CANDIDA; DRUG MECHANISM; FUNGUS ISOLATION; FUNGUS MUTATION; HUMAN; INTENSIVE CARE UNIT; NONHUMAN; REVIEW; TREATMENT FAILURE; CANDIDIASIS; DRUG EFFECTS; MICROBIAL SENSITIVITY TEST;

ANTIFUNGAL AGENTS; CANDIDA; CANDIDIASIS; HUMANS; INTENSIVE CARE UNITS; MICROBIAL SENSITIVITY TESTS;

EID: 84906935477     PISSN: 03424642     EISSN: 14321238     Source Type: Journal    
DOI: 10.1007/s00134-014-3404-7     Document Type: Review

References (120)

1. León C, Ostrosky-Zeichner L, Schuster M (2014) What's new in the clinical and diagnostic management of invasive candidiasis in critically ill patients. Intensive Care Med. doi:10.1007/s00134-014-3281-0
2. Guery BP, Arendrup MC, Auzinger G et al (2009) Management of invasive candidiasis and candidemia in adult non-neutropenic intensive care unit patients: part II. Treatment Intensive Care Med 35:206-214. doi:10.1007/s00134- 008-1339-6
3. Fournier P, Schwebel C, Maubon D et al (2011) Antifungal use influences Candida species distribution and susceptibility in the intensive care unit. J Antimicrob Chemother 66:2880-2886
4. Lortholary O, Desnos-Ollivier M, Sitbon K et al (2011) Recent exposure to caspofungin or fluconazole influences the epidemiology of candidemia: a prospective multicenter study involving 2,441 patients. Antimicrob Agents Chemother 55:532-538. doi:10.1128/AAC.01128-10
5. Alexander BD, Johnson MD, Pfeiffer CD 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
6. Shields RK, Nguyen MH, Press EG et al (2013) Caspofungin MICs correlate with treatment outcomes among patients with Candida glabrata invasive candidiasis and prior echinocandin exposure. Antimicrob Agents Chemother 57:3528-3535. doi:10.1128/AAC.00136-13
7. Perlin DS (2011) Current perspectives on echinocandin class drugs. Future Microbiol 6:441-457. doi:10.2217/fmb.11.19
8. Odds FC, Brown AJP, Gow NAR (2003) Antifungal agents: mechanisms of action. Trends Microbiol 11:272-279 (Pubitemid 36725017)
9. Sorgo AG, Heilmann CJ, Dekker HL et al (2011) Effects of fluconazole on the secretome, the wall proteome, and wall integrity of the clinical fungus Candida albicans. Eukaryot Cell 10:1071-1081. doi:10.1128/EC.05011-11
10. Pfaller M, Riley J (1992) Effects of fluconazole on the sterol and carbohydrate composition of four species of Candida. Eur J Clin Microbiol Infect Dis 11:152-156
11. Gray KC, Palacios DS, Dailey I et al (2012) Amphotericin primarily kills yeast by simply binding ergosterol. Proc Natl Acad Sci U S A 109:2234-2239. doi:10.1073/pnas.1117280109
12. Anderson TM, Clay MC, Cioffi AG et al (2014) Amphotericin forms an extramembranous and fungicidal sterol sponge. Nat Chem Biol 10:400-406. doi:10.1038/nchembio.1496
13. Kotler-Brajtburg J, Price HD, Medoff G et al (1974) Molecular basis for the selective toxicity of amphotericin B for yeast and filipin for animal cells. Antimicrob Agents Chemother 5:377-382
14. Hamill RJ (2013) Amphotericin B formulations: a comparative review of efficacy and toxicity. Drugs 73:919-934. doi:10.1007/s40265-013-0069-4
15. Walker LA, Gow NAR, Munro CA (2010) Fungal echinocandin resistance. Fungal Genet Biol 47:117-126. doi:10.1016/j.fgb.2009.09.003
16. Sanglard D, Ischer F, Marchetti O et al (2003) Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 48:959-976 (Pubitemid 36628262)
17. LaFayette SL, Collins C, Zaas AK et al (2010) PKC signaling regulates drug resistance of the fungal pathogen Candida albicans via circuitry comprised of Mkc1, calcineurin, and Hsp90. PLoS Pathog 6:e1001069. doi:10.1371/journal. ppat.1001069
18. Lee KK, Maccallum DM, Jacobsen MD et al (2012) Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob Agents Chemother 56:208-217. doi:10.1128/AAC.00683-11
19. Rueda C, Cuenca-Estrella M, Zaragoza O (2014) Paradoxical growth of Candida albicans in the presence of caspofungin is associated with multiple cell wall rearrangements and decreased virulence. Antimicrob Agents Chemother 58:1071-1083. doi:10.1128/AAC.00946-13
20. Arendrup MC, Cuenca-Estrella M, Lass-Flörl C, Hope WW (2014) Breakpoints for antifungal agents: an update from EUCAST focussing on echinocandins against Candida spp and triazoles against Aspergillus spp. Drug Resist Updat 16(6):81-95. doi:10.1016/j.drup.2014.01.001
21. Coste A, Selmecki A, Forche A et al (2007) Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot Cell 6:1889-1904 (Pubitemid 47585577)
22. Sanglard D, Coste A, Ferrari S (2009) Antifungal drug resistance mechanisms in fungal pathogens from the perspective of transcriptional gene regulation. FEMS Yeast Res 9:1029-1050. doi:10.1111/j.1567-1364.2009.00578.x
23. Coste A, Turner V, Ischer F et al (2006) 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 172:2139-2156. doi:10.1534/genetics.105.054767
24. Morio F, Loge C, Besse B et al (2010) Screening for amino acid substitutions in the Candida albicans Erg11 protein of azole-susceptible and azole-resistant clinical isolates: new substitutions and a review of the literature. Diagn Microbiol Infect Dis 66:373-384. doi:10.1016/j.diagmicrobio. 2009.11.006
25. Morio F, Pagniez F, Lacroix C et al (2012) Amino acid substitutions in the Candida albicans sterol Δ5,6-desaturase (Erg3p) confer azole resistance: characterization of two novel mutants with impaired virulence. J Antimicrob Chemother 67:2131-2138. doi:10.1093/jac/dks186
26. Poláková S, Blume C, Zárate JA et al (2009) Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc Natl Acad Sci U S A 106:2688-2693. doi:10.1073/pnas.0809793106
27. Ferrari S, Sanguinetti M, De Bernardis F et al (2011) Loss of mitochondrial functions associated with azole resistance in Candida glabrata results in enhanced virulence in mice. Antimicrob Agents Chemother 55:1852-1860. doi:10.1128/AAC.01271-10
28. Vincent BM, Lancaster AK, Scherz-Shouval R et al (2013) Fitness tradeoffs restrict the evolution of resistance to amphotericin B. PLoS Biol 11:e1001692. doi:10.1371/journal.pbio.1001692
29. Spampinato C, Leonardi D (2013) Candida infections, causes, targets, and resistance mechanisms: traditional and alternative antifungal agents. Bio Med Res Int 2013:204237. doi: 10.1155/2013/204237
30. Florent M, Noël T, Ruprich-Robert G et al (2009) Nonsense and missense mutations in FCY2 and FCY1 genes are responsible for flucytosine resistance and flucytosine-fluconazole cross-resistance in clinical isolates of Candida lusitaniae. Antimicrob Agents Chemother 53:2982-2990. doi:10.1128/AAC.00880-08
31. Delattin N, Cammue BPA, Thevissen K (2014) Reactive oxygen species-inducing antifungal agents and their activity against fungal biofilms. Future Med Chem 6:77-90. doi:10.4155/fmc.13.189
32. Kuhn DM, George T, Chandra J et al (2002) Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob Agents Chemother 46:1773-1780 (Pubitemid 34535196)
33. Choi HW, Shin JH, Jung SI et al (2007) Species-specific differences in the susceptibilities of biofilms formed by Candida bloodstream isolates to echinocandin antifungals. Antimicrob Agents Chemother 51:1520-1523. doi:10.1128/AAC.01141-06 (Pubitemid 46586842)
34. Lamfon H, Porter SR, McCullough M, Pratten J (2004) Susceptibility of Candida albicans biofilms grown in a constant depth film fermentor to chlorhexidine, fluconazole and miconazole: a longitudinal study. J Antimicrob Chemother 53:383-385. doi:10.1093/jac/dkh071 (Pubitemid 38239979)
35. Taff HT, Mitchell KF, Edward JA, Andes DR (2013) Mechanisms of Candida biofilm drug resistance. Future Microbiol 8:1325-1337. doi:10.2217/fmb.13.101
36. Tobudic S, Kratzer C, Lassnigg A, Presterl E (2012) Antifungal susceptibility of Candida albicans in biofilms. Mycoses 55:199-204. doi:10.1111/j.1439-0507.2011.02076.x
37. Mathé L, Van Dijck P (2013) Recent insights into Candida albicans biofilm resistance mechanisms. Curr Genet. doi:10.1007/s00294-013-0400-3
38. Mitchell KF, Taff HT, Cuevas MA et al (2013) Role of matrix β-1,3 glucan in antifungal resistance of non-albicans Candida biofilms. Antimicrob Agents Chemother 57:1918-1920. doi:10.1128/AAC.02378-12
39. Robbins N, Uppuluri P, Nett J et al (2011) Hsp90 governs dispersion and drug resistance of fungal biofilms. PLoS Pathog 7:e1002257. doi:10.1371/journal. ppat.1002257
40. Martins M, Henriques M, Lopez-Ribot JL, Oliveira R (2012) Addition of DNase improves the in vitro activity of antifungal drugs against Candida albicans biofilms. Mycoses 55:80-85. doi:10.1111/j.1439-0507.2011.02047.x
41. EUCAST (2008) EUCAST definitive document EDef 7.1: method for the determination of broth dilution MICs of antifungal agents for fermentative yeasts. Clin Microbiol Infect 14:398-405
42. CLSI Clinical and Laboratory Standards Institute (2008) Reference method for broth dilution antifungal susceptibility testing of yeasts. Third informational supplement. CLSI document M27-S3. Clinical and Laboratory Standards Institute, Wayne
43. Chryssanthou E, Cuenca-Estrella M (2002) Comparison of the antifungal susceptibility testing subcommittee of the European Committee on Antibiotic Susceptibility Testing proposed standard and the E-test with the NCCLS broth microdilution method for voriconazole and caspofungin susceptibility testing of yeast species. J Clin Microbiol 40:3841-3844
44. Cuenca-Estrella M, Gomez-Lopez A, Alastruey-Izquierdo A et al (2010) Comparison of the Vitek 2 antifungal susceptibility system with the clinical and laboratory standards institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST) broth microdilution reference methods and with the sensititre yeastone and Etest techniques for in vitro detection of antifungal resistance in yeast isolates. J Clin Microbiol 48:1782-1786. doi:10.1128/JCM.02316-09
45. Lombardi G, Farina C, Andreoni S et al (2004) Comparative evaluation of Sensititre YeastOne vs. the NCCLS M27A protocol and E-test for antifungal susceptibility testing of yeasts. Mycoses 47:397-401. doi:10.1111/j.1439-0507. 2004.01013.x (Pubitemid 39469828)
46. Pfaller MA, Diekema DJ, Andes D et al (2011) Clinical breakpoints for the echinocandins and Candida revisited: integration of molecular, clinical, and microbiological data to arrive at species-specific interpretive criteria. Drug Resist Updat 14:164-176. doi:10.1016/j.drup.2011.01.004
47. Arendrup MC, Garcia-Effron G, Buzina W et al (2009) Breakthrough Aspergillus fumigatus and Candida albicans double infection during caspofungin treatment: laboratory characteristics and implication for susceptibility testing. Antimicrob Agents Chemother 53:1185-1193. doi:10.1128/AAC.01292-08
48. Pfaller MA, Andes D, Diekema DJ et al (2010) Wild-type MIC distributions, epidemiological cutoff values and species-specific clinical breakpoints for fluconazole and Candida: time for harmonization of CLSI and EUCAST broth microdilution methods. Drug Resist Updat 13:180-195. doi:10.1016/j.drup.2010.09. 002
49. Espinel-Ingroff A, Arendrup MC, Pfaller MA 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
50. Pfaller MA, Messer SA, Diekema DJ et al (2014) Use of micafungin as a surrogate marker to predict susceptibility and resistance to caspofungin among 3,764 clinical isolates of Candida by use of CLSI methods and interpretive criteria. J Clin Microbiol 52:108-114. doi:10.1128/JCM.02481-13
51. Eschenauer GA, Nguyen MH, Shoham S et al (2014) Real-world experience with echinocandin MICs against Candida species in a multicenter study of hospitals that routinely perform susceptibility testing of bloodstream isolates. Antimicrob Agents Chemother 58:1897-1906. doi:10.1128/AAC.02163-13
52. Shields RK, Nguyen MH, Press EG et al (2013) Anidulafungin and micafungin minimum inhibitory concentration breakpoints are superior to caspofungin for identifying FKS mutant Candida glabrata and echinocandin resistance. Antimicrob Agents Chemother. doi:10.1128/AAC.01451-13
53. Park BJ, Arthington-Skaggs BA, Hajjeh RA et al (2006) Evaluation of amphotericin B interpretive breakpoints for Candida bloodstream isolates by correlation with therapeutic outcome. Antimicrob Agents Chemother 50:1287-1292. doi:10.1128/AAC.50.4.1287-1292.2006
54. Krogh-Madsen M, Arendrup MC, Heslet L, Knudsen JD (2006) Amphotericin B and caspofungin resistance in Candida glabrata isolates recovered from a critically ill patient. Clin Infect Dis 42:938-944. doi: 10.1086/500939
55. Guinea J, Recio S, Escribano P et al (2010) Rapid antifungal susceptibility determination for yeast isolates by use of Etest performed directly on blood samples from patients with fungemia. J Clin Microbiol 48:2205-2212. doi:10.1128/JCM.02321-09
56. Wiederhold NP, Grabinski JL, Garcia-Effron G et al (2008) Pyrosequencing to detect mutations in FKS1 that confer reduced echinocandin susceptibility in Candida albicans. Antimicrob Agents Chemother 52:4145-4148. doi:10.1128/AAC. 00959-08
57. Park S, Perlin DS (2005) Establishing surrogate markers for fluconazole resistance in Candida albicans. Microb Drug Resist 11:232-238. doi:10.1089/mdr.2005.11.232 (Pubitemid 41434167)
58. Loeffler J, Hagmeyer L, Hebart H et al (2000) Rapid detection of point mutations by fluorescence resonance energy transfer and probe melting curves in Candida species. Clin Chem 46:631-635 (Pubitemid 30318417)
59. Wang H, Kong F, Sorrell TC et al (2009) Rapid detection of ERG11 gene mutations in clinical Candida albicans isolates with reduced susceptibility to fluconazole by rolling circle amplification and DNA sequencing. BMC Microbiol 9:167. doi:10.1186/1471-2180-9-167
60. Pham CD, Bolden CB, Kuykendall RJ, Lockhart SR (2013) Development of a Luminex-based multiplex assay for detection of mutations conferring resistance to echinocandins in Candida glabrata. J Clin Microbiol. doi:10.1128/JCM.03378-13
61. Zhao Y, Stensvold CR, Perlin DS, Arendrup MC (2013) Azole resistance in Aspergillus fumigatus from bronchoalveolar lavage fluid samples of patients with chronic diseases. J Antimicrob Chemother 68:1497-1504. doi:10.1093/jac/dkt071
62. Bassetti M, Merelli M, Righi E 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
63. Pfaller MA, Messer SA, Moet GJ et al (2011) Candida bloodstream infections: comparison of species distribution and resistance to echinocandin and azole antifungal agents in intensive care unit (ICU) and non-ICU settings in the SENTRY antimicrobial surveillance program (2008-2009). Int J Antimicrob Agents 38:65-69. doi:10.1016/j.ijantimicag.2011.02.016
64. Puig-Asensio M, Pemán J, Zaragoza R et al (2014) Impact of therapeutic strategies on the prognosis of candidemia in the ICU. Crit Care Med 42:1423-1432. doi:10.1097/CCM.0000000000000221
65. Montagna MT, Caggiano G, Lovero G et al (2013) Epidemiology of invasive fungal infections in the intensive care unit: results of a multicenter Italian survey (AURORA Project). Infection 41:645-653. doi:10.1007/s15010-013-0432-0
66. Diekema D, Arbefeville S, Boyken L et al (2012) The changing epidemiology of healthcare-associated candidemia over three decades. Diagn Microbiol Infect Dis 73:45-48. doi:10.1016/j.diagmicrobio.2012.02.001
67. Chow JK, Golan Y, Ruthazer R et al (2008) Factors associated with candidemia caused by non-albicans Candida species versus Candida albicans in the intensive care unit. Clin Infect Dis 46:1206-1213. doi:10.1086/529435 (Pubitemid 351589904)
68. Kanafani ZA, Perfect JR (2008) Resistance to antifungal agents: mechanisms and clinical impact. Clin Infect Dis 46:120-128. doi:10.1086/524071 (Pubitemid 351263573)
69. Guinea J (2014) Global trends in the distribution of Candida species causing candidemia. Clin Microbiol Infect. doi:10.1111/1469-0691.12539
70. Pfaller MA, Diekema DJ (2010) Epidemiology of invasive mycoses in North America. Crit Rev Microbiol 36:1-53
71. Guitard J, Angoulvant A, Letscher-Bru V et al (2013) Invasive infections due to Candida norvegensis and Candida inconspicua: report of 12 cases and review of the literature. Med Mycol. doi:10.3109/13693786.2013.807444
72. Pfaller MA, Diekema DJ, Colombo AL et al (2006) Candida rugosa, an emerging fungal pathogen with resistance to azoles: geographic and temporal trends from the ARTEMIS DISK antifungal surveillance program. J Clin Microbiol 44:3578-3582. doi:10.1128/JCM.00863-06 (Pubitemid 46768813)
73. Garcia-Effron G, Katiyar SK, Park S et al (2008) A naturally occurring proline-to-alanine amino acid change in FKS1p in Candida parapsilosis, Candida orthopsilosis, and Candida metapsilosis accounts for reduced echinocandin susceptibility. Antimicrob Agents Chemother 52:2305-2312. doi:10.1128/AAC.00262- 08 (Pubitemid 351915657)
74. Cantón E, Pemán J, Sastre M et al (2006) Killing kinetics of caspofungin, micafungin, and amphotericin B against Candida guilliermondii. Antimicrob Agents Chemother 50:2829-2832. doi:10.1128/AAC.00524-06
75. Kabbara N, Lacroix C, Peffault de Latour R et al (2008) Breakthrough C. parapsilosis and C. guilliermondii blood stream infections in allogeneic hematopoietic stem cell transplant recipients receiving long-term caspofungin therapy. Haematologica 93:639-640. doi:10.3324/haematol.11149 (Pubitemid 351536400)
76. Pfeiffer CD, Garcia-Effron G, Zaas AK et al (2010) Breakthrough invasive candidiasis in patients on micafungin. J Clin Microbiol 48:2373-2380
77. Anderson JB (2005) Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat Rev Microbiol 3:547-556. doi:10.1038/nrmicro1179
78. Marco F, Lockhart SR, Pfaller MA et al (1999) Elucidating the origins of nosocomial infections with Candida albicans by DNA fingerprinting with the complex probe Ca3. J Clin Microbiol 37:2817-2828 (Pubitemid 29391894)
79. Stéphan F, Bah MS, Desterke C et al (2002) Molecular diversity and routes of colonization of Candida albicans in a surgical intensive care unit, as studied using microsatellite markers. Clin Infect Dis 35:1477-1483. doi:10.1086/344648
80. Pfaller MA, Castanheira M, Lockhart SR et al (2012) Frequency of decreased susceptibility and resistance to echinocandins among fluconazole-resistant bloodstream isolates of Candida glabrata. J Clin Microbiol 50:1199-1203. doi:10.1128/JCM.06112-11
81. Cleveland AA, Farley MM, Harrison LH 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
82. Garcia-Effron G, Chua DJ, Tomada JR et al (2010) Novel FKS mutations associated with echinocandin resistance in Candida species. Antimicrob Agents Chemother 54:2225-2227. doi:10.1128/AAC.00998-09
83. Garcia-Effron G, Kontoyiannis DP, Lewis RE, Perlin DS (2008) Caspofungin-resistant Candida tropicalis strains causing breakthrough Fungemia in patients at high risk for hematologic malignancies. Antimicrob Agents Chemother 52:4181-4183. doi:10.1128/AAC.00802-08
84. Hakki M, Staab JF, Marr KA (2006) Emergence of a Candida krusei Isolate with reduced susceptibility to Caspofungin during therapy. Antimicrob Agents Chemother 50:2522-2524. doi:10.1128/AAC.00148-06 (Pubitemid 43993195)
85. Fekkar A, Meyer I, Brossas JY et al (2013) Rapid emergence of echinocandin resistance during Candida kefyr fungemia treatment with caspofungin. Antimicrob Agents Chemother 57:2380-2382. doi:10.1128/AAC.02037-12
86. Pfaller MA (2012) Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med 125:S3-S13. doi:10.1016/j.amjmed.2011. 11.001
87. Bizerra FC, Jimenez-Ortigosa C, Souza ACR et al (2014) Breakthrough candidemia due to multidrug resistant C. glabrata during prophylaxis with low dose of micafungin. Antimicrob Agents Chemother 58:2438-2440. doi:10.1128/AAC.02189-13
88. Chan TSY, Gill H, Hwang Y-Y et al (2014) Breakthrough invasive fungal diseases during echinocandin treatment in high-risk hospitalized hematologic patients. Ann Hematol 93:493-498. doi:10.1007/s00277-013-1882-2
89. Sun H-Y, Singh N (2010) Characterisation of breakthrough invasive mycoses in echinocandin recipients: an evidence-based review. Int J Antimicrob Agents 35:211-218. doi:10.1016/j.ijantimicag.2009.09.020
90. Myoken Y, Kyo T, Sugata T et al (2006) Breakthrough fungemia caused by fluconazole-resistant Candida albicans with decreased susceptibility to voriconazole in patients with hematologic malignancies. Haematologica 91:287-288
91. Beyda ND, John J, Kilic A et al (2014) FKS mutant Candida glabrata; risk factors and outcomes in patients with candidemia. Clin Infect Dis. doi:10.1093/cid/ciu407
92. Lackner M, Tscherner M, Schaller M et al (2014) Positions and numbers of FKS mutations in Candida albicans selectively influence in vitro and in vivo susceptibilities to echinocandin treatment. Antimicrob Agents Chemother 58:3626-3635. doi:10.1128/AAC.00123-14
93. Liu W, Tan J, Sun J et al (2014) Invasive candidiasis in intensive care units in China: in vitro antifungal susceptibility in the China-SCAN study. J Antimicrob Chemother 69:162-167. doi:10.1093/jac/dkt330
94. Chapeland-Leclerc F, Hennequin C, Papon N et al (2010) Acquisition of flucytosine, azole, and caspofungin resistance in Candida glabrata bloodstream isolates serially obtained from a hematopoietic stem cell transplant recipient. Antimicrob Agents Chemother 54:1360-1362. doi:10.1128/AAC.01138-09
95. Pfaller MA, Diekema DJ (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20:133-163. doi:10.1128/CMR.00029-06 (Pubitemid 46167771)
96. Yang Y-L, Li S-Y, Cheng H-H et al (2005) The trend of susceptibilities to amphotericin B and fluconazole of Candida species from 1999 to 2002 in Taiwan. BMC Infect Dis 5:99. doi:10.1186/1471-2334-5-99
97. Kontoyiannis DP, Lewis RE (2002) Antifungal drug resistance of pathogenic fungi. Lancet 359:1135-1144. doi:10.1016/S0140-6736(02)08162-X (Pubitemid 34270742)
98. Silva S, Negri M, Henriques M et al (2012) Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev 36:288-305. doi:10.1111/j.1574-6976. 2011.00278.x
99. Segal BH, Herbrecht R, Stevens DA et al (2008) Defining responses to therapy and study outcomes in clinical trials of invasive fungal diseases: Mycoses Study Group and European Organization for Research and Treatment of Cancer consensus criteria. Clin Infect Dis 47:674-683. doi:10.1086/590566
100. Walsh TJ, Finberg RW, Arndt C et al (1999) Liposomal amphotericin B for empirical therapy in patients with persistent fever and neutropenia. N Engl J Med 340:764-771. doi:10.1056/NEJM199903113401004 (Pubitemid 29114295)
101. Moen MD, Lyseng-Williamson KA, Scott LJ (2009) Liposomal amphotericin B. Drugs 69:361-392. doi:10.2165/00003495-200969030-00010
102. Andes DR, Safdar N, Baddley JW et al (2012) Impact of treatment strategy on outcomes in patients with candidemia and other forms of invasive candidiasis: a patient-level quantitative review of randomized trials. Clin Infect Dis 54:1110-1122. doi:10.1093/cid/cis021
103. Puig-Asensio M, Pemán J, Zaragoza R et al (2014) Impact of therapeutic strategies on the prognosis of candidemia in the ICU. Crit Care Med. doi:10.1097/CCM.0000000000000221
104. Cornely OA, Bassetti M, Calandra T et al (2012) ESCMID guideline for the diagnosis and management of Candida diseases 2012: non-neutropenic adult patients. Clin Microbiol Infect 18(Suppl 7):19-37. doi:10.1111/1469-0691.12039
105. Pfaller MA, Messer SA, Boyken L et al (2002) In vitro activities of 5-fluorocytosine against 8,803 clinical isolates of Candida spp.: global assessment of primary resistance using national committee for clinical laboratory standards susceptibility testing methods. Antimicrob Agents Chemother 46:3518-3521 (Pubitemid 35192920)
106. Felton T, Troke PF, Hope WW (2014) Tissue penetration of antifungal agents. Clin Microbiol Rev 27:68-88. doi:10.1128/CMR.00046-13
107. Glöckner A, Cornely OA (2013) Practical considerations on current guidelines for the management of non-neutropenic adult patients with candidaemia: practical considerations on current guidelines. Mycoses 56:11-20. doi:10.1111/j.1439-0507.2012.02208.x
108. Shields RK, Nguyen MH, Press EG et al (2012) The presence of an FKS mutation rather than MIC is an independent risk factor for failure of echinocandin therapy among patients with invasive candidiasis due to Candida glabrata. Antimicrob Agents Chemother 56:4862-4869. doi:10.1128/AAC.00027-12
109. Baixench M-T, Aoun N, Desnos-Ollivier M et al (2007) Acquired resistance to echinocandins in Candida albicans: case report and review. J Antimicrob Chemother 59:1076-1083. doi:10.1093/jac/dkm095 (Pubitemid 47073317)
110. Bourgeois N, Laurens C, Bertout S et al (2014) Assessment of caspofungin susceptibility of Candida glabrata by the Etest®, CLSI, and EUCAST methods, and detection of FKS1 and FKS 2 mutations. Eur J Clin Microbiol Infect Dis. doi:10.1007/s10096-014-2069-z
111. Cohen Y, Karoubi P, Adrie C et al (2010) Early prediction of Candida glabrata fungemia in nonneutropenic critically ill patients. Crit Care Med 38:826-830. doi:10.1097/CCM.0b013e3181cc4734
112. Ruhnke M, Rickerts V, Cornely OA et al (2011) Diagnosis and therapy of Candida infections: joint recommendations of the German Speaking Mycological Society and the Paul-Ehrlich-Society for Chemotherapy. Mycoses 54:279-310. doi:10.1111/j.1439-0507.2011.02040.x
113. Colombo AL, Guimarães T, Camargo LFA et al (2013) Brazilian guidelines for the management of candidiasis - a joint meeting report of three medical societies: Sociedade Brasileira de Infectologia, Sociedade Paulista de Infectologia and Sociedade Brasileira de Medicina Tropical. Braz J Infect Dis 17:283-312. doi:10.1016/j.bjid.2013.02.001
114. Bow EJ, Evans G, Fuller J et al (2010) Canadian clinical practice guidelines for invasive candidiasis in adults. Can J Infect Dis Med Microbiol 21:e122-e150
115. Castagna L, Bramanti S, Sarina B et al (2012) ECIL 3-2009 update guidelines for antifungal management. Bone Marrow Transpl 47:866
116. Pappas PG, Kauffman CA, Andes D et al (2009) Candida-clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 48:503-535. doi:10.1086/596757
117. Leroux S, Ullmann AJ (2013) Management and diagnostic guidelines for fungal diseases in infectious diseases and clinical microbiology: critical appraisal. Clin Microbiol Infect 19:1115-1121. doi:10.1111/1469-0691.12426
118. Deshpande A, Gaur S, Bal AM (2013) Candidaemia in the non-neutropenic patient: a critique of the guidelines. Int J Antimicrob Agents 42:294-300. doi:10.1016/j.ijantimicag.2013.06.005
119. Bassetti M, Righi E, Ansaldi F et al (2014) A multicenter study of septic shock due to candidemia: outcomes and predictors of mortality. Intensive Care Med 40:839-845. doi:10.1007/s00134-014-3310-z
120. Mermel LA, Allon M, Bouza E et al (2009) Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 49:1-45. doi:10.1086/599376