Echinocandin resistance in Candida species: Mechanisms of reduced susceptibility and therapeutic approaches;Resistencia a equinocandinas en especies de candida: Mecanismos de susceptibilidad reducida y alternativas terapéuticas

Annals of Pharmacotherapy

Volumn 46, Issue 7-8, 2012, Pages 1086-1096

  Beyda, Nicholas D ^a   Lewis, Russell E ^a   Garey, Kevin W ^a  

^a UNIVERSITY OF HOUSTON   (United States)

Author keywords

Anidulafungin; Candidemia; Caspofungin; FKS mutations; Micafungin

Indexed keywords

AMINOCANDIN; AMPHOTERICIN B; AMPHOTERICIN B LIPID COMPLEX; ANIDULAFUNGIN; ANTIFUNGAL AGENT; CASPOFUNGIN; CHITIN; CHITIN SYNTHASE INHIBITOR; CYCLOSPORIN A; ECHINOCANDIN; EFUNGUMAB; FKS PROTEIN; FLUCONAZOLE; FUNGAL PROTEIN; GLUCAN SYNTHASE; HEAT SHOCK PROTEIN 90 INHIBITOR; MICAFUNGIN; NIKKOMYCIN; NIKKOMYCIN Z; TACROLIMUS; UNCLASSIFIED DRUG; VORICONAZOLE;

ABDOMINAL ABSCESS; ABDOMINAL INFECTION; ANTIFUNGAL ACTIVITY; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; CANDIDA; CANDIDA PARAPSILOSIS; CANDIDEMIA; CANDIDIASIS; CELL WALL; CELLULAR STRESS RESPONSE; DOSE RESPONSE; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG MEGADOSE; DRUG POTENTIATION; DRUG SURVEILLANCE PROGRAM; FEBRILE NEUTROPENIA; FUNGAL CELL; FUNGAL ENDOCARDITIS; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS ISOLATION; GENE MUTATION; HUMAN; LUNG MYCOSIS; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); PICHIA GUILLIERMONDII; PRIORITY JOURNAL; SURVIVAL RATE; SURVIVAL TIME; TREATMENT FAILURE; WILD TYPE;

ANTIFUNGAL AGENTS; CANDIDA; CANDIDIASIS; DRUG RESISTANCE, FUNGAL; ECHINOCANDINS; GLUCOSYLTRANSFERASES; HUMANS; MICROBIAL SENSITIVITY TESTS; MUTATION;

EID: 84864742371     PISSN: 10600280     EISSN: None     Source Type: Journal    
DOI: 10.1345/aph.1R020     Document Type: Article

References (72)

1. Hidron AI, Edwards JR, Patel J, et al. NHSN annual update: antimicrobial- resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect Control Hosp Epidemiol 2008;29:996-1011.
2. Zilberberg MD, Shorr AF, Kollef MH. Secular trends in candidemia-related hospitalizations in the United States, 2000-2005. Infect Control Hosp Epidemiol 2008;29:978-990.
3. Zaoutis TE, Argon J, Chu J, Berlin JA, Walsh TJ, Feudtner C. The epidemiology and attributable outcomes of candidemia in adults and children hospitalized in the United States: a propensity analysis. Clin Infect Dis 2005;41:1232-1239.
4. Arendrup MC. Epidemiology of invasive candidiasis. Curr Opin Crit Care 2010;16:445-452.
5. Pfaller MA, Moet GJ, Messer SA, Jones RN, Castanheira M. Candida bloodstream infections: comparison of species distributions and antifungal resistance patterns in community-onset and nosocomial isolates in the SENTRY antimicrobial surveillance program, 2008-2009. Antimicrob Agents Chemother 2010;55:561-566.
6. Pappas PG, Kauffman CA, Andes D, et al. Clinical practice guidelines for the management of candidiasis: 2009 update by the Infectious Diseases Society of America. Clin Infect Dis 2009;48:503-535.
7. Cleary JD, Garcia-Effron G, Chapman SW, Perlin DS. Reduced Candida glabrata susceptibility secondary to an FKS1 mutation developed during candidemia treatment. Antimicrob Agents Chemother 2008;52:2263-2265.
8. Daneman N, Chan AK, Poutanen SM, Rennie R, Sand C, Porter S. The emergence of caspofungin resistance during treatment of recurrent Candida glabrata candidaemia (abstract p1204). 16th European Congress of Clinical Microbiology and Infectious Diseases, Nice, France, April 1- 4, 2006.
9. Dodgson KJ, Dodgson AR, Pujol C, Messer SA, Soll DR, Pfaller MA. Caspofungin resistant C. glabrata (abstract 1134.02.357). 15th European Congress of Clinical Microbiology and Infectious Diseases, Copenhagen, Denmark, April 2-5, 2005.
10. Hakki M, Staab JF, Marr KA. Emergence of a Candida krusei isolate with reduced susceptibility to caspofungin during therapy. Antimicrob Agents Chemother 2006;50:2522-2524.
11. Krogh-Madsen M, Arendrup MC, Heslet L, Knudsen JD. Amphotericin B and caspofungin resistance in Candida glabrata isolates recovered from a critically ill patient. Clin Infect Dis 2006;42:938-944.
12. Moudgal V, Little T, Boikov D, Vazquez JA. Multi echinocandin- and multiazole-resistant Candida parapsilosis isolates serially obtained during therapy for prosthetic valve endocarditis. Antimicrob Agents Chemother 2005;49:767-769.
13. Park S, Kelly R, Kahn JN, et al. Specific substitutions in the echinocandin target Fks1p account for reduced susceptibility of rare laboratory and clinical Candida sp. isolates. Antimicrob Agents Chemother 2005;49: 3264-3273.
14. Garcia-Effron G, Kontoyiannis DP, Lewis RE, Perlin DS. Caspofunginresistant Candida tropicalis strains causing breakthrough fungemia in patients at high risk for hematologic malignancies. Antimicrob Agents Chemother 2008;52:4181-4183.
15. Kabbara N, Lacroix C, Peffault de Latour R, Socie G, Ghannoum M, Ribaud P. Breakthrough C Parapsilosis and C. guilliermondii blood stream infections in allogeneic hematopoietic stem cell transplant recipients receiving long-term caspofungin therapy. Haematologica 2008;93:639-640.
16. Kofteridis DP, Lewis RE, Kontoyiannis DP. Caspofungin-non-susceptible Candida isolates in cancer patients. J Antimicrob Chemother 2009; 65:293-295.
17. Arendrup MC, Garcia-Effron G, Buzina W, et al. Breakthrough Aspergillus fumigatus and Candida albicans double infection during caspofungin treatment: laboratory characteristics and implication for susceptibility testing. Antimicrob Agents Chemother 2009;53:1185-1193.
18. Chapeland-Leclerc F, Hennequin C, Papon N, et al. Acquisition of flucytosine, azole, and caspofungin resistance in Candida glabrata bloodstream isolates serially obtained from a hematopoietic stem cell transplant recipient. Antimicrob Agents Chemother 2010;54:1360-1362.
19. Niimi K, Monk BC, Hirai A, et al. Clinically significant micafungin resistance in Candida albicans involves modification of a glucan synthase catalytic subunit GSC1 (FKS1) allele followed by loss of heterozygosity. J Antimicrob Chemother 2010;65:842-852.
20. Costa-de-Oliveira S, Marcos Miranda I, Silva RM, et al. FKS2 mutations associated with decreased echinocandin susceptibility of Candida glabrata following anidulafungin therapy. Antimicrob Agents Chemother 2011;55:1312-1314.
21. Ishikawa T, Takata T, Akamatsu S, et al. Analysis of Candida glabrata strains with reduced sensitivity to micafungin in vitro isolated from a patient with persistent Candidemia. Jpn J Infect Dis 2010;63:332-337.
22. Thompson GR, Wiederhold NP, Vallor AC, Villareal NC, Lewis JS 2nd, Patterson TF. Development of caspofungin resistance following prolonged therapy for invasive candidiasis secondary to Candida glabrata infection. Antimicrob Agents Chemother 2008;52:3783-3785.
23. Garcia-Effron G, Chua DJ, Tomada JR, et al. Novel FKS mutations associated with echinocandin resistance in Candida species. Antimicrob Agents Chemother 2010;54:2225-2227.
24. Arendrup MC, Bruun B, Christensen JJ, et al. National surveillance of fungemia in Denmark (2004 to 2009). J Clin Microbiol 2011;49:325-334.
25. Castanheira M, Woosley LN, Diekema DJ, Messer SA, Jones RN, Pfaller MA. Low prevalence of fks1 hot spot 1 mutations in a worldwide collection of Candida strains. Antimicrob Agents Chemother 2010;54: 2655-2659.
26. Garcia-Effron G, Park S, Perlin DS. Correlating echinocandin MIC and kinetic inhibition of fks1 mutant glucan synthases for Candida albicans: implications for interpretive breakpoints. Antimicrob Agents Chemother 2009;53:112-122.
27. Garcia-Effron G, Lee S, Park S, Cleary JD, Perlin DS. Effect of Candida glabrata FKS1 and FKS2 mutations on echinocandin sensitivity and kinetics of 1,3-beta-D-glucan synthase: implication for the existing susceptibility breakpoint. Antimicrob Agents Chemother 2009;53:3690-3699.
28. Arendrup MC, Garcia-Effron G, Lass-Florl C, et al. Echinocandin susceptibility testing of Candida species: comparison of EUCAST EDef 7.1, CLSI M27-A3, Etest, disk diffusion, and agar dilution methods with RPMI and isosensitest media. Antimicrob Agents Chemother 2010;54: 426-439.
29. Chen SC-A, Slavin MA, Sorrell TC. Echinocandin antifungal drugs in fungal infections: a comparison. Drugs 2011;71:30.
30. Pfaller MA, Diekema DJ, Andes D, et al. Clinical breakpoints for the echinocandins and Candida revisited: integration of molecular, clinical, and microbiological data to arrive at species-specific interpretive criteria. Drug Resistance Updates 2011;14:164-176.
31. Walker LA, Gow NAR, Munro CA. Fungal echinocandin resistance. Fungal Genet Biol 2010;47:117-126.
32. Walker LA, Munro CA, de Bruijn I, Lenardon MD, McKinnon A, Gow NA. Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 2008;4:e1000040.
33. Cota JM, Grabinski JL, Talbert RL, et al. Increases in SLT2 expression and chitin content are associated with incomplete killing of Candida glabrata by caspofungin. Antimicrob Agents Chemother 2008;52:1144-146.
34. Stevens DA, Ichinomiya M, Koshi Y, Horiuchi H. Escape of Candida from caspofungin inhibition at concentrations above the MIC (paradoxical effect) accomplished by increased cell wall chitin; evidence for beta- 1,6-glucan synthesis inhibition by caspofungin. Antimicrob Agents Chemother 2006;50:3160-3161.
35. Munro CA, Selvaggini S, de Bruijn I, et al. The PKC, HOG and Ca2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol Microbiol 2007;63:1399-1413.
36. Chamilos G, Lewis RE, Albert N, Kontoyiannis DP. Paradoxical effect of echinocandins across Candida species in vitro: evidence for echinocandin- specific and Candida species-related differences. Antimicrob Agents Chemother 2007;51:2257-2259.
37. Stevens DA, Espiritu M, Parmar R. Paradoxical effect of caspofungin: reduced activity against Candida albicans at high drug concentrations. Antimicrob Agents Chemother 2004;48:3407-3441.
38. Shields RK, Nguyen MH, Du C, Press E, Cheng S, Clancy CJ. Paradoxical effect of caspofungin against Candida bloodstream isolates is mediated by multiple pathways but eliminated in human serum. Antimicrob Agents Chemother 2011;55:2641-2647.
39. Wiederhold NP, Kontoyiannis DP, Prince RA, Lewis RE. Attenuation of the activity of caspofungin at high concentrations against Candida albicans: possible role of cell wall integrity and calcineurin pathways. Antimicrob Agents Chemother 2005;49:5146-5148.
40. Drakulovski P, Dunyach C, Bertout S, Reynes J, Mallie M. A Candida albicans strain with high MIC for caspofungin and no FKS1 mutations exhibits a high chitin content and mutations in two chitinase genes. Med Mycol 2011;49:467-474.
41. Marine M, Pastor FJ, Sahand IH, Ponton J, Quindos G, Guarro J. Paradoxical growth of Candida dubliniensis does not preclude in vivo response to echinocandin therapy. Antimicrob Agents Chemother 2009;53: 5297-5299.
42. Bayegan S, Majoros L, Kardos G, et al. In vivo studies with a Candida tropicalis isolate exhibiting paradoxical growth in vitro in the presence of high concentration of caspofungin. J Microbiol 2010;48:170-173.
43. Clemons KV, Espiritu M, Parmar R, Stevens DA. Assessment of the paradoxical effect of caspofungin in therapy of candidiasis. Antimicrob Agents Chemother 2006;50:1293-1297.
44. Perlin D. Resistance to echinocandin-class antifungal drugs. Drug Resistance Updates 2007;10:121-130.
45. Pfaller MA, Diekema DJ, Boyken L, et al. Effectiveness of anidulafungin in eradicating Candida species in invasive candidiasis. Antimicrob Agents Chemother 2005;49:4795-4797.
46. Arendrup M, Horn T, Frimodt-Moller N. In vivo pathogenicity of eight medically relevant Candida species in an animal model. Infection 2002; 30:286-291.
47. Andes D, Diekema DJ, Pfaller MA, Bohrmuller J, Marchillo K, Lepak A. In vivo comparison of the pharmacodynamic targets for echinocandin drugs against Candida species. Antimicrob Agents Chemother 2010;54: 2497-2506.
48. Pfaller MA, Diekema DJ, Ostrosky-Zeichner L, et al. Correlation of MIC with outcome for Candida species tested against caspofungin, anidulafungin, and micafungin: analysis and proposal for interpretive MIC breakpoints. J Clin Microbiol 2008;46:2620-2629.
49. Pfaller MA, Boyken L, Hollis RJ, et al. In vitro susceptibility of invasive isolates of Candida spp. to anidulafungin, caspofungin, and micafungin: six years of global surveillance. J Clin Microbiol 2008;46:150-156.
50. Slater JL, Howard SJ, Sharp A, et al. Disseminated candidiasis caused byCandida albicans with amino acid substitutions in Fks1 at position Ser645 cannot be successfully treated with micafungin. Antimicrob Agents Chemother 2011;55:3075-3083.
51. Wiederhold NP, Najvar LK, Bocanegra RA, Kirkpatrick WR, Patterson TF. Caspofungin dose escalation for invasive candidiasis due to resistant Candida albicans. Antimicrob Agents Chemother 2011;55:3254-3260.
52. Lortholary O, Desnos-Ollivier M, Sitbon K, Fontanet A, Bretagne S, Dromer F. Recent exposure to caspofungin or fluconazole influences the epidemiology of candidemia: a prospective multicenter study involving 2,441 patients. Antimicrob Agents Chemother 2010;55:532-538.
53. Pfaller MA, Messer SA, Moet GJ, Jones RN, Castanheira M. 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 2011;38:65-69.
54. Sun HY, Singh N. Characterisation of breakthrough invasive mycoses in echinocandin recipients: an evidence-based review. Int J Antimicrob Agents 2010;35:211-218.
55. Pfeiffer CD, Garcia-Effron G, Zaas AK, Perfect JR, Perlin DS, Alexander BD. Breakthrough invasive candidiasis in patients on micafungin. J Clin Microbiol 2010;48:2373-2380.
56. Ben-Ami R, Garcia-Effron G, Lewis RE, et al. Fitness and virulence costs of Candida albicans FKS1 hot spot mutations associated with echinocandin resistance. J Infect Dis 2011;204:626-635.
57. Kurtz MB, Abruzzo G, Flattery A, et al. Characterization of echinocandin- resistant mutants of Candida albicans: genetic, biochemical, and virulence studies. Infect Immun 1996;64:3244-3251.
58. Bourgeois C, Majer O, Frohner IE, Tierney L, Kuchler K. Fungal attacks on mammalian hosts: pathogen elimination requires sensing and tasting. Curr Opin Microbiol 2010;13:401408.
59. Kartsonis N, Killar J, Mixson L, et al. Caspofungin susceptibility testing of isolates from patients with esophageal candidiasis or invasive candidiasis: relationship of MIC to treatment outcome. Antimicrob Agents Chemother 2005;49:3616-3623.
60. Brzankalski GE, Najvar LK, Wiederhold NP, et al. Evaluation of aminocandin and caspofungin against Candida glabrata including isolates with reduced caspofungin susceptibility. J Antimicrob Chemother 2008;62:1094-1100.
61. Wiederhold NP, Najvar LK, Bocanegra R, Molina D, Olivo M, Graybill JR. In vivo efficacy of anidulafungin and caspofungin against Candida glabrata and association with in vitro potency in the presence of sera. Antimicrob Agents Chemother 2007;51:1616-1620.
62. Singh SD, Robbins N, Zaas AK, Schell WA, Perfect JR, Cowen LE. Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathogens 2009;5:e1000532.
63. Sirohi B, Powles RL, Chopra R, et al. A study to determine the safety profile and maximum tolerated dose of micafungin (FK463) in patients undergoing haematopoietic stem cell transplantation. Bone Marrow Transplant 2006;38:47-51.
64. Paderu P, Garcia-Effron G, Balashov S, Delmas G, Park S, Perlin DS. Serum differentially alters the antifungal properties of echinocandin drugs. Antimicrob Agents Chemother 2007;51:2253-2256.
65. Cowen LE, Singh SD, Kohler JR, et al. Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc Natl Acad Sci U S A 2009;106:2818-2823.
66. Douglas CM, Foor F, Marrinan JA, et al. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-beta-D-glucan synthase. Proc Natl Acad Sci U S A 1994;91:12907-12911.
67. Hector RF. Compounds active against cell walls of medically important fungi. Clin Microbiol Rev 1993;6:1-21.
68. Sandovsky-Losica H, Shwartzman R, Lahat Y, Segal E. Antifungal activity against Candida albicans of nikkomycin Z in combination with caspofungin, voriconazole or amphotericin B. J Antimicrob Chemother 2008;62:635-637.
69. Stevens DA. Drug interaction studies of a glucan synthase inhibitor (LY 303366) and a chitin synthase inhibitor (nikkomycin Z) for inhibition and killing of fungal pathogens. Antimicrob Agents Chemother 2000;44:2547-2548.
70. Mitchell AP, Singh SD, Robbins N, et al. Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathogens 2009;5:e1000532.
71. Louie A, Stein DS, Zack JZ, et al. Dose range evaluation of Mycograb C28Y variant, a human recombinant antibody fragment to heat shock protein 90, in combination with amphotericin B-desoxycholate for treatment of murine systemic candidiasis. Antimicrob Agents Chemother 2011;55:3295-3304.
72. Pachl J, Svoboda P, Jacobs F, et al. A randomized, blinded, multicenter trial of lipid-associated amphotericin B alone versus in combination with an antibody-based inhibitor of heat shock protein 90 in patients with invasive candidiasis. Clin Infect Dis 2006;42:1404-1413.