The current role of the reference procedures by CLSI and EUCAST in the detection of resistance to antifungal agents in vitro

Expert Review of Anti-Infective Therapy

Volumn 8, Issue 3, 2010, Pages 267-276

  Cuenca Estrella, Manuel ^a   Rodriguez Tudela, Juan Luis ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Antifungal breakpoint; Antifungal epidemiological cut off; CLSI; EUCAST

Indexed keywords

AMPHOTERICIN B; ANIDULAFUNGIN; ANTIFUNGAL AGENT; CASPOFUNGIN; ECHINOCANDIN; FLUCONAZOLE; ITRACONAZOLE; MICAFUNGIN; VORICONAZOLE;

AGAR DIFFUSION; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; CANDIDA; CLINICAL LABORATORY; FUNGAL DETECTION; FUNGUS ISOLATION; IN VITRO STUDY; INCUBATION TIME; INOCULATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; REFERENCE VALUE; REVIEW; SPECIES DIFFERENCE;

ANTIFUNGAL AGENTS; DRUG RESISTANCE, FUNGAL; FUNGI; HUMANS; MICROBIAL SENSITIVITY TESTS; MYCOSES; REFERENCE VALUES; YEASTS;

EID: 77649283879     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/eri.10.2     Document Type: Review

References (82)

1. Rex JH, Pfaller MA. Has antifungal susceptibility testing come of age? Clin. Infect. Dis. 35(8), 982-989 (2002).
2. Clinical Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi; Approved Standard - Second Edition. CLSI document M38-A2. Clinical Laboratory Standards Institute, Wayne, PA, USA (2008).
3. Clinical Laboratory Standards Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeast; Approved Standard - Third Edition. CLSI document M27-A3. Clinical Laboratory Standards Institute, Wayne, PA, USA (2008).
4. Rodriguez-Tudela JL, Barchiesi F, Bille J et al. Method for the determination of minimum inhibitory concentration (MIC) by broth dilution of fermentative yeasts. Clin. Microbiol. Infect. 9(8), I-VIII (2003).
5. Rodriguez-Tudela JL, Arendrup MC, Barchiesi F et al. EUCAST definitive document EDef 7.1: method for the determination of broth dilution MICs of antifungal agents for fermentative yeasts. Clin. Microbiol. Infect. 14(4), 398-405 (2008).
6. Rodriguez-Tudela JL, Donnelly JP, Arendrup MC et al. EUCAST technical note on fluconazole. Clin. Microbiol. Infect. 14(2), 193-195 (2008).
7. Rodriguez-Tudela JL, Donnelly JP, Arendrup MC et al. EUCAST technical note on voriconazole - subcommittee on antifungal susceptibility testing (AFST) of the ESCMID European committee for antimicrobial susceptibility testing (EUCAST). Clin. Microbiol. Infect. 14(10), 985-987 (2008).
8. Kahlmeter G, Brown DFJ, Goldstein FW et al. European Committee on Antimicrobial Susceptibility Testing (EUCAST) technical notes on antimicrobial susceptibility testing. Clin. Microbiol. Infect. 12(6), 501-503 (2006).
9. Kahlmeter G, Brown DFJ, Goldstein FW et al. European harmonization of MIC breakpoints for antimicrobial susceptibility testing of bacteria. J. Antimicrob Chemother. 52(2), 145-148 (2003).
10. Cuenca-Estrella M, Lee-Yang W, Ciblak MA et al. Comparative evaluation of NCCLS M27-A and EUCAST broth microdilution procedures for antifungal susceptibility testing of Candida species. Antimicrob. Agents Chemother. 46(11), 3644-3647 (2002).
11. Espinel-Ingroff A, Barchiesi F, Cuenca-Estrella M et al. International and multicenter comparison of EUCAST and CLSI M27-A2 broth microdilution methods for testing susceptibilities of Candida spp. to fluconazole, itraconazole, posaconazole, and voriconazole. J. Clin. Microbiol. 43(8), 3884-3889 (2005).
12. Rodriguez-Tudela JL, Donnelly JP, Pfaller MA et al. Statistical analyses of correlation between fluconazole MICs for Candida spp. assessed by standard methods set forth by the European Committee on Antimicrobial Susceptibility Testing (E.Dis. 7.1) and CLSI (M27-A2). J. Clin. Microbiol. 45(1), 109-111 (2007).
13. Canton E, Espinel-Ingroff A, Peman J. Trends in antifungal susceptibility testing using CLSI reference and commercial methods. Expert Rev. Anti Infect. Ther. 7(1), 107-119 (2009).
14. Cuenca-Estrella M, Gomez-Lopez A, Mellado E, Rodriguez-Tudela JL. Correlation between the procedure for antifungal susceptibility testing for Candida spp. of the European Committee on Antibiotic Susceptibility Testing (EUCAST) and four commercial techniques. Clin. Microbiol. Infect. 11(6), 486-492 (2005).
15. Cuenca-Estrella M, Gomez-Lopez A, Gutierrez MO, Buitrago MJ, Rodriguez-Tudela JL. Reliability of the WIDERYST susceptibility testing system for detection of in vitro antifungal resistance in yeasts. Antimicrob. Agents Chemother. 52(3), 1062-1065 (2008).
16. Morace G, Amato G, Bistoni F et al. Multicenter comparative evaluation of six commercial systems and the national committee for clinical laboratory standards M27-A broth microdilution method for fluconazole susceptibility testing of Candida species. J. Clin. Microbiol. 40(8), 2953-2958 (2002).
17. Arikan S, Gur D, Akova M. Comparison of Etest, microdilution and colorimetric dilution with reference broth macrodilution method for antifungal susceptibility testing of clinically significant Candida species isolated from immunocompromised patients. Mycoses 40(7-8), 291-296 (1997).
18. Barry AL, Pfaller MA, Rennie R P, Fuchs PC, Brown SD. Precision and accuracy of fluconazole susceptibility testing by broth microdilution, Etest, and disk diffusion methods. Antimicrob. Agents Chemother. 46(6), 1781-1784 (2002).
19. De Vos MM, Cuenca-Estrella M, Boekhout T et al. Vulvovaginal candidiasis in a Flemish patient population. Clin. Microbiol. Infect. 11(12), 1005-1011 (2005).
20. Espinel-Ingroff A, Pfaller M, Messer SA, Knapp CC, Holliday N, Killian SB. Multicenter comparison of the Sensititre YeastOne colorimetric antifungal panel with the NCCLS M27-A2 reference method for testing new antifungal agents against clinical isolates of Candida spp. J. Clin. Microbiol. 42(2), 718-721 (2004).
21. Espinel-Ingroff A, Canton E. Comparison of Neo-Sensitabs tablet diffusion assay with CLSI broth microdilution M38-A and disk diffusion methods for testing susceptibility of filamentous fungi with amphotericin B, caspofungin, itraconazole, posaconazole, and voriconazole. J. Clin. Microbiol. 46(5), 1793-1803 (2008).
22. Espinel-Ingroff A, Arthington-Skaggs B, Iqbal N et al. Multicenter evaluation of a new disk agar diffusion method for susceptibility testing of filamentous fungi with voriconazole, posaconazole, itraconazole, amphotericin B, and caspofungin. J. Clin. Microbiol. 45(6), 1811-1820 (2007).
23. Pfaller MA, Messer SA, Mills K, Bolmstrom A, Jones RN. Evaluation of Etest method for determining caspofungin (MK-0991) susceptibilities of 726 clinical isolates of Candida species. J. Clin. Microbiol. 39(12), 4387-4389 (2001).
24. Cuenca-Estrella M, Diaz-Guerra TM, Mellado E, Rodriguez-Tudela JL. Detection of resistance to amphotericin B in Candida isolates by using iso-sensitest broth. Antimicrob. Agents Chemother. 45(7), 2070-2074 (2001).
25. Rex JH, Cooper CR Jr, Merz WG, Galgiani JN, Anaissie EJ. Detection of amphotericin B-resistant Candida isolates in a broth-based system. Antimicrob. Agents Chemother. 39(4), 906-909 (1995).
26. Pfaller MA, Diekema DJ, Sheehan DJ. Interpretive breakpoints for fluconazole and Candida revisited: a blueprint for the future of antifungal susceptibility testing. Clin. Microbiol. Rev. 19(2), 435-447 (2006).
27. Rex JH, Pfaller MA, Galgiani JN et al. Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and candida infections. Subcommittee on Antifungal Susceptibility Testing of the National Committee for Clinical Laboratory Standards. Clin. Infect. Dis. 24(2), 235-247 (1997).
28. 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. 46(8), 2620-2629 (2008).
29. Bonate PL. A brief introduction to Monte Carlo simulation. Clin. Pharmacokinet. 40(1), 15-22 (2001).
30. Debruyne D, Ryckelynck JP. Clinical pharmacokinetics of fluconazole. Clin. Pharmacokinet. 24(1), 10-27 (1993).
31. Drusano GL, DArgenio DZ, Preston SL et al. Use of drug effect interaction modeling with Monte Carlo simulation to examine the impact of dosing interval on the projected antiviral activity of the combination of abacavir and amprenavir. Antimicrob. Agents Chemother. 44(6), 1655-1659 (2000).
32. Drusano GL, Preston SL, Hardalo C et al. Use of preclinical data for selection of a Phase II/III dose for evernimicin and identification of a preclinical MIC breakpoint. Antimicrob. Agents Chemother. 45(1), 13-22 (2001).
33. Mouton JW, Schmitt-Hoffmann A, Shapiro S, Nashed N, Punt NC. Use of Monte Carlo simulations to select therapeutic doses and provisional breakpoints of BAL9141. Antimicrob. Agents Chemother. 48(5), 1713-1718 (2004).
34. Mouton JW, Punt N, Vinks AA. A retrospective analysis using Monte Carlo simulation to evaluate recommended ceftazidime dosing regimens in healthy volunteers, patients with cystic fibrosis, and patients in the intensive care unit. Clin. Ther. 27(6), 762-772 (2005).
35. Mouton JW. Antifungals and children: pharmacokinetic and pharmacodynamics issues. Presented at: 2nd Trends in Medical Mycology. Berlin, Germany, 23 October 2005.
36. Cuenca-Estrella M, Rodriguez D, Almirante B et al. In vitro susceptibilities of bloodstream isolates of Candida species to six antifungal agents: results from a population-based active surveillance programme, Barcelona, Spain, 2002-2003. J. Antimicrob. Chemother. 55(2), 194-199 (2005).
37. Cuenca-Estrella M, Gomez-Lopez A, Mellado E, Buitrago MJ, Monzon A, Rodriguez-Tudela JL. Head-to-head comparison of the activities of currently available antifungal agents against 3,378 Spanish clinical isolates of yeasts and filamentous fungi. Antimicrob. Agents Chemother. 50(3), 917-921 (2006).
38. Cuenca-Estrella M, Gomez-Lopez A, Mellado E, Monzon A, Buitrago MJ, Rodriguez-Tudela JL. Analysis of the activity profile in vitro of micafungin against Spanish clinical isolates of common and emerging species of yeasts and moulds. Antimicrob. Agents Chemother. 53(5), 2192-2195 (2009).
39. Laguna F, Rodriguez-Tudela JL, Martinez-Suarez JV et al. Patterns of fluconazole susceptibility in isolates from human immunodeficiency virus-infected patients with oropharyngeal candidiasis due to Candida albicans. Clin. Infect. Dis. 24(2), 124-130 (1997).
40. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20(1), 133-163 (2007).
41. Almirante B, Rodriguez D, Park BJ et al. Epidemiology and predictors of mortality in cases of Candida bloodstream infection: results from population-based surveillance, Barcelona, Spain, from 2002 to 2003. J. Clin. Microbiol. 43(4), 1829-1835 (2005).
42. Arendrup MC, Fuursted K, Gahrn-Hansen B et al. Semi-national surveillance of fungaemia in Denmark 2004-2006: increasing incidence of fungaemia and numbers of isolates with reduced azole susceptibility Clin. Microbiol. Infect. 14(5), 487-494 (2008).
43. Asmundsdottir LR, Erlendsdottir H, Gottfredsson M. Increasing incidence of candidemia: results from a 20-year nationwide study in Iceland. J. Clin. Microbiol. 40(9), 3489-3492 (2002).
44. Bedini A, Venturelli C, Mussini C et al. Epidemiology of candidaemia and antifungal susceptibility patterns in an Italian tertiary-care hospital. Clin. Microbiol. Infect. 12(1), 75-80 (2006).
45. Chen S, Slavin M, Nguyen Q et al. Active surveillance for candidemia, Australia. Emerg. Infect. Dis. 12(10), 1508-1516 (2006).
46. Gonzalez GM, Elizondo M, Ayala J. Trends in species distribution and susceptibility of bloodstream isolates of Candida collected in Monterrey, Mexico, to seven antifungal agents: results of a 3-year (2004 to 2007) surveillance study J. Clin. Microbiol. 46(9), 2902-2905 (2008).
47. Hajjeh RA, Sofair AN, Harrison LH et al. Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J. Clin. Microbiol. 42(4), 1519-1527 (2004).
48. Kao AS, Brandt ME, Pruitt WR et al. The epidemiology of candidemia in two United States cities: results of a population-based active surveillance. Clin. Infect. Dis. 29(5), 1164-1170 (1999).
49. Laupland KB, Gregson DB, Church DL, Ross T, Elsayed S. Invasive Candida species infections: a 5 year population-based assessment. J. Antimicrob. Chemother. 56(3), 532-537 (2005).
50. Odds FC, Hanson MF, Davidson AD et al. One year prospective survey of Candida bloodstream infections in Scotland. J. Med. Microbiol. 56(8), 1066-1075 (2007).
51. Poikonen E, Lyytikainen O, Anttila VJ, Ruutu P. Candidemia in Finland, 1995-1999. Emerg. Infect. Dis. 9(8), 985-990 (2003).
52. Rennert G, Rennert HS, Pitlik S, Finkelstein R, Kitzes-Cohen R. Epidemiology of candidemia - a nationwide survey in Israel. Infection 28(1), 26-29 (2000).
53. Sandven P, Bevanger L, Digranes A, Haukland HH, Mannsaker T, Gaustad P. Candidemia in Norway (1991 to 2003): results from a nationwide study. J. Clin. Microbiol. 44(6), 1977-1981 (2006).
54. Takakura S, Fujihara N, Saito T et al. National surveillance of species distribution in blood isolates of Candida species in Japan and their susceptibility to six antifungal agents including voriconazole and micafungin. J. Antimicrob. Chemother. 53(2), 283-289 (2004).
55. Zepelin MB, Kunz L, Ruchel R, Reichard U, Weig M, Gross U. Epidemiology and antifungal susceptibilities of Candida spp. to six antifungal agents: results from a surveillance study on fungaemia in Germany from July 2004 to August 2005. J. Antimicrob. Chemother. 60(2), 424-428 (2007).
56. Klingspor L, Tornqvist E, Johansson A, Petrini B, Forsum U, Hedin G. A prospective epidemiological survey of candidaemia in Sweden. Scand. J. Infect. Dis. 36(1), 52-55 (2004).
57. Peman J, Canton E, Gobernado M. Epidemiology and antifungal susceptibility of Candida species isolated from blood: results of a 2-year multicentre study in Spain. Eur. J. Clin. Microbiol. Infect. Dis. 24(1), 23-30 (2005).
58. Tortorano AM, Peman J, Bernhardt H et al. Epidemiology of candidaemia in Europe: results of 28-month European Confederation of Medical Mycology (ECMM) hospital-based surveillance study. Eur. J. Clin. Microbiol. Infect. Dis. 23(4), 317-322 (2004).
59. Tortorano AM, Kibbler C, Peman J, Bernhardt H, Klingspor L, Grillot R. Candidaemia in Europe: epidemiology and resistance. Int. J. Antimicrob. Agents 27(5), 359-366 (2006).
60. Horn DL, Neofytos D, Anaissie EJ et al. Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry Clin. Infect. Dis. 48(12), 1695-1703 (2009).
61. Colombo AL, Nucci M, Park BJ et al. Epidemiology of candidemia in Brazil: a nationwide sentinel surveillance of candidemia in eleven medical centers. J. Clin. Microbiol. 44(8), 2816-2823 (2006).
62. Cuesta I, Bielza C, Larranaga P et al. Data mining validation of fluconazole breakpoints established by the European committee on antimicrobial susceptibility testing. Antimicrob. Agents Chemother. 53(7), 2949-2954 (2009).
63. Rodriguez-Tudela JL, Almirante B, Rodriguez-Pardo D et al. Correlation of the MIC and dose/MIC ratio of fluconazole to the therapeutic response of patients with mucosal candidiasis and candidemia. Antimicrob. Agents Chemother. 51(10), 3599-3604 (2007).
64. Pfaller MA, Diekema DJ. Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20(1), 133-163 (2007).
65. 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. 46(1), 150-156 (2008).
66. 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. 53(1), 112-122 (2009).
67. Perlin DS. Antifungal drug resistance: do molecular methods provide a way forward? Curr. Opin, Infect. Dis. 22(6), 568-573 (2009).
68. Powderly WG, Kobayashi GS, Herzig GP, Medoff G. Amphotericin B-resistant yeast infection in severely immunocompromised patients. Am. J. Med. 84(5), 826-832 (1988).
69. Hsueh PR, Lau YJ, Chuang YC et al. Antifungal susceptibilities of clinical isolates of Candida species, Cryptococcus neoformans, and Aspergillus species from Taiwan: surveillance of multicenter antimicrobial resistance in Taiwan program data from 2003. Antimicrob. Agents Chemother. 49(2), 512-517 (2005).
70. Perkins A, Gomez-Lopez A, Mellado E, Rodriguez-Tudela JL, Cuenca-Estrella M. Rates of antifungal resistance among Spanish clinical isolates of Cryptococcus neoformans var. neoformans. J. Antimicrob. Chemother. 56(6), 1144-1147 (2005).
71. Sar B, Monchy D, Vann M, Keo C, Sarthou JL, Buisson Y. Increasing in vitro resistance to fluconazole in Cryptococcus neoformans Cambodian isolates: April 2000 to March 2002. J. Antimicrob. Chemother. 54(2), 563-565 (2004).
72. Gomez-Lopez A, Zaragoza O, Dos Anjos MM, Melhem MC, Rodriguez-Tudela JL, Cuenca-Estrella M. In vitro susceptibility of Cryptococcus gattii clinical isolates. Clin. Microbiol. Infect. 14(7), 727-730 (2008).
73. Gomez-Lopez A, Mellado E, Rodriguez-Tudela JL, Cuenca-Estrella M. Susceptibility profile of 29 clinical isolates of Rhodotorula spp. and literature review. J. Antimicrob. Chemother. 55(3), 312-316 (2005).
74. Munoz P, Bouza E, Cuenca-Estrella M et al. Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin. Infect. Dis. 40(11), 1625-1634 (2005).
75. Rodriguez-Tudela JL, Diaz-Guerra TM, Mellado E et al. Susceptibility patterns and molecular identification of Trichosporon species. Antimicrob. Agents Chemother. 49(10), 4026-4034 (2005).
76. Rodriguez-Tudela JL, Alcazar-Fuoli L, Mellado E, Alastruey-Izquierdo A, Monzon A, Cuenca-Estrella M. Epidemiological cutoffs and cross-resistance to azole drugs in Aspergillus fumigatus. Antimicrob. Agents Chemother. 52(7), 2468-2472 (2008).
77. Snelders E, van der Lee HA, Kuijpers J et al. Emergence of azole resistance in Aspergillus fumigatus and spread of a single resistance mechanism. PLoS Med. 5(11), e219 (2008).
78. Lass-Florl C, Griff K, Mayr A et al. Epidemiology and outcome of infections due to Aspergillus terreus: 10-year single centre experience. Br. J. Haematol. 131(2), 201-207 (2005).
79. Cuenca-Estrella M, Bernal-Martinez L, Isla G, Gomez-Lopez A, Alcazar-Fuoli L, Buitrago MJ. Incidence of zygomycosis in transplant recipients. Clin. Microbiol. Infect. 15(Suppl. 5), 37-40 (2009).
80. Guarro J, Kantarcioglu AS, Horre R et al. Scedosporium apiospermum: changing clinical spectrum of a therapy-refractory opportunist. Med. Mycol. 44(4), 295-327 (2006).
81. Kauffman CA, Malani AN. Zygomycosis: an emerging fungal infection with new options for management. Curr. Infect. Dis. Rep. 9(6), 435-440 (2007).
82. Rodriguez-Tudela JL, Berenguer J, Guarro J et al. Epidemiology and outcome of Scedosporium prolificans infection, a review of 162 cases. Med. Mycol. 47(4), 359-370 (2009).