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Mycology

Echinocandin and Triazole Antifungal Susceptibility Profiles for Clinical Opportunistic Yeast and Mold Isolates Collected from 2010 to 2011: Application of New CLSI Clinical Breakpoints and Epidemiological Cutoff Values for Characterization of Geographic and Temporal Trends of Antifungal Resistance

Michael A. Pfaller, Shawn A. Messer, Leah N. Woosley, Ronald N. Jones, Mariana Castanheira
Michael A. Pfaller
JMI Laboratories, North Liberty, Iowa, USA
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Shawn A. Messer
JMI Laboratories, North Liberty, Iowa, USA
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Leah N. Woosley
JMI Laboratories, North Liberty, Iowa, USA
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Ronald N. Jones
JMI Laboratories, North Liberty, Iowa, USA
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Mariana Castanheira
JMI Laboratories, North Liberty, Iowa, USA
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DOI: 10.1128/JCM.00308-13
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  • Table 1

    Geographic distribution of organisms collected during 2010 to 2011 in medical centers participating in the SENTRY Antimicrobial Surveillance Program

    Organism/organism groupNo. of isolates in each indicated geographic region:Total
    North AmericaEuropeLatin AmericaAsia-Pacific
    Total, yeasts and molds1,3491,1914923843,418
    Yeast
        All Candida spp.1,2111,0974333663,107
            C. albicans5035521861641,405
            C. glabrata3061753852571
            C. parapsilosis17319510493565
            C. tropicalis109897644318
            C. krusei40288379
            Other Candida spp.a80582110169
        Cryptococcus neoformans369291084
        Other yeastsb82110241
    Mold
        All Aspergillus spp.7451156146
            Aspergillus fumigatus453413497
            Other Aspergillus spp.c29162249
        Other moldsd2015540
    • ↵a Other Candida spp. include C. bracarensis (1 strain), C. catenulata (2 strains), C. dubliniensis (50 strains), C. fabianii (1 strain), C. fermentati (8 strains), C. guilliermondii (19 strains), C. haemulonii (2 strains), C. inconspicua (2 strains), C. kefyr (16 strains), C. lipolytica (4 strains), C. lusitaniae (55 strains), C. nivariensis (2 strains), C. norvegensis (1 strains), C. pararugosa (2 strains), C. pelliculosa (1 strain), and C. intermedia/C. pseudointermedia (3 strains).

    • ↵b Other yeasts include Aureobasidium pullulans (1 strain), Debaryomyces fabryi (1 strain), Dipodascus capitatus (3 strains), Lodderomyces elongisporus (2 strains), Rhodotorula mucilaginosa (5 strains), Saccharomyces cerevisiae (6 strains), Trichosporon asahii (9 strains), Trichosporon mycotoxinivorans (1 strain), Trichosporon spp. (5 strains), and unidentified yeasts (6 strains).

    • ↵c Other Aspergillus spp. include A. alabamensis (2 strains), A. flavus species complex (SC) (19 strains), A. foetidus (1 strain), A. nidulans (2 strains), A. niger SC (15 strains), A. sydowii (2 strains), A. terreus SC (7 strains), and A. ustus SC (1 strain).

    • ↵d Other molds include Absidia (Lichtheimia) corymbifera (1 strain), Acremonium strictum genogroup III (1 strain), Coprinellus radians (1 strain), Fusarium solani SC (3 strains), Gibberella fujikuroi SC (6 strains), Paecilomyces variotii (2 strains), Penicillium roqueforti group (1 strain), Penicillium subgenus Aspergilloides (3 strains), Penicillium subgenus Furcatum (1 strain), Penicillium subgenus Terverticillata (2 strains), Penicillium variabile (1 strain), Phialemonium curvatum (1 strain), Rhizomucor pusillus (1 strain), Rhizopus microsporus group (1 strain), Rhizopus oryzae (1 strain), Sarocladium (Acremonium) kiliense (2 strains), Scedosporium apiospermum (4 strains), Alternaria spp. (2 strains), Curvularia spp. (1 strain), Fusarium spp. (1 strain), Penicillium spp. (1 strain), Trichoderma spp. (1 strain), and Exophiala dermatitidis (1 strain).

  • Table 2

    Frequency of antifungal resistance among clinical isolates of Candida spp. by geographic region in the 2010-2011 SENTRY Surveillance Program

    Candida speciesAntifungal agentNo. of isolates (% resistanta to each antifungal agent) by region
    North AmericaEuropeLatin AmericaAsia-PacificTotal
    C. albicansAnidulafungin503 (0.0)552 (0.0)186 (0.0)164 (0.0)1,405 (0.0)
    Caspofungin503 (0.0)552 (0.4)186 (0.0)164 (0.6)1,405 (0.2)
    Micafungin503 (0.0)552 (0.4)186 (0.0)164 (0.0)1,405 (0.1)
    Fluconazole503 (0.6)552 (0.2)186 (0.0)164 (0.6)1,405 (0.4)
    Posaconazolec503 (0.6)552 (8.3)186 (6.5)164 (0.6)1,405 (4.4)
    Voriconazole503 (0.6)552 (0.2)186 (0.0)164 (0.6)1,405 (0.4)
    C. glabrataAnidulafungin306 (1.6)175 (1.7)38 (0.0)52 (3.8)571 (1.8)
    Caspofungin306 (1.6)175 (1.7)38 (0.0)52 (1.9)571 (1.6)
    Micafungin306 (1.3)175 (1.1)38 (0.0)52 (1.9)571 (1.2)
    Fluconazole306 (9.8)175 (6.3)38 (5.3)52 (13.5)571 (8.8)
    Posaconazolec306 (3.3)175 (2.9)38 (5.3)52 (5.8)571 (3.5)
    Voriconazoleb306 (11.1)175 (9.1)38 (7.9)52 (13.5)571 (10.5)
    C. parapsilosisAnidulafungin173 (1.2)195 (0.0)104 (1.0)93 (0.0)565 (0.5)
    Caspofungin173 (0.0)195 (0.0)104 (0.0)93 (0.0)565 (0.0)
    Micafungin173 (0.0)195 (0.0)104 (0.0)93 (0.0)565 (0.0)
    Fluconazole173 (0.0)195 (3.1)104 (1.0)93 (5.4)565 (2.1)
    Posaconazolec173 (1.2)195 (0.5)104 (3.9)93 (6.5)565 (2.3)
    Voriconazole173 (0.0)195 (0.0)104 (0.0)93 (1.1)565 (0.2)
    C. tropicalisAnidulafungin109 (0.0)89 (0.0)76 (0.0)44 (0.0)318 (0.0)
    Caspofungin109 (0.0)89 (0.0)76 (0.0)44 (0.0)318 (0.0)
    Micafungin109 (0.0)89 (0.0)76 (0.0)44 (0.0)318 (0.0)
    Fluconazole109 (2.7)89 (1.1)76 (0.0)44 (0.0)318 (1.3)
    Posaconazolec109 (7.3)89 (7.9)76 (2.6)44 (0.0)318 (5.3)
    Voriconazole109 (0.9)89 (0.0)76 (0.0)44 (0.0)318 (0.3)
    C. kruseiAnidulafungin40 (0.0)28 (0.0)8 (0.0)3 (0.0)79 (0.0)
    Caspofungin40 (0.0)28 (0.0)8 (0.0)3 (0.0)79 (0.0)
    Micafungin40 (0.0)28 (0.0)8 (0.0)3 (0.0)79 (0.0)
    Posaconazolec40 (17.5)28 (7.1)8 (25.0)3 (33.3)79 (15.2)
    Voriconazole40 (2.5)28 (0.0)8 (0.0)3 (0.0)79 (1.3)
    • ↵a Resistance is defined as an MIC of >0.5 μg/ml for anidulafungin, caspofungin, and micafungin against C. albicans, C. tropicalis, and C. krusei, an MIC of >4 μg/ml against C. parapsilosis, an MIC of >0.25 μg/ml for anidulafungin and caspofungin, and an MIC of >0.12 μg/ml for micafungin against C. glabrata; an MIC of >4 μg/ml for fluconazole against C. albicans, C. tropicalis, and C. parapsilosis, an MIC of >32 μg/ml against C. glabrata; and an MIC of >0.5 μg/ml for voriconazole against C. albicans, C. tropicalis, and C. parapsilosis.

    • ↵b In lieu of clinical breakpoints for voriconazole against C. glabrata, the epidemiological cutoff value (ECV) of >0.5 μg/ml was used to identify non-wild-type (non-WT) isolates.

    • ↵c Posaconazole ECVs were used to identify non-WT isolates of C. albicans (ECV > 0.06 μg/ml), C. glabrata (ECV > 2 μg/ml), C. parapsilosis (ECV > 0.25 μg/ml), C. tropicalis (ECV > 0.12 μg/ml), and C. krusei (ECV > 0.5 μg/ml).

  • Table 3

    Comparison of in vitro susceptibilities of three echinocandins versus isolates of Candida collected during two different time periodsa

    Candida speciesAntifungal agentbYearscNo. of isolates tested% of isolates at an MIC (μg/ml) of:
    ≤0.0080.0150.030.060.120.250.5124≥8
    C. albicansANF2003-20074,2837.929.836.020.95.00.3<0.1
    2010-20111,4059.322.635.424.77.00.50.4
    CSF2003-20074,2832.127.647.621.01.60.1
    2010-20111,4050.716.245.725.910.00.90.40.10.1
    MCF2003-20074,28314.268.914.62.10.1
    2010-20111,4054.240.247.66.31.10.20.30.1
    C. glabrataANF2003-20071,2360.613.057.825.92.10.20.20.20.1
    2010-20115710.715.252.025.74.60.41.10.20.2
    CSF2003-20071,23610.759.126.62.10.60.60.10.2
    2010-20115711.258.523.313.02.50.50.70.20.2
    MCF2003-20071,23616.875.65.71.00.30.20.10.20.1
    2010-20115719.868.517.52.10.90.20.70.20.2
    C. parapsilosisANF2003-20071,2380.10.20.10.11.14.025.861.86.90.1
    2010-20115650.20.54.210.132.039.313.10.5
    CSF2003-20071,2380.20.42.510.244.032.29.11.30.10.2
    2010-20115650.41.410.452.426.28.80.4
    MCF2003-20071,2380.20.20.10.85.321.154.617.80.2
    2010-20115650.20.92.513.552.929.60.5
    C. tropicalisANF2003-20079964.125.549.517.42.40.70.10.3
    2010-201131811.937.138.710.71.30.3
    CSF2003-20079961.731.948.416.21.20.40.10.1
    2010-20113180.618.957.917.04.70.9
    MCF2003-20079964.640.237.715.01.70.60.10.2
    2010-20113182.227.750.317.31.90.6
    C. kruseiANF2003-20072701.558.933.75.20.40.4
    2010-2011791.37.631.645.612.71.3
    CSF2003-20072700.451.929.314.83.00.70.4
    2010-2011791.32.530.421.539.212.9
    MCF2003-20072701.510.478.17.82.2
    2010-2011791.31.327.868.41.3
    • ↵a All isolates were tested using CLSI broth microdilution methods (17).

    • ↵b ANF, anidulafungin; MCF, micafungin; CSF, caspofungin.

    • ↵c Data from the 2003-2007 period were compiled from the work of Pfaller et al. (36).

  • Table 4

    Summary of fks alterations detected in echinocandin-resistant Candida sp. strains

    OrganismState or countryYearMIC (μg/ml) for each indicated antifungal:1,3-β-d-Glucan synthase alterations ina:
    AnidulafunginCaspofunginMicafunginfks1 HS1fks1 HS2fks2 HS1bfks2 HS2b
    Candida glabrataIndiana2010140.06WTWTF641VWT
    C. glabrataBelgium2010110.06WTWTWTWT
    C. glabrataMichigan20100.250.50.03WTWTD648EWT
    C. glabrataTexas20100.50.250.03WTWTF641YWT
    C. glabrataGermany201010.50.5WTWTL644WWT
    C. glabrataNew York20100.250.250.5WTWTWTWT
    Candida parapsilosisNew York2010821WTWTNTNT
    C. parapsilosisNew York2010811WTWTNTNT
    C. parapsilosisArgentina2010811WTWTNTNT
    Candida albicansSweden20110.511S654PWTNTNT
    C. albicansScotland20110.521S629PWTNTNT
    C. albicansChina20110.2510.5S645PWTNTNT
    C. glabrataAustralia20110.50.250.12F625SWTWTWT
    C. glabrataCanada2011110.25WTWTS659YWT
    C. glabrataIndiana201110.50.5WTWTS663YWT
    C. glabrataAustralia2011110.5WTWTS663PWT
    C. glabrataGreece2011211WTWTS663PWT
    C. glabrataLouisiana20114162S629PWTWTWT
    • ↵a WT, wild-type.

    • ↵b NT, not tested.

  • Table 5

    Frequency of decreased susceptibility of Aspergillus fumigatus to azole antifungal agents by geographic region using CLSI epidemiological cutoff values

    Antifungal agentECVb (μg/ml)No. of isolatesa (% non-wild-type to each antifungal agent) by region
    North AmericaEuropeLatin AmericaAsia-PacificTotal
    Itraconazole145 (4.4)34 (0.0)13 (0.0)4 (0.0)96 (2.0)
    Posaconazole0.545 (15.6)34 (2.9)13 (7.7)4 (0.0)96 (9.4)
    Voriconazole145 (2.2)34 (0.0)13 (0.0)4 (0.0)96 (1.0)
    • ↵a All isolates tested using CLSI broth microdilution methods (19).

    • ↵b ECVs as published by Espinel-Ingroff et al. (37).

  • Table 6

    MIC distributions for azole and echinocandin antifungal agents tested against isolates of uncommon species of Candida and Aspergillus, as well as non-Candida yeasts and non-Aspergillus molds identified by molecular methods (≥5 isolates per species) in SENTRY, 2010 to 2011

    Species (no. tested)Antifungal agentaNo. at an MIC/MEC (μg/ml) of:
    0.0070.0150.030.060.120.250.51248163264128
    Candida species
        C. dubliniensis (50)ANF13171883
    CSF22142381
    MCF46231241
    FLC161617
    ITR110191442
    PSC2728571
    VRC41621
        C. fermentati (8)ANF44
    CSF422
    MCF161
    FLC111311
    ITR2411
    PSC3311
    VRC2231
        C. guilliermondii (19)ANF15841
    CSF333442
    MCF1154521
    FLC1743211
    ITR47251
    PSC5545
    VRC167311
        C. kefyr (16)ANF8422
    CSF11311
    MCF6721
    FLC1582
    ITR13732
    PSC13732
    VRC133
        C. lusitaniae (55)ANF1321819111
    CSF141220135
    MCF2237251051
    FLC121311844111
    ITR11131681141
    PSC15101971111
    VRC34126111
    Non-Candida yeasts
        Cryptococcus neoformans (84)ANF84
    CSF1173
    MCF84
    FLC3142426152
    ITR8182422111
    PSC14193016122
    VRC41729295
        Rhodotorula mucilaginosa (5)ANF5
    CSF23
    MCF5
    FLC5
    ITR221
    PSC221
    VRC23
        Saccharomyces cerevisiae (6)ANF1122
    CSF231
    MCF51
    FLC321
    ITR222
    PSC222
    VRC321
        Trichosporon asahii (9)ANF9
    CSF135
    MCF9
    FLC2511
    ITR1152
    PSC2331
    VRC123111
        Trichosporon spp. (5)ANF5
    CSF23
    MCF5
    FLC221
    ITR1121
    PSC2111
    VRC32
    Aspergillus species
        A. flavus SC (19)ANF1612
    CSF496
    MCF1522
    ITR127
    PSC3151
    VRC1171
        A. niger SC (15)ANF1032
    CSF5811
    MCF1212
    ITR86
    PSC95
    VRC841
        A. terreus SC (7)ANF3211
    CSF331
    MCF511
    ITR133
    PSC43
    VRC16
    Non-Aspergillus molds
        Gibberella fujikuroi SC (6)ANF15
    CSF6
    MCF6
    ITR15
    PSC12111
    VRC11211
    • ↵a ANF, anidulafungin; MCF, micafungin; CSF, caspofungin; ITR, itraconazole; PSC, posaconazole; VRC, voriconazole.

Additional Files

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    Files in this Data Supplement:

    • Supplemental file 1 -

      Table showing MIC distributions for azole and echinocandin antifungal agents tested against isolates of uncommon species of Candida and Aspergillus as well as non-Candida yeasts and non-Aspergillus molds identified by molecular methods (SENTRY, 2010 to 2011)

      PDF, 239K

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Echinocandin and Triazole Antifungal Susceptibility Profiles for Clinical Opportunistic Yeast and Mold Isolates Collected from 2010 to 2011: Application of New CLSI Clinical Breakpoints and Epidemiological Cutoff Values for Characterization of Geographic and Temporal Trends of Antifungal Resistance
Michael A. Pfaller, Shawn A. Messer, Leah N. Woosley, Ronald N. Jones, Mariana Castanheira
Journal of Clinical Microbiology Jul 2013, 51 (8) 2571-2581; DOI: 10.1128/JCM.00308-13

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Echinocandin and Triazole Antifungal Susceptibility Profiles for Clinical Opportunistic Yeast and Mold Isolates Collected from 2010 to 2011: Application of New CLSI Clinical Breakpoints and Epidemiological Cutoff Values for Characterization of Geographic and Temporal Trends of Antifungal Resistance
Michael A. Pfaller, Shawn A. Messer, Leah N. Woosley, Ronald N. Jones, Mariana Castanheira
Journal of Clinical Microbiology Jul 2013, 51 (8) 2571-2581; DOI: 10.1128/JCM.00308-13
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