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Mycology

Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: a 10.5-Year Analysis of Susceptibilities of Candida Species to Fluconazole and Voriconazole as Determined by CLSI Standardized Disk Diffusion

M. A. Pfaller, D. J. Diekema, D. L. Gibbs, V. A. Newell, D. Ellis, V. Tullio, A. Rodloff, W. Fu, T. A. Ling
and and the Global Antifungal Surveillance Group
M. A. Pfaller
Departments of Pathology
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  • For correspondence: michael-pfaller@uiowa.edu
D. J. Diekema
Departments of PathologyMedicine, Roy J. and Lucille A. Carver College of Medicine, University of Iowa, Iowa City, Iowa
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D. L. Gibbs
Giles Scientific, Inc., Santa Barbara, California
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V. A. Newell
Giles Scientific, Inc., Santa Barbara, California
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D. Ellis
Women's and Children's Hospital, North Adelaide, Australia
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V. Tullio
Universita degli Studi di Torino, Turin, Italy
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A. Rodloff
Institute for Medical Microbiology, Leipzig, Germany
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W. Fu
Husa Shan Hospital, Shanghai, China
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T. A. Ling
Singapore General Hospital, Singapore
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DOI: 10.1128/JCM.02117-09
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Tables

  • TABLE 1.

    Species distribution of Candida isolates over 10.5 yearsa

    OrganismIsolates tested by period:
    1997-20002001-20042005-20071997-2007
    No.% of totalNo.% of totalNo.% of totalNo.% of total
    Candida albicans39,15270.971,02762.957,59865.0167,77765.3
    C. glabrata5,63410.212,96311.510,34211.728,93911.3
    C. tropicalis2,9965.48,4967.57,0508.018,5427.2
    C. parapsilosis2,6334.87,7836.95,0055.615,4216.0
    C. krusei1,2072.22,8402.52,2392.56,2862.4
    C. guilliermondii3670.79020.85080.61,7770.7
    C. lusitaniae2760.56740.65590.61,5090.6
    C. kefyr1820.35270.55170.61,2260.5
    C. inconspicua90.022760.22900.35750.2
    C. famata1230.23750.32470.37450.3
    C. rugosa350.064690.41340.26380.2
    C. dubliniensis1<0.011130.11970.23110.1
    C. norvegensis110.021350.11130.12590.1
    C. lipolytica70.01800.07500.061370.05
    C. sake200.02670.08870.03
    C. pelliculosa1<0.01470.04400.05880.03
    C. apicola570.06570.02
    C. zeylanoides4<0.01500.04200.02740.03
    C. valida9<0.01120.0121<0.01
    C. intermedia10<0.01140.0124<0.01
    C. pulcherrima6<0.018<0.0114<0.01
    C. haemulonii6<0.013<0.019<0.01
    C. stellatoidea7<0.017<0.01
    C. utilis6<0.016<0.01
    C. humicola2<0.014<0.016<0.01
    C. lambica5<0.015<0.01
    C. ciferrii2<0.012<0.01
    C. colliculosa2<0.012<0.01
    C. holmii1<0.011<0.01
    C. marina1<0.011<0.01
    C. sphaerica1<0.011<0.01
    Candida spp. NOSb2,5914.76,1865.53,5584.012,3354.8
    Total55,229100.0112,996100.088,647100.0256,882100.0
    • ↵a Includes all specimen types and all locations in hospitals from 142 institutions in 41 countries.

    • ↵b Candida spp. NOS, Candida species not otherwise identified.

  • TABLE 2.

    Geographic variation in frequency of common and uncommon species of Candida: ARTEMIS, 2001 to 2007a

    SpeciesSpecies distribution (%) by region (total no. of isolates)b:
    APAC (44,674)EU (109,643)AF/ME (8,259)LAM (27,395)NAM (11,682)Total (201,653)
    C. albicans64.467.967.151.848.963.8
    C. glabrata12.611.38.87.421.111.6
    C. tropicalis11.74.96.613.27.37.7
    C. parapsilosis7.44.26.010.313.66.3
    C. krusei1.23.41.61.43.12.5
    C. guilliermondii0.40.50.12.20.50.7
    C. inconspicua<0.10.5<0.1<0.10.3
    C. rugosa0.4<0.1<0.11.2<0.10.3
    C. norvegensis<0.10.2<0.1<0.10.20.1
    • ↵a Includes all specimen types and all locations in hospitals from 133 institutions.

    • ↵b Abbreviations: APAC, Asia-Pacific; EU, Europe; AF/ME, Africa-Middle East; LAM, Latin America; NAM, North America.

  • TABLE 3.

    In vitro susceptibilities of Candida spp. to fluconazole and voriconazole as determined by CLSI disk diffusion testinga

    SpeciesFluconazolebVoriconazoleb
    No. of isolates tested% S% RNo. of isolates tested% S% R
    C. albicans128,62598.01.4125,96598.51.2
    C. glabrata23,30568.715.722,96882.910.0
    C. tropicalis15,54691.04.115,19889.55.4
    C. parapsilosis12,78893.23.612,45397.01.8
    C. krusei5,0798.678.35,00583.27.6
    C. guilliermondii1,41073.511.41,37590.55.7
    C. lusitaniae1,23392.15.41,21596.72.0
    C. kefyr1,04496.52.71,03298.70.9
    C. inconspicua56622.653.256390.63.9
    C. famata62279.110.360690.35.0
    C. rugosa60349.941.858069.321.2
    C. dubliniensis31096.12.630898.41.0
    C. norvegensis24841.940.724791.54.0
    C. lipolytica13066.228.512877.314.1
    C. sake8785.111.58792.06.9
    C. pelliculosa8789.76.98694.24.7
    C. apicola5798.21.85798.21.8
    C. zeylanoides7067.124.36785.16.0
    C. valida2123.861.92281.813.6
    C. intermedia2495.84.225100.00.0
    C. pulcherrima14100.00.014100.00.0
    C. haemulonii988.911.1988.911.1
    C. stellatoidea785.70.0785.714.3
    C. utilis683.30.07100.00.0
    C. humicola650.050.0650.033.3
    C. lambica50.080.0540.020
    C. ciferrii250.050.0250.00.0
    C. colliculosa2100.00.02100.00.0
    C. holmii1100.00.01100.00.0
    C. marina10.00.01100.00.0
    C. sphaerica1100.00.01100.00.0
    Candida spp.c9,74486.28.99,57793.64.1
    • ↵a Isolates were obtained from 133 institutions, 2001 to 2007.

    • ↵b Fluconazole and voriconazole disk diffusion testing was performed in accordance with CLSI document M44-A (7). The interpretive breakpoints (zone diameters) were as follows: S, ≥19 mm (fluconazole) and ≥17 mm (voriconazole); R, ≤14 mm (fluconazole) and ≤13 mm (voriconazole).

    • ↵c Candida species, not otherwise specified.

  • TABLE 4.

    In vitro susceptibilities of fluconazole-resistant isolates of Candida spp. to voriconazole as determined by CLSI disk diffusion testinga

    SpeciesNo. of isolates tested% S% SDD% R
    C. albicans1,78228.18.463.6
    C. glabrata3,55019.121.759.2
    C. tropicalis62917.015.367.7
    C. parapsilosis43139.220.440.4
    C. krusei3,88979.611.39.2
    C. guilliermondii15743.916.639.5
    C. lusitaniae6355.617.527.0
    C. kefyr2766.77.425.9
    C. inconspicua29783.810.16.1
    C. famata6237.124.238.7
    C. rugosa24228.121.550.4
    C. dubliniensis862.50.037.5
    C. norvegensis10081.010.09.0
    C. lipolytica3729.727.043.2
    C. sake944.411.144.4
    C. pelliculosa616.716.766.7
    C. apicola10.00.0100.0
    C. zeylanoides1546.726.726.7
    C. valida1471.47.121.4
    C. intermedia1100.00.00.0
    C. haemulonii10.00.0100.0
    C. humicola30.033.366.7
    C. lambica425.050.025.0
    C. ciferrii10.0100.00.0
    Candida spp.b85047.614.637.8
    • ↵a Isolates obtained from 133 institutions, 2001 to 2007. The zone diameters for voriconazole disk diffusion susceptibility categories were as follows: S, ≥17 mm; SDD, 14 to 16 mm; R, ≤13 mm.

    • ↵b Candida species not otherwise identified.

  • TABLE 5.

    Trends in in vitro resistance to fluconazole among Candida spp. as determined by CLSI disk diffusion testing over a 10.5-year perioda,b

    Species1997-20002001-20042005-2007
    No. of isolates tested% RNo. of isolates tested% RNo. of isolates tested% R
    C. albicans39,1520.971,0271.457,5981.4
    C. glabrata5,63419.212,96315.910,34215.4
    C. tropicalis2,9963.68,4964.57,0503.6
    C. parapsilosis2,6332.57,7833.55,0053.6
    C. krusei1,20765.82,84077.52,23979.3
    C. guilliermondii36712.59029.950814.2
    C. lusitaniae2762.96744.35596.6
    C. kefyr1823.35273.65171.7
    C. inconspicua955.627652.229054.1
    C. famata12317.137512.52476.9
    C. rugosa3534.323850.713410.4
    C. dubliniensis10.01132.71972.0
    C. norvegensis1154.513536.311346.0
    C. lipolytica70.08037.55014.0
    C. sake2010.06711.9
    C. pelliculosa10.0470.04015.0
    C. apicola571.8
    C. zeylanoides40.05028.02015.0
    C. valida966.71258.3
    C. intermedia100.0147.1
    C. pulcherrima60.080.0
    C. haemulonii60.0333.3
    C. stellatoidea70.0
    C. utilis60.0
    C. humicola250.0450.0
    C. lambica580.0
    C. ciferrii250.0
    C. colliculosa20.0
    C. holmii10.0
    C. marina10.0
    C. sphaerica10.0
    Candida spp.c2,59110.56,1868.23,55810.1
    • ↵a Includes all specimen types and all hospital locations in 141 institutions.

    • ↵b % R, percent resistant (zone diameter, ≤14 mm).

    • ↵c Candida species not otherwise identified.

  • TABLE 6.

    Trends in in vitro resistance to voriconazole among Candida spp. as determined by CLSI disk diffusion testing over a 7-year perioda,b

    Species2001-2004200520062007
    No. of isolates tested% RNo. of isolates tested% RNo. of isolates tested% RNo. of isolates tested% R
    C. albicans68,5751.218,6301.518,9651.019,7951.0
    C. glabrata12,64310.33,1859.53,41310.23,7279.4
    C. tropicalis8,1716.12,1364.52,3173.82,5745.1
    C. parapsilosis7,4641.81,5811.91,7241.31,6871.8
    C. krusei2,7657.76847.97426.58148.0
    C. guilliermondii8724.91846.51559.71645.5
    C. lusitaniae6551.81633.11950.52023.0
    C. kefyr5140.81732.91530.01920.0
    C. inconspicua2745.5772.6892.21232.4
    C. famata3596.4871.1721.4885.7
    C. rugosa44626.7333.0380.0634.8
    C. dubliniensis1110.9570.0701.4701.4
    C. norvegensis1342.2360.04710.4296.9
    C. lipolytica7917.7170.01414.31811.1
    C. sake200.0137.72711.1277.4
    C. pelliculosa470.01414.3195.3616.7
    C. apicola442.3130.0
    C. zeylanoides488.370.020.0100.0
    C. valida911.1728.610.050.0
    C. intermedia100.080.030.040.0
    C. pulcherrima60.020.040.020.0
    C. haemulonii60.0250.010.0
    C. stellatoidea714.3
    C. utilis10.020.040.0
    C. humicola250.0250.020.0
    C. lambica20.0333.3
    C. ciferrii10.010.0
    C. colliculosa10.010.0
    C. holmii10.0
    C. marina10.0
    C. sphaerica10.0
    Candida spp.c6,0224.71,1834.91,0312.41,3412.0
    • ↵a Isolates were obtained from 133 institutions.

    • ↵b % R, percent resistant (zone diameter, ≤13 mm).

    • ↵c Candida species not otherwise identified.

  • TABLE 7.

    Geographic variation in the in vitro susceptibilities of common and uncommon species of Candida to fluconazole and voriconazole, 2001 to 2007a

    SpeciesAntifungal agentAPACEUAF/MELAMNAM
    No. of isolates% RNo. of isolates% RNo. of isolates% RNo. of isolates% RNo. of isolates% R
    C. albicansFluconazole28,7810.974,4081.35,5390.614,1782.15,7185.1
    Voriconazole27,8270.872,8731.15,5020.313,7111.75,6813.6
    C. glabrataFluconazole5,62913.012,43916.372816.22,03915.12,47019.5
    Voriconazole5,5158.212,2889.87058.12,00011.32,46014.6
    C. tropicalisFluconazole5,1786.55,3492.95442.63,6252.68504.4
    Voriconazole5,0628.45,1283.95422.43,5223.78365.3
    C. parapsilosisFluconazole3,2944.34,5782.649915.02,8302.11,5873.5
    Voriconazole3,1201.74,4871.149611.12,7790.91,5172.4
    C. kruseiFluconazole53273.53,67880.813472.437066.836174.0
    Voriconazole5165.03,6377.71344.535114.03635.5
    C. guilliermondiiFluconazole17813.556713.8128.35909.0637.9
    Voriconazole17510.95586.1120.05673.7634.8
    C. inconspicuaFluconazole425.055853.02100.02100.0
    Voriconazole40.05553.8250.020.0
    C. rugosaFluconazole16532.18910.110.033955.5922.2
    Voriconazole1456.9871.110.033832.8911.1
    C. norvegensisFluconazole714.320449.010.0130.0210.0
    Voriconazole70.02034.910.0130.0210.0
    • ↵a For definitions of abbreviations, see Table 2, footnote b.

  • TABLE 8.

    Susceptibilities of C. krusei, C. inconspicua, and C. norvegensis to fluconazole and voriconazole by clinical servicea

    Clinical service (total no. of isolates)Antifungal agentC. kruseiC. inconspicuaC. norvegensis
    No. of isolates tested% RbNo. of isolates tested% RNo. of isolates tested% R
    Hematology-oncology (11,930)Fluconazole75783.111351.32450.0
    Voriconazole7419.61135.3244.2
    Medical (47,024)Fluconazole1,12879.910142.66833.8
    Voriconazole1,1067.81014.0682.9
    Surgical (12,659)Fluconazole31678.56261.32528.0
    Voriconazole3205.6621.6250.0
    ICU (27,758)Fluconazole70679.07850.02642.3
    Voriconazole6926.6762.6260.0
    Dermatology (3,001)Fluconazole3271.9475.020.0
    Voriconazole316.5450.020.0
    Urology (1,954)Fluconazole4060.0425.0683.3
    Voriconazole407.540.0616.7
    Outpatient (15,810)Fluconazole21274.51723.52334.8
    Voriconazole21310.3175.9220.0
    Other NOS (81,517)Fluconazole1,88875.918761.57447.3
    Voriconazole1,8627.01863.2748.1
    • ↵a Isolates were obtained from 133 institutions.

    • ↵b % R, percent resistant (zone diameter, ≤14 mm [fluconazole] and ≤13 mm [voriconazole]).

  • TABLE 9.

    Susceptibilities of C. krusei, C. inconspicua, and C. norvegensis to fluconazole and voriconazole by specimen typea

    Specimen type/site (total no. of isolates)Antifungal agentC. kruseiC. inconspicuaC. norvegensis
    No. of isolates tested% RbNo. of isolates tested% RNo. of isolates tested% R
    Blood (20,704)Fluconazole45974.52437.5137.7
    Voriconazole4598.5244.2130.0
    NSBF (8,650)Fluconazole24680.54551.11855.6
    Voriconazole2434.5454.4180.0
    Urine (25,881)Fluconazole51880.12653.82356.5
    Voriconazole51611.4267.7238.7
    Respiratory tract (56,961)Fluconazole1,78779.223151.56442.2
    Voriconazole1,7607.82292.2631.6
    Skin/soft tissue (11,221)Fluconazole25281.72326.1238.7
    Voriconazole2518.0234.3230.0
    Genital tract (44,839)Fluconazole56671.96262.91952.6
    Voriconazole5536.9624.8190.0
    Miscellaneous NOS (33,397)Fluconazole1,25179.215558.78843.2
    Voriconazole1,2235.81545.2888.0
    • ↵a Isolates were obtained from 133 institutions.

    • ↵b % R, percent resistant (zone diameter, ≤14 mm [fluconazole] and ≤13 mm [voriconazole]).

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Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: a 10.5-Year Analysis of Susceptibilities of Candida Species to Fluconazole and Voriconazole as Determined by CLSI Standardized Disk Diffusion
M. A. Pfaller, D. J. Diekema, D. L. Gibbs, V. A. Newell, D. Ellis, V. Tullio, A. Rodloff, W. Fu, T. A. Ling and the Global Antifungal Surveillance Group
Journal of Clinical Microbiology Mar 2010, 48 (4) 1366-1377; DOI: 10.1128/JCM.02117-09

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Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: a 10.5-Year Analysis of Susceptibilities of Candida Species to Fluconazole and Voriconazole as Determined by CLSI Standardized Disk Diffusion
M. A. Pfaller, D. J. Diekema, D. L. Gibbs, V. A. Newell, D. Ellis, V. Tullio, A. Rodloff, W. Fu, T. A. Ling and the Global Antifungal Surveillance Group
Journal of Clinical Microbiology Mar 2010, 48 (4) 1366-1377; DOI: 10.1128/JCM.02117-09
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