This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Diekema, D. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Diekema, D. J.

 Previous Article  |  Next Article 

Journal of Clinical Microbiology, October 2005, p. 5208-5213, Vol. 43, No. 10
0095-1137/05/$08.00+0     doi:10.1128/JCM.43.10.5208-5213.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Comparison of Results of Voriconazole Disk Diffusion Testing for Candida Species with Results from a Central Reference Laboratory in the ARTEMIS Global Antifungal Surveillance Program

M. A. Pfaller,1,2* L. Boyken,1 S. A. Messer,1 S. Tendolkar,1 R. J. Hollis,1 and D. J. Diekema1,3

Departments of Pathology,1 Epidemiology,2 Medicine, Roy J. and Lucille A. Carver College of Medicine and College of Public Health, University of Iowa, Iowa City, Iowa 522423

Received 16 May 2005/ Returned for modification 20 June 2005/ Accepted 18 July 2005


arrow
ABSTRACT
 
The accuracy of antifungal susceptibility testing is important for reliable resistance surveillance and for the clinical management of patients with serious infections. Our primary objective was to compare the results of voriconazole disk diffusion testing of Candida spp. performed by centers participating in the ARTEMIS program with disk diffusion and MIC results obtained by the central reference laboratory. A total of 2,934 isolates of Candida spp. were tested by CLSI disk diffusion and reference broth microdilution methods in the central reference laboratory. These results were compared to the results of disk diffusion testing performed in the 54 participating centers. All tests were performed and interpreted following CLSI recommendations, as follows: susceptible (S), MIC of ≤1 µg/ml (≥17 mm); susceptible dose dependent (SDD), MIC of 2 µg/ml (14 to 16 mm); and resistant (R), MIC of ≥4 µg/ml (≤13 mm). The overall categorical agreement between participant disk diffusion test results and reference laboratory MIC results was 94.1%, with 0.1% very major errors (VME) and 3.4% major errors (ME). The categorical agreement between disk diffusion test results obtained in the reference laboratory and the MIC test results was 99.0%. Likewise, good agreement was observed between participant disk diffusion test results and reference laboratory disk diffusion test results, with an agreement of 93.8%, 0.2% VME, and 3.4% ME. The disk diffusion test was reliable for detecting those isolates of Candida spp. that were characterized as resistant (MIC of ≥4 µg/ml) by MIC testing. External quality assurance data obtained by surveillance programs such as the ARTEMIS Global Antifungal Surveillance Program ensure the generation of useful surveillance data and result in the continued improvement of antifungal susceptibility testing practices.


arrow
INTRODUCTION
 
One of the important by-products of the standardization of antifungal susceptibility testing methods has been the ability to conduct active surveillance of resistance to antifungal agents (12, 17, 18, 21, 23, 24). Meaningful large-scale studies of antifungal susceptibility and resistance conducted over time would not be possible without a standardized microdilution method for performing in vitro studies (6, 22-24). Many such studies have now been published and include studies of isolates from patients in intensive care units (4, 16, 25) and of nosocomial bloodstream infections (BSI) in the United States and other countries worldwide (1, 5-8, 14, 15, 21, 23, 24, 30, 32, 33). Furthermore, studies of resistance trends to commonly used antifungal agents such as fluconazole (1, 5-8, 10, 14, 21, 23, 24, 35) and comparative analyses of newly licensed and established antifungal agents (9, 10, 18, 21, 25-31) have provided large amounts of useful data and have been greatly facilitated by a standardized microdilution method (19).

In addition to broth microdilution (BMD) MIC determination methods, disk diffusion testing of fluconazole and voriconazole activities against Candida spp. has been developed and standardized in order to provide a simple inexpensive method for monitoring susceptibilities to these agents in a variety of laboratory settings (3, 12, 15, 17, 20, 30, 31). The Clinical and Laboratory Standards Institute (CLSI; formerly the NCCLS) M44-A agar disk diffusion method (20) has been used for more than 4 years to monitor the susceptibility of Candida spp. to fluconazole and voriconazole as part of the ARTEMIS Global Antifungal Surveillance Program (12, 17, 34, 36). In the ARTEMIS program, fluconazole and voriconazole disk diffusion testing is performed in accordance with CLSI M44-A in more than 120 laboratories in 39 countries (ARTEMIS DISK Surveillance Study), and the data are used to follow trends in fluconazole and voriconazole susceptibility patterns worldwide (12, 17, 36). In addition to on-site testing, BSI isolates of Candida spp. collected by ARTEMIS participants are sent to a central reference laboratory at the University of Iowa for confirmatory testing using CLSI disk diffusion and BMD methods (30, 31, 34). Data generated from this program have been useful for documenting the sustained activities of both fluconazole and voriconazole against clinical isolates of Candida (12, 17, 30, 34, 36).

Although the ARTEMIS DISK Surveillance Study (12, 17, 36) generates massive amounts of data, it is recognized that despite the use of a standard protocol, any surveillance system based on susceptibility tests performed by the participating laboratories must include some measure of quality assurance, beyond simple quality control testing, in order to provide an independent assessment of laboratory performance and a validation of results generated from the various laboratories (13, 34, 37). As such, we have recently documented a good agreement between ARTEMIS participant disk diffusion results for fluconazole and reference laboratory disk diffusion and BMD MIC test results (34). In the present study, we assess the accuracy of the ARTEMIS participant voriconazole disk diffusion results by comparing them to those obtained for the same isolates tested in the central reference laboratory by disk diffusion and BMD methods recommended by the CLSI.


arrow
MATERIALS AND METHODS
 
Study design. The ARTEMIS program was established to monitor the species and antifungal susceptibility patterns of Candida spp. isolated from clinically significant sites of infection (e.g., blood and normally sterile sites [NSSI]) via a broad network of sentinel laboratories in North America, Latin America, Europe, Africa, and Asia. Candida spp. causing invasive disease (in blood and NSSI) and the accompanying voriconazole disk zone diameters were reported from 54 different medical centers in 2001 and 2002.

Each participant medical center contributed results (organism identification and voriconazole disk zone diameters) for consecutive blood and NSSI culture isolates (one isolate per patient) of Candida spp. judged to be clinically significant by local criteria and detected in each calendar month during the study. All isolates were saved on agar slants and were sent to the University of Iowa College of Medicine (Iowa City) for storage and further characterization by reference identification methods and susceptibility testing (11, 19, 20). In the central reference laboratory, isolates were tested by both CLSI disk diffusion (20) and BMD (19) methods.

Organism identification. All Candida sp. isolates were identified at participating institutions by the routine method used in each laboratory. Upon receipt at the University of Iowa, the isolates were subcultured onto potato dextrose agar (Remel, Lenexa, Kans.) and CHROMagar Candida medium (Hardy Laboratories, Santa Maria, Calif.) to ensure their viability and purity. Confirmation of the species identification was performed with Vitek and API products (bioMérieux, St. Louis, Mo.), as recommended by the manufacturer, or by conventional methods as required (11). Isolates were stored as suspensions in water or on agar slants at ambient temperature until needed.

Susceptibility testing. Disk diffusion testing of voriconazole was performed in both participant laboratories and the central reference laboratory according to the methods described in CLSI document M44-A (20). MIC testing was performed by the CLSI BMD reference method M27-A2 (19). Standard voriconazole reference powder was obtained from Pfizer Pharmaceuticals (Groton, Conn.), and 1-µg voriconazole disks were obtained from Becton Dickinson (Sparks, Md.).

Disk diffusion testing of voriconazole was performed as described by Hazen et al. (12) and in CLSI document M44-A (20). Agar plates (150-mm diameter) containing Mueller-Hinton agar supplemented with 2% glucose and 0.5 µg of methylene blue per ml at a depth of 4.0 mm were used. The agar surface was inoculated by using a swab dipped in a cell suspension adjusted to the turbidity of a 0.5 McFarland standard. The plates were incubated in air at 35 to 37°C and read at 18 to 24 h. Zone diameter end points were read at 80% growth inhibition by using the BIOMIC image analysis plate reader system (version 5.9; Giles Scientific, Santa Barbara, Calif.) (10, 30).

MIC interpretive criteria for voriconazole were those approved by CLSI (Minutes of CLSI Antifungal Subcommittee Meeting, 2005), as follows: susceptible, MIC of ≤1 µg/ml; susceptible dose dependent, MIC of 2 µg/ml; and resistant, MIC of ≥4 µg/ml. The interpretive criteria for the voriconazole disk diffusion test were those used by CLSI (Minutes of CLSI Antifungal Subcommittee Meeting, 2005), as follows: susceptible, zone diameter of ≥17 mm; susceptible dose dependent, zone diameter of 14 to 16 mm; and resistant, zone diameter of ≤13 mm.

Quality control. Quality control was performed in accordance with CLSI documents M27-A2 (19) and M44-A (20) by using Candida krusei ATCC 6258 and C. parapsilosis ATCC 22019 (2, 19, 20).

Analysis of results. The diameters of the zones of inhibition (in millimeters) surrounding the voriconazole disks after 24 h of incubation obtained in the participant laboratories and in the reference laboratory were plotted against their respective BMD MICs read at 48 h (Fig. 1 and 2) (3, 30, 34). Similarly, the diameters of the zones of inhibition surrounding the voriconazole disks after 24 h of incubation obtained in the participant laboratories were plotted against their respective zones obtained in the reference laboratory at 24 h. The interpretive breakpoints recently approved by CLSI (Minutes of the CLSI Antifungal Subcommittee Meeting, 2005) were used to determine the categorical agreement between disk diffusion and BMD MIC results and between participant and reference disk diffusion results. Major errors (ME) were classified as resistant by disk diffusion (participant or central laboratory) and susceptible by BMD or resistant by the participant disk diffusion test and susceptible by the central laboratory disk diffusion test. Very major errors (VME) were classified as susceptible by the participant or central laboratory disk diffusion test and resistant by BMD or susceptible by the participant disk diffusion test and resistant by the central laboratory disk diffusion test. Minor errors (M) occurred when the result of one of the tests was susceptible or resistant and that of the other test was susceptible dose dependent.



View larger version (16K):
[in this window]
[in a new window]
  		FIG. 1. Zones of inhibition around 1-µg/ml voriconazole disks tested in ARTEMIS participating laboratories plotted against the MICs determined at 48 h by using the reference BMD method for 2,934 isolates of Candida spp. The numbers represent the number of results (isolates) for each data point, and the dotted line is the regression line.



View larger version (16K):
[in this window]
[in a new window]
  		FIG. 2. Zones of inhibition around 1-µg/ml voriconazole disks tested in the ARTEMIS central reference laboratory plotted against the MICs determined at 48 h by using the reference BMD method for 2,934 isolates of Candida spp. The numbers represent the number of results (isolates) for each data point, and the dotted line is the regression line.


arrow
RESULTS AND DISCUSSION
 
During the 2001-2002 study period, a total of 2,934 isolates of Candida spp. from blood and other NSSI and their accompanying voriconazole disk diffusion zone diameters were submitted from 54 participating centers in North America (8 centers), Latin America (12 centers), Europe (20 centers), and the Asia-Pacific region (14 centers). The frequencies of infections due to the various species of Candida identified in the central reference laboratory are presented in Table 1 and represent a total of 14 different species.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Isolates of Candida spp. tested by participant and reference laboratories in the ARTEMIS Global Antifungal Surveillance Program

In vitro susceptibility testing performed in both participant laboratories (disk diffusion test) and the reference laboratory (disk diffusion and MIC tests) indicated that resistance to voriconazole was very uncommon among isolates of Candida from blood and NSSI (Table 2). As seen in our previous study with fluconazole (34), more isolates of all species appeared resistant to voriconazole by disk diffusion testing in both participant and reference laboratories, with the greatest resistance observed with disk diffusion testing performed in participant laboratories (Table 2). Overall, the level of categorical agreement between the disk diffusion test results and the reference MIC results was excellent in both participant (94.1%) and reference (99.0%) laboratories (Table 2), exceeding the levels reported previously for fluconazole (87.4% and 92.8%, respectively) (34). Although resistant isolates were uncommon, it is important that there were very few VME, indicating that the disk diffusion test was reliable for detecting isolates resistant to voriconazole by MIC testing (MIC, ≥4 µg/ml). The level of agreement between disk diffusion and MIC results was highest for C. albicans and lowest for C. glabrata and C. tropicalis. The decreased level of agreement with C. glabrata and C. tropicalis was largely due to false-resistant disk diffusion results (ME) reported by the participant laboratories.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Interpretive agreement between results of voriconazole disk diffusion tests and of standard 48-h BMDa

A similar level of agreement was seen when disk diffusion results obtained in the participant laboratories were compared with those obtained in the reference laboratory (Table 3). The overall categorical agreement was excellent, at 93.8%, and the number of VME, ME, and M was very low. As with the comparison to BMD testing, agreement was highest for C. albicans and lowest for C. glabrata and C. tropicalis, with most of the errors in the ME category.


View this table:
[in this window]
[in a new window]
  		TABLE 3. Overall interpretive agreement between results of voriconazole disk diffusion tests performed in participant and reference laboratoriesa

Over 99% of the quality control tests at participating ARTEMIS centers were in control.

Taken together with our previous study of fluconazole disk testing (34), this study constitutes the largest available body of data validating the performance of disk diffusion testing in surveillance program participant laboratories. We demonstrate that in addition to fluconazole testing, voriconazole disk diffusion testing using the CLSI M44-A method can be performed with a high degree of accuracy in more than 50 laboratories worldwide. The participant results were validated not only by voriconazole disk diffusion testing performed in the central reference laboratory but also by reference BMD MIC testing. The data reported herein also represent the first application of the newly approved disk zone and MIC interpretive criteria for voriconazole and document the very low level of resistance to this agent among a large group of clinically significant isolates of Candida.

In summary, we have shown that voriconazole disk diffusion testing performed in accordance with the CLSI M44-A method can be performed with a high degree of accuracy in a wide range of laboratory settings throughout the world. The test was reliable in identifying those strains of Candida characterized as resistant by reference BMD MIC testing. As seen with fluconazole, false-resistant results may be an issue with C. glabrata and other non-C. albicans species. Further assessment of such isolates by BMD should be performed if clinically indicated. This external validation of antifungal susceptibility testing results is an important component of the ARTEMIS Global Antifungal Surveillance Program and ensures the generation of useful antifungal surveillance data and the continued improvement of antifungal susceptibility testing practices.


arrow
ACKNOWLEDGMENTS
 
This study was supported in part by research and educational grants from Pfizer Inc., Pfizer Global Pharmaceuticals, New York, N.Y.

We thank Linda Elliott for secretarial assistance with the preparation of the manuscript. We appreciate the participation of all ARTEMIS site participants. A list of ARTEMIS participants can be found at the following website: http://www.medicine.uiowa.edu/pathology /path_folder/research/acknowledgements/artemis_participants.pdf.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Medical Microbiology Division, C606 GH, Department of Pathology, University of Iowa College of Medicine, Iowa City, IA 52242. Phone: (319) 384-9566. Fax: (319) 356-4916. E-mail: michael-pfaller{at}uiowa.edu. Back


arrow
REFERENCES
 
    1
  1. Asmundsdottir, L. R., H. Erlendsdottir, and M. Gottfredsson. 2002. Increasing incidence of candidemia: results from a 20-year nationwide study in Iceland. J. Clin. Microbiol. 40:3489-3492.[Abstract/Free Full Text]
    2. 2
  2. Barry, A. L., M. A. Pfaller, S. D. Brown, A. Espinel-Ingroff, M. A. Ghannoum, C. Knapp, R. P. Rennie, J. H. Rex, and M. G. Rinaldi. 2000. Quality control limits for broth microdilution susceptibility tests of ten antifungal agents. J. Clin. Microbiol. 38:3457-3459.[Abstract/Free Full Text]
    3. 3
  3. Barry, A. L., M. A. Pfaller, R. P. Rennie, P. C. Fuchs, and S. D. Brown. 2002. Precision and accuracy of fluconazole susceptibility tests by broth microdilution, Etest, and disk diffusion methods. Antimicrob. Agents Chemother. 46:1781-1784.[Abstract/Free Full Text]
    4. 4
  4. Blumberg, H. M., W. R. Jarvis, J. M. Soucie, J. E. Edwards, J. E. Patterson, M. A. Pfaller, M. S. Rangel-Frausto, M. G. Rinaldi, L. Saiman, R. T. Wiblin, and R. P. Wenzel. 2001. Risk factors for candidal bloodstream infections in surgical intensive care unit patients: the NEMIS prospective multicenter study. Clin. Infect. Dis. 33:177-186.[CrossRef][Medline]
    5. 5
  5. Brandt, M. E., M. A. Pfaller, R. A. Hajjeh, R. J. Hamill, P. G. Pappas, A. L. Reingold, D. Rimland, D. E. Warnock, and the Cryptococcal Disease Active Surveillance Project. 2001. Trends in antifungal drug susceptibility of Cryptococcus neoformans isolates in the United States: 1992 to 1994 and 1996 to 1998. Antimicrob. Agents Chemother. 45:3065-3069.[Abstract/Free Full Text]
    6. 6
  6. Chen, Y.-C., S.-C. Chang, K.-T. Luh, and W.-C. Hsieh. 2003. Stable susceptibility of Candida blood isolates to fluconazole despite increasing use during the past 10 years. J. Antimicrob. Chemother. 52:71-77.[Abstract/Free Full Text]
    7. 7
  7. Cuenca-Estrella, M., L. Rodero, G. Garcia-Effron, and J. L. Rodriguez-Tudela. 2002. Antifungal susceptibility of Candida spp. isolated from blood in Spain and Argentina, 1996-1999. J. Antimicrob. Chemother. 49:981-987.[Abstract/Free Full Text]
    8. 8
  8. Datta, K., N. Jain, S. Sethi, A. Rattan, A. Casadeval, and U. Banerjee. 2003. Fluconazole and itraconazole susceptibility of clinical isolates of Cryptococcus neoformans at a testing care center in India: a need for care. J. Antimicrob. Chemother. 52:683-686.[Abstract/Free Full Text]
    9. 9
  9. Diekema, D. J., S. A. Messer, R. J. Hollis, R. N. Jones, and M. A. Pfaller. 2003. Activities of caspofungin, itraconazole, posaconazole, ravuconazole, voriconazole, and amphotericin B against 448 recent clinical isolates of filamentous fungi. J. Clin. Microbiol. 41:3623-3626.[Abstract/Free Full Text]
    10. 10
  10. Hajjeh, R. A., A. N. Sofair, L. H. Harrison, G. M. Lyon, B. A. Arthington-Skaggs, S. A. Mirza, M. Phelan, J. Morgan, W. Lee-Yang, M. A. Ciblak, L. E. Benjamin, L. T. Sanza, S. Huie, S. F. Yeo, M. E. Brandt, and D. W. Warnock. 2004. Incidence of bloodstream infection 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. 42:1519-1527.[Abstract/Free Full Text]
    11. 11
  11. Hazen, K. C., and S. A. Howell. 2003. Candida, Cryptococcus, and other yeasts of medical importance, p. 1693-1711. In P. R. Murray, E. J. Baron, J. H. Jorgensen, M. A. Pfaller, and R. H. Yolken (ed.), Manual of clinical microbiology, 8th ed. ASM Press, Washington, D.C.
    12. 12
  12. Hazen, K. C., E. J. Baron, A. L. Colombo, C. Girmenia, A. Sanchez-Sousa, A. del Palacio, C. de Bedout, D. L. Gibbs, and The Global Antifungal Surveillance Group. 2003. Comparison of the susceptibilities of Candida spp. to fluconazole and voriconazole in a 4-year global evaluation using disk diffusion. J. Clin. Microbiol. 41:5623-5632.[Abstract/Free Full Text]
    13. 13
  13. Kahlmeter, G., and D. F. J. Brown. 2002. Resistance surveillance studies—comparability of results and quality assurance of methods. J. Antimicrob. Chemother. 50:775-777.[Free Full Text]
    14. 14
  14. Kibbler, C. C., S. Seaton, R. A. Barnes, W. R. Grandsen, R. E. Holliman, E. M. Johnson, J. D. Perry, D. J. Sullivan, and J. A. Wilson. 2003. Management and outcome of bloodstream infections due to Candida species in England and Wales. J. Hosp. Infect. 54:18-24.[CrossRef][Medline]
    15. 15
  15. Lee, S.-C., C.-P. Fung, N. Lee, L.-C. See, J.-S. Huang, C.-J. Tsai, K.-S. Chen, and W.-B. Shieh. 2001. Fluconazole disk diffusion test with methylene blue- and glucose-enriched Mueller-Hinton agar for determining susceptibility of Candida species. J. Clin. Microbiol. 39:1615-1617.[Abstract/Free Full Text]
    16. 16
  16. Leone, M., J. Albanese, A. Michel-Nguyen, M.-C. Blanc-Bimar, and C. Martin. 2003. Long-term epidemiological survey of Candida species: comparison of isolates found in an intensive care unit and in conventional wards. J. Hosp. Infect. 55:169-174.[Medline]
    17. 17
  17. Meis, J., M. Petrore, J. Bille, D. Ellis, D. Gibbs, and the Global Antifungal Surveillance Group. 2000. A global evaluation of the susceptibility of Candida species to fluconazole by disk diffusion. Diagn. Microbiol. Infect. Dis. 36:215-223.[CrossRef][Medline]
    18. 18
  18. Messer, S. A., J. T. Kirby, H. S. Sader, T. R. Fritsche, and R. N. Jones. 2004. Initial results from a longitudinal international surveillance programme for anidulafungin. J. Antimicrob. Chemother. 54:1051-1056.[Abstract/Free Full Text]
    19. 19
  19. National Committee for Clinical Laboratory Standards. 2002. Reference method for broth dilution testing of yeasts: approved standard, 2nd ed., M27-A2. National Committee for Clinical Laboratory Standards, Wayne, Pa.
    20. 20
  20. National Committee for Clinical Laboratory Standards. 2004. Method for antifungal disk diffusion susceptibility testing of yeasts: approved guideline M44-A. National Committee for Clinical Laboratory Standards, Wayne, Pa.
    21. 21
  21. Ostrosky-Zeichner, L., J. H. Rex, R. G. Pappas, R. J. Hamil, R. A. Larsen, H. W. Horowitz, W. G. Powerly, N. Hyslop, C. A. Kauffman, J. Cleary, J. E. Mangino, and J. Lee. 2003. Antifungal susceptibility survey of 2,000 bloodstream Candida isolates in the United States. Antimicrob. Agents Chemother. 47:3149-3154.[Abstract/Free Full Text]
    22. 22
  22. Pfaller, M. A., and W. L. Yu. 2001. Antifungal susceptibility testing: new technology and clinical applications. Infect. Dis. Clin. N. Am. 15:1227-1261.[CrossRef][Medline]
    23. 23
  23. Pfaller, M. A., and D. J. Diekema. 2002. Role of sentinel surveillance of candidemia: trends in species distribution and antifungal susceptibility. J. Clin. Microbiol. 40:3551-3557.[Free Full Text]
    24. 24
  24. Pfaller, M. A., and D. J. Diekema. 2004. Twelve years of fluconazole in clinical practice: global trends in species distribution and fluconazole susceptibility of bloodstream isolates of Candida. Clin. Microbiol. Infect. Dis. 10(Suppl. 1):11-23.
    25. 25
  25. Pfaller, M. A., D. J. Diekema, R. N. Jones, H. S. Sader, A. C. Fluit, R. J. Hollis, S. A. Messer, and The SENTRY Participant Group. 2001. International surveillance of bloodstream infections due to Candida species: frequency of occurrence and in vitro susceptibilities to fluconazole, ravuconazole, and voriconazole of isolates collected from 1997 through 1999 in the SENTRY Antimicrobial Surveillance Program. J. Clin. Microbiol. 39:3254-3259.[Abstract/Free Full Text]
    26. 26
  26. Pfaller, M. A., S. A. Messer, R. J. Hollis, and R. N. Jones. 2001. In vitro activities of posaconazole (Sch 56592) compared with those of itraconazole and fluconazole against 3,685 clinical isolates of Candida spp. and Cryptococcus neoformans. Antimicrob. Agents Chemother. 45:2862-2864.[Abstract/Free Full Text]
    27. 27
  27. Pfaller, M. A., S. A. Messer, L. Boyken, H. Huynh, R. J. Hollis, and D. J. Diekema. 2002. In vitro activities of 5-fluorocytosine against 8,830 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.[Abstract/Free Full Text]
    28. 28
  28. Pfaller, M. A., S. A. Messer, R. J. Hollis, R. N. Jones, and D. J. Diekema. 2002. In vitro activities of ravuconazole and voriconazole compared with those of four approved systemic antifungal agents against 6,970 clinical isolates of Candida spp. Antimicrob. Agents Chemother. 46:1723-1727.[Abstract/Free Full Text]
    29. 29
  29. Pfaller, M. A., D. J. Diekema, S. A. Messer, R. J. Hollis, and R. N. Jones. 2003. In vitro activities of caspofungin compared with those of fluconazole and itraconazole against 3,959 clinical isolates of Candida spp., including 157 fluconazole-resistant isolates. Antimicrob. Agents Chemother. 47:1068-1071.[Abstract/Free Full Text]
    30. 30
  30. Pfaller, M. A., D. J. Diekema, S. A. Messer, L. Boyken, and R. J. Hollis. 2003. Activities of fluconazole and voriconazole against 1,586 recent clinical isolates of Candida species determined by broth microdilution, disk diffusion, and Etest methods: report from the ARTEMIS Global Antifungal Susceptibility Program 2001. J. Clin. Microbiol. 41:1440-1446.[Abstract/Free Full Text]
    31. 31
  31. Pfaller, M. A., D. J. Diekema, L. Boyken, S. A. Messer, S. Tendolkar, and R. J. Hollis. 2003. Evaluation of the Etest and disk diffusion methods for determining susceptibilities of 235 bloodstream isolates of Candida glabrata to fluconazole and voriconazole. J. Clin. Microbiol. 41:1875-1880.[Abstract/Free Full Text]
    32. 32
  32. Pfaller, M. A., S. A. Messer, L. Boyken, C. Rice, S. Tendolkar, R. J. Hollis, and D. J. Diekema. 2004. In vitro susceptibility testing of caspofungin against Candida species: further standardization of broth microdilution methodology using an international collection of more than 3,000 clinical isolates. J. Clin. Microbiol. 42:3117-3119.[Abstract/Free Full Text]
    33. 33
  33. Pfaller, M. A., S. A. Messer, L. Boyken, R. J. Hollis, C. Rice, S. Tendolkar, and D. J. Diekema. 2004. In vitro activities of voriconazole, posaconazole, and fluconazole against 4,169 clinical isolates of Candida spp. and Cryptococcus neoformans collected during 2001 and 2002 in the ARTEMIS Global Antifungal Surveillance Program. Diagn. Microbiol. Infect. Dis. 48:201-205.[CrossRef][Medline]
    34. 34
  34. Pfaller, M. A., K. C. Hazen, S. A. Messer, L. Boyken, S. Tendolkar, R. J. Hollis, and D. J. Diekema. 2004. Comparison of results of fluconazole disk diffusion testing for Candida species with results from a central reference laboratory in the ARTEMIS Global Antifungal Surveillance Program. J. Clin. Microbiol. 42:3607-3612.[Abstract/Free Full Text]
    35. 35
  35. Pfaller, M. A., S. A. Messer, L. Boyken, C. Rice, S. Tendolkar, R. J. Hollis, G. V. Doern, and D. J. Diekema. 2005. Global trends in the antifungal susceptibility of Cryptococcus neoformans: 1990 to 2004. J. Clin. Microbiol. 43:2163-2167.[Abstract/Free Full Text]
    36. 36
  36. Pfaller, M. A., D. J. Diekema, M. G. Rinaldi, R. Barnes, B. Hu, A. V. Veselov, N. Tiraboschi, E. Nagy, D. L. Gibbs, and the Global Antifungal Surveillance Group. Results from the ARTEMIS DISK Global Antifungal Surveillance Study: a 6.5-year analysis of the worldwide susceptibility of yeasts to fluconazole and voriconazole using standardized disk diffusion testing. J. Clin. Microbiol., in press.
    37. 37
  37. Tenover, F. C., M. J. Mohammed, J. Stelling, T. O'Brien, and R. Williams. 2001. Ability of laboratories to detect emerging antimicrobial resistance: proficiency testing and quality control results from the World Health Organization's external quality assurance system for antimicrobial susceptibility testing. J. Clin. Microbiol. 39:241-250.[Abstract/Free Full Text]

Journal of Clinical Microbiology, October 2005, p. 5208-5213, Vol. 43, No. 10
0095-1137/05/$08.00+0     doi:10.1128/JCM.43.10.5208-5213.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Pfaller, M. A., Diekema, D. J., Gibbs, D. L., Newell, V. A., Bijie, H., Dzierzanowska, D., Klimko, N. N., Letscher-Bru, V., Lisalova, M., Muehlethaler, K., Rennison, C., Zaidi, M., the Global Antifungal Surveillance Group, (2009). Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2007: 10.5-Year Analysis of Susceptibilities of Noncandidal Yeast Species to Fluconazole and Voriconazole Determined by CLSI Standardized Disk Diffusion Testing. J. Clin. Microbiol. 47: 117-123 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J., Procop, G. W., Rinaldi, M. G. (2007). Multicenter Comparison of the VITEK 2 Antifungal Susceptibility Test with the CLSI Broth Microdilution Reference Method for Testing Amphotericin B, Flucytosine, and Voriconazole against Candida spp.. J. Clin. Microbiol. 45: 3522-3528 [Abstract] [Full Text]  
  • Milici, M. E., Maida, C. M., Spreghini, E., Ravazzolo, B., Oliveri, S., Scalise, G., Barchiesi, F. (2007). Comparison between Disk Diffusion and Microdilution Methods for Determining Susceptibility of Clinical Fungal Isolates to Caspofungin. J. Clin. Microbiol. 45: 3529-3533 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J., Gibbs, D. L., Newell, V. A., Meis, J. F., Gould, I. M., Fu, W., Colombo, A. L., Rodriguez-Noriega, E., and the Global Antifungal Surveillance Group, (2007). Results from the ARTEMIS DISK Global Antifungal Surveillance Study, 1997 to 2005: an 8.5-Year Analysis of Susceptibilities of Candida Species and Other Yeast Species to Fluconazole and Voriconazole Determined by CLSI Standardized Disk Diffusion Testing. J. Clin. Microbiol. 45: 1735-1745 [Abstract] [Full Text]  
  • Mokaddas, E. M., Al-Sweih, N. A., Khan, Z. U. (2007). Species distribution and antifungal susceptibility of Candida bloodstream isolates in Kuwait: a 10-year study. J Med Microbiol 56: 255-259 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J. (2007). Epidemiology of Invasive Candidiasis: a Persistent Public Health Problem. Clin. Microbiol. Rev. 20: 133-163 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J., Mendez, M., Kibbler, C., Erzsebet, P., Chang, S.-C., Gibbs, D. L., Newell, V. A., the Global Antifungal Surveillance Group, (2006). Candida guilliermondii, an Opportunistic Fungal Pathogen with Decreased Susceptibility to Fluconazole: Geographic and Temporal Trends from the ARTEMIS DISK Antifungal Surveillance Program.. J. Clin. Microbiol. 44: 3551-3556 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J., Colombo, A. L., Kibbler, C., Ng, K. P., Gibbs, D. L., Newell, V. A., the Global Antifungal Surveillance Group, (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 [Abstract] [Full Text]  
  • Posteraro, B., Tumbarello, M., La Sorda, M., Spanu, T., Trecarichi, E. M., De Bernardis, F., Scoppettuolo, G., Sanguinetti, M., Fadda, G. (2006). Azole Resistance of Candida glabrata in a Case of Recurrent Fungemia.. J. Clin. Microbiol. 44: 3046-3047 [Abstract] [Full Text]  
  • Girmenia, C., Pizzarelli, G., Cristini, F., Barchiesi, F., Spreghini, E., Scalise, G., Martino, P. (2006). Candida guilliermondii Fungemia in Patients with Hematologic Malignancies.. J. Clin. Microbiol. 44: 2458-2464 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J., Rex, J. H., Espinel-Ingroff, A., Johnson, E. M., Andes, D., Chaturvedi, V., Ghannoum, M. A, Odds, F. C., Rinaldi, M. G., Sheehan, D. J., Troke, P., Walsh, T. J., Warnock, D. W. (2006). Correlation of MIC with Outcome for Candida Species Tested against Voriconazole: Analysis and Proposal for Interpretive Breakpoints.. J. Clin. Microbiol. 44: 819-826 [Abstract] [Full Text]  
  • Pfaller, M. A., Diekema, D. J., Rinaldi, M. G., Barnes, R., Hu, B., Veselov, A. V., Tiraboschi, N., Nagy, E., Gibbs, D. L., the Global Antifungal Surveillance Group, (2005). Results from the ARTEMIS DISK Global Antifungal Surveillance Study: a 6.5-Year Analysis of Susceptibilities of Candida and Other Yeast Species to Fluconazole and Voriconazole by Standardized Disk Diffusion Testing. J. Clin. Microbiol. 43: 5848-5859 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Diekema, D. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pfaller, M. A.
Right arrow Articles by Diekema, D. J.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»