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Journal of Clinical Microbiology, October 2002, p. 3841-3844, Vol. 40, No. 10
0095-1137/02/$04.00+0     DOI: 10.1128/JCM.40.10.3841-3844.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Comparison of the Antifungal Susceptibility Testing Subcommittee of the European Committee on Antibiotic Susceptibility Testing Proposed Standard and the E-Test with the NCCLS Broth Microdilution Method for Voriconazole and Caspofungin Susceptibility Testing of Yeast Species

Erja Chryssanthou1* and Manuel Cuenca-Estrella2

Department of Clinical Microbiology, Karolinska Hospital, Stockholm, Sweden,1 Servicio de Micología, Centro Nacional de Microbiología, Instituto de Salud Carlos III, 28220 Majadahonda, Spain2

Received 25 February 2002/ Returned for modification 8 May 2002/ Accepted 28 June 2002


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ABSTRACT
 
The proposed standard of the Antifungal Susceptibility Testing Subcommittee of the European Committee on Antibiotic Susceptibility Testing (AFST-EUCAST) and the E-test procedures were compared with the NCCLS reference broth microdilution method for voriconazole and caspofungin susceptibility testing of 102 clinical Candida species and Saccharomyces cerevisiae isolates. The voriconazole MIC at which 50% of strains were inhibited (MIC50) was <=0.125 mg/liter for all yeast species except for Candida glabrata and Candida krusei, which yielded MIC50 values of 0.25 to 1 mg/liter depending on the method. Caspofungin exhibited in vitro activity (MIC50 of <=0.125 to 2 mg/liter) against all yeast species except for Candida guilliermondii. The agreements between MICs within ±2 dilutions obtained by the NCCLS method and the EUCAST standard were 97% for voriconazole and 96% for caspofungin. Intraclass correlation coefficients were statistically significant (P < 0.05). The agreements between voriconazole MICs provided by the E-test and the NCCLS and between the E-test and the AFST-EUCAST method were 100 and 90%, respectively. Because of lower caspofungin MICs provided by the E-test, the agreement was slightly poorer with the NCCLS method (89%) than with the AFST-EUCAST procedure (94%). Both the EUCAST and the E-test procedures can be reliable techniques for susceptibility testing of yeasts to voriconazole and caspofungin.


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TEXT
 
Voriconazole and caspofungin are two new antifungal agents presenting a broad spectrum of activity. These compounds are well tolerated and achieve significant activity in systemic diseases (7). Voriconazole is a new triazole derivative which is more lipid soluble than fluconazole. It has an improved activity against fluconazole-resistant Candida spp. In addition, it is active against Cryptococcus neoformans, emerging yeast pathogens, and dimorphic and filamentous fungi (5, 6, 9). It has been reported to be effective in the treatment of candidosis and acute aspergillosis and could be a suitable alternative for empirical antifungal therapy in patients with neutropenia and persistent fever (7, 18). Voriconazole can be given orally or intravenously and will be available for clinical practice shortly. The echinocandin lipopeptide caspofungin belongs to a new class of antifungal compounds that inhibit the synthesis of 1,3-ß-D-glucan, a major component of the cell wall of fungi (12). Caspofungin is active against Candida spp., Aspergillus spp., some other molds, and Pneumocystis carinii (8). It has been approved recently by the U.S. Food and Drug Administration for the parenteral treatment of invasive aspergillosis in patients who are refractory to or intolerant of other therapies. Phase III clinical trials in patients with candidemia and in persistently febrile neutropenic patients requiring empirical antifungal therapy are ongoing (11).

The Antifungal Susceptibility Testing Subcommittee of the European Committee on Antibiotic Susceptibility Testing (AFST-EUCAST) has proposed a standard for the determination of MICs by broth dilution of fermentative yeasts (17). The proposed standard of EUCAST is based on the reference NCCLS M27-A procedures (13), but it incorporates some modifications in order to get an objective and automated AFST and to shorten the incubation time for MIC determination (24 h). The modifications include the use of RPMI 1640 supplemented with 2% dextrose as assay medium, an inoculum size of 0.5 x 105 to 2.5 x 105 CFU/ml, flat-bottom trays, spectrophotometric reading, and 50% inhibition as the endpoint for azole agents and flucytosine. Recent reports have pointed out that susceptibility results obtained by using the proposed standard of EUCAST show high percentages of agreement with those obtained by the NCCLS reference procedure (4). However, the agreement between these methods has not been evaluated for new antifungal agents such as voriconazole and caspofungin.

Several reports indicate that the E-test is a viable alternative to the reference methods for susceptibility testing of yeasts (2, 3, 19). Procedures based on E-test strips are straightforward, economical to perform, and offer a practical method for a clinical laboratory.

The aim of the present study was to evaluate the agreement between MICs of voriconazole and caspofungin obtained by using three different methods: (i) the NCCLS reference broth microdilution method; (ii) the proposed AFST-EUCAST procedure; and (iii) the E-test.

Yeast isolates. A total of 102 clinical isolates were selected for testing. They comprised 31 Candida albicans, 17 Candida glabrata, 12 Candida parapsilosis, 11 Candida tropicalis, 7 Candida lusitaniae, 5 Candida krusei, 4 Candida guilliermondii, 1 Candida kefyr, 1 Candida inconspicua, 1 Candida lambica, 1 Candida norvegensis, 1 Candida famata, 1 Candida dubliniensis, and 9 Saccharomyces cerevisiae isolates. The isolates were cultured from various clinical specimens (43 blood, 24 respiratory tract, 12 vagina, 8 feces, 6 urine, 3 esophagus, 3 gastric juice, 2 skin, 1 abscess) at the Karolinska Hospital, Stockholm, Sweden, during 2001. Strains were identified by colony morphology and pigmentation observed on CHROMagar plates (CHROMagar Co., Paris, France) and by ID 32C (bioMerieux, Marcy l'Etoile, France). They were stored on Sabouraud dextrose agar (Oxoid) until use. Strains were subcultured onto fresh agar 24 to 48 h prior to testing. The Candida spp. strains used as controls are discussed below.

Susceptibility testing. Stock solutions of voriconazole (Pfizer Pharmaceuticals) and caspofungin (Merck & Co., Inc.) were prepared as 100x stocks in dimethyl sulfoxide and in sterile distilled water, respectively, and stored at -70°C until use. The final concentrations of voriconazole were 0.004 to 32 mg/liter, and the final concentrations of caspofungin were 0.0313 to 16 mg/liter.

(i)NCCLS broth microdilution method. The NCCLS method was performed as described in the M27-A document (13). Microdilution trays were read visually after 24 and 48 h of incubation. For voriconazole, the MIC endpoint was defined as the lowest concentration which produced a prominent decrease (80% inhibition) in turbidity compared with that of the growth control. For caspofungin, the MIC endpoint was defined as the lowest concentration which completely or nearly completely (>=95%) inhibited growth.

(ii) AFST-EUCAST procedure. The AFST-EUCAST procedure was performed according to the proposed method (17). The yeast inoculum of 0.5 x 105 to 2.5 x 105 CFU/ml was prepared in sterile water and validated by colony counts. The assay medium was a double-strength solution of RPMI 1640 with L-glutamine buffered to pH 7.0 with 0.165 M morpholinepropanesulfonic acid and supplemented with 18 g of glucose per liter. Twofold serial dilutions of antifungal drugs were prepared in microdilution trays with flat-bottom wells. The trays were incubated at 35°C, and the MICs were determined spectrophotometrically at 450 nm after 24 and 48 h of incubation. For voriconazole and caspofungin, the MIC endpoint was defined as the lowest concentration which produced 50% or more and 95% or more reduction of growth compared with that of the control well, respectively.

(iii) E-test. E-test strips with voriconazole and caspofungin were kindly supplied by AB Biodisk (Stockholm, Sweden). The yeast inoculum was adjusted with a spectrophotometer by adding sterile 0.85% NaCl to match the transmittance that was produced by a 0.5 McFarland standard at 530 nm. The inoculum was diluted 1:5 in sterile 0.85% NaCl, and the surface of RPMI 1640-2% glucose agar (AB Biodisk) was flooded with the suspension. The excess was poured off, and the plate was let to dry before the strips were applied. The MICs were read after 24 and 48 h of incubation at 35°C. The MIC was read as the lowest concentration at which the border of the elliptical inhibition zone intersected the scale on the strip. Microcolonies inside the inhibition zone were ignored. Because of the continuous gradient of antifungal agents, the MIC endpoint was elevated to the next twofold dilution concentration, which matched the dilution schema of the micromethods. The strips of voriconazole and caspofungin contained concentration gradients of 0.004 to 32 mg/liter.

Quality control strains. C. krusei ATCC 6258 and C. parapsilosis ATCC 22019 were included as quality controls. The MICs were within the control ranges for voriconazole and caspofungin as established by Barry et al. (1).

Analysis of results. Both on-scale and off-scale results were included in the analysis. The low off-scale MICs were left unchanged, and the high off-scale MICs were converted to the next highest concentration. Agreement was evaluated by concordance between the MICs determined by the different susceptibility testing methods. It was defined as a difference in MICs equal to two twofold dilutions. In addition, intraclass correlation coefficients (ICCs) were calculated for the MICs transformed on log2 data. The ICC is a reverse measurement of the variability of the MICs of strains and is expressed over a maximum value of 1 and with a confidence interval of 95%. A P value of <0.05 was considered significant. All statistical analysis was done with Statistical Package for the Social Sciences software (version 10.0; SPSS S.L., Madrid, Spain).

This is the first study in which the AFST-EUCAST proposed method has been compared with the NCCLS and E-test techniques for voriconazole and caspofungin susceptibility testing. The susceptibilities of 102 Candida spp. and S. cerevisiae isolates to voriconazole and caspofungin as determined by the three methods are summarized in Table 1. The voriconazole MICs obtained were very similar to those reported previously, with MIC50 values of <=0.125 mg/liter for all yeast species, except for C. glabrata and C. krusei, which yielded MIC50 values of 0.25 to 1 mg/liter depending on the method (10, 14, 15). Caspofungin exhibited good activity in vitro, with a MIC50 of <=0.125 to 2 mg/liter, depending on the method, against all species except C. guilliermondii, matching up with results from other studies (8, 16).


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  		TABLE 1. Voriconazole and caspofungin MIC ranges and MIC50 and MIC90 values for the isolates by the NCCLS (at 48 h), EUCAST (at 24 h), and E-test (at 48 h) methods

Overall, the agreement and the correlation between methodologies were high (Table 2). The agreements between MICs obtained by the NCCLS procedure (48 h of incubation) and MICs by the EUCAST standard (24 h of incubation) were 97 and 96% for voriconazole and caspofungin, respectively. The agreements of voriconazole MICs between those provided by the E-test (48 h of incubation) and the NCCLS and between those of the E-test and the EUCAST method were 100 and 90%, respectively. These data agree with the results of Pfaller et al. (15) that showed an overall agreement of 98% between the E-test and the NCCLS reference method for voriconazole. When discrepancies were observed between voriconazole MICs by the three methods, the E-test (48 h of incubation) provided voriconazole MIC90 values for C. glabrata isolates that were more than two twofold dilutions higher. However, the corresponding E-test MIC50 and MIC90 values, determined after 24 h of incubation, were 0.125 and 0.25 mg/liter, respectively (data not shown). It was also determined that the agreement for voriconazole MICs was higher between the E-test and AFST-EUCAST when the E-tests were read after 24 h (98%) rather than after 48 h (90%).


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  		TABLE 2. Agreement and ICCs between antifungal susceptibility testing methods

The agreement for caspofungin was slightly poorer between the NCCLS method and the E-test (87% at 24 h and 89% at 48 h) because of lower caspofungin MICs provided by the E-test for several Candida species. Similar discrepancies were recently demonstrated for C. parapsilosis and C. tropicalis (16). Higher agreements were obtained for caspofungin between the AFST-EUCAST method and the E-test (94% at 24 h and 95% at 48 h). It should be noted that the MIC50 of caspofungin for C. guilliermondii isolates was 1 mg/liter when using the E-test strips and >16 mg/liter by both the NCCLS and EUCAST methods. This difference is significant and could indicate that the E-test may not be a reliable technique for testing susceptibility of C. guilliermondii strains to this antifungal agent.

It was recently shown that the agreement between the AFST-EUCAST and the NCCLS methods was very good for amphotericin B, flucytosine, fluconazole, and itraconazole susceptibility testing (M. Cuenca-Estrella et al., Abstr. 41st Intersci. Conf. Antimicrob. Agents Chemother., abstr. J-570, 2001). In the present study, good agreement between all the methods was achieved for two new antifungal agents, voriconazole and caspofungin. Moreover, ICCs were statistically significant (P < 0.05) (Table 2), indicating a good reproducibility and correlation among MICs obtained by the NCCLS method, the EUCAST proposed standard, and the E-test procedure.

In conclusion, MICs of voriconazole and caspofungin obtained by the AFST-EUCAST proposed standard and the E-test exhibited a high agreement and a good correlation with those achieved by the NCCLS reference micromethod. Both the EUCAST and E-test procedures can be reliable techniques for susceptibility testing of yeasts to voriconazole and caspofungin.


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FOOTNOTES
 
* Corresponding author. Mailing address: Department of Clinical Microbiology, L202 Karolinska Hospital, S-171 76 Stockholm, Sweden. Phone: 46 851773566. Fax: 46 8308099. E-mail: erja.chryssanthou{at}ks.se. Back


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Journal of Clinical Microbiology, October 2002, p. 3841-3844, Vol. 40, No. 10
0095-1137/02/$04.00+0     DOI: 10.1128/JCM.40.10.3841-3844.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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