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Journal of Clinical Microbiology, September 1998, p. 2586-2589, Vol. 36, No. 9
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Evaluation of the Etest Method for Determining
Fluconazole Susceptibilities of 402 Clinical Yeast Isolates by
Using Three Different Agar Media
M. A.
Pfaller,1,*
S. A.
Messer,1
Å.
Karlsson,2 and
A.
Bolmström2
Department of Pathology, University of Iowa
College of Medicine, Iowa City, Iowa,1 and
AB BIODISK, Solna, Sweden2
Received 20 April 1998/Returned for modification 26 May
1998/Accepted 16 June 1998
 |
ABSTRACT |
The performance of the Etest for fluconazole susceptibility testing
of 402 yeast isolates was assessed against the National Committee for
Clinical Laboratory Standards (NCCLS) microdilution broth method. The
NCCLS method employed RPMI 1640 broth medium, and MICs were read after
incubation for 48 h at 35°C. Etest MICs were determined with
RPMI agar containing 2% glucose (RPG), Casitone agar (CAS), and
Mueller-Hinton agar (MHA) and were read after incubation for 48 h
at 35°C. The yeast isolates included Candida albicans
(n = 161), Candida glabrata
(n = 41), Candida tropicalis (n = 35), Candida parapsilosis
(n = 29), Candida krusei
(n = 32), Candida lusitaniae
(n = 31), Candida species
(n = 19), Cryptococcus neoformans
(n = 40), and miscellaneous yeast species
(n = 14). The Etest results correlated well with
reference MICs. Overall agreement was 94% with RPG, 97% with CAS, and
53% with MHA. When RPG was used, agreement ranged from 89% for
Candida spp. to 100% for C. krusei. When CAS
was utilized, agreement ranged from 93% for Cryptococcus
neoformans to 100% for C. tropicalis, C. parapsilosis, C. lusitaniae, Candida
spp., and miscellaneous yeast species. With MHA, agreement ranged from
17% for C. parapsilosis to 90% for C. krusei.
Both RPG and CAS supported growth of all yeast species, whereas growth
on MHA was comparatively weaker. Etest results were somewhat easier to
read on CAS. The Etest method using either RPG or CAS, but not MHA,
appears to be a viable alternative to the NCCLS reference method for
determining fluconazole susceptibilities of yeasts.
| |
INTRODUCTION |
The assessment of alternative
antifungal susceptibility testing methods such as the colorimetric MIC
microdilution procedure (8-10, 18) and agar-based methods
like the disk diffusion method (1) and Etest stable gradient
method (2-4, 6, 12, 16, 17, 19) has become possible with
the standardization of broth dilution methods for in vitro
susceptibility testing of yeasts (7, 13, 15). Studies by
Sewell et al. (16) and Colombo et al. (3, 4)
demonstrated that the Etest was potentially useful for in vitro testing
of susceptibility to fluconazole and other azoles. Additional
evaluations with the Etest have suggested that the use of RPMI 1640 agar supplemented with 2% glucose (RPG) or Casitone agar may optimize
the growth of certain yeasts and facilitate the examination of MIC
endpoints for azoles (6, 12, 19).
It is well known that a concentration-dependent partial inhibition of
fungal growth by fluconazole and other azoles results in the so-called
trailing endpoints and causes problems with reliable interpretation of
MIC results (5, 14). Partial inhibition in the Etest
corresponds to the presence of microcolonies around or inside the whole
area of a discernable inhibition ellipse (2-4, 6). This
trailing is minimized by adding 2% glucose to RPMI agar and is less
frequently seen on Casitone agar (6). In the present study,
we provided an expanded evaluation of the Etest, using RPMI, Casitone,
and Mueller-Hinton agars, in comparison to the National Committee for
Clinical Laboratory Standards (NCCLS) reference microdilution method by
testing the susceptibilities of 402 clinical yeast isolates to
fluconazole.
| |
MATERIALS AND METHODS |
Test organisms.
Four hundred and two clinical yeast isolates
were selected for testing. The collection included 161 Candida
albicans, 41 Candida glabrata, 35 Candida
tropicalis, 29 Candida parapsilosis, 32 Candida krusei, 31 Candida lusitaniae, 19 Candida
spp. (five Candida quilliermondii, four Candida
lipolytica, five Candida rugosa, two Candida
kefyr, and three Candida zeylanoides), 40 Cryptococcus neoformans, and 14 miscellaneous yeast species
(two Cryptococcus laurentii, one Cryptococcus
albidus, four Trichosporon beigelii, four
Rhodotorula spp., and three Saccharomyces
cerevisiae) isolates. The members of this collection were all
recent clinical isolates from geographically diverse medical centers in
the United States. The majority were isolated from blood or normally
sterile body fluids. The isolates were identified by standard methods
(20) and were stored as suspensions in water at ambient
temperature until used in the study. Prior to testing, each isolate was
subcultured at least twice on Sabouraud dextrose agar (Remel, Lenexa,
Kans.) to ensure optimal growth characteristics.
Antifungal agents.
Etest strips containing fluconazole
(0.016 to 256 µg/ml) were supplied by AB BIODISK (Solna, Sweden).
Fluconazole was obtained as a reagent-grade powder from Pfizer
Pharmaceuticals, Roerig Division (New York, N.Y.). Stock solutions
prepared in water were further diluted in RPMI 1640 medium buffered to
pH 7.0 with 0.165 M morpholinepropanesulfonic acid (MOPS) buffer
(Sigma, St. Louis, Mo.) and dispensed into 96-well microdilution trays.
Trays containing a 0.1-ml aliquot of appropriate drug solution (two
times the final concentration) in each well were subjected to quality
control (QC) and then sealed and stored at 
70°C until they were
used. The final concentrations of fluconazole were 0.12 to 128 µg/ml.
Media.
Agar formulations used for the Etest were RPMI 1640 medium (American Biorganics, Buffalo, N.Y.) supplemented with 1.5%
agar and 2% glucose (RPG) and buffered with MOPS, Casitone agar
(Difco), and Mueller-Hinton agar (BBL). The RPMI 1640 broth medium used for the microdilution testing was buffered with MOPS in accordance with
the NCCLS M27-A method (7).
Antifungal susceptibility test methods.
Broth microdilution
tests were performed according to NCCLS document M27-A (7).
An inoculum concentration of 0.5 × 103 to 2.5 × 103 cells per ml was standardized spectrophotometrically.
Microdilution trays were incubated at 35°C and read after 48 h
of incubation. With trailing endpoints, the MIC was determined visually
according to NCCLS recommendations of an 80% reduction in turbidity.
For the Etest, 90-mm-diameter plates containing agar at a depth of 4.0 mm were used. The agar surface was inoculated by using a nontoxic swab
dipped in a cell suspension adjusted spectrophotometrically to the
turbidity of a 0.5 McFarland standard. After excess moisture was
absorbed into the agar and the surface was completely dry, an Etest
strip was applied to each plate. The plates were incubated at 35°C
and read at 24 and 48 h. The MIC was read at the lowest concentration at which the border of the elliptical inhibition zone
intercepted the scale on the strip. Any growth, such as microcolonies, throughout a discernable inhibition ellipse was ignored.
QC.
QC, in accordance with NCCLS document M27-A
(7), was performed by testing C. krusei ATCC 6258 and C. parapsilosis ATCC 22019. QC determinations made on
each day of testing were within the control limits for fluconazole
(7, 11).
Analysis of results.
Etest MICs read at 24 and 48 h on
the three media were compared to reference microdilution MICs read at
48 h. The reference microdilution and Etest MIC determinations
were performed in two physically separate laboratories and were read
independently; i.e., the testing was blinded. Since the Etest scale has
a continuous gradient of concentrations, the MIC values in between
twofold dilutions were raised to the next twofold level of the
reference method for comparison (3, 4). Off-scale MICs at
the upper limit were converted to the next higher concentration, and
off-scale results at the lower limit were left unchanged. Discrepancies between MIC values of no more than two dilutions were used to calculate
the percent agreement.
| |
RESULTS AND DISCUSSION |
Table 1 summarizes the in vitro
susceptibilities of 402 yeast isolates to fluconazole as determined by
the reference broth microdilution panel. A broad range of MICs was
observed for each organism group. In general, the fluconazole MICs
obtained were typical for individual yeast species (8, 9, 13, 16, 17). Both fluconazole-susceptible and -resistant strains were represented in the collection (15).
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TABLE 1.
In vitro activity of fluconazole against 402 clinical
yeast isolates as determined by the reference broth
microdilution methoda
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Table 2 summarizes the percentage of 48-h
fluconazole MICs obtained by the Etest on the three agar media that
were within two dilutions of the reference method result. Overall, the
percent agreement was 94% with RPMI and 97% with Casitone. The
agreement between the Etest and microdilution MICs was 
90% for all
species with Casitone agar and for all species with the exception of
Candida spp. (89%) with RPMI agar. The agreement between
Etest and microdilution MICs was poor when Mueller-Hinton agar was used
(53%), with 80% agreement achieved with only C. krusei
(90%), Cryptococcus neoformans (87%), and miscellaneous
species (85%).
An acceptable level of agreement was also achieved when Etest MICs were
read after 24 h of incubation (Table
3). This agreement was independent of the
species of yeast tested. The overall level of agreement was 90% or
greater with both RPMI (95%) and Casitone (97%) agar. The
Mueller-Hinton agar results were slightly better (62% agreement) at
24 h but still inferior to those obtained with either RPMI or
Casitone agar.
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TABLE 3.
Effect of Etest incubation time on agreement of resultant
data with NCCLS reference MICs of fluconazole against 402 yeast isolates
|
|
The results of this study provide further documentation of the
applicability of the Etest stable agar gradient method for determining
the in vitro susceptibilities of yeast isolates to fluconazole.
Previous studies in our laboratory using RPMI agar without additional
glucose (0.2% final concentration) found poor agreement between Etest
and broth dilution MICs for fluconazole tested against C. tropicalis and C. glabrata (16). The
supplementation of RPMI agar with additional glucose (2% final
concentration) provided optimal growth of these species as well as
Cryptococcus neoformans and led to excellent agreement with
the MICs obtained by the microdilution reference method (Tables 2 and
3). Similarly, the problem of trailing endpoints due to partial
inhibition of growth by azoles was minimized with the use of either RPG
or Casitone agar and specific criteria for reading Etest MICs as
described in the Etest package insert and technical guide for yeasts
(AB BIODISK). In this study, the inhibition ellipses were quite clear with most isolates tested on either RPG or Casitone agar. Good agreement with broth dilution MICs was obtained when discernable growth
within the ellipse was ignored. Thus, if an ellipse was visualized, the
MIC was read at the point at which the ellipse intersected the strip,
irrespective of the presence of inner colonies or a lawn of weaker or
less-pigmented growth within the ellipse (Fig.
1). For those isolates in which such
inner growth was observed, retesting the organisms from the inner
growth produced the same result and did not indicate that the inner
colonies exhibited a greater degree of resistance. However, it is
important to distinguish the microcolonies from isolated macrocolonies
that can be seen especially with C. glabrata and C. tropicalis on RPMI and Casitone agars (Fig.
2). These often represent subpopulations
which on retesting can give higher MICs. Thus, the presence of
macrocolonies, as shown in Fig. 2, should be considered indicative of a
resistant subpopulation. It is notable that the presence of growth
within the inhibition ellipse was almost completely eliminated with
Casitone agar for a significant number of isolates (Fig. 1).
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FIG. 1.
Fluconazole (FL) Etest reading patterns for C. albicans. (A) Growth of microcolonies inside the entire inhibition
zone (ellipse); MIC, 0.38 µg/ml. (B) Clear ellipse on Casitone agar;
MIC, 0.5 µg/ml. The numbers on the scale correspond to the
fluconazole concentrations on the strip (in micrograms per
milliliter).
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FIG. 2.
Fluconazole (FL) Etest reading patterns for C. glabrata. A resistant subpopulation appears as macrocolonies
within the ellipse on Casitone agar. MIC, >256 µg/ml. The numbers on
the scale correspond to fluconazole concentrations on the strip (in
micrograms per milliliter).
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|
The use of RPG or Casitone agar also allows for earlier (24 h) reading
of fluconazole Etest MICs. As noted by others (3, 4, 16),
occasional isolates of Candida spp. and all
Cryptococcus neoformans isolates require 48 h of
incubation for optimal growth. We encountered seven isolates of
Candida spp. that required 48 h of incubation on RPG or
Casitone agar before MICs could be read. The ability to determine MIC
results within 24 h is potentially advantageous for an early
clinical application of antifungal susceptibility testing results.
We included Mueller-Hinton agar in this comparison in an effort to
evaluate the applicability of an agar medium that is widely available
and used in clinical laboratories for agar-based susceptibility testing
of bacterial isolates. Unfortunately, the performance of this medium
for fluconazole susceptibility testing by Etest was suboptimal. In
general, MICs obtained by Etest on Mueller-Hinton agar were
considerably lower than those obtained by either the reference broth
dilution or the Etest with RPG or Casitone agar. The likely explanation
for the poor agreement with MICs obtained with Mueller-Hinton agar is
the relatively poor growth of most isolates on this medium.
In summary, we have provided further documentation of the ability of
the Etest to generate fluconazole MIC data that are comparable to those
obtained by the NCCLS broth microdilution method. The use of
more-enriched media, such as Casitone agar and RPG, provides optimal
growth for a broad range of yeast species and improves the ease of
fluconazole MIC endpoint determination by the Etest. Both RPG and
Casitone agar performed equally well in this study, with Casitone agar
providing clearer MIC endpoints. We recommend the use of either of
these media, but not Mueller-Hinton agar, for performing fluconazole
susceptibility testing by the Etest.
| |
ACKNOWLEDGMENTS |
The excellent secretarial support of K. Meyer is greatly
appreciated.
This study was supported in part by Pfizer Pharmaceuticals, Roerig
Division, and by AB BIODISK.
| |
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.
| |
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Journal of Clinical Microbiology, September 1998, p. 2586-2589, Vol. 36, No. 9
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
