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Journal of Clinical Microbiology, January 2000, p. 341-344, Vol. 38, No. 1
0095-1137/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Antifungal Susceptibility Testing of Dermatophytes:
Establishing a Medium for Inducing Conidial Growth and Evaluation
of Susceptibility of Clinical Isolates
C. J.
Jessup,
J.
Warner,
N.
Isham,
I.
Hasan, and
M. A.
Ghannoum*
Mycology Reference Laboratory, Center for
Medical Mycology, Department of Dermatology, Case Western Reserve
University, and University Hospitals of Cleveland, Cleveland, Ohio
Received 21 July 1999/Returned for modification 16 September
1999/Accepted 9 October 1999
 |
ABSTRACT |
A standardized reference method for dermatophyte in vitro
susceptibility testing is lacking. In a previous study, Norris et al.
(H. A. Norris, B. E. Elewski, and M. A. Ghannoum,
J. Am. Acad. Dermatol. 40(6, part 2):S9-S13) established the
optimal medium and other growth variables. However, the earlier study
did not address two issues: (i) selection of an optimal medium for
conidial formation by dermatophytes and (ii) validation of the method
with a large number of dermatophytes. The present study addresses these two points. To select which agar medium best supported conidial growth,
representative isolates of dermatophytes were grown on different agars.
Preliminary experiments showed that only oatmeal cereal agar supported
the production of conidia by Trichophyton rubrum. We tested
the abilities of 251 T. rubrum isolates to form conidia
using three different cereal agars and potato dextrose agar. Overall,
oatmeal cereal and rice agar media were comparable in their abilities
to support T. rubrum conidial growth. Next, we used the
oatmeal cereal agar for conidial formation along with the optimal
conditions for dermatophyte susceptibility testing proposed by Norris
et al. and determined the antifungal susceptibilities of 217 dermatophytes to fluconazole, griseofulvin, itraconazole, and
terbinafine. Relative to the other agents tested, terbinafine possessed
the highest antifungal activity against all of the dermatophytes. The
mean ± standard error of the mean MICs of fluconazole,
itraconazole, terbinafine, and griseofulvin were 2.07 ± 0.29, 0.13 ± 0.01, 0.002 ± 0.0003, and 0.71 ± 0.05 µg/ml,
respectively. This study is the first step in the identification of
optimal conditions that could be used for the standardization of the
antifungal susceptibility testing method for dermatophytes. Inter- and
intralaboratory agreement as well as clinical correlations need to be established.
| |
INTRODUCTION |
In the last two decades the
incidence of infections caused by dermatophytes and other fungi has
increased considerably (1, 7, 11). With an increasing
variety of drugs available for the treatment of dermatophytoses, the
need for a reference method for the testing of the antifungal
susceptibilities of dermatophytes has become apparent (3, 7, 9,
11). Establishment of a reference susceptibility testing method
may allow the clinician to select the appropriate therapy for the
treatment of infections caused by dermatophytic fungi. Recently, a
standard method for antifungal susceptibility testing of yeasts has
been established by the National Committee for Clinical Laboratory
Standards (NCCLS;M27-A document) (6). This reference method
for yeast is the first step in the establishment of a reliable,
standardized, and clinically useful technique for the susceptibility
testing of filamentous and dermatophytic fungi. Efforts to develop a
reference method for broth dilution antifungal susceptibility testing
of filamentous fungi are being pursued by NCCLS (1a, 8).
This paper represents the first attempt at standardizing the antifungal
susceptibility testing of dermatophytes.
In developing this method for antifungal susceptibility testing of
dermatophytic fungi, many variables need to be considered. An earlier
investigation by Norris et al. (7) evaluated inoculum size,
temperature and duration of incubation, medium, and endpoint determination. Although the earlier study established many important variables concerning those conditions necessary for optimization of the
susceptibility testing method for dermatophytes, it did not address
which medium is appropriate for conidial formation. Identification of
such a medium is critical since dermatophytes (particularly
Trichophyton rubrum) are known to be poor producers of
conidia (11). An isolate's inability to produce conidia
will hamper our ability to determine the susceptibility or resistance of that particular isolate.
In this study, we established oatmeal cereal agar and rice agar as the
optimal agar media for support of conidial growth. We also expanded the
antifungal susceptibility findings of Norris et al. (7) by
determining the antifungal susceptibilities of a larger number of
dermatophytes isolates to four clinically used antifungal agents. The
results from this study serve as a foundation for the development of a
standardized susceptibility testing method for dermatophytes.
| |
MATERIALS AND METHODS |
Identification of an appropriate medium for production of conidia
by various dermatophytes. (i) Agar.
Three types of agar media were
initially used to evaluate the conidial growth of the selected
dermatophyte isolates (see below): Mycosel agar with 1% yeast extract,
potato dextrose agar (both from Becton Dickinson and Company,
Cockeysville, Md.), and Heinz oatmeal cereal (H. J. Heinz Co.,
Pittsburgh, Pa.). On the basis of preliminary data, a continuation
study evaluating a larger number of isolates for their conidial growth
was performed by using two different cereal agars (mixed grains
[H. J. Heinz Co.] and Beech-Nut Rice [Beech-Nut Nutrition
Corp., St. Louis, Mo.]), along with oatmeal cereal agar and potato
dextrose agar. To prepare the cereal agars, 100 g of the dried
ingredients was mixed with 15 g of Bacto agar (Difco Laboratories,
Detroit, Mich.). These components were then stirred into 1 liter of
distilled water and were mixed thoroughly. The mixture was then
autoclaved for 20 min and was then allowed to cool by placing it into a
10°C water bath. Once it was cooled, the mixture was autoclaved again
for an additional 20 min. Preliminary experiments revealed that the hold time and the second autoclaving are critical to kill any Bacillus spores present in the mixture.
(ii) Organisms.
We initially tested 43 isolates of
dermatophytes including 10 strains each of T. rubrum,
Trichophyton mentagrophytes, and Trichophyton
tonsurans, 7 strains of Epidermophyton floccosum, and 6 strains of Microsporum canis. The continuation study for conidial growth involved 251 strains of T. rubrum. All
strains were clinical isolates obtained from nail or hair specimens
received from clinicians by the Center for Medical Mycology, University Hospitals of Cleveland. Dermatophytes were identified to the species level by conventional methods (5). Isolates were stored at 
80°C on potato dextrose agar slants until the time of use.
(iii) Determination of conidial growth.
Dermatophytes were
grown on different agar media at 30°C for 4 to 7 days. At the end of
the incubation period, cellophane tape preparations were used to
quantitate the conidial formation microscopically. For each isolate the
numbers of conidia were determined in five viewing fields. The average
numbers of conidia were calculated for each strain. The ability of
various media to support conidial formation was scored on a scale of
from 0 to 3, where 0 implies no conidiation and 3 implies proliferative conidiation. The data were expressed as conidial formation as a
percentage of that for T. rubrum isolates forming conidia on different agar media.
In vitro susceptibility testing. (i) Organisms.
We tested
217 isolates of dermatophytes including T. rubrum (n = 132), T. mentagrophytes (n = 32), T. tonsurans
(n = 42), E. floccosum (n = 3), and
M. canis (n = 8). Two American Type Culture
Collection (ATCC; Rockville, Md.) quality control organisms were used:
Candida parapsilosis ATCC 22019 and Paecilomyces
variotti ATCC 22319. All strains were clinical isolates obtained
from nail or hair specimens received from clinicians by the Center for
Medical Mycology, University Hospitals of Cleveland. Dermatophytes were identified and were stored as described above.
(ii) Antifungal agents.
Four antifungal drugs, supplied by
the manufacturers as powders, were used: fluconazole (Pfizer
Pharmaceuticals Group, New York, N.Y.), terbinafine (Novartis, E. Hanover, N.J.), itraconazole (Janssen Research Foundation, Beerse,
Belgium), and griseofulvin (Sigma Chemical Company, St. Louis, Mo.).
Fluconazole was dissolved in sterile water, itraconazole and
griseofulvin were dissolved in 100% dimethyl sulfoxide (Curtin
Matheson Scientific Inc., Houston, Tex.), and terbinafine was dissolved
in dimethyl sulfoxide with 5% Tween 80 (Curtin Matheson Scientific
Inc., Houston, Tex.). All drugs were prepared as stock solutions of 1 mg/ml.
(iii) Medium.
RPMI 1640 (American Biorganics Inc., Niagara
Falls, N.Y.) with L-glutamine but without sodium
bicarbonate and buffered at pH 7.0 with
3-(N-morpholino)propanesulfonic acid, monosodium salt (MOPS), was the medium used for broth microdilution susceptibility testing.
(iv) Drug dilutions.
Serial twofold dilutions were prepared
according to the NCCLS M27-A (6) proposed standard.
Fluconazole and griseofulvin had MIC ranges of 0.13 to 64.0 µg/ml.
Itraconazole and terbinafine had MIC ranges of 0.06 to 32.0 µg/ml.
(v) Inoculum preparation.
We prepared a standardized
inoculum by counting the microconidia microscopically. Cultures were
grown on oatmeal cereal agar slants for 7 days at 30°C. Sterile
normal saline (85%) was added to the slant, and the culture was gently
swabbed with a cotton tip applicator to dislodge the conidia from the
hyphal mat. The suspension was transferred to a sterile centrifuge
tube, and the volume was adjusted to 5 ml with sterile normal saline.
The resulting suspension was counted on a hemocytometer and was diluted
in RPMI 1640 to the desired concentration.
(vi) Broth microdilution testing.
Microdilution plates were
set up in accordance with the NCCLS M27-A (6) reference
method; the exception was the inoculum preparation, which was set up as
described above. Column 1 was filled with 200 µl of medium to serve
as a sterility control. Columns 2 through 11 were filled with 100 µl
of the inoculum and 100 µl of the serially diluted antifungal agent.
Column 12 was filled with 200 µl of the inoculum and served as a
growth control.
(vii) Incubation time and temperature.
The microdilution
plates were incubated at 35°C and were read visually after 4 days of incubation.
(viii) Endpoint criteria.
The MIC was defined as the point
at which the organism was inhibited 80% compared with the growth in
the control well. All isolates were run in duplicate and the results
were read visually. For the two isolates tested with fluconazole as
quality controls, MICs were within the expected range (for C. parapsilosis, 4.0 µg/ml; for P. variotti, 64.0 µg/ml) specified in document M-27A (6).
| |
RESULTS |
Comparison of conidial growth of common dermatophytes on different
agar media.
Three types of agar media (potato dextrose, Mycosel
with 1% yeast extract, and Heinz oatmeal cereal) were compared for
their abilities to induce conidiation. The representative dermatophyte isolates tested were T. rubrum (n = 10), T.
mentagrophytes (n = 10), T. tonsurans (n = 10), E. floccosum (n = 7), and M. canis (n = 6). All isolates of the last four species produced
abundant conidia (
26 conidia/field), irrespective of the medium used. The ability of T. rubrum to form conidia was medium
dependent. Potato dextrose agar and Mycosel supported only limited
growth of T. rubrum conidia at both 4 and 7 days of
incubation; i.e., between 10 and 60% of the isolates were able to
produce a small number of conidia (1 to 15 conidia/field). In contrast,
by 4 days, oatmeal cereal agar promoted the production of a large
number of conidia (26 conidia/field) from all T. rubrum
isolates examined in this preliminary screen. Comparison of the
abilities of various isolates to produce conidia at 4 and 7 days showed
that 4 days was sufficient for growth of abundant conidia from all
isolates of T. mentagrophytes, T. tonsurans,
E. floccosum, and M. canis. T. rubrum,
on the other hand, produced abundant conidia following growth for 4 and
7 days when it was cultured on oatmeal cereal but not potato dextrose
or Mycosel (Table 1). On the last two media, conidial production by T. rubrum was enhanced when
the organisms were incubated for 7 days. However, there was no conidial growth for 30 to 40% of the isolates even after 7 days of incubation.
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TABLE 1.
Percentages of conidium-forming T. rubrum
isolates on three types of agar media at 4 and 7 days
of incubationa
|
|
Having identified oatmeal cereal agar as a potentially useful medium
for conidial formation for all dermatophytic species
tested, we wanted
to test the ability of a large number of
T. rubrum isolates
(
n = 251) to form conidia with three different
cereal
agars (oatmeal cereal, rice, and mixed grains) and potato
dextrose
agar. Overall, even though the oatmeal cereal agar was
slightly more
effective than rice in its ability to support production
of conidia by
approximately 84% of the
T. rubrum isolates tested,
these
two media were comparable in their abilities to support
T. rubrum conidial growth, as seen in Table
2. About 15% of
T. rubrum
isolates failed to produce conidia in any of the media
tested.
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|
TABLE 2.
Percentages of conidium-forming T. rubrum
isolates on three types of cereal media agar and potato dextrose
agar at 7 days of incubationa
|
|
Determination of antifungal susceptibilities of 217 dermatophytes
by using optimized conditions.
By using the optimized conditions
the MICs of griseofulvin, itraconazole, terbinafine, and fluconazole
for 217 dermatophyte isolates including T. rubrum (n = 132), T. mentagrophytes (n = 32), T. tonsurans
(n = 42), E. floccosum (n = 3), and
M. canis (n = 8) were determined. Our data show
that terbinafine was the most active antifungal agent tested against
dermatophytes. As shown in Fig. 1, the
mean ± standard error of the mean MICs v were 2.07 ± 0.29, 0.13 ± 0.01, 0.002 ± 0.0003, and 0.71 ± 0.05 µg/ml
for fluconazole, itraconazole, terbinafine, and griseofulvin, respectively. Additionally, the MIC at which 50% of isolates are inhibited (MIC50) and the MIC90 of terbinafine
(MIC50, 0.001 µg/ml; MIC90, 0.004 µg/ml)
were 130- and 250-fold lower, respectively, than those of the second
most active antifungal agent (itraconazole), as seen in Table
3.
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|
FIG. 1.
Mean MICs of fluconazole, itraconazole, terbinafine, and
griseofulvin for 217 dermatophytes by the proposed method for in vitro
susceptibility testing.
|
|
| |
DISCUSSION |
A standardized dermatophyte susceptibility testing technique
should encompass the following: an ideal growth medium, a specific protocol with reference to the initial inoculum size, a specific incubation time, a specific incubation temperature, and an MIC endpoint
determination which is applicable to all dermatophytes. Another
important factor for the determination of antifungal susceptibility which is particularly important for the testing of dermatophytes is the
selection of the most appropriate medium that will support conidial
growth. Norris et al. (7) were the first to identify the
optimal parameters to be used in performing antifungal susceptibility testing of dermatophytes. In their study, variables such as growth medium, inoculum size, and length and temperature of incubation were addressed.
In this study, we showed that, of those media tested, oatmeal cereal
agar and rice agar preparations are the most appropriate for the
production of conidia from various dermatophyte species, specifically,
T. rubrum. Identification of an appropriate medium for
conidial production is of critical importance since an inability to
produce spores will limit our ability to prepare the necessary inoculum
for the initiation of testing. Although the majority of dermatophytes
are capable of producing conidia in different media, the induction of
conidiation by T. rubrum has proven to be difficult
(7). Since T. rubrum is an important pathogen responsible for a significant number of dermatophyte infections (e.g.,
over 90% of nail infections are caused by this organism) (1), we decided to investigate the medium appropriate for
induction of conidiation by this species. Our data suggest that both
oatmeal cereal agar and rice agar could be adopted as media for the
induction of conidiation for the standard in vitro dermatophyte
susceptibility testing method. Unfortunately, approximately 15% of the
isolates tested failed to produce conidia even in the most efficient
media (oatmeal cereal and rice). Determination of the antifungal
susceptibilities of these organisms will not be possible by currently
accepted methods. Other conditions or media that may enhance the
sporulation ability of these T. rubrum strains for which
induction of sporulation is difficult should be investigated.
In this study we extended the findings of Norris et al. (7)
and provided a more comprehensive investigation by testing a larger
number of isolates. Using the proposed conditions, we were able to
determine the susceptibility profiles of the antifungal agents used to
treat dermatophyte infections. Importantly, this profile agrees with
earlier reports (10) comparing the in vitro activities of
various agents. For example, our data confirm earlier reports showing
that terbinafine has the highest level of activity against
dermatophytes (10). Furthermore, there was very little difference in the activity of terbinafine against different species, illustrating its uniformly high level of activity.
Our study shows that various parameters, RPMI 1640 medium, an
incubation temperature of 35°C, an incubation time of 4 days, and an
inoculum of 103 conidia/ml, are optimal for determination
of the antifungal susceptibilities of dermatophytes. These conditions,
along with our suggested agar medium (oatmeal cereal or rice), combine
to provide optimal conditions by which one can obtain the MICs of
antifungal agents for dermatophytes. Therefore, these proposed
parameters form the foundation for a standardized antifungal
susceptibility testing method for dermatophytes. A number of future
studies that use these conditions are proposed. A larger sample of
dermatophytes needs to be tested to determine the inter- and
intralaboratory agreements of such a method. Additionally, MICs need to
be correlated with clinical outcome to develop interpretive breakpoints
for dermatophyte susceptibility testing.
| |
ACKNOWLEDGMENT |
We thank Michael Pfaller for useful comments and suggestions in
reading our manuscript.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Center for
Medical Mycology, Mycology Reference Laboratory, University Hospitals
of Cleveland, 11100 Euclid Ave., Cleveland, OH 44106-5028. Phone: (216)
844-8580. Fax: (216) 844-1076. E-mail: mag3{at}po.cwru.edu.
| |
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Journal of Clinical Microbiology, January 2000, p. 341-344, Vol. 38, No. 1
0095-1137/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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Top
Abstract
Introduction
