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Journal of Clinical Microbiology, January 2001, p. 323-327, Vol. 39, No. 1
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.1.323-327.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Differentiation of Candida dubliniensis from
Candida albicans on Staib Agar and Caffeic Acid-Ferric
Citrate Agar
Asmaa
Al Mosaid,1
Derek
Sullivan,1
Ira F.
Salkin,2
Diarmuid
Shanley,1 and
David C.
Coleman1,*
Microbiology Research Unit, Department of
Oral Medicine and Oral Pathology, School of Dental Science and
Dublin Dental Hospital, Trinity College, University of Dublin, Dublin
2, Republic of Ireland,1 and
Wadsworth Center, New York State Department of Health, Albany,
New York2
Received 20 July 2000/Returned for modification 23 September
2000/Accepted 21 October 2000
 |
ABSTRACT |
The methods currently available for the identification of the
pathogenic yeast Candida dubliniensis all have
disadvantages in that they are time-consuming, expensive, and/or, in
some cases, unreliable. In a recent study (P. Staib and J. Morschhäuser, Mycoses 42:521-524; 1999) of 14 C. dubliniensis and 11 C. albicans isolates, it was
suggested that the ability of C. dubliniensis to produce
rough colonies and chlamydospores (chlamydoconidia) on
Staib agar (SA) provided a simple means of differentiating it from its
close relative C. albicans. In the present investigation, we examined the colony morphology and chlamydospore
production of 130 C. dubliniensis and 166 C. albicans isolates on SA and on the related defined medium caffeic
acid-ferric citrate agar (CAF). All of the C. dubliniensis
and C. albicans isolates produced chlamydospores on the control medium, i.e., rice-agar-Tween
agar. However, while none of the C. albicans isolates
produced chlamydospores on either SA or CAF, 85.4 and
83.8% of the C. dubliniensis isolates produced
chlamydospores on SA and CAF, respectively. All of the C. albicans isolates grew as smooth, shiny colonies on SA
after 48 to 72 h of incubation at 30°C, while 97.7% of the
C. dubliniensis isolates grew as rough colonies, many
(65%) with a hyphal fringe. In contrast, 87.4% of the C. albicans and 93.8% of the C. dubliniensis isolates
yielded rough colonies on CAF. Although the results of this study
confirm that SA is a good medium for distinguishing between C. dubliniensis and C. albicans, we believe that
discrimination between these two species is best achieved on the basis
of colony morphology rather than chlamydospore production.
| |
INTRODUCTION |
Due to the increasing incidence of
fungal infections and the recent emergence of novel opportunistic
fungal pathogens, there is a growing need for the development of
simple, rapid, and accurate identification methods for potential fungal
pathogens recovered in the clinical microbiology laboratory
(18). This is particularly true of the newly described
yeast species Candida dubliniensis. Although first
associated with oral candidiasis in human immunodeficiency virus
(HIV)-infected patients (25), it has more recently been recognized as a cause of superficial and systemic disease in
HIV-negative individuals (3, 11, 16, 17, 24, 26). The
close genotypic relationship between C. dubliniensis and
C. albicans results in their sharing a broad range of
phenotypic characteristics, which hampers the accurate and rapid
differentiation of the two species (23). Although the
majority of C. dubliniensis isolates are susceptible to
currently used antifungal drugs, it has been shown that isolates of
this species, unlike C. albicans, can rapidly develop stable
resistance to fluconazole upon exposure in vitro (12, 13).
This ability, the emergence of C. dubliniensis worldwide, its growing importance as a cause of systemic disease, and the introduction of novel antifungal agents all indicate that a thorough investigation of the incidence and epidemiology of C. dubliniensis is required. In order to be able to achieve this,
simple and reliable tests for differentiating C. dubliniensis from C. albicans need to be developed. The
"gold standard" methods for the identification of C. albicans are based on its ability to produce germ tubes and
chlamydospores (chlamydoconidia) on appropriate nutrient
media. However, since C. dubliniensis also produces these
structures, many isolates of C. dubliniensis have been
misidentified as C. albicans (4, 14, 15).
Therefore, in order to perform urgently required epidemiological
studies of C. dubliniensis infections, there is a need to
develop inexpensive, accurate, and easy to perform tests that will
allow the differentiation of isolates of the two species which have
been recovered from clinical samples. In this regard, a variety of
procedures have been developed and assessed in laboratories around the
world, including, among others, colony color on CHROMagar Candida
medium (19), lack of growth at 45°C (16),
immunofluorescence (1), carbohydrate assimilation profiles
(15), 
-glucosidase activity (2),
coaggregation with Fusobacterium nucleatum (8),
and PCR tests (5). Some of these tests (e.g., PCR) are
very reliable but are not yet used routinely by many clinical
microbiology laboratories, while others rely on reagents which are not
widely available (e.g., immunofluorescence with anti-C.
dubliniensis antibodies) and yet others (e.g., colony color on
CHROMagar Candida medium) are unreliable. In the original description
of C. dubliniensis, it was noted that this species produces
much higher numbers of chlamydospores than C. albicans when grown on rice-agar-Tween agar (RAT; 25) but subsequent studies have shown that this trait does not provide a definitive means of
differentiating between the two species (9). In a recent study of 14 C. dubliniensis and 11 C. albicans
strains, Staib and Morschhäuser (21) reported that
colony morphology and chlamydospore production by
C. dubliniensis on Staib agar (SA; a medium originally developed for the identification of Cryptococcus neoformans)
could form the basis of a simple and accurate test for distinguishing this species from C. albicans.
In the present study, we evaluated the usefulness of colony morphology
and chlamydospore production on SA and on caffeic
acid-ferric citrate agar (CAF; a defined medium also developed to aid
in the identification of C. neoformans) as a means of
differentiating C. albicans from C. dubliniensis
using a large collection of C. dubliniensis isolates
recovered from individuals in 18 different countries around the world.
| |
MATERIALS AND METHODS |
Yeast isolates.
The yeast isolates and reference strains
used in this investigation are listed in Table
1. A total of 296 isolates were studied, including 130 C. dubliniensis isolates and 166 C. albicans isolates. All isolates were from the culture collection
of the Microbiology Research Laboratory, Department of Oral Medicine
and Oral Pathology, School of Dental Science, Trinity College,
University of Dublin, Dublin, Republic of Ireland. Each isolate was
originally recovered from one or more specimens from a separate
individual, and its identity was confirmed using the API ID 32C
(bioMérieux, Marcy l'Étoile, France) yeast
identification system, growth at 45°C, and PCR analysis with C. dubliniensis-specific primers (5, 15, 16).
Chemicals, enzymes, and oligonucleotides.
Analar-grade or
molecular biology grade chemicals were purchased from Sigma-Aldrich or
BDH (Poole, Dorset, United Kingdom). Enzymes were purchased from Roche
Diagnostics Ltd. (Lewes, East Sussex, United Kingdom) or the Promega
Corporation (Madison, Wis.) and used in accordance with the
manufacturer's instructions. Custom-synthesized oligonucleotides were
purchased from Sigma-Genosys Biotechnologies (Pampisford, Cambridge,
United Kingdom).
Culture media and growth conditions.
Stock cultures of yeast
isolates were maintained on plastic beads in Protect cryovials
(Technical Service Consultants Ltd., Lancashire, United Kingdom) at
80°C. For each isolate, two or three plastic beads were removed
from their respective cryovials using a sterile plastic loop, allowed
to thaw, and then used to inoculate potato dextrose agar (PDA; Oxoid)
medium. Forty-eight-hour-old PDA medium cultures grown at 37°C were
used as the source of inoculua for subsequent experiments with SA and
CAF. SA (20) and CAF (7) were prepared fresh
as described previously and used immediately. SA was prepared by first
making an aqueous extract of Guizotia abyssinica seed (Power
Seeds, Kildare, Republic of Ireland) by pulverizing 50 g of seed
in a Moulinex B57 domestic blender for 2.5 min and then adding the
ground seeds to 1 liter of distilled water, followed by boiling for 30 min. The seed extract was cooled and filtered, and the following
ingredients were added: glucose, 1 g;
KH2PO4, 1 g; creatinine, 1 g. The pH
was adjusted to 5.5, the volume was readjusted to 1 liter, and 15 g of agar (Difco) was then added before autoclaving. The composition of
CAF (per liter) was as follows: NHSO4, 5 g; glucose,
5 g; yeast extract, 2 g; K2HPO4,
0.8 g; MgSO4 · 7H2O, 0.7 g;
caffeic acid, 0.18 g; chloramphenicol, 0.05 g; ferric
citrate, 0.002 g.
A 48-h-old single colony from a PDA medium plate culture of each
isolate to be tested was separately streak inoculated with
a sterile
wire loop onto SA and CAF, respectively, contained in
90-mm-diameter
petri dishes (25 ml of agar per plate) and incubated
at 30°C for 72 to 120 h. Gross colony morphologic features were
examined visually
on both media at 24-h intervals, and the data
were recorded. Yeast
colonies were also evaluated microscopically
to detect the presence or
absence of chlamydospore formation following
48 to 120 h of incubation on SA and on CAF. For each isolate,
10 well-separated
single colonies were chosen at random and stained
by the addition of 1 drop of 1% (wt/vol) lactophenol cotton blue
stain (
10) to
enhance the detection of chlamydospores. Lactophenol
cotton
blue preferentially stains chlamydospores more intensely
than suspensor cells, pseudomycelium, and blastospores (blastoconidia;
25). Colonies were allowed to stain for 5 min and then covered
with
sterile glass coverslips and examined microscopically under
bright-field illumination using a ×40 objective. Plates containing
isolates that did not exhibit detectable chlamydospore
formation
within 120 h were re-examined following further
incubation at
intervals of 24 h for up to 3 weeks in total. All
isolates were
also tested for chlamydospore formation on
RAT (bioMérieux) as
described previously (
25).
All of the isolates included in this study were examined on SA and CFA
on at least two separate occasions with different batches
of medium
prepared from different lots of
reagents.
| |
RESULTS AND DISCUSSION |
Growth of Candida isolates on SA and CFA.
All 296 yeast isolates grew on both SA and CAF and yielded grey-white colonies.
On SA, all of the 166 C. albicans isolates tested
produced smooth, shiny colonies after 48 h of incubation (Fig.
1a). In all but three isolates, the
colonies were found upon microscopic examination to be composed only of
blastospores. Colonies of the three isolates consisted mainly of
blastospores with a few pseudohyphal elements after 48 and 72 h of
incubation. Similar findings were observed after 96 and 120 h of
incubation.
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FIG. 1.
Morphological appearance of C. dubliniensis and C. albicans colonies on SA
following 72 h of incubation at 30°C. (a) Smooth, shiny
colonies exhibited by C. albicans strain 132A
(6). (b) Rough colonies exhibited by C. dubliniensis strain CD36 (25) displaying a hyphal
fringe or halo.
|
|
In contrast, 127 (97.7%) of the 130
C. dubliniensis
isolates tested on SA yielded rough colonies, the majority (84; 64.6%)
of which also exhibited a hyphal halo or fringe around the colonies
visible to the naked eye after 72 h of incubation (Fig.
1b). The
rough colonies were composed of mycelial forms (predominantly
pseudohyphae) and blastospores. The three remaining
C. dubliniensis isolates (two from Norway and one from Canada)
produced smooth,
shiny colonies on SA that were similar in
appearance and composition
to those of
C. albicans isolates,
even after 2 weeks of incubation.
The identity of these isolates
as
C. dubliniensis was reconfirmed
using PCR with
C. dubliniensis-specific primers, by carbohydrate
assimilation profile analysis with the API ID 32C system, and
by
absence of growth at 45°C. Apart from these three isolates,
the
difference between the
C. dubliniensis and
C. albicans isolates
was particularly evident on SA after 48 h
of incubation, and became
further enhanced after 72 h of
incubation, in the area of heavy
culture growth where the primary
inoculum was streaked (i.e.,
the
C. dubliniensis culture
growth appeared rough and the
C. albicans culture
growth appeared smooth and shiny). These findings indicated
that the
different colony morphologies exhibited by isolates of
C. dubliniensis and
C. albicans were due predominantly to
the
production of mycelial forms by
C. dubliniensis
isolates. These
results confirm the findings recently reported by Staib
and Morschhäuser
(
21) that SA can be used as a
useful means to discriminate between
isolates of
C. dubliniensis and
C. albicans. However, the method
is
not absolute, as a small minority (3 [2.3%]) of the 130
C. dubliniensis isolates tested were indistinguishable from
C. albicans based on colony morphology on
SA.
Several isolates each of
C. tropicalis,
C. glabrata, and
C. parapsilosis were also tested on SA in order to
determine whether
they could be distinguished from isolates of
C. albicans and
C. dubliniensis. The
five oral
C. glabrata isolates tested yielded
smooth,
grey-white colonies similar to those of
C. albicans on
this medium. Furthermore, of the five
C. tropicalis
isolates tested,
three yielded rough colonies similar to those of
C. dubliniensis and two yielded smooth colonies similar
to those of
C. albicans. Of the six
C. parapsilosis isolates tested, four yielded smooth,
shiny
colonies similar to those of
C. albicans and two
yielded
rough colonies similar to those of
C. dubliniensis. These findings
indicated that it would not be
possible to identify colonies of
C. albicans and
C. dubliniensis on SA based on colony morphology
alone
following primary isolation from a clinical specimen. Therefore,
we
propose that SA be used to assess clinical isolates which have
been shown to be germ tube positive or to confirm the identity
of
C. dubliniensis isolates presumptively identified
following
primary isolation on CHROMagar Candida medium or by other
means.
The use of SA to differentiate
C. dubliniensis
and
C. albicans isolates has a number of advantages
over carbohydrate assimilation
profile analysis. Firstly, the use of SA
is considerably less
expensive. Secondly, it is amenable to the
analysis of large numbers
of isolates. Finally, whereas the databases
used with many of
the commonly used commercial yeast identification
systems (e.g.,
the bioMérieux API 20C AUX and ID 32C systems)
have been updated
in recent years to include
C. dubliniensis profiles, they are
far from comprehensive. In this
regard, recent studies have highlighted
the necessity to revise the
databases to improve the accuracy
of identification of
C. dubliniensis (
15).
SA was originally developed as a means of identifying colonies of
C. neoformans, which, unlike other members of this
genus,
develops dark pigmentation on this medium. Strachan et al.
(
22)
demonstrated that similar results could be obtained
on a growth
medium containing caffeic acid extracted from
G. abyssinia seeds.
Since SA was found to be excellent for
distinguishing between
C. dubliniensis and
C. albicans, we investigated the usefulness
of the more
defined CAF to differentiate between isolates of these
species. Of the
166
C. albicans isolates included in the study,
145 (87.4%) yielded rough colonies with a mycelial halo visible
to the
naked eye after 5 days incubation. The remaining 21 (12.6%)
isolates
yielded smooth, nonshiny colonies on this medium. In
comparison, 122 (93.8%) of the 130
C. dubliniensis isolates, including
the 3 isolates which exhibited a smooth-colony phenotype on SA,
yielded
rough colonies with a mycelial halo after 5 days of incubation.
The
remaining eight (6.2%) isolates yielded rough colonies without
a
mycelial halo. Colonies of the
C. dubliniensis isolates
were
noticeably smaller (~2 mm in diameter) than the
C. albicans colonies
(~3 mm) after 5 days of incubation on CAF.
These findings indicated
that, unlike that on SA, colony morphology on
CAF could not be
used to differentiate between
C. dubliniensis and
C. albicans isolates.
Chlamydospore production on SA and CAF.
None of the 166 C. albicans isolates tested produced
chlamydospores on SA or CAF, even after prolonged
incubation periods of up to 3 weeks (Table 1). In contrast, all
isolates produced chlamydospores within 48 to 72 h on
RAT. Similarly, all 130 of the C. dubliniensis isolates
formed chlamydospores on RAT but not all produced
chlamydospores on either SA or CAF (Tables 1 and
2). A total of 111 (85.4%) of the 130 C. dubliniensis isolates formed
chlamydospores on SA, and 100 (90.1%) of these 111 produced abundant chlamydospores within 72 h, whereas
11 (9.9%) of them produced relatively few chlamydospores,
which were only detected following incubation periods of up to a week.
Similarly, 109 (83.8%) of the 130 C. dubliniensis
isolates produced chlamydospores on CAF, all but 5 within 120 h (Tables 1 and 2). Eighty-three (63.9%) of the
C. dubliniensis isolates produced
chlamydospores on both SA and CAF, whereas the remainder
produced chlamydospores on one or the other medium only
(Table 2).
On the basis of these data, we agree with Staib and Morschhäuser
that growth on SA is an efficient means of discriminating
between
C. dubliniensis and
C. albicans.
However, our results
suggest that colony morphology, rather than
chlamydospore formation,
is a more accurate criterion for
species identification, since
a significant proportion of
C. dubliniensis isolates failed to
produce chlamydospores
on SA. The disparity between our data and
that of Staib and
Morschhäuser could be due to either different
supplies of
G. abyssinica seed, to seed of different ages, or
to seed
storage conditions. However, the most likely explanation
lies in the
larger and more diverse group of
C. dubliniensis
isolates
examined in the present
study.
SA is inexpensive and readily available in many clinical mycology
laboratories and provides a simple test for the accurate
differentiation of
C. dubliniensis from
C. albicans. We propose
that colony morphology on SA is a reliable
and inexpensive phenotypic
test for confirming the identification of
C. dubliniensis and
will be of benefit for researchers
interested in studying the
incidence and epidemiology of this emerging
pathogen. We suggest
that germ tube-positive oral isolates from
HIV-positive and AIDS
patients, as well as germ tube-positive
isolates from sterile
sites from other immunocompromised
groups, should be tested on
SA in association with other
phenotypic tests for
C. dubliniensis.
The molecular basis of the phenotypic differences observed
between
C. dubliniensis and
C. albicans following growth on these
media has yet to be
established. However, comparative analysis
of gene expression on these
media could prove helpful in increasing
our understanding of dimorphism
in these
species.
| |
ACKNOWLEDGMENTS |
This study was supported by Irish Health Research Board grant
05.97. A. Al Mosaid was supported by the Ministry for Education, King
Saud University, Saudi Arabia.
We thank all of our colleagues throughout the world who have sent us
strains of C. dubliniensis.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: University of
Dublin, Microbiology Research Unit, Department of Oral Medicine and
Oral Pathology, School of Dental Science, Trinity College, Dublin 2, Republic of Ireland. Phone: 353 1 6127276. Fax: 353 1 6127295. E-mail:
dcoleman{at}dental.tcd.ie.
| |
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Journal of Clinical Microbiology, January 2001, p. 323-327, Vol. 39, No. 1
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.1.323-327.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
