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Journal of Clinical Microbiology, October 1998, p. 2869-2873, Vol. 36, No. 10
Department of Bacteriology and Mycology,
Janssen Research Foundation, 2340 Beerse, Belgium
Received 2 April 1998/Returned for modification 26 June
1998/Accepted 10 July 1998
To establish the historical prevalence of the novel yeast
species Candida dubliniensis, a survey of 2,589 yeasts
originally identified as Candida albicans and maintained in
a stock collection dating back to the early 1970s was undertaken. A
total of 590 yeasts, including 93 (18.5%) Candida dubliniensis is a
newly described yeast species that is closely related to Candida
albicans (25). The new species forms germ tubes and
chlamydospores that are almost indistinguishable from those of
C. albicans, and definitive identification of
C. dubliniensis requires evidence of nonreactivity of
its DNA with the C. albicans-specific oligonucleotide
probe Ca3 (25). C. dubliniensis appears to
have a worldwide distribution (23, 24). It has been found
primarily in oral samples from persons infected with the human
immunodeficiency virus (HIV) (3, 22-25), but it has also
been isolated from some vaginal samples from HIV-negative and
HIV-positive women (23, 25). Isolates of C. dubliniensis rapidly develop a stable fluconazole-resistant
phenotype on exposure to this antifungal agent in vitro (6).
Recognition of phenotypic characteristics that allow simple detection
and differentiation of C. dubliniensis remains a
problem in routine yeast identification. Colonies of C. dubliniensis often have an unusually dark green color within
48 h at 37°C when freshly isolated from clinical material on the
differential medium CHROMagar Candida, but this property is not
retained in subculture (21). We have observed informally
that C. dubliniensis colonies usually show a dark green
colony phenotype on this medium, even in subcultures, when incubation
is prolonged for 4 days or more. However, the normally pale green color
of some C. albicans colonies can also darken under
these circumstances, so that the color is no longer specific to
C. dubliniensis. Indeed, with prolonged incubation other color aberrations such as yellowing and purpling have
occasionally been noted with C. albicans isolates
(unpublished observations).
Another phenotypic characteristic specific for C. dubliniensis is a negative result in tests for intracellular
The earliest reports of "unusual" and "atypical" C. albicans isolates that can now be reliably recognized from their
DNA fingerprints as representing isolations of C. dubliniensis date back to 1990 (19), although older
examples of "atypical" C. albicans isolates that
may be examples of C. dubliniensis are known
(22). The oldest confirmed isolate of the species came from
a yeast culture collection where it was deposited in 1957 as
Candida stellatoidea (23, 25). The prevalence of
the species in clinical material before the mid-1990s is so far
unknown. The present survey was therefore undertaken to examine the
prevalence of isolates of C. dubliniensis existing in a
large stock collection of yeasts predominantly obtained from human
material. The findings show that isolates of C. dubliniensis from clinical material date back at least as far as
1973 and that although the species seems to be particularly associated
with HIV-infected individuals, it has also been isolated in the past
from HIV-negative subjects as well.
Cultures and reidentification.
The 2,589 yeasts studied had
been stored since the early 1970s. The isolates had originally been
identified phenotypically as C. albicans on the basis
of a positive germ tube test, together with other standard morphologic
and physiologic criteria when necessary. A total of 1,349 isolates had
been maintained in sterile distilled water (7), and 1,240 had been kept at
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Prevalence of Candida dubliniensis Isolates in a
Yeast Stock Collection
ABSTRACT
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
-glucosidase-negative
isolates among 502 isolates that showed abnormal colony colors on a
differential chromogenic agar and 497 other isolates, were subjected to
DNA fingerprinting with the moderately repetitive sequence Ca3. On this
basis, 53 yeasts were reidentified as C. dubliniensis
(including the C. dubliniensis type strain, included
as a blind control in the panel of yeasts). The 52 newly found isolates
came from 36 different persons, and a further 3 C. dubliniensis isolates were detected by DNA fingerprinting of
previously untested isolates from one of these individuals. The
prevalence of C. dubliniensis among yeasts in
oral and fecal samples was significantly higher than that among yeasts
from other anatomical sites and was significantly higher among human
immunodeficiency virus (HIV)-infected individuals than among known or
presumed HIV-negative individuals. However, a single vaginal isolate
and two oral isolates from healthy volunteers confirmed that the
species is restricted neither to gastrointestinal sites nor to patients
with overt disease. The oldest examples of C. dubliniensis were from oral samples of three patients in the
United Kingdom in 1973 and 1975. In comparison with age-matched control
isolates of C. albicans, the
C. dubliniensis isolates showed slightly higher levels
of susceptibility in vitro to amphotericin B and flucytosine and
slightly lower levels of susceptibility to three azole antifungal
agents.
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
-glucosidase activity (1, 21, 25). However, in its
present form this test is too expensive and complex to be used
routinely for the screening of yeast isolates on a large scale.
Recently, the absence of growth of C. dubliniensis at
45°C has been shown to be a simple and reliable characteristic for
differentiation of this species from C. albicans
(17).
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
70°C in 10% glycerol. Most of the yeasts were
originally isolated from clinical material; a small number came from
other culture collections or from inanimate sources. Some of the yeasts
have been the subject of previous publications, including several
epidemiologic studies of C. albicans from various
patient groups, anatomical sources, and geographical locations (2,
8, 9, 11-14, 16, 19). Among the 2,589 yeasts, 81 (3.1%) were
originally isolated in the 1970s, 990 (38.2%) were originally isolated
in the 1980s, and 1,216 (47.0%) were originally isolated between 1990 and 1996. For 302 of the specimens (11.7%) the date of isolation was
unknown. The number of yeasts from 1995 and 1996 was unusually small,
only 66 isolates, since most of the C. albicans and
C. dubliniensis isolates obtained in those years were
the subject of a prospective study that has already been described
(21) and were therefore not included as part of the present
retrospective study. The exception was the type strain of C. dubliniensis, which was included in the panel under its collection
number as a control for the blind detection of C. dubliniensis.
-glucosidase activity (1, 21) and DNA
fingerprinting by Southern blotting with the moderately repetitive,
C. albicans-specific oligonucleotide sequence Ca3
(20, 21). A random selection of 896 isolates with the
typical C. albicans green colony color was also tested by one or both of these methods. All isolates that gave negative results in the -glucosidase tests were retested to confirm the negative result; only isolates that were negative on retesting were
recorded as testing true negative by the test. All isolates that were
tested by DNA fingerprinting and that showed only weak hybridization
with the Ca3 probe in the region of high-molecular-weight bands were
identified as C. dubliniensis. The tests were done by
operators who knew only the stock reference number of each isolate and
who were therefore blinded for possible biases concerning sources and
other information about the isolates at the times that the
retrospective screening tests were done.
Susceptibility testing. Isolates of C. dubliniensis were tested for susceptibility to amphotericin B, flucytosine, fluconazole, ketoconazole, and itraconazole by a spectrophotometric broth microdilution method (15) based on the U.S. National Committee for Clinical Laboratory Standards M27 reference method. For each C. dubliniensis isolate tested, a C. albicans isolate from the stock collection was tested in parallel; in each case the control isolate was the C. albicans isolate with the closest possible stock number to the corresponding C. dubliniensis isolate.
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RESULTS |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Reidentification of C. dubliniensis isolates.
Among the 2,589 yeasts cultured on CHROMagar Candida, 502 (19.4%)
demonstrated some abnormality of the green colony color characteristic of C. albicans after prolonged
incubation at 37°C. Among these 502 isolates, 93 (18.5%) were
negative in tests for -glucosidase activity. Among the 2,087 yeasts whose colonies retained the color characteristic of
C. albicans even after prolonged incubation, 896 were
randomly tested for intracellular -glucosidase activity and 30 (3.3%) were negative. These results indicate a significant association
between abnormal colony color and negative -glucosidase tests
(
2 = 92; P < 0.0001).
-glucosidase-negative
isolates, was studied by DNA fingerprinting with the Ca3
probe. Of these, 53 (9.0%) gave hybridization patterns characteristic of C. dubliniensis; the remaining 537 all gave strong
Ca3 hybridization with patterns confirming their original
identification as C. albicans. All of the 53 isolates reidentified by DNA fingerprinting as C. dubliniensis (these included the C. dubliniensis type strain) were negative in the test for
-glucosidase activity, and 51 of them had given abnormal green
colony colors on the differential medium. Of the 537 isolates shown to
be C. albicans by DNA fingerprinting, 406 had shown an
abnormal green color on CHROMagar Candida medium, with 41 of these
negative for -glucosidase activity. Of the 131 C. albicans isolates that gave a normal green colony color, 26 were
negative for -glucosidase activity.
When the details for the 53 isolates reidentified as C. dubliniensis were analyzed (see below) a further three isolates of the species were found in the stock collection. These gave normal green
colonies on the differential medium, but they were negative for
-glucosidase activity. The final total of C. dubliniensis isolates found by rescrutiny of the yeast stock
collection was therefore 56, comprising 55 newly reidentified isolates
and the C. dubliniensis type strain. The overall
prevalence of C. dubliniensis among the whole panel of
putative C. albicans isolates tested was therefore 55 of 2,588, or 2.1%.
C. dubliniensis: epidemiologic aspects.
Table
1 presents the frequency of occurrence of
the 55 newly reidentified C. dubliniensis isolations as
a function of date of isolation, country of isolation, anatomical site
of isolation, and clinical setting of the patient for the samples for
which this information was known. The majority of C. dubliniensis isolates came from oral and fecal samples, with only
a single isolate from a vulvovaginal sample and none from deep organs,
skin, or nail (2 = 19.4; P < 0.01).
There was also a statistically significant difference in the prevalence
of C. dubliniensis between patient types, with the
highest prevalence among isolates from HIV-infected patients
(2 = 15.0; P < 0.05). With the
exception of the small number of samples from the period from 1980 to
1984, about 10 to 12% of the yeasts originally deposited in the
culture collection as C. albicans in each time period
since 1970 and selected for DNA fingerprinting were now reidentified as
C. dubliniensis. Some differences in the prevalence of
C. dubliniensis isolates between countries of origin
were evident, but these were not statistically significant (2 = 9.2; P > 0.05).
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-glucosidase test and with the Ca3 fingerprinting gel: its characteristics were definitely those of C. albicans, not C. dubliniensis. For patient LB, 12 positive yeast cultures had been stocked in distilled water, of which 2 represented a single isolate and were stocked twice with different
reference numbers. Retesting of the three isolates from patient LB that had not been detected as C. dubliniensis in the blinded
screening showed that these were also isolates of C. dubliniensis according to their DNA fingerprinting patterns. These
three isolates were also negative for -glucosidase activity, but
they had not shown colony color abnormalities in the blinded screening.
Hematology patient LB was therefore the source of 12 C. dubliniensis isolates from 11 fecal or oral specimens obtained
over a 3-month period in 1986.
From a survey of oral Candida isolates from AIDS patients in
the United Kingdom (19), seven yeasts were now reidentified as C. dubliniensis (Table 2). They came from three
patients: patients TT, JB, and NE. Three other isolates in the
collection from patient TT were confirmed as C. albicans, but the four isolates from patient JB and the two
isolates from patient NE that are listed in Table 2 were the only
isolates from these individuals available in the stock collection.
Among the 15 C. dubliniensis isolates found in the
collection among cultures stocked since 1990, each one came from a
separate patient, all but three of whom were HIV positive.
Susceptibility testing.
Some differences in antifungal
susceptibilities between the C. dubliniensis isolates
and their matched C. albicans controls were apparent.
In total, 58 isolates of each species were tested in two separate runs
of susceptibility determinations. The C. dubliniensis
isolates tested included 49 of the 55 strains reidentified in the
present study, the C. dubliniensis type strain, and 8 isolates obtained in 1995 in a prospective study of Candida
carriage in HIV-positive patients (21). Few of the isolates
were resistant to any of the five agents tested except for flucytosine
and fluconazole. One isolate of C. dubliniensis was
susceptible to flucytosine only at 32 µg/ml, and another was
inhibited by fluconazole only at 64 µg/ml. Among the 58 C. albicans isolates, 4 were resistant to
flucytosine (MIC, >64 µg/ml) and 3 were resistant to
fluconazole (MIC, 
64 µg/ml). The geometric mean MICs for the panels
of isolates suggested a trend toward higher levels of susceptibility to
amphotericin B (0.25 versus 0.43 µg/ml) and flucytosine (0.074 versus
0.21 µg/ml) for the C. dubliniensis isolates than for
the C. albicans isolates. For the three azole
antifungal agents, by contrast, the geometric mean MICs were
consistently higher for the C. dubliniensis isolates than for the C. albicans isolates:
fluconazole, 0.83 versus 0.34 µg/ml; itraconazole, 0.027 versus
0.009 µg/ml; ketoconazole, 0.017 versus 0.007 µg/ml.
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DISCUSSION |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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This study has shown that C. dubliniensis isolates dating back to 1973 could be found by retesting of a collection of 2,589 yeasts, mostly of clinical origin. In total, 55 isolates of C. dubliniensis from 36 different persons were found by the process of reidentification. C. dubliniensis was reidentified under blinded test conditions more than once in different samples from the same patient and even from the same sample restocked under different reference numbers in two instances. This finding suggests that the quality of the stock collection was high and that the older isolates now identified as C. dubliniensis are genuine early examples of the species. If some or all of the C. dubliniensis isolates found in this study had been the result of cross contamination of specimens now or at previous times of reisolation and restockage of the yeasts, then they would be expected to have assumed a more random distribution in the collection rather than an association with specimens from particular patients.
Primary recognition of C. dubliniensis remains a
technical problem. In the present study the green color of yeast
colonies after prolonged incubation on a differential medium was
intended to be used as a primary indicator of yeast phenotypes likely
to be different from C. albicans, with the more complex
test for intracellular -glucosidase activity used as a secondary
test to exclude C. albicans isolates. However, the
colony color was not a reliable criterion for the detection of
C. dubliniensis among the stock yeast isolates. Two
isolates of the species gave normal colony colors in the blind phase of
screening; three further isolates with normal colony colors were
subsequently found to be C. dubliniensis by specific
rescrutiny of isolates from one patient of particular interest.
The test for -glucosidase activity, while not specific for
C. dubliniensis (we found 67 -glucosidase-negative
isolates of C. albicans among 537 isolates tested),
nevertheless gave negative results for all 56 C. dubliniensis isolates tested. Indeed, -glucosidase-positive strains of C. dubliniensis have not yet been described
anywhere, to our knowledge (1, 21-23). We tested a total of
1,398 yeasts from the stock collection for -glucosidase activity
over a period of 10 months; to have tested all 2,589 yeasts would have
been prohibitively expensive in terms of both cost and the labor
involved. We can be confident that all C. dubliniensis
isolates among those 1,398 isolates were detected, since all
-glucosidase-negative isolates were subjected to DNA fingerprinting.
However, there remain 1,191 yeast isolates among which there may still
be examples of C. dubliniensis that were not detected
because they gave normal colony colors on the differential medium.
Since C. dubliniensis often gives atypical results in
carbohydrate assimilation tests (21-25), it is also
possible that isolates of C. dubliniensis identified as
species other than C. albicans have been deposited in
our collection, although the morphologic phenotype of C. dubliniensis should have minimized such occurrences.
Since this study was completed and first submitted for publication, Pinjon and colleagues (17) have shown that growth (C. albicans) versus nongrowth (C. dubliniensis) of germ tube-forming yeasts at 45°C is a reliable and simple test for the differentiation of the two species. Differential growth at 45°C could have been used as a cheap and simple means of detecting possible C. dubliniensis isolates in our collection.
Sullivan et al. (24) established that the distribution
of C. dubliniensis is widespread
probably
worldwideand that the species has been found in patients
outside the groups of HIV-positive individuals in whom its high degree
of prevalence led to its initial discovery (22-24). Almost
all studies of C. dubliniensis so far have been of oral
isolates. Among oral isolates from patients with and without HIV
infection, Coleman et al. (3) reported an overall
prevalence of 26.4% among 382 HIV-positive patients and 6.1% among
HIV-negative patients. In the present study, isolates from
HIV-positive patients were certainly the richest single source of
C. dubliniensis (Table 2), and the five Spanish drug
abusers from whom C. dubliniensis was isolated may well
also have included some HIV-positive individuals. However, we also
frequently found the species among patients with hematologic
malignancies undergoing or about to undergo chemotherapy. C. dubliniensis has recently been found to be the cause of three
cases of candidemia among patients in this clinical setting
(4).
The occurrence of C. dubliniensis in fecal samples is also a novel finding of the present study. The single vaginal isolate and the two oral isolates from healthy student volunteers suggest that the distribution of C. dubliniensis may in fact be very similar to that of C. albicans. The standard practice of many laboratories of reporting as "C. albicans" all yeast isolates that form germ tubes in serum is an obstacle to the routine recognition of C. dubliniensis. Definition of the true prevalence of this species in material from patients and from healthy subjects will depend on improvements in techniques for the differential recognition of C. dubliniensis and C. albicans.
Like Moran and colleagues (6), we found most of our isolates of C. dubliniensis to be susceptible to systemically used antifungal agents. Those investigators found fluconazole MICs at or above the 16 µg/ml for 4 of 20 C. dubliniensis isolates. The prevalence of such isolates among our test panel was 3 among 58 isolates. A single isolate was resistant to both fluconazole and itraconazole according to the breakpoints established by the National Committee for Clinical Laboratory Standards (MICs, 64 and 1.0 µg/ml, respectively) (18). We did not attempt experiments similar to those of Moran et al. (6) to evaluate the ease of induction of fluconazole resistance in our C. dubliniensis isolates.
The oldest known isolate of C. dubliniensis so far confirmed by DNA fingerprinting had been deposited in a stock collection as "C. stellatoidea" in 1957 (22, 24). Our survey confirms that C. dubliniensis was present in clinical samples decades before the new species was first described. It has been encountered in samples from HIV-negative patients, including healthy individuals, as well as in oral samples from AIDs patients, in whom its prevalence is highest. It accounted for at least 2% of the yeasts initially identified as C. albicans among the isolates in our stock collection and for approximately 10% of the isolates selected for DNA fingerprinting. Its detection and differentiation from C. albicans in primary cultures require new strategies for routine yeast isolation in clinical laboratories: differential growth at 45°C provides a straightforward test for the presumptive differentiation of germ tube-positive yeast isolates. Determination of the clinical importance of C. dubliniensis requires further study.
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ACKNOWLEDGMENTS |
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We express our gratitude to the very many physicians, mycologists, and others whose collaboration and cooperation over many years has led to the creation of the large yeast stock collection examined in this study. We gratefully acknowledge the skilled technical assistance of Peter De Backker and Frank Geenen.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Bacteriology and Mycology, Janssen Research Foundation, B-2340 Beerse, Belgium. Phone: (32) 14-603004. Fax: (32) 14-605403. E-mail: fodds{at}janbe.jnj.com.
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REFERENCES |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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| 1. | Boerlin, P., F. Boerlin-Petzold, C. Durrussel, M. Addo, J. Pagani, J. Chave, and J. Bille. 1995. Cluster of atypical Candida albicans isolates in a group of human immunodeficiency virus-positive drug users. J. Clin. Microbiol. 33:1129-1135[Abstract]. |
| 2. | Burnie, J. P., F. C. Odds, W. Lee, C. Webster, and J. D. Williams. 1985. Outbreak of systemic Candida albicans in intensive care unit caused by cross infection. Br. Med. J. 290:746-748. |
| 3. | Coleman, D. C., D. J. Sullivan, D. E. Bennett, G. P. Moran, H. J. Barry, and D. B. Shanley. 1997. Candidiasis: the emergence of a novel species, Candida dubliniensis. AIDS 11:557-567[Medline]. |
| 4. | Meis, J. Personal communication. |
| 5. | Miro, J. M., J. Puig de la Bellacasa, F. C. Odds, F. C., B. K. Gill, J. Bisbe, J. M. Gatell, J. Gonzalez, X. Latorre, M. T. Jiminez de Anta, E. Soriano, and J. Garcia San Miguel. 1987. Systemic candidiasis in Spanish heroin addicts: a possible source of infection. J. Infect. Dis. 156:857-858[Medline]. |
| 6. | Moran, G. P., D. J. Sullivan, M. C. Henman, C. E. McCreary, B. J. Harrington, D. B. Shanley, and D. C. Coleman. 1997. Antifungal drug susceptibilities of oral Candida dubliniensis isolates from human immunodeficiency virus (HIV)-infected and non-HIV-infected subjects and generation of stable fluconazole-resistant derivatives in vitro. Antimicrob. Agents Chemother. 41:617-623[Abstract]. |
| 7. | Odds, F. C. 1991. Long-term preservation of pathogenic yeasts under distilled water. J. Med. Vet. Mycol. 29:413-415[Medline]. |
| 8. | Odds, F. C., A. B. Abbott, T. A. G. Reed, and F. E. Willmott. 1983. Candida albicans strain types from the genitalia of patients with and without Candida infection. Eur. J. Obstet. Gynecol. 15:37-43[Medline]. |
| 9. |
Odds, F. C.,
A. B. Abbott,
R. L. Stiller,
H. J. Scholer,
A. Polak, and D. A. Stevens.
1983.
Analysis of Candida albicans phenotypes from different geographical and anatomical sources.
J. Clin. Microbiol.
18:849-857 |
| 10. |
Odds, F. C., and R. Bernaerts.
1994.
CHROMagar Candida, a new, differential isolation medium for the presumptive identification of clinically important Candida species.
J. Clin. Microbiol.
32:1923-1929 |
| 11. |
Odds, F. C., and E. G. V. Evans.
1980.
Distribution of pathogenic yeasts and humoral antibodies to Candida among hospitalized patients.
J. Clin. Pathol.
33:750-756 |
| 12. | Odds, F. C., E. G. V. Evans, M. A. R. Taylor, and J. K. Wales. 1978. Prevalence of pathogenic yeasts and humoral antibodies to Candida in diabetic patients. J. Clin. Pathol. 3:840-844. |
| 13. |
Odds, F. C.,
C. C. Kibbler,
E. Walker,
A. Bhamra,
H. G. Prentice, and P. Noone.
1989.
Carriage of Candida species and C. albicans biotypes in patients undergoing chemotherapy or bone marrow transplantation for haematological diseases.
J. Clin. Pathol.
42:1259-1266 |
| 14. |
Odds, F. C.,
A. Palacio-Hernanz,
J. Cuadra, and J. Sanchez.
1987.
Disseminated Candida infection syndrome in heroin addictsdominance of a single Candida albicans biotype.
J. Med. Microbiol.
23:275-277 |
| 15. | Odds, F. C., L. Vranckx, and F. Woestenborghs. 1995. Antifungal susceptibility testing of yeasts: evaluation of technical variables for test automation. Antimicrob. Agents Chemother. 39:2051-2060[Abstract]. |
| 16. | Odds, F. C., C. E. Webster, V. C. Riley, and P. G. Fisk. 1987. Epidemiology of vaginal Candida infection: significance of numbers of vaginal yeasts and their biotypes. Eur. J. Obstet. Gynecol. Reprod. Biol. 25:53-66[Medline]. |
| 17. |
Pinjon, E.,
D. Sullivan,
I. Salkin,
D. Shanley, and D. Coleman.
1998.
Simple, inexpensive, reliable method for differentiation of Candida dubliniensis from Candida albicans.
J. Clin. Microbiol.
36:2093-2095 |
| 18. | Rex, J. H., M. A. Pfaller, J. N. Galgiani, M. S. Bartlett, A. Espinel-Ingroff, M. A. Ghannoum, M. Lancaster, F. C. Odds, M. G. Rinaldi, T. J. Walsh, and A. L. Barry. 1997. Development of interpretive breakpoints for antifungal susceptibility testing: conceptual framework and analysis of in vitro-in vivo correlation data for fluconazole, itraconazole, and Candida infections. Clin. Infect. Dis. 124:235-247. |
| 19. |
Schmid, J.,
F. C. Odds,
M. W. Wiselka,
K. G. Nicholson, and D. R. Soll.
1992.
Genetic similarity and maintenance of Candida albicans strains from a group of AIDS patients, demonstrated by DNA fingerprinting.
J. Clin. Microbiol.
30:935-941 |
| 20. |
Schmid, J.,
E. Voss, and D. R. Soll.
1990.
Computer-assisted methods for assessing strain relatedness in Candida albicans by fingerprinting with the moderately repetitive sequence Ca3.
J. Clin. Microbiol.
28:1236-1243 |
| 21. | Schoofs, A., F. C. Odds, R. Colebunders, M. Ieven, and H. Goossens. 1997. Recognition and identification of Candida dubliniensis isolates from HIV patients: use of specialized isolation media. Eur. J. Clin. Microbiol. Infect. Dis. 16:296-300[Medline]. |
| 22. | Sullivan, D., and D. Coleman. 1997. Candida dubliniensis: an emerging opportunistic pathogen. Curr. Top. Med. Mycol. 8:15-25[Medline]. |
| 23. |
Sullivan, D., and D. Coleman.
1998.
Candida dubliniensis: characteristics and identification.
J. Clin. Microbiol.
36:329-334 |
| 24. | Sullivan, D., K. Haynes, J. Bille, P. Boerlin, L. Rodero, S. Lloyd, M. Henman, and D. Coleman. 1997. Widespread geographic distribution of oral Candida dubliniensis strains in human immunodeficiency virus-infected individuals. J. Clin. Microbiol. 35:960-964[Abstract]. |
| 25. |
Sullivan, D. J.,
T. J. Westerneng,
K. A. Haynes,
D. E. Bennett, and D. C. Coleman.
1995.
Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals.
Microbiology
141:1507-1521 |
Journal of Clinical Microbiology, October 1998, p. 2869-2873, Vol. 36, No. 10
0095-1137/98/$04.00+0
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(2004). Tobacco Agar, a New Medium for Differentiating Candida dubliniensis from Candida albicans. J. Clin. Microbiol.
42: 4796-4798
[Abstract] [Full Text] -
Ahmad, S., Khan, Z., Mokaddas, E., Khan, Z. U.
(2004). Isolation and molecular identification of Candida dubliniensis from non-human immunodeficiency virus-infected patients in Kuwait. J Med Microbiol
53: 633-637
[Abstract] [Full Text] -
Pinjon, E., Moran, G. P., Jackson, C. J., Kelly, S. L., Sanglard, D., Coleman, D. C., Sullivan, D. J.
(2003). Molecular Mechanisms of Itraconazole Resistance in Candida dubliniensis. Antimicrob. Agents Chemother.
47: 2424-2437
[Abstract] [Full Text] -
Kim, J. O., Garofalo, L., Blecker-Shelly, D., McGowan, K. L.
(2003). Candida dubliniensis Infections in a Pediatric Population: Retrospective Identification from Clinical Laboratory Isolates of Candida albicans. J. Clin. Microbiol.
41: 3354-3357
[Abstract] [Full Text] -
Montour, L., Tey, R., Xu, J.
(2003). Isolation of Candida dubliniensis in an Aboriginal Community in Ontario, Canada. J. Clin. Microbiol.
41: 3423-3426
[Abstract] [Full Text] -
Blignaut, E., Pujol, C., Joly, S., Soll, D. R.
(2003). Racial Distribution of Candida dubliniensis Colonization among South Africans. J. Clin. Microbiol.
41: 1838-1842
[Abstract] [Full Text] -
Sancak, B., Rex, J. H., Paetznick, V., Chen, E., Rodriguez, J.
(2003). Evaluation of a Method for Identification of Candida dubliniensis Bloodstream Isolates. J. Clin. Microbiol.
41: 489-491
[Abstract] [Full Text] -
Perea, S., Lopez-Ribot, J. L., Wickes, B. L., Kirkpatrick, W. R., Dib, O. P., Bachmann, S. P., Keller, S. M., Martinez, M., Patterson, T. F.
(2002). Molecular Mechanisms of Fluconazole Resistance in Candida dubliniensis Isolates from Human Immunodeficiency Virus-Infected Patients with Oropharyngeal Candidiasis. Antimicrob. Agents Chemother.
46: 1695-1703
[Abstract] [Full Text] -
Ramage, G., Vande Walle, K., Wickes, B. L., Lopez-Ribot, J. L.
(2001). Biofilm Formation by Candida dubliniensis. J. Clin. Microbiol.
39: 3234-3240
[Abstract] [Full Text] -
Guiver, M, Levi, K, Oppenheim, B A
(2001). Rapid identification of candida species by TaqMan PCR. J. Clin. Pathol.
54: 362-366
[Abstract] [Full Text] -
Stevens, D. A., Coleman, D. C., Sullivan, D. J.
(2001). First Report of Candida dubliniensis in the Middle East. J. Clin. Microbiol.
39: 416-416
[Full Text] -
Peltroche-Llacsahuanga, H., Schmidt, S., Seibold, M., Lütticken, R., Haase, G.
(2000). Differentiation between Candida dubliniensis and Candida albicans by Fatty Acid Methyl Ester Analysis Using Gas-Liquid Chromatography. J. Clin. Microbiol.
38: 3696-3704
[Abstract] [Full Text] -
Meis, J. F. G. M., Verduyn Lunel, F. M., Verweij, P. E., Voss;, A., Coleman, D.
(2000). One-Year Prevalence of Candida dublinienis in a Dutch University Hospital. J. Clin. Microbiol.
38: 3139-3140
[Full Text] -
Chen, Y. C., Eisner, J. D., Kattar, M. M., Rassoulian-Barrett, S. L., LaFe, K., Yarfitz, S. L., Limaye, A. P., Cookson, B. T.
(2000). Identification of Medically Important Yeasts Using PCR-Based Detection of DNA Sequence Polymorphisms in the Internal Transcribed Spacer 2 Region of the rRNA Genes. J. Clin. Microbiol.
38: 2302-2310
[Abstract] [Full Text] -
Jabra-Rizk, M. A., Falkler, W. A. Jr., Merz, W. G., Baqui, A. A. M. A., Kelley, J. I., Meiller, T. F.
(2000). Retrospective Identification and Characterization of Candida dubliniensis Isolates among Candida albicans Clinical Laboratory Isolates from Human Immunodeficiency Virus (HIV)-Infected and Non-HIV-Infected Individuals. J. Clin. Microbiol.
38: 2423-2426
[Abstract] [Full Text] -
Tintelnot, K., Haase, G., Seibold, M., Bergmann, F., Staemmler, M., Franz, T., Naumann, D.
(2000). Evaluation of Phenotypic Markers for Selection and Identification of Candida dubliniensis. J. Clin. Microbiol.
38: 1599-1608
[Abstract] [Full Text] -
Polacheck, I., Strahilevitz, J., Sullivan, D., Donnelly, S., Salkin, I. F., Coleman, D. C.
(2000). Recovery of Candida dubliniensis from Non-Human Immunodeficiency Virus-Infected Patients in Israel. J. Clin. Microbiol.
38: 170-174
[Abstract] [Full Text] -
Gales, A. C., Pfaller, M. A., Houston, A. K., Joly, S., Sullivan, D. J., Coleman, D. C., Soll, D. R.
(1999). Identification of Candida dubliniensis Based on Temperature and Utilization of Xylose and alpha -Methyl-D-Glucoside as Determined with the API 20C AUX and Vitek YBC Systems. J. Clin. Microbiol.
37: 3804-3808
[Abstract] [Full Text] -
Pincus, D. H., Coleman, D. C., Pruitt, W. R., Padhye, A. A., Salkin, I. F., Geimer, M., Bassel, A., Sullivan, D. J., Clarke, M., Hearn, V.
(1999). Rapid Identification of Candida dubliniensis with Commercial Yeast Identification Systems. J. Clin. Microbiol.
37: 3533-3539
[Abstract] [Full Text] -
Jabra-Rizk, M. A., Falkler, W. A. Jr., Merz, W. G., Kelley, J. I., Baqui, A. A. M. A., Meiller, T. F.
(1999). Coaggregation of Candida dubliniensis with Fusobacterium nucleatum. J. Clin. Microbiol.
37: 1464-1468
[Abstract] [Full Text] -
Jabra-Rizk, M. A., Baqui, A. A. M. A., Kelley, J. I., Falkler, W. A. Jr., Merz, W. G., Meiller, T. F.
(1999). Identification of Candida dubliniensis in a Prospective Study of Patients in the United States. J. Clin. Microbiol.
37: 321-326
[Abstract] [Full Text] -
Koehler, A. P., Chu, K.-C., Houang, E. T. S., Cheng, A. F. B.
(1999). Simple, Reliable, and Cost-Effective Yeast Identification Scheme for the Clinical Laboratory. J. Clin. Microbiol.
37: 422-426
[Abstract] [Full Text]
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