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Journal of Clinical Microbiology, October 1998, p. 3007-3012, Vol. 36, No. 10
Departments of
Medicine1 and
Pathology,
Received 14 May 1998/Returned for modification 16 June
1998/Accepted 7 July 1998
Candida dubliniensis has been associated with
oropharyngeal candidiasis in patients infected with human
immunodeficiency virus (HIV). C. dubliniensis isolates may
have been improperly characterized as atypical Candida
albicans due to the phenotypic similarity between the two
species. Prospective screening of oral rinses from 63 HIV-infected
patients detected atypical dark green isolates on CHROMagar Candida
compared to typical C. albicans isolates, which are light
green. Forty-eight atypical isolates and three control strains were
characterized by germ tube formation, differential growth at 37, 42, and 45°C, identification by API 20C, fluorescence, chlamydoconidium
production, and fingerprinting by Ca3 probe DNA hybridization patterns.
All isolates were germ tube positive. Very poor or no growth occurred
at 42°C with 22 of 51 isolates. All 22 poorly growing isolates at
42°C and one isolate with growth at 42°C showed weak hybridization
of the Ca3 probe with genomic DNA, consistent with C. dubliniensis identification. No C. dubliniensis isolate but only 18 of 28 C. albicans isolates grew at
45°C. Other phenotypic or morphologic tests were less reliable in
differentiating C. dubliniensis from C. albicans. Antifungal susceptibility testing showed fluconazole
MICs ranging from Oropharyngeal candidiasis (OPC)
continues to be a common opportunistic infection in patients infected
with human immunodeficiency virus (HIV) or who have AIDS
(8-11). Candida albicans is the most common
causative agent; however, other species, such as C. glabrata, C. tropicalis, and C. krusei have
become increasingly prominent pathogens (10-12, 19). A
recently described species, C. dubliniensis, has been
associated with the presence of OPC in HIV-infected patients and has
also been recovered from healthy, non-HIV-infected patients (1,
16-18). C. dubliniensis has been reported from
patients worldwide (17) including the United States
(13), but the prevalence and antifungal susceptibility of
this species in patients from the United States has not been reported.
C. dubliniensis is closely related to C. albicans, and many C. dubliniensis isolates may have
been improperly characterized as atypical C. albicans due to
the phenotypic similarity of the two species (4, 15, 16).
For example, both species produce germ tubes and chlamydoconidia,
typically used to identify C. albicans. Variation in the
ability to differentiate the two species by using phenotypic
characteristics has led researchers to investigate more
reliable methods for proper differentiation of these isolates (15, 17) and dictates the use of a combination of
mycological, biochemical, and molecular techniques to unequivocally
identify C. dubliniensis (2, 7, 13, 16, 18).
C. dubliniensis has been reported to produce a distinctive
dark green color on CHROMagar Candida (15). However, this
atypical color may not persist after serial passage of the organism and may be less useful for identifying isolates (16). In the
present study, atypical yeast isolates were prospectively identified by serial evaluation of primary CHROMagar Candida cultures from
HIV-infected patients with OPC in San Antonio, Tex. These atypical
isolates were then screened for C. dubliniensis by using
phenotypic and genotypic assays, and the identification and prevalence
of C. dubliniensis in this population was established.
Little information is available on susceptibility patterns of clinical
isolates of C. dubliniensis. Fluconazole susceptibility testing by a modified microbroth dilution method on 20 C. dubliniensis isolates, including 15 oral isolates from
HIV-infected patients, demonstrated MICs ranging from (This study was presented in part at the 98th General Meeting of the
American Society for Microbiology, Atlanta, Ga., 17 to 21 May 1998 [abstract F48].)
Specimen collection.
Clinical samples were obtained from
HIV-infected patients enrolled in a longitudinal study of OPC at the
University of Texas Health Science Center at San Antonio and the South
Texas Veterans Health Care System, Audie L. Murphy Division, San
Antonio, Tex. (9, 10). These patients had advanced AIDS with
mean CD4 cell counts of <50/mm3. Samples were obtained
weekly during therapy and quarterly as surveillance cultures by
patients swishing and spitting 10 ml of normal saline to be used for
culture (6, 9). One-hundred microliters of swish solution
was plated on media with and without fluconazole at concentrations of 8 and 16 µg/ml and incubated at 30°C for 48 h before growth was
assessed. CHROMagar Candida (CHROMagar Company, Paris, France) with
fluconazole was used to improve detection of non-C. albicans
species and resistant isolates (6). Colonies with a
light-green color on CHROMagar Candida were considered typical C. albicans, whereas those with a dark-green color were considered
atypical C. albicans (10, 11). Isolate color was
recorded, and three to five yeast colonies from each culture were
stored on Sabouraud dextrose slants (BBL, Cockeysville, Md.) at
Reference strains.
Three control strains, including the
C. albicans reference strain 3153A, generously provided by
D. R. Soll (University of Iowa, Iowa City, Ia), the C. dubliniensis type strain NCPF 3949, kindly provided by J. R. Naglik (UMDS Guy's Hospital, London, England), and a laboratory
control strain, fluconazole-resistant C. albicans 279, were
included in this study.
Phenotypic identification tests.
All dark green atypical
C. albicans isolates were further characterized by analysis
of germ tube formation in human serum at 37°C for 3 h, growth at
37, 42, and 45°C on Sabouraud dextrose agar (BBL), identification by
API 20C (bioMérieux, Marcy-l'Etoile, France), fluorescence on
methyl-blue 93 Sabouraud dextrose agar (Difco Laboratories, Detroit,
Mich.) with illumination at 365 nm, and degree of chlamydoconidium
production on cornmeal agar (Difco Laboratories, Detroit, Mich.)
supplemented with 1% Tween 80 (Sigma, St. Louis, Mo.).
Genotypic identification tests.
Organism identification was
further investigated by restriction fragment length polymorphism (RFLP)
and DNA fingerprinting with the moderately repetitive Ca3 probe, which
as previously described is specific for C. albicans
(14). Chromosomal DNA from each isolate was prepared in
agarose plugs and separated by pulsed-field gel electrophoresis
(Bio-Rad, Hercules, Calif.). Pulsed-field gel electrophoresis was
performed using ramped switch times of 5 to 35 s for 18 h at
3 V/cm. RFLP patterns were obtained by digestion of chromosomal DNA
with EcoRI (Boehringer-Mannheim, Indianapolis, Ind.).
Digested DNA present in the RFLP gels was transferred to nylon
membranes (Nytran; Schleicher and Schuell, Keene, N.H.) and hybridized
under stringent conditions with a Ca3 probe radioactively labeled by
random priming (Random Primers DNA Labeling System; GibcoBRL,
Gaithersburg, Md.) (14). After being washed, the membranes
were exposed to autoradiography film (Du Pont, Wilmington, Del.). Films
were scanned and imported to Adobe Photoshop (Adobe Systems, Mountain
View, Calif.).
Antifungal susceptibility testing.
Susceptibility testing
was performed according to the National Committee for Clinical
Laboratory Standards macrobroth method M27-A (5). Inocula
were standardized at 85% transmittance at 530 nm by using a
spectrophotometer. Antibiotic medium 3 (Difco Laboratories) was used
for testing amphotericin B (Bristol-Myers Squibb, Princeton, N.J.)
(0.03 to 16 µg/ml), and RPMI-1640 buffered with
morpholinepropanesulfonic acid (MOPS) (American Biorganics, Niagara
Falls, N.Y.) was used for testing fluconazole (Pfizer, Inc., New York,
N.Y.) (0.125 to 64 µg/ml), itraconazole (Janssen Pharmaceutica,
Beerse, Belgium) (0.015 to 16 µg/ml), voriconazole (Pfizer, Inc.,
Sandwich, United Kingdom) (0.125 to 64 µg/ml), and SCH 56592 (Schering Plough, Kenilworth, N.J.) (0.03 to 16 µg/ml). Amphotericin
B and fluconazole were prepared from pharmaceutical solutions in
sterile water. Itraconazole, voriconazole, and SCH 56592 were prepared
from powder to stock solutions of 1,600 µg/ml in 100% polyethylene
glycol. Tubes were incubated at 35°C and read at 24 and 48 h.
Twenty-three of 63 (37%) HIV-infected patients had atypical, dark
green colonies on CHROMagar Candida in 48 episodes of OPC. Colonies
with light green color (Fig. 1, left side
of plate) were considered typical for C. albicans, whereas
those with a dark green color on primary isolation were initially
considered atypical C. albicans (Fig. 1, right side of
plate) and were subjected to further investigation.
Results of other phenotypic and genotypic identification assays are
shown in Table 1. All isolates produced
germ tubes. Abundant chlamydoconidium production was seen in only 17 of
51 (33%) isolates. Overall, of the isolates ultimately identified as
C. dubliniensis (see below), 16 of 23 (70%) had abundant
chlamydoconidium production, indicative of C. dubliniensis,
while only 1 of 28 (4%) of those identified as C. albicans
had abundant chlamydoconidium production (Table 1). With API 20C, 25 of
28 (89%) C. albicans isolates were identified as C. albicans, while 8 of 23 (35%) C. dubliniensis isolates
were misidentified as C. albicans (Table 1). Xylose utilization was negative in all 23 isolates identified as C. dubliniensis and was positive in all 28 C. albicans
strains. A total of 42 of 51 (82%) isolates were positive for
fluorescence (with illumination at 365 nm) on methyl-blue 93 Sabouraud
dextrose agar. Fluorescence was seen in 25 of 28 (89%) C. albicans isolates and in 17 of 23 (74%) C. dubliniensis isolates (Table 1).
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Detection of Candida dubliniensis in
Oropharyngeal Samples from Human Immunodeficiency Virus-Infected
Patients in North America by Primary CHROMagar Candida Screening
and Susceptibility Testing of Isolates
ABSTRACT
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
0.125 to 64 µg/ml. Two isolates were resistant to
fluconazole (MIC, 64 µg/ml) and one strain was dose dependent
susceptible (MIC, 16 µg/ml). MICs of other azoles, including
voriconazole, itraconazole, and SCH 56592, for these isolates were
lower. C. dubliniensis was identified in 11 of 63 (17%)
serially evaluated patients. Variability in phenotypic characteristics dictates the use of molecular and biochemical techniques to identify C. dubliniensis. This study identifies C. dubliniensis in HIV-infected patients from San Antonio, Tex., and
shows that C. dubliniensis is frequently detected in those
patients by using a primary CHROMagar screen.
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
1 to 32 µg/ml, with MICs of 1 µg/ml being determined for 80% of isolates
tested (4). In this study antifungal susceptibilities to
amphotericin B and four azole agents were tested for one C. dubliniensis type strain and 22 clinical isolates of C. dubliniensis from HIV-infected patients with oropharyngeal
candidiasis.
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
70°C. Forty-eight atypical clinical isolates from 23 patients were
detected and were further characterized by phenotypic and genotypic
identification tests.
RESULTS
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
View larger version (152K):
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FIG. 1.
Color comparison of typical C. albicans
(left) and atypical C. albicans (right) on CHROMagar Candida
following 48 h of incubation at 30°C.
TABLE 1.
Phenotypic and genotypic characteristics of clinical
isolates identified as atypical C. albicans upon primary
isolation on CHROMagar Candidaa
Differential temperature growth is shown in Table 1. Fifty of 51 (98%) isolates grew well at 37°C. Very poor or no growth occurred at 42 and 45°C in 22 of 51 (43%) and 33 of 51 (65%) isolates, respectively. One isolate grew poorly at all temperature settings. Twenty-eight of 29 (97%) isolates that grew well at 42°C showed good hybridization of the moderately repetitive Ca3 probe with genomic DNA, indicative of C. albicans (Fig. 2). All 22 isolates with negligible growth at 42°C and 1 strain with growth at 42°C showed weak hybridization of genomic DNA with the Ca3 probe, consistent with C. dubliniensis identification. All 23 C. dubliniensis strains demonstrated negligible or no growth at 45°C, but growth was seen in only 18 of 28 (64%) C. albicans isolates.
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Overall, 22 clinical C. dubliniensis isolates were identified from 11 of 63 (17%) serially evaluated patients. C. dubliniensis was associated with infection in 16 of 22 episodes but was detected on surveillance cultures from the remaining 6 episodes. Isolation occurred after 2.9 ± 0.2 episodes (mean ± standard error; range, 1 to 8), although isolation occurred in the initial episode for five patients. Isolation of C. dubliniensis occurred in mixed yeast cultures including C. albicans and other yeasts in 11 of 22 (50%) cases (Table 2).
Antifungal susceptibility testing was performed on the 22 isolates plus a C. dubliniensis type strain according to the
National Committee for Clinical Laboratory Standards method M-27A with amphotericin B, fluconazole, itraconazole, voriconazole, and SCH 56592 (Table 2). Isolates were all susceptible
to amphotericin B, with the MIC for 16 of 23 isolates being 0.125 µg/ml (range 0.125 to 0.5 µg/ml) at 48 h. The azoles
demonstrated a wide range of MICs. Fluconazole MICs ranged from 0.125
to 64 µg/ml. The results for the other azoles were as follows: SCH
56592, MICs of 0.03 to 0.5 µg/ml; itraconazole, MICs of 0.03 to 1 µg/ml; and voriconazole, MICs of 0.125 to 2 µg/ml. Two isolates
were resistant to fluconazole (MICs of 64 µg/ml at 48 h), and
one showed dose-dependent susceptibility (MIC = 16 µg/ml). MICs
of the other azoles for these isolates were lower: SCH 56592, MICs of
0.25 to 0.5 µg/ml; itraconazole, MICs of 0.25 to 1 µg/ml; and
voriconazole, MICs of 0.5 to 2 µg/ml.
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Although C. dubliniensis has been reported in association with oropharyngeal infection from patients in the United States (13), the prevalence and antifungal susceptibility of C. dubliniensis from patients in the United States has not been reported. In this study, the detection and prevalence of C. dubliniensis was established in a cohort of patients from San Antonio, Tex., with recurrent OPC and advanced AIDS who were serially evaluated. The prevalence of C. dubliniensis in this population was similar to that reported in HIV-infected patients in Ireland (32%) and confirms the widespread geographic distribution of this species (1, 17). However, it should be noted that the 22 clinical C. dubliniensis isolates identified in this study represent <1% of the more than 5,500 isolates collected from these 63 patients in this ongoing serial evaluation (9, 10), suggesting that these isolates appear to remain uncommon in HIV-infected patients with oropharyngeal infection.
Isolates were screened for further study by selecting for atypical, dark green color on primary CHROMagar Candida cultures. Variable results using CHROMagar Candida to identify C. dubliniensis have been reported (15, 16), which may be due to the fact that color may vary after serial passage. In this study, 22 of 48 (46%) clinical isolates initially considered to be atypical C. albicans were subsequently identified as C. dubliniensis. Since only atypical C. albicans isolates were screened for this study, it is possible that the reported prevalence could be an underestimate of the true prevalence in this population. However, more than 50 typical light green CHROMagar Candida isolates were confirmed to be C. albicans by phenotypic assays and the Ca3 probe in other studies (data not shown). These results suggest that primary isolation of atypical C. albicans colonies on chromogenic media could be used as a screening assay for additional identification studies.
Phenotypic assays demonstrated variable utility in identifying C. dubliniensis, but trends appear to exist. The use of chlamydoconidium production to identify C. dubliniensis isolates produced highly variable results and did not fully distinguish these isolates. However, of the isolates identified as C. dubliniensis, 16 of 23 (70%) had abundant chlamydoconidium production, indicative of C. dubliniensis, whereas only 1 of 28 (4%) of those identified as C. albicans had abundant chlamydoconidium production. In addition, most isolates tested were positive for fluorescence, which stands in contrast to data presented by Schoofs et al. (15) where all C. dubliniensis isolates failed to fluoresce. In the present study, 6 of 23 (29%) of the isolates showing poor Ca3 hybridization did not fluoresce, but of the isolates with Ca3 probe banding patterns indicative of C. albicans, only 3 of 28 (11%) did not fluoresce. Variability in the results obtained by using these phenotypic methods limit their utility for identifying these isolates.
API 20C was useful only when identification was confirmed as C. albicans. Fifteen of 23 (65%) of the isolates subsequently identified as C. dubliniensis were assigned "no ID" by API 20C, yet only 3 of 28 (11%) isolates identified as C. albicans by the Ca3 probe hybridization were not identified by API 20C. However, as reported by Salkin and colleagues previously (13), xylose assimilation was present in all 28 C. albicans isolates and in none of the 23 C. dubliniensis isolates. However, expense prohibits the routine use of API 20C in identifying germ tube-positive yeasts.
Differential temperature was useful in distinguishing C. albicans from C. dubliniensis. At 42 and 45°C, C. dubliniensis demonstrated negligible or no growth. All isolates identified as C. albicans grew well at 37 or 42°C. All twenty-two (100%) isolates with negligible growth at 42°C and one with growth at 42°C were confirmed as C. dubliniensis by using the Ca3 probe. However, in this study it should be noted that C. albicans did not grow as well at 42°C and that slight growth of C. dubliniensis can occur at 42°C, although growth was significantly reduced compared to that of C. albicans.
Pinjon and colleagues showed that all C. dubliniensis strains tested failed to grow at 45°C compared to growth of all but one strain of C. albicans at that temperature (7). However, in the present study, while none of the C. dubliniensis strains grew at 45°C, only 18 of 28 (64%) C. albicans isolates grew at that temperature, indicating that as a screening method, 45°C would falsely suggest the presence of C. dubliniensis in some cases.
Identification of C. albicans and C. dubliniensis was confirmed with fingerprinting of genomic DNA with the Ca3 probe. Twenty-eight of 29 isolates that grew well at 42°C had distinct hybridization patterns characteristic of C. albicans while 22 of 22 (100%) of the isolates that grew poorly at 42°C hybridized poorly and in a distinctive pattern, indicative of C. dubliniensis. Probes have recently been developed which are specific for C. dubliniensis, although use of these methods would be limited to a research setting (2, 3).
Although the pathogenicity of this yeast has not been established, C. dubliniensis was associated with clinical oropharyngeal infection in 16 of 22 (73%) cases and was present as the sole yeast isolate in 11 of 22 (50%) episodes. Risk factors and significance of this organism in oropharyngeal disease have also not been established. Isolation frequently occurred after several episodes of oropharyngeal infection but was found in the initial episode of oropharyngeal infection in five patients. Most strains remained susceptible to fluconazole although resistance or dose-dependent susceptibility occurred for three isolates. Increased susceptibility for the resistant strains was seen with itraconazole and the newer azoles, voriconazole and SCH 56592. Some isolates are resistant to fluconazole and may be more susceptible to other azole compounds.
In summary, the presence of atypical colonies on primary CHROMagar Candida cultures was used to identify isolates for further study. Differential temperature screening was extremely useful as a simple and inexpensive method for presumptively identifying C. dubliniensis from atypical C. albicans isolates for additional molecular studies (7). Twenty-two clinical isolates from 48 episodes of OPC in 63 patients were confirmed as C. dubliniensis by using a primary CHROMagar screening method followed by differential temperature growth and molecular studies to establish identity. Late-stage HIV-infected patients were found to have a C. dubliniensis prevalence rate of 17% in oropharyngeal samples by this approach. These isolates may show decreased susceptibility to fluconazole and may have increased susceptibility to newer azoles. Additional studies are needed to establish the epidemiology and significance of this organism in recurrent OPC.
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ACKNOWLEDGMENTS |
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This work was supported by Public Health Service grants 1 R01 DE11381 (to T.F.P.), 1 R29 AI42401 (to J.L.L.-R.), and M01-RR-01346 for the Frederic C. Bartter General Clinical Research Center and by a grant from Pfizer Inc. New York, N.Y. R.A.C. was supported by a Summer Research Fellowship of the Medical Hispanic Center of Excellence at the University of Texas Health Science Center at San Antonio, Tex.
We thank Kevin Hazen and Julian Naglik for helpful comments and suggestions. CHROMagar Candida was provided by the CHROMagar Company, Paris, France.
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FOOTNOTES |
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* Corresponding author. Mailing address: The University of Texas Health Science Center at San Antonio, Department of Medicine, Division of Infectious Diseases, 7703 Floyd Curl Dr., San Antonio, TX 78284-7881. Phone: (210) 567-4823. Fax: (210) 567-4670. E-mail: patterson{at}uthscsa.edu.
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REFERENCES |
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Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Journal of Clinical Microbiology, October 1998, p. 3007-3012, Vol. 36, No. 10
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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[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] -
Horvath, L. L., Hospenthal, D. R., Murray, C. K., Dooley, D. P.
(2003). Direct Isolation of Candida spp. from Blood Cultures on the Chromogenic Medium CHROMagar Candida. J. Clin. Microbiol.
41: 2629-2632
[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] -
Fotedar, R., Al Hedaithy, S. S. A.
(2003). Candida dubliniensis at a University Hospital in Saudi Arabia. J. Clin. Microbiol.
41: 1907-1911
[Abstract] [Full Text] -
Borst, A., Theelen, B., Reinders, E., Boekhout, T., Fluit, A. C., Savelkoul, P. H. M.
(2003). Use of Amplified Fragment Length Polymorphism Analysis To Identify Medically Important Candida spp., Including C. dubliniensis. J. Clin. Microbiol.
41: 1357-1362
[Abstract] [Full Text] -
Mosca, C. O., Moragues, M. D., Llovo, J., Al Mosaid, A., Coleman, D. C., Ponton, J.
(2003). Casein Agar: a Useful Medium for Differentiating Candida dubliniensis from Candida albicans. J. Clin. Microbiol.
41: 1259-1262
[Abstract] [Full Text] -
Fitzgerald, D. H., Coleman, D. C., O'Connell, B. C.
(2003). Susceptibility of Candida dubliniensis to Salivary Histatin 3. Antimicrob. Agents Chemother.
47: 70-76
[Abstract] [Full Text] -
Hospenthal, D. R., Murray, C. K., Beckius, M. L., Green, J. A., Dooley, D. P.
(2002). Persistence of Pigment Production by Yeast Isolates Grown on CHROMagar Candida Medium. J. Clin. Microbiol.
40: 4768-4770
[Abstract] [Full Text] -
Moran, G., Sullivan, D., Morschhauser, J., Coleman, D.
(2002). The Candida dubliniensis CdCDR1 Gene Is Not Essential for Fluconazole Resistance. Antimicrob. Agents Chemother.
46: 2829-2841
[Abstract] [Full Text] -
Martinez, M., Lopez-Ribot, J. L., Kirkpatrick, W. R., Coco, B. J., Bachmann, S. P., Patterson, T. F.
(2002). Replacement of Candida albicans with C. dubliniensis in Human Immunodeficiency Virus-Infected Patients with Oropharyngeal Candidiasis Treated with Fluconazole. J. Clin. Microbiol.
40: 3135-3139
[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] -
Martinez, M., Lopez-Ribot, J. L., Kirkpatrick, W. R., Bachmann, S. P., Perea, S., Ruesga, M. T., Patterson, T. F.
(2002). Heterogeneous mechanisms of azole resistance in Candida albicans clinical isolates from an HIV-infected patient on continuous fluconazole therapy for oropharyngeal candidosis. J Antimicrob Chemother
49: 515-524
[Abstract] [Full Text] -
Tamura, M., Watanabe, K., Mikami, Y., Yazawa, K., Nishimura, K.
(2001). Molecular Characterization of New Clinical Isolates of Candida albicans and C. dubliniensis in Japan: Analysis Reveals a New Genotype of C. albicans with Group I Intron. J. Clin. Microbiol.
39: 4309-4315
[Abstract] [Full Text] -
Jabra-Rizk, M. A., Ferreira, S. M. S., Sabet, M., Falkler, W. A., Merz, W. G., Meiller, T. F.
(2001). Recovery of Candida dubliniensis and Other Yeasts from Human Immunodeficiency Virus-Associated Periodontal Lesions. J. Clin. Microbiol.
39: 4520-4522
[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] -
Al Mosaid, A., Sullivan, D., Salkin, I. F., Shanley, D., Coleman, D. C.
(2001). Differentiation of Candida dubliniensis from Candida albicans on Staib Agar and Caffeic Acid-Ferric Citrate Agar. J. Clin. Microbiol.
39: 323-327
[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] -
Park, S., Wong, M., Marras, S. A. E., Cross, E. W., Kiehn, T. E., Chaturvedi, V., Tyagi, S., Perlin, D. S.
(2000). Rapid Identification of Candida dubliniensis Using a Species-Specific Molecular Beacon. J. Clin. Microbiol.
38: 2829-2836
[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] -
Kirkpatrick, W. R., Lopez-Ribot, J. L., Mcatee, R. K., Patterson, T. F.
(2000). Growth Competition between Candida dubliniensis and Candida albicans under Broth and Biofilm Growing Conditions. J. Clin. Microbiol.
38: 902-904
[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] -
Cowen, L. E., Sirjusingh, C., Summerbell, R. C., Walmsley, S., Richardson, S., Kohn, L. M., Anderson, J. B.
(1999). Multilocus Genotypes and DNA Fingerprints Do Not Predict Variation in Azole Resistance among Clinical Isolates of Candida albicans. Antimicrob. Agents Chemother.
43: 2930-2938
[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] -
Redding, S. W., Zellars, R. C., Kirkpatrick, W. R., McAtee, R. K., Caceres, M. A., Fothergill, A. W., Lopez-Ribot, J. L., Bailey, C. W., Rinaldi, M. G., Patterson, T. F.
(1999). Epidemiology of Oropharyngeal Candida Colonization and Infection in Patients Receiving Radiation for Head and Neck Cancer. J. Clin. Microbiol.
37: 3896-3900
[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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