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The International Arabic Journal

of Antimicrobial Agents ISSN 2174-9094

Efficacies of echinocandins
versus azoles antifungal agents
against Candida albicans and
Candida dubliniensis isolates

2014
Vol. 4 No. 2:4
doi: 10.3823/751

Heba A. Mohtady1,
Takwa E Meawed1,
Amani Nassar2 and
Nermin Samir1
1Medical Microbiology and Immunology
Department, Faculty of Medicine,
Zagazig University
2 Dermatology and Venerology,
Department Faculty of Medicine,
Zagazig University, Egypt.

Corresponding author:

Abstract

Takwa E Meawed

Background: Candida infection is a world wide problem with greatly

changed epidemiology. Candida dubliniensis is an emerging non-albicans, shares several phenotypic and genotypic characteristics and
closely related to Candida albicans. Fluconazole-resistant Candida spp.
becomes a significant life-threatening problem especially in high risk
patients. Echinocandins are promising antifungals with no recorded
resistance.
This study was done, first to differentiate C. dubliniensis from C. albicans by different phenotypic and molecular methods and to compare
in vitro activities of echinocandins versus azoles against Candida spp.

 takwa_farid@hotmail.com

Subjects and Methods: One hundred fifty-seven oral and vaginal swabs
collected from Dermatology Outpatients Clinic of Zagazig University
Hospitals. Cultivation was done on Brilliance Candida agar. Growth
at elevated temperature;t obacco agar VITECK2-YST and PCR were
investigated. Antifungal susceptibility testing was done to C. albicans
and C. dubliniensis to fluconazole and caspofungin by microdilution
method.
Results: A total of 76 Candida isolates were identified. Most of them
(61.8%) were C. albicans, followed by C. glabrata, C. dubliniensis and
the least was C. krusei (14.5%), (13.2%) and (10.5%), respectively. For
further differentiation between C. albicans and C. dubliniensis, PCR
had the highest sensitivity (100%). However, tobacco agar, growth
at elevated temperature and VITECK2-YST had (82.5%), (59.6%) and
(84.2%) sensitivities, respectively. The Percentage of fluconazole-resis-

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The International Arabic Journal of Antimicrobial Agents

ISSN 2174-9094

2014
Vol. 4 No. 2:4
doi: 10.3823/751

tant C. dubliniensis and C. albicans were (55.6%) and 23 (49%), respectively, and with MIC 64 g/ml for both species. Both C. albicans
and C. dubliniensis isolates were (100%) susceptible to caspofungin at
MIC range of 0.06-1 g/ml.
Conclusion: This study demonstrated that Brillance Candida Agar is a
reliable culture medium for differentiation of Candida spp., and caspofungin showed good activity against fluconazole-resistant C. albicans
and C. dubliniensis.
Key words: C. dubliniensis, C. albicans, Caspofungin, Fluconazole resistance.

Introduction
Invasive infections caused by Candida species had
been increasing worldwide in last decades. The most
frequently isolated Candida species is C.albicans,
but non-albicans Candida (NAC) is increasing cause
of significant morbidity and mortality in seriously ill
patients [1].
Exogenous and endogenous predisposing factors
render some individuals more vulnerable to infections by genus Candida such as HIV-infected patients, those under chemotherapy, broad-spectrum
antibiotics and corticosteroids for long time, terminally ill patients with hematologic diseases, transplanted patients, and patients with diabetes mellitus
[2].
Candida species accounts for about one-third of
vulvovaginitis affecting most women [3]. C. dubliniensis is an emerging pathogen causing oropharyngeal, vaginal and systemic infections. Inspite the
fact of being similar to C. albicans phenotypically,
it differs from in epidemiology, certain virulent attributes and its ability to rapidly develop fluconazole
resistance [4].

Phenotypic tests are useful tools for primary identification of C.dubliniensis, including growth at 42 and
45C, change in carbohydrate assimilation, production of chlamydospores on tobacco agar medium.
Chromogenic media such as Candidachromogenic
agarhave been developed to improve yeast identification and rapid differentiation between C. albicans
and NAC based on colonial morphology and color
production especially in mixed cultures. They are
technically simple and cost effective compared to
expensive and time consuming conventional method [5, 6,7]. Molecular methods permit a conclusive
identification by using rapid and easy differention
between C. albicans and C. dubliniensis [2].
Extensive use of azoles for treatment of Candida
infection or discontinuing their use before infection
is fully eliminated will result in changes the pattern
of fungal susceptibility. This process will promote selection of innately resistant strains or development
of secondary resistance to these drugs in a previously susceptible C.albicans [8, 9].
Echinocandins are fungicidal against fluconazole
resistant C.albicans. Guidelines favor use of echinocandins as first line therapy in haemo- dynamiThis article is available from: www.iajaa.org / www.medbrary.com

The International Arabic Journal of Antimicrobial Agents

ISSN 2174-9094

cally unstable patients, because of lack of crossresistance to azole, limited toxicity and a favorable
drug-drug interactions profile [10, 11].
The objectives of this work were first to identify
closely related species C. dubliniensis from C. albicans using phenotypic and molecular methods and
to compare in vitro their susceptibility to both caspofungin and fluconazole.

Material and Methods

Study design
A prospective cross-sectional study was carried out
over 12-month. The investigations were performed
at the Microbiology and Immunology Department
and Dermatology Outpatients Clinic, Faculty of
Medicine, Zagazig University Hospitals. All patients
with suspected fungal infections, and those with
repeated or chronic infections, patients showing no
response to antibiotic therapy or diabetics and patients with malignancies were included.

Ethical consideration
The study was approval by the Scientific Ethical
Committee at Zagazig University Hospital and informed consent from each patient was obtained.
The following laboratory procedures were performed for all collected non-repetitive specimens
from nail, skin scrapping, oral and vaginal swabs of
investigated patients:
Direct film was done using lactophenol cotton blue
for all specimens.
Primary isolation was done on Sabarauds dextrose
agar and Brain heart infusion agar (Oxoid, United
Kingdom) at 25C and 37C, respectively for primary fungal isolation.
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2014
Vol. 4 No. 2:4
doi: 10.3823/751

Germ tube test

For species differentiation: Cultivation was done on
Brilliance Candida agar (Oxoid, England).

Phenotypic methods
All Candida isolates were examined by growth at
elevated temperature 42C, 45C and cultivation
on Tobacco agar medium (according to Khan et
al., 2004). Identification of Candida species isolates
were performed by Vitek 2 ID yeast system. Vitek
2 cards were incubated at 35.5 C for 18 h, and
optical density readings were taken automatically
every 15 min. A final identification of excellent, very
good, good, acceptable, or low-discrimination was
considered to be correct.

PCR test
The identity of C. albicans and C. dubliniensis was
confirmed by PCR using the following method.
Extraction of DNA from Candida isolates was performed using Genomic BYF DNA Extraction Mini
Kit (INTRON, Biotechnology, Inc, Korea). Amplification was done by ready to go PCR beads Amersham
Biosciences, England. The following primers (Pioneer,
Germany) were used: First Primers for C. dubliniensis
sense: CDU2 5AGT TAC TCT TTC GGG GGT GGC
CT 3; Anti-sense: NL4CAL 5 AAG ATC ATT ATG
CCA ACA TCC TAG GTA AA 3). Second primer C.
albicans Sense: CAL5 5 TGT TGC TCT CTC GGG
GGC GGC CG3; Anti-sense: NL4CAL 5 AAG ATC
ATT ATG CCA ACA TCC TAG GTA AA 3). PCR cycles
were run in thermal cycler according to Mannarelli
et al. [12]. Conditions consisted of an initial denaturation at 94C for 2 minutes followed by 40 cycles of
denaturation at 94C for 30 seconds. Primer annealing at 34C for one minute and elongation at 72C
for one minute followed by an extended elongation
step at 72C for 5 minutes. PCR product underwent
agarose gel electrophoresis (2%), followed by staining with ethidium bromide solution. Amplified DNA

2014

The International Arabic Journal of Antimicrobial Agents

Vol. 4 No. 2:4

doi: 10.3823/751

ISSN 2174-9094

fragments were detected using UV transilluminator,

and the size of the amplicons was estimated by comparing them with the Gene Ruler TM 1 Kb plus 1 kb
DNA ladder (Thermo Fisher Scientific, USA).
A
ntifungal susceptibility testing was done for
C.albicans and C. dubliniensis isolates to both
fluconazole and caspofungin [13].
B
roth microdilution testing was performed according to NCCLS guidelines document M27-A2.
An inoculum concentration adjusted to (1.5 1.0)
103 cells/ml and RPMI 1640 medium buffered
to pH 7.
A
 0.1 ml of yeast inoculum was added to each
tube. Serial two-fold dilutions were adjusted. Final
concentrations of the antifungal agents ranged
from 0.007 to 8 g/ml for caspofungin (Merck &
Co., Whitehouse Station, Pa., USA) and from 0.12
to 128 g/ml for fluconazole (Pfizer, Inc., New
York, N.Y., USA).
T he susceptibility trays were incubated at 35C.
MIC end points were read after 48 h. Drug free
and yeast free controls were included.
A quality control strain of C. albicans (ATCC 10231)
was obtained from Pharma, Suid, Egypt, were included.

Statistical analysis of data

The collected data were presented, summarized,
tabulated & analyzed using computerized software
statistical packages (EPI-info Version 6.04 & SPSS
version 19 Inc. Chicago, USA), A P-value <0.05
was considered to be statistically significant at 95%
confidence interval. Chi-square & fisher exact tests
were used to compare proportions. Sensitivity =
(true positive) 100 / (true positive + false negative)
Specificity = (true negative) 100 / (true negative+
false positive)

Results
Distribution and identification
of Candida species
Cultivation and identification of the Candida isolates
on Brilliance Candida agar revealed the following:
A total of 47 (61.8%) were C. albicans as shown by
the presence of parrot green color. Eleven isolates
(14.5%) were identified as C. glabrata by their beige
yellow colonies. Ten isolates (13.2%) as C. dubliniensis by their dark green colonies, and 8 (10.5%)
of isolates were C. krusei identified by brown-pink

Table 1. Prevalence of Candida species in different clinical specimens.

Candida species/No.

Vaginal (no. 59)

Oral (no. 17)

No.

No.

C. albicans/47

41

87%

13%

C. dubliniensis/10

30%

70%

C. glabrata/11

73%

27%

C. krusei/8

88%

12%

Total no.

16.16

<0.001**

76

**P value < 0.001=highly significant.

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The International Arabic Journal of Antimicrobial Agents

ISSN 2174-9094

colonies (Table 1). Out of 47 C. albicans and 10 C.

dubliniensis isolates, 52 isolates (91%) were positive
for germ tube test, including 9 and 43 isolates from
oral vaginal samples, respectively. While the rest isolates were germ tube negative. This result was statistically significant (P<0.001), regarding comparison
between C. albicans and non-albicans Candida species isolates (Table 1). Regarding growth at elevated
temperatures 42C and 45C, thermotolerance of
C. albicans isolates showed, growth of 7 and 40
at the corresponding grades. While poor growth
of C. dubliniensis isolates was detected with higher
temperature, 9 and 1 grew at these temperatures
respectively. These results showed statistically significant difference regarding growth of Candida albicans at 45C (P value < 0.05). Culture on tobacco
agar media showed 8 isolates produced orange colonies with peripheral hyphal fringe and chlamydospores, suggesting C. dubliniensis, while 44 of the
isolates grew as white-cream-colored colonies with
no hyphal fringe or chlamydospores suggesting C.
albicans isolates. Vitek 2 compact ID-YST system
identified excellently 51/ 57 (89.5%) of isolates , in-

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cluding 8 (14%) of C. dubliniensis (6 isolates from

oral and 2 isolates from vaginal samples) and 23
(40%) of C. albicans (2 isolates from oral and 21
isolates from vaginal samples). Very good identification level was detected in 20 (35%) of C. albicans
(4 isolates from oral and 16 isolates from vaginal
samples), while only good identification level was
detected in 3 (5%) of C. dubliniensis isolates from
oral samples with acceptable low-discrimination
level. Also, 3 isolates (4.3%) from vaginal sample
were misidentified (Table 2).

Antifungal susceptibility testing

The identity of all isolates of C. albicans (47) and
C. dubliniensis (10) were first confirmed by PCR.
Antifungal susceptibility testing to fluconazole revealed that resistance pattern was recorded at MIC
64 g/ml for 23 (49%) of the tested C.albicans.
Another 23 (49%) of the isolates were intermediate
susceptible with MIC ranged from (16-32) g/ml,
and only one isolate was full susceptible with MIC
0.5 g/ml. A total of 50% C. dubliniensis isolates

Table 2. Performance comparison of different methods used for differentiation of C. albicans

and C. dubliniensis
Identification method for
testedisolates (no.=57)

C. albicans
(no. = 47)

C. dubliniensis
(no. = 10)

Sensitivity

Specificity

Accuracy

Tobacco agar

White-cream Colonies,
no hyphal fringe or
chlamydospores
44

Orange colonies
with peripheral
hyphal fringe
8

82.5%

91%

91.2%

Temperature (42C)
(45C)

7
40

9
1

59.6%

63.2%

71.9%

VITEK 2 Ex

----

VG

23

----

20

----

84.2%

84.2%

94.7%

Acc

----

47

10

100%

100%

100%

PCR band = 175 bp

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2014

The International Arabic Journal of Antimicrobial Agents

Vol. 4 No. 2:4

doi: 10.3823/751

ISSN 2174-9094

Table 3. A
 ntifungal susceptibility testing results of C. albicans and C. dubliniensis isolates to fluconazole.

Candida species
(No.)

S
(MIC < 8g/ml))

I
(MIC = 16-32g/ml)

R
( MIC 64g/ml)

No.

No.

No.

C. albicans (47)

2%

23

49%

23

49%

C. dubliniensis (10)

50%

50%

P value

0.22

0.89

S: sensitive R: resistant I: intermediate.

were resistant and the remaining were intermediate

susceptible (Table 3). Both Candida species were
susceptible to caspofungin with MIC50 and MIC90
of ( 0.5g/ml and 0.25g/ml) and ( 1 and 0.5
g g/ml) for C. albicans and C.dubliniensis isolates,
respectively. Quality control C.albicans strain showed
MIC 0.25 g/ml according to Tobudic et al. [14].

The predominance of C.albicans over NAC as well

as the incidence of other Candida spp. is shown
in (Table 1). These results were similar to study of
Burman et al. (2013), which has reported the incidence rates of C. albicans with 76.6%, followed
by C. tropicalis, C. krusei, C. parapsilosis (11.7%),
(6.7%) and (5%), respectively [18].

The epidemiology of Candida infections has changed

over the last two decades and the number of patients suffering from such infections has increased
dramatically. Furthermore, non-albicansCandida (NAC)
species have become more numerous than Candida
albicans [15].

This study has also demonstrated that the majority of

C. albican isolates grew better at higher temperature
than C. dubliniensis, and only 15% of the isolates
were unable to grow at 45Cas shown in Table 2.
A study of Momani et al (2005) has demonstrated
similar results [19]. Therefore, we suggest that temperature growth method can be used as screening
test for initial identification of C.dubliniensisamong
germ tube-producing Candidastrains [20].

The present study indicated that non-albicans Candida accounted for 38.2% of all clinical isolates.
Similar result was also recorded by other study
where the incidence of NAC species was 30.1%
[16] (Table 1). A study by Kremery and Barmes [17]
found that NAC species caused 65% of all candidiasis in the general population. This variation in
incidence of NAC may be attributed to differences
in population types, and frequent exposure to the
different antifungal agents lead to a selective pressure toward increasing resistant isolates.

Tobaco agar medium was described by for primary

isolation of Cryptococcus neoformans [21], however,
later this medium was recommended for differentiation of C. albicans and C. dubliniensis [22]. In this
study, Tobacco agar medium was evaluated and it
has found to be highly specific and has accuracy
of 91% and 91.2% for detection of C.albicans and
C.dubliniensis , respectiviely (Table (2). However,
other study has recorded 100% accuracy of Tobacco agar as simple mean differentiating between C.
dubliniensis and C. albicans [22].

Discussion

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The International Arabic Journal of Antimicrobial Agents

ISSN 2174-9094

2014
Vol. 4 No. 2:4
doi: 10.3823/751

Table 4. MIC50 and MIC90 of tested isolates of C. albicans and C. dubliniensis to caspofungin
Candida species
(No.)

MIC50

MIC90

Candida albicans (47)

0.5 g/ml

1 g/ml

Candida dubliniensis (10)

0.25 g/ml

0.5 g/ml

The current study showed the results of automated

Vitek 2 compact ID-YST system in detection of both
C.dubliniensis and C. albicans has reached 84.2%
specificity and 94.7% accuracy (Table 2). Many
other studies evaluated Vitek 2 compact ID-YST
card and demonstrated variable identification rates
(84% to 99%) between Candida species [23, 24].
However, Meletiadis et al. [25], observed 15% species misidentification by Vitek 2-YST among Candida
isolates. In general, automated system might misidentified certain number of Candida strains which
are involved in outbreaks of nosocomial infections
and prevent application of necessary measurements
to control their infection [25].
Culture based phenotypic identification techniques
are slow and can be resulted infungal misidentification. In recent years, DNA-based methods have
been developed and proved to be excellent to diagnose Candidainfections, especially methods of PCR
and RAPD with high level of sensitivity, specificity
and accuracy [26].
This study has demonstrated that our used methods
for Candida species identification were highly sensitive and specific (statistically significant (P = 0.05).
Except growth at elevated temperature showed low
sensitivity and specificity (59.6%) and (63.2%), respectively.
The present study showed that PCR method is a
reliable molecular technique, and it has the highest
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sensitivity, specificity and accuracy to detect pure

DNA of C.albicans in gel-electrophoresis with the
size of 175 bp. However, PCR alone lacks the discriminatory power to differentiate between both
C. albicans and C. dubliniensis strains in a mixed
sample with sense and antisense primers for both
types according to other study [12]. Moreover, our
results gave a supportive validity and reliability to
Brilliance Candida agar which showed concordant
results to that obtained by PCR.
Candidal systemic infections are associated with
high mortality rate as they are difficult to treat
due to their intrinsically low susceptibility to many
antifungal drugs including fluconazole. While caspofungin as part of echinocandins has currently
more clinical use due to their solubility, antifungal
spectrum, and pharmacokinetic properties; it disrupts the cell walls of Candida species by inhibiting -1.3-D-glucan synthase and results in cell
rupture and death. The presented MIC results of
C. albicans isolates to fluconazole and caspofungin (Table 3 and 4) were in agreement with other
studies which showed similar results obtained from
160 medical centers worldwide in association with
Merck Clinical Microbiology Laboratory [13,27-28].
However, a study carried by Adhikary and Joshi [29]
from South India reported different results to our
as their total Candida isolates from various clinical
samples were susceptible only 75% to fluconazole.
Complete resistance of C. dubliniensis isolates to
fluconazole is of critical importance in treatment of

The International Arabic Journal of Antimicrobial Agents

ISSN 2174-9094

immune compromised patients with serious infections. Therefore, antifungal susceptibility testing in
vitro is a recommended tool to predict the efficacy
of the agent before its use in treatment.
A large multicenter studies described that caspofungin retains mostly activity against azole-resistant
Candida isolates. Caspofungin has demonstrated an
excellent safety profile with few serious drug-related
side effects and toxicity in treatment of patients [28].
Despite their close taxonomic similarities, C. albicans and C. dubliniensis differed markedly in their

2014
Vol. 4 No. 2:4
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antifungal responses. C. dubliniensis showed more

resistance to fluconazole antifungal than that observed with C. albicans isolates [29].
In conclusion, this study demonstrated that Brillance
Candida Agar is a reliable culture medium for phenotypic of Candida spp. A similar result was also
observed using PCR for differentiation between
Candida spp. Fluconazole-resistant C. albicans and
C.dubliniensis isolates from our patients were highly
susceptible to caspofungin.
There is no conflict of interest

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The International Arabic Journal of Antimicrobial Agents

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The Journal is an open access peer-reviewed journal that
publishes scientific papers about all aspects of antimicrobials.
The journal will publish original research articles, reviews,
brief reports and case reports dealing with basic and
clinical antibacterial agents, antiviral, antiprotozoals,
antituberculuous, antifungal and antihelminthes agents.
All manuscripts must be prepared in English, and are subject
to a rigorous and fair peer-review process. Accepted papers
will immediately appear online.
The journal aims to advance the knowledge, attitude and the
research of chemotherapy in the Arabic world in cooperation
with international, national scientific and public societies as
well as research centers with similar aims and objectives.
Submit your manuscript here:
www.iajaa.org

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