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Transcript
ORIGINAL ARTICLE
MYCOLOGY
Epidemiological study of a large cluster of fungaemia cases due to
Kodamaea ohmeri in an Indian tertiary care centre
A. Chakrabarti1, S. M. Rudramurthy1, P. Kale1, P. Hariprasath1, M. Dhaliwal1, S. Singhi2 and K. L. N. Rao3
1) Department of Medical Microbiology, 2) Paediatric Medicine and 3) Paediatric Surgery, Postgraduate Institute of Medical Education and Research, Chandigarh,
India
Abstract
While performing molecular confirmation of phenotypically identified Candida tropicalis isolates, we re-identified a few isolates as Kodamaea
ohmeri. This led us to the present epidemiological investigation of K. ohmeri fungaemia cases. All phenotypically identified C. tropicalis blood
isolates during October 2008 through to December 2009 at our advanced paediatric centre were included for molecular identification by
sequencing of the internal transcribed spacer and D1/D2 regions of rDNA. After identifying a large cluster K. ohmeri fungaemia cases, a
case–control study was carried out retrospectively to analyse potential risk factors for K. ohmeri fungaemia. Molecular typing of the isolates
was performed using a fluorescent amplified fragment length polymorphism (FAFLP) technique. The antifungal susceptibility testing was
performed as per the M27-A3 protocol of CLSI. Thirty-eight (25.7%) of 148 phenotypically identified C. tropicalis isolates were confirmed as
K. ohmeri by sequencing and FAFLP. By case–control analysis, piperacillin-tazobactam was significantly associated with the K. ohmeri
fungaemia. The FAFLP analysis showed that all K. ohmeri isolates had >92% similarity. The azoles and echinocandins had good in vitro activity
against K. ohmeri, though 86.8% of the isolates had MIC of 1 mg/L for amphotericin B. The response to antifungal therapy could be evaluated
in 27 patients and 70.4% of patients recovered after antifungal therapy. The present study reports the largest cluster of K. ohmeri fungaemia
from a single centre. The study also stresses the need for accurate identification of clinical yeast isolates.
Keywords: Antifungal susceptibility testing, Candida tropicalis, candidaemia, diagnosis, epidemiology, fungaemia, identification, Kodamaea
ohmeri, molecular typing
Original Submission: 20 March 2013; Revised Submission: 3 July 2013; Accepted: 12 July 2013
Editor: E. Roilides
Article published online: 18 July 2013
Clin Microbiol Infect 2014; 20: O83–O89
10.1111/1469-0691.12337
Corresponding author: A. Chakrabarti, Department of Medical
Microbiology, Postgraduate Institute of Medical Education and
Research (PGIMER), Chandigarh, PIN 160012, India
E-mail: [email protected]
Introduction
Nosocomial fungaemia due to Candida spp. and related yeasts
has become a persistent health problem in both developed and
developing countries. The incidence of fungaemia varies at 8–
10% of all nosocomial sepsis and 30–50% of these fungaemia
cases occur in patients undergoing treatment in intensive care
units [1–5]. The incidence and spectrum of causative agents of
fungaemia varies in geographical regions. Though a higher rate
of fungaemia due to non-albicans Candida species has been
observed across the world, the proportion is almost 90% at
certain hospitals in Asia [6–9]. While Candida glabrata and
Candida parapsilosis are the leading non-albicans Candida spp. in
the USA and European countries [1–5], Candida tropicalis is
reported as the commonest agent in Asian countries [6–9].
The reason for the emergence of candidaemia due to
C. tropicalis in Asian countries is not clear. Furthermore, large
outbreaks due to unusual species like Pichia anomala, have also
been reported from India [9].
While studying the molecular epidemiology of C. tropicalis
candidaemia at our institute, we identified a few clinical isolates
as Kodamaea ohmeri by sequencing. Those isolates had been
identified earlier as C. tropicalis on the basis of phenotypic
characters. Kodamaea ohmeri is a rare pathogen and the
ª2013 The Authors
Clinical Microbiology and Infection ª2013 European Society of Clinical Microbiology and Infectious Diseases
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Clinical Microbiology and Infection, Volume 20 Number 2, February 2014
majority of cases are reported from Asian countries. Previously known as Pichia ohmeri and Yamadazyma ohmeri, K. ohmeri is an ascosporogenous yeast and a teleomorph of Candida
guilliermondii var. membranaefaciens, belongs to the class
Ascomycetes and family Saccharomycetaceae. Of the five
species reported under the genus Kodamaea, only K. ohmeri
has the ability to grow at 37°C. The clinical importance of
other Kodamaea species (K. anthrophila, K. kakaduensis, K. laetipori K. nitidulidarum) is not known [10]. Kodamaea ohmeri is
reported to cause high mortality (50%) in paediatric populations [11–21]. From our tertiary care centre with 1740 beds
we report a very high incidence of fungaemia (300–500 cases
every year) and C. tropicalis is the commonest isolate [8,22–
24]. However, K. ohmeri fungaemia had never been reported.
We therefore planned a detailed epidemiological investigation
of K. ohmeri fungaemia cases.
Materials and Methods
Epidemiological investigation
The Postgraduate Institute of Medical Education and Research
is a 1740-bed multispecialty tertiary care centre in north India
with an advanced paediatric centre with 243 beds.
Isolates and identification. Candida tropicalis isolates (n = 148;
identified conventionally earlier by germ-tube test, urease
production, morphology on corn-meal agar, and sugar fermentation and assimilation tests) from blood of patients
admitted to the advanced paediatric centre from August 2008
to December 2009 were included in the study. Isolates from
the hands of healthcare workers, which were collected by
standard bag broth technique [9] twice (October 2008 and July
2009) from the neonatal surgical intensive care unit during the
same period, were also included in the study. All 148 isolates
used in the present study were re-identified by sequencing the
internal transcribed spacer region and D1/D2 region of 26S
ribosomal DNA [25,26].
Patients. Detailed clinical histories of patients with K. ohmeri
fungaemia were retrieved from the archive and noted.
Case–control study. A retrospective case–control study was
performed in the neonatal surgical intensive care unit
(because the maximum number of cases of K. ohmeri
fungaemia was identified from this area) to determine the
potential risk factors of K. ohmeri infection. Consecutive
patients with K. ohmeri fungaemia (30 cases), C. tropicalis
fungaemia (25 cases) and patients without fungaemia who
stayed in hospital for >7 days (22 cases) during October 2008
CMI
to December 2009 were studied. The last two groups served
as controls.
Fluorescent amplified fragment length polymorphism. Molecular
typing of the K. ohmeri isolates was performed using a fluorescent amplified fragment length polymorphism (FAFLP) technique [27]. The details have been provided in the Supplementary
material (Supplementary text). In short, restriction enzymes
MseI and HpyCH4IV (New England Biolabs, Ipswich, MA, USA)
and corresponding adapters were used. Amplification was
performed using per-selective primers of HpyCH4IV (5′-GTAGACTGCGTACCCGT-3′) and MseI (5′-GATGAGTCCTGACTAA-3′). HpyCH4IV primer with one selective residue
(5′-GTAGACTGCGTACCCGTC-3′), and MseI primer with
two selective residues were used (5′-GATGAGTCCTGACTAACA-3′) and the primers were labelled with 6-FAM.
Capillary electrophoresis of the amplified products (labelled
with 6-carboxy fluorescein) and LIZ 500 (standard marker) was
performed in an ABI automated DNA Sequencer 3130 (Applied
Bioscience, Foster City, CA, USA). Typing data were imported
to BIONUMERICS v 6.6 software (Applied Maths, Ghent, Belgium).
The fingerprint curves were converted into bands and correct
bands of each lane were assigned using the band position of the
reference dye (LIZ500). The similarity coefficient was determined by Pearson correlation with negative similarities clip to
zero. Cluster analysis was performed by Unweighted Pair Group
Method with Arithmetic Mean using BIONUMERICS software.
Antifungal susceptibility testing. The MICs of the K. ohmeri
isolates were determined by reference microbroth dilution
antifungal susceptibility testing of yeasts as per document
M27-A3 of CLSI [28]. The antifungal drugs included in the
study were amphotericin B (Sigma Aldrich, Bangalore, India),
fluconazole (Sigma Aldrich, India), itraconazole (Janssen
Research Foundation, Beerse, Belgium), voriconazole (Pfizer
Central Research, Tadworth, UK), posaconazole (Merck Sharp
and Dohme, Gurgaon, India) and caspofungin (Merck Sharp
and Dohme, India).
Statistical analysis. The results of the study for the patient and
the control groups were compared by multivariate analysis
test. Normalcy of the three groups was determined by
Kolmogorov–Smirnov test. Variables like age, duration of
hospital stay and the time after which infection occurred were
described in terms of means. The non-parametric Mann–
Whitney U-test was applied to compare the differences
between the groups. Qualitative variables like the sex of
patient, risk factors, and antibiotics and antifungals used were
compared using the Pearson chi-squared test. All the statistical
tests were carried out using an a error of 5% and a b error of
ª2013 The Authors
Clinical Microbiology and Infection ª2013 European Society of Clinical Microbiology and Infectious Diseases, CMI, 20, O83–O89
CMI
Chakrabarti et al.
20%. A p value <0.05 was considered statistically significant. All
analyses used SPSS (version 19.0 for Windows) software.
Kodamaea ohmeri fungaemia
O85
patients with K. ohmeri fungaemia were neonates and 79% (30/
38) of them were from the neonatal surgical intensive care
unit. The response to antifungal therapy could be evaluated in
27 patients, because eight patients died before the start of
antifungal therapy and three patients left the hospital against
medical advice. Twenty-three (85.1%) patients received fluconazole and four received caspofungin; 15 (65.2%) patients
receiving fluconazole and all four patients receiving caspofungin
recovered (the details of individual patients are available in the
Supplementary material) (Table S2).
Results
Isolates and identification
Of 398 culture-proven fungaemia cases that occurred during
the study period of 17 months (August 2008 to December
2009) at the advanced paediatric centre, 148 isolates had been
identified previously as C. tropicalis on the basis of biochemical
and morphological tests. During the present study 38 (25.7%)
of those 148 isolates were re-identified as K. ohmeri by
genotypic characters. The K. ohmeri isolates had 98–100%
identity with the sequence of standard strains (ATCC 46053,
CBS 5367). The DNA sequences of the representative isolates
have been deposited in the EMBL nucleotide sequence
database with the Accession nos HG313954 to HG313978.
Monthwise distribution of cases in pediatric ward is provided
in Table S1. The details of each patient and isolate are
presented in the Supplementary material (Table S2). During
the same period, 47 yeasts were isolated from the hands of
healthcare workers at the neonatal surgical intensive care unit
and one isolate was identified as K. ohmeri (n = 1, 2%). Other
yeasts were identified as: C. parapsilosis (n = 26, 55%), C. albicans (n = 8, 17%), C. glabrata (n = 5, 11%), Pichia guilliermondii
(n = 3, 6%) and C. tropicalis (n = 1, 2%), Kluveromyces marxianus (n = 1, 2%), Wickeromyces anomalus (n = 1.2%), and
Clavispora lusitanae (n = 1, 2%). The identity of all K. ohmeri
isolates including the hand isolates was further confirmed as
same species by FAFLP, because all those isolates showed a
similarity coefficient of >92% [29].
Case–control study
Risk factor analysis is presented in Table 1. In comparison to the
C. tropicalis fungaemia, the only significant risk factor for acquiring
K. ohmeri fungaemia in the hospital was piperacillin-tazobactam
use (p 0.032). Whereas comparing the K. ohmeri fungaemia and
non-fungaemia groups, prolonged hospital stay (p 0.037), piperacillin-tazobactam use (p 0.044), endotracheal intubation
(p 0.002) and mechanical ventilation (p 0.033), were significant
risk factors for the development of K. ohmeri fungaemia.
Mortality was also significantly higher (50%) in K. ohmeri fungaemia patients compared with patients with C. tropicalis fungaemia
(24%) or non-fungaemia (18.2%) groups. The attributable
mortality in K. ohmeri fungaemia cases was 31.8%.
FAFLP
Thirty-eight isolates (37 from patients and one from the hands
of a healthcare worker) were included for the FAFLP analysis.
FAFLP profiles yielded fragments ranging from 40 to 500 bp
but only fragments in the range of 50–250 bp were included
for the analysis. A total of ~110 fragments were analysed. All
K. ohmeri isolates had >92% similarity co-efficient. The FAFLP
profile yielded eight clusters (Fig. 2). The similarity of ‘A’ ‘B’
and ‘C’ clusters was >96% with inter-cluster difference of >1%.
The ‘D’, ‘E’, ‘F’ ‘G’ and ‘H’ clusters had 91–95% similarities.
Except for one isolate (K5), all blood isolates from 2008 were
in one cluster, including the hand isolate (cluster H). The hand
isolate (isolated during October 2008) was close to two blood
Patients
The distribution of K. ohmeri cases during the study period is
given in Fig. 1. The median age of the patients was 7 days,
mean 87 days, range 1 day to 8 years with male preponderance (male : female ratio 2.4 : 1). The majority (87%) of the
6
5
Neonatal surgery
Intensive care unit
4
Paediatric
medicine
3
Paediatric
pulmonology
2
Paediatric
Intensive care unit
Dec-09
Oct-09
Nov-09
Sep-09
Jul-09
Aug-09
Jun-09
Apr-09
May-09
Mar-09
Jan-09
Feb-09
Dec-08
Oct-08
Nov-08
fungaemia cases in different paediatric wards.
Sep-08
0
FIG. 1. The distribution of Kodamaea ohmeri
Aug-08
1
ª2013 The Authors
Clinical Microbiology and Infection ª2013 European Society of Clinical Microbiology and Infectious Diseases, CMI, 20, O83–O89
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CMI
Clinical Microbiology and Infection, Volume 20 Number 2, February 2014
TABLE 1. Evaluation of potential risk factors for Kodamaea ohmeri infection among patients of a neonatal surgical intensive care
unit in a case–control study
Factor analysed
K. ohmeri
(n = 30)
No. (%)
Number (%)
Candida tropicalis
(n = 25)
No. (%)
Non-candidaemia
(n = 22)
No. (%)
K. ohmeri vs.
Candida tropicalis
p value
K. ohmeri
vs.
non-candidaemia
Steroid intake
Prematurity
Lower segment caesarean section
Home delivery
Intrauterine growth retardation
Revised surgery
Prolonged hospital stay
Central line
H/o Intravenous infusion in community
Malnourishment
Gastroenteritis
Prolonged antibiotic use
Piperacillin-tazobactum use
Vancomycin use
Urinary catheter insertion
Endotracheal intubation
Mechanical ventilation
Total parenteral nutrition
Intravenous fluid infusion
Renal failure
Haemodialysis
Anaemia
Death
10 (33.3)
6 (20)
6 (20)
4 (13.3)
0 (0)
2 (6.7)
30 (100)
11 (36.7)
0 (0)
0 (0)
2 (6.7)
26 (86.7)
5 (16.7)
14 (46.7)
23 (76.7)
20 (66.7)
14 (46.7)
1 (3.3)
30 (100)
0 (0)
0 (0)
2 (6.7)
15 (50)
9 (37.5)
4 (16)
7 (28)
7 (28)
2 (8)
2 (8.0)
24 (96.0)
12 (48)
0 (0)
2 (8.0)
0 (0)
24 (96.0)
0 (0)
7 (28.0)
17 (68.0)
11 (44)
11 (44)
0 (0)
24 (96.0)
0 (0)
0 (0)
0 (0)
6 (24)
3 (13.6)
3 (13.6)
4 (18.2)
3 (13.6)
0 (0)
3 (14.3)
19 (86.4)
6 (27.3)
1 (4.5)
6 (27.3)
1 (4.5)
20 (90.9)
0 (0)
6 (27.3)
13 (59.1)
5 (22.7)
4 (18.2)
0 (0)
22 (100)
2 (9.1)
0 (0)
0 (0)
4 (18.2)
0.750
0.702
0.487
0.176
0.115
0.850
0.269
0.396
–
0.115
0.118
0.231
0.032*
0.156
0.472
0.091
0.843
0.357
0.269
–
–
0.188
0.048*
0.105
0.652
0.869
0.975
–
0.368
0.037*
0.476
0.238
0.002*
0.746
0.636
0.044*
0.156
0.175
0.002*
0.033*
0.387
–
0.092
–
0.217
0.019*
*p <0.05 statistically significant with Pearson chi-squared test.
isolates of 2008 (K2 and K6) with variation of <4%. The
C. tropicalis isolate had only 40% similarity with K. ohmeri
isolates.
Antifungal susceptibility testing
The in vitro activities of each antifungal agent against the
K. ohmeri isolates including the range of MIC, geometric mean,
MIC50 and MIC90 and cumulative percentage of the isolates
inhibited at the MIC at various concentrations of antifungal
agents are presented in Table 2 and Table S3. MIC90 of azoles
and echinocandins were ≤0.50 mg/L. However, 33 (86.8%)
isolates had MIC of 1 mg/L against amphotericin B. Only one
isolate had high MICs against azoles (fluconazole MIC >64 mg/L,
voriconazole 8 mg/L, itraconazole 8 mg/L, and posaconazole
4 mg/L). The response to antifungal therapy in the patient
harbouring the K. ohmeri isolate with high MIC against azoles
could not be evaluated because the patient left against medical
advice.
Discussion
The present series of K. ohmeri fungaemia is the largest cluster
(38 cases) of such cases from a single centre reported and the
majority (78.9%) of those were reported from a neonatal
surgical intensive care unit. The infection was often serious and
fatal (attributable mortality 31.8%). Kodamaea ohmeri is rarely
reported to cause human infection [11–21]. Before the
present report, only 39 cases of K. ohmeri infection had been
reported. Among them, 30 (76.9%) cases presented as
bloodstream infections [11,12,16,19], and the remaining
occurring as peritonitis (two cases), endocarditis (three cases),
urinary tract infection (one case), polymicrobial wound
infection (one case) and oral ulcer (three cases)
[13,17,18,20]. The majority (75%) of those patients were
immunosuppressed when they acquired the infection and had
38% mortality. Kodamaea ohmeri fungaemia may not be rare in
India, as the fungus was isolated from ~1% of fungaemia cases
from nine of 27 intensive care units in a recently conducted
study across India (unpublished observation).
A high incidence of fungaemia due to non-albicans Candida
species has been reported from Asian countries including India
[6–8,22–24], and C. tropicalis is reported as the commonest
non-albicans Candida species in contrast to C. glabrata and
C. parapsilosis in the USA and Europe[1–5]. The emergence of
C. glabrata is linked to widespread use of azole antifungal
agents and C. parapsilosis is linked with catheter use [1–3].
However, such an explanation could not be provided for the
emergence of our C. tropicalis isolates, as the resistance to
azoles in those isolates was not beyond 10% [8,22,23]. This
could be a result of suboptimal infection control practices in
hospitals in developing countries [30]. Similarly, the majority
(97.3%) of K. ohmeri isolates in the present study had low MIC
against azoles and echinocandins.
To investigate the reasons for emergence we conducted a
case–control analysis. Prolonged hospital stay, endotracheal
intubation and mechanical ventilation were significantly associated with K. ohmeri fungaemia. These risk factors are already
ª2013 The Authors
Clinical Microbiology and Infection ª2013 European Society of Clinical Microbiology and Infectious Diseases, CMI, 20, O83–O89
CMI
Chakrabarti et al.
Kodamaea ohmeri fungaemia
O87
FIG. 2. Fluorescent amplified fragment length
polymorphism analysis of 38 Kodamaea ohmeri
isolates. Only bands in the range of 50–250 bp
are included for the analysis. The numbers
indicate the isolate number, ward where it was
isolated and month and year of isolation.
TABLE 2. In-vitro antifungal susceptibility data (MIC, mg/L)
of 38 Kodamaea ohmeri isolates against six antifungal agents
Antifungal agent
Range
GM
50%
90%
Amphotericin B
Itraconazole
Voriconazole
Posaconazole
Fluconazole
Caspofungin
0.25–1
0.06–4
0.03–8
0.06–4
0.5–64
0.12–1
0.89
0.24
0.09
0.11
0.89
0.32
1
0.25
0.06
0.12
1
0.25
1
0.50
0.12
0.25
2
0.5
GM, geometric mean.
known as risk factors for fungaemia [1–3]. The other common
risk factors for fungaemia, such as central line and surgery, were
not found to be significant in this risk factor analysis. However,
while comparing commonly occurring C. tropicalis candidaemia
cases, piperacillin-tazobactam use was found to be a significant
risk factor for K. ohmeri fungaemia. This single risk factor could
not explain the emergence of K. ohmeri fungaemia. Moreover,
we did not find any change of clinical and laboratory procedures
and hospital care practices during the study period. Kodamaea
ohmeri is commonly used in the food industry, especially in the
preparation of pickles because of its fermentation capability
[10]. Though Indians are fond of pickles, they are not usually
supplied in the diet of hospitalized children. Therefore, it is
difficult to ascertain the actual reason for the emergence of
K. ohmeri fungaemia. The patients with K. ohmeri fungaemia had
significantly higher (50%) mortality than those with C. tropicalis
fungaemia and than patients without fungaemia. The high
mortality due to K. ohmeri infection may be related to the
virulence factors of the organism, though no study has yet been
conducted to confirm this.
We performed molecular typing of the K. ohmeri isolates
both from patients and the hand isolate. In an earlier study,
pulsed-field gel electrophoresis was used to type K. ohmeri
clinical isolates, which differentiated 13 isolates into six
different types [11]. As amplified fragment length polymorphism is a more robust technique, we employed the
fluorescence-based technique to differentiate the isolates.
The resulting FAFLP pattern indicates that the majority
(63.2%) of the isolates (Group A and B) had a possible
clonal origin with >96% similarity. Interpretation of the
ª2013 The Authors
Clinical Microbiology and Infection ª2013 European Society of Clinical Microbiology and Infectious Diseases, CMI, 20, O83–O89
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Clinical Microbiology and Infection, Volume 20 Number 2, February 2014
FAFLP data has no clear guidelines. Savelkol et al. mentioned
that patterns with 90–100% homology are considered to be
derived from identical strains whereas patterns with 60–90%
homology indicate different strain from the same species
[29]. However, these percentages are arbitrary and may be
influenced by many technical variations and imperfections.
The minimal change among the isolates of 2008 and 2009
may be due to chromosomal instability or rearrangement.
We could not ascertain the method of spread of the
organism in our hospital because it was a retrospective
study and we had only one hand isolate. Reports in the
literature reveal that K. ohmeri isolates have low MIC to all
antifungal agents except for a high range of MIC against
fluconazole in a few isolates [11–13,21]. Similarly, all isolates
in the present study, except one, had low MIC to azoles and
caspofungin. However, 86.8% of our isolates had moderately
high MIC (MIC 1 mg/L) to amphotericin B, in contrast to
earlier reported cases [13,21]. This observation is relevant
because amphotericin B deoxycholate is a commonly used
systemic antifungal agent in India despite its toxicity due to
low cost. One isolate (K6) with high MIC to three
commonly used azoles was isolated in 2008. Fortunately
that strain either did not spread or underwent loss of
fitness. This high MIC isolate was closely related (99%
similarity) to another isolate (K2) that had a low MIC to all
the azoles tested, and was isolated from the same ward
during the same period.
Though echinocandins are recommended for management
of candidaemia in intensive care units [31] and most (84.2%)
of the patients were from ICUs in the present study, 85.1%
of patients were treated with fluconazole and 65.2% of
patients responded to fluconazole therapy. It is possible that
clinicians prescribed fluconazole because of its low cost and
that the isolates had low MICs against fluconazole.
The difference in phenotypic characteristics of K. ohmeri and
C. tropicalis is minimal. Inclusion of raffinose and D-xylose in the
routine panel of sugars that is used in the assimilation test for
yeast identification may differentiate the two species, as
K. ohmeri can assimilate raffinose but not D-xylose whereas
C. tropicalis can assimilate D-xylose but not raffinose (Table S4)
[10]. However, the majority of laboratories in India do not
perform a full battery of sugar assimilation tests when
identifying Candida species. The commercial systems Vitek-2
(bioMérieux, Inc., Hazelwood, MO, USA) and API 20
(bioMérieux SA, Marcy-l’Etoile, France) may differentiate the
two species. Sequencing of the internal transcribed spacer
region and D1/D2 region of ribosomal DNA accurately
identifies most yeast species. However, commercial systems
and molecular identification are rarely employed in public
sector hospitals in India because of their high cost and
CMI
laboratories mostly rely on restricted biochemical tests and
morphological identification of yeasts. As K. ohmeri has the
potential to cause outbreaks in hospitals [11], it is important to
identify this fungus.
In conclusion, the present study highlights the epidemiology
of the largest cluster of K. ohmeri fungaemia from a tertiary
care centre in Asia. The study also emphasizes the need for
accurate identification of clinical yeast isolates.
Funding
This work was supported by the Indian Council of Medical
Research (ICMR), New Delhi under the project ‘Centre of
Advanced Research in Medical Mycology’.
Acknowledgements
We acknowledge the support of Dr Corne H Kallassen,
Canisius Wilhelmina Hospital, Nijmegen, the Netherlands for
his input while analysing the FAFLP results. Parts of the results
were presented in IDSA 2010 and TIMM 2011.
Transparency Declaration
The authors have no conflicts of interest.
Supporting Information
Additional Supporting Information may be found in the online
version of this article:
Table S1. Monthwise distribution of Kodamaea ohmeri
isolates at different wards in the Advanced Paediatric Centre
of the Institute.
Table S2. The clinical details of 38 patients with Kodamaea
ohmeri fungaemia.
Table S3. Minimum inhibitory concentrations (in lg/mL) of
Kodamaea ohmeri isolates against different antifungal agents.
Table S4. Phenotypic characters of Kodamaea ohmeri and
Candida tropicalis.
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ª2013 The Authors
Clinical Microbiology and Infection ª2013 European Society of Clinical Microbiology and Infectious Diseases, CMI, 20, O83–O89