Journal of Hospital Infection 146 (2024) 31e36

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Journal of Hospital Infection

journal homepage: www.elsevier.com/locate/jhin

Proposal for a screening protocol for Candida auris

colonization
S.E. Leonhard a, G.M. Chong a, D.E. Foudraine a, L.G.M. Bode a, P. Croughs a,
S. Popping a, E. Schaftenaar a, b, C.H.W. Klaassen a, y, J.A. Severin a, *, y
a
Department of Medical Microbiology and Infectious Diseases, Erasmus MC University Medical Center, Rotterdam, The
Netherlands
b
Department of Medical Microbiology and Immunology, St Antonius Hospital, Nieuwegein, The Netherlands

A R T I C L E I N F O S U M M A R Y

Article history: Background: Candida auris is an emerging multidrug-resistant yeast which can cause
Received 1 September 2023 severe infection in hospitalized patients. Since its first detection in 2009, C. auris has
Accepted 21 December 2023 spread globally. The control and elimination of this pathogen in a hospital setting is par-
Available online 27 January ticularly challenging because of its ability to form biofilms, allowing for long-term patient
2024 colonization and persistence in the environment. Identification of C. auris from cultures is
difficult due to the morphologic similarities to other yeasts, its slow growth, and the low
Keywords: culture sensitivity when using standard agars and temperatures.
Candida Aim: We have developed a screening protocol for C. auris colonization using an in-house-
Fungal drug resistance developed polymerase chain reaction (PCR), combined with confirmatory culture in
Molecular diagnostic techniques optimized conditions.
Hospitals Methods: C. auris-specific primers and probe were developed, targeting the internal
transcribed spacer (ITS) region, and specificity was confirmed in silico using the BLAST
tool. The PCR was validated using a panel of 12 C. auris isolates and 103 isolates from 22
other Candida species and was shown to be 100% accurate. The limit of detection of the
assay was determined at approximately four cells per PCR.
Findings: C. auris screening was introduced on February 15th, 2023, and was used for
patients who had been admitted to a healthcare facility abroad in the two months prior to
admission to our hospital. The screening protocol included swabs from nose, throat,
rectum, axilla, and groin. In the first eight months, 199 patients were screened and seven
were found positive (4%).
Conclusion: Our proposed screening protocol may contribute to control C. auris in hospitals.
ª 2024 The Authors. Published by Elsevier Ltd
on behalf of The Healthcare Infection Society. This is an open access article
under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Introduction
* Corresponding author. Address: Department of Medical Micro-
Candida auris is a pathogenic yeast and is considered a rising
biology and Infectious Diseases, Erasmus MC University Medical Centre
healthcare emergency worldwide [1]. C. auris is characterized
Rotterdam, P.O. Box 2040, 3000 CA, Rotterdam, The Netherlands. Tel.:
þ31 10 70 33510. by a high rate of antifungal resistance with reduced suscepti-
E-mail address: j.severin@erasmusmc.nl (J.A. Severin). bility to triazoles, polyenes, and echinocandins [2e4]. The
y control and elimination of this pathogen in a hospital setting is
These authors contributed equally to this study.

https://doi.org/10.1016/j.jhin.2023.12.019
0195-6701/ª 2024 The Authors. Published by Elsevier Ltd on behalf of The Healthcare Infection Society. This is an open access article
under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
32 S.E. Leonhard et al. / Journal of Hospital Infection 146 (2024) 31e36
particularly challenging because of its high salt- and thermo-
tolerance and ability to form a biofilm, allowing for long-
term patient colonization and persistence in the environment
[5].
C. auris was first cultured in 2009 from an ear swab of a 70-
year-old Japanese woman, although retrospectively C. auris
strains were found in South Korea as early as 1996 [3,6]. In the
years after its first description, C. auris spread across four
global regions (South and East Asia, Africa and South America)
and whole-genome sequencing analysis showed that these
strains were part of different clades, indicating an independ-
ent spread [7]. The first case of C. auris in the USA was reported
in 2016, and an alarming increase in cases was seen between
2019 and 2021, with a total of 1471 clinical cases and 4041 cases
found by screening identified in 2021 [8]. In Europe, several
outbreaks in healthcare settings have been reported in Den-
mark, France, Germany, Greece, and Italy [9]. A total of 1812
C. auris cases were reported by the European Centre for Dis-
ease Prevention and Control between 2013 and 2021, and the
number of cases nearly doubled between 2020 and 2021 [9].
However, this is most likely an underestimation as most Euro-
pean countries, including the Netherlands, do not actively
screen patients for presence of C. auris. In the Netherlands,
only five imported cases have been reported in the past five
years [9].
Colonization of C. auris has been described in several body
sites, including skin (especially axilla/groin), urine (especially
in patients with an indwelling catheter), nose, throat, vagina,
and deeper airways. Data of samples collected during a C. auris
outbreak in the State of New York showed that the greatest
yield can be expected when using a combination of axilla,
groin, and nose swabs when screening for C. auris [4].
Unlike most other Candida spp., C. auris grows especially
well at 40e42  C and in media with 10% saline [5]. At 30e35  C,
growth is slower or absent. On Sabouraud agar, C. auris colo-
nies are beigeewhite, and, on most traditional chromogenic
media, colonies appear white or pink, although some may
appear red or purple [10,11]. Based on culture morphology, it is
not possible to reliably distinguish C. auris colonies from other
Candida spp. Therefore, culture alone is not sufficient as an
identification method [11]. Although previously matrix-assisted
laser desorption/ionization time-of-flight (MALDI-TOF) was
unable to differentiate C. auris from genetically related
Candida spp., including C. haemulonii and C. duobus
haemulonii, updated databases have recorded a sensitivity and
specificity of 100% [10]. Molecular methods have demonstrated
their ability to identify C. auris and are based on sequencing
the D1eD2 region of the 28S rDNA or the internal transcribed
spacer (ITS) region of rDNA. Furthermore, several real-time
polymerase chain reaction (PCR) assays have been developed
for the detection of C. auris [4,12e14]. The sensitivity of these
assays is high (>93%) in several studies with a limit of detection
as low as one colony-forming unit (cfu) per PCR [13e15].
Here we describe the development of a screening protocol
for C. auris colonization using real-time PCR with culture for
PCR-positive sites. In addition, we report on our experiences in
the first eight months after implementation of the protocol.
Methods
Implementation of C. auris screening protocol
Screening for C. auris colonization was added to the
standard screening protocol for patients admitted to the
Erasmus MC University Medical Center (Erasmus MC) with a high
risk of infection or colonization with multidrug-resistant micro-
organisms (MDROs) (Figure 1) [16]. This includes patients who
have been admitted to a healthcare facility outside of the
Netherlands for more than 24 h in the past two months.
Patients directly transferred from a healthcare facility abroad
or those with additional risk factors for MDRO carriage were
also screened, regardless of the duration of admittance in the
facility abroad. All these patients were kept in an isolation
room and healthcare workers wore gloves, gowns, IIR medical
masks, and caps until results of the MDRO screening were
known and negative. The standard screening protocol includes
swabs of the nose, throat, and perineum for meticillin-
resistant Staphylococcus aureus (MRSA), and the throat and
rectum for all other MDRO. For C. auris screening, swabs of the
axilla and groin were added to this protocol and, if present,
swabs of wounds, indwelling catheters, or insertion sites of a
central venous catheter were also taken. Finally, sputum or
tracheal aspirate was obtained in case of productive cough or
intubation. The perineum swab was not used for C. auris
screening. E-swabs (Copan Diagnostics, Brescia, Italy) were

E-swab medium of PCR MALDI-TOF

positive body site inoculated determination Sensititre®
on CHROM- and SABGenta performed on all Yeast-one
agar at 40°C for 14 days suspected colonies

Positive

Dry swabs taken Inoculation of all dry MALDI-TOF

E-swab: nose, C. auris real time PCR on
of nose, throat, swabs on CHROM- and determination Sensititre®
throat, rectum, E-swab medium of all
rectum, axilla, SABGenta agar at 40°C performed on all Yeast-one
axilla, groin screened patients
groin for 14 days suspected colonies

Negative Stop

Figure 1. Flow diagram of Candida auris screening protocol. PCR, polymerase chain reaction; MALDI-TOF, matrix-assisted laser
desorption/ionization time-of-flight mass spectrometry.
 S.E. Leonhard et al. / Journal of Hospital Infection 146 (2024) 31e36 33

Table I
Primer/probe combinations tested
Primer/probe name (Reporter)eSequencee(Quencher) Concentration (mM) Reference
Cauris-F1 CCT-GTT-TGA-GCG-TGA-TGT-CT 0.1 This study
Cauris-R1 CGT-GCA-AGC-TGT-AAT-TTT-GTG 0.5 This study
Cauris-P1 (FAM)eCAA-CGC-CAC-CGC-GAA-GAT-TGe(EDQ) 0.1 This study
Cauris-F2 CAG-ACG-TGA-ATC-ATC-GAA-TCT 0.2 [11]
Cauris-R2 TTT-CGT-GCA-AGC-TGT-AAT-TT 0.2 [11]
Cauris-P2 (Cy5)eAAT-CTT-CGC-GGT-GGC-GTT-GCA-TTC-Ae(BHQ-2) 0.05 [11]
PhHV-F GGG-CGA-ATC-ACA-GAT-TGA-ATC 0.5 [19]
PhHV-R GCG-GTT-CCA-AAC-GTA-CCA-A 0.5 [19]
PhHV-P (Yakima Yellow)eTTT-TTA-TGT-GTC-CGC-CAC-CAT-CTG-GAT-C 0.1 [19]
e(EDQ)

used for sample collection. If the sample tested PCR positive, Table II
10 mL of the E-swab medium was inoculated on a Chromagar Overview of Candida species tested in PCR validation
and a Sabouraud agar with 4% glucose, gentamicin, and
Species No. tested PCR result
chloramphenicol (SABGenta, MP Biomedicals, Santa Ana, CA,
USA) and incubated for 14 days at 40  C. Furthermore, new Candida auris 12 þ
swabs (cotton tip, no transport medium; Copan Diagnostics) of Candida albicans 10 e
the aforementioned body sites were requested and sub- Candida glabrata 10 e
sequently inoculated on ChromAgar and SABGenta agar and Candida tropicalis 10 e
incubated for 14 days at 40  C. MALDI-TOF determination was Candida parapsilosis 10 e
performed on all C. auris-suspected colonies. When determi- Pichia kudriavzevii (Candida krusei) 10 e
nation confirmed identification of C. auris, the MICs of tri- Candida dubliniensis 6 e
azoles, echinocandins, and amphotericin-B were determined Candida norvegensis 5 e
using the Sensititre Yeast-one (Trek Diagnostic Systems Ltd, Kluyveromyces marxianus (Candida 4 e
East Grinstead, UK) and the results were interpreted according kefyr)
to the tentative MIC breakpoints of the Centers for Disease Clavispora lusitaniae (Candida 4 e
Control and Prevention [17]. All positive isolates were stored lusitaniae)
at e80  C. All positively screened patients were treated in Candida guilliermondii 3 e
isolation, and after discharge or transfer their rooms were Pichia cactophila (Candida inconspicua) 3 e
cleaned and subsequently disinfected with 1000 ppm chlorine Nakaseomyces bracarensis (Candida 2 e
[18]. bracarensis)
Candida haemulonii 2 e
Candida metapsilosis 2 e
Real-time PCR assay Nakaseomyces nivariensis (Candida 2 e
nivariensis)
The developed method is based on real-time PCR using Wickerhamomyces anomalus (Candida 2 e
Taqman probes and uses PhHV (phocine herpes virus) as an pelliculosa)
internal process control. DNA was isolated from 200 mL of e- Candida blankii 1 e
swab medium using the MagNA Pure 96 in combination with the Cyberlindnera fabianii (Candida 1 e
MagNA Pure 96 DNA and Viral Nucleic Acid Small Volume Kit fabianii)
(Roche Diagnostics, Almere, the Netherlands). Amplification Pichia fermentans (Candida lambica) 2 e
reactions (20 mL) contained 5 mL of DNA and primers/probe Yarrowia lipolytica (Candida lipolytica) 1 e
(Table I) in 1 LightCycler 480 Probes Master (Roche Diag- Pichia kluyveri 1 e
nostics) and were subjected to amplification on a LightCycler Total 103
480 (Roche Diagnostics) using the following protocol: after an
PCR, polymerase chain reaction.
initial denaturation for 5 min at 95  C, 50 cycles were applied of
denaturation for 5 s at 95  C and annealing 30 s at 60  C after
which the samples were cooled down. Primer/probe concen- blast.ncbi.nlm.nih.gov). Specificity of the assay was also
trations were optimized for maximum sensitivity under our assessed in vitro by testing 103 isolates from 23 other Can-
reaction conditions. dida spp. and formerly named Candida spp. (Table II) taken
Two primer/probe combinations targeting the ITS region from our clinical strain collection and identified by MALDI-
were evaluated (Table I). One design was taken from liter- TOF. An additional 50 clinical faeces samples were included
ature, a second design was based on all available ITS to assess the performance in clinical samples. Twelve C. auris
sequences in the non-redundant BLAST database. Specificity strains were used as positive controls; the analytical limit of
of the primer/probe combinations was assessed in silico by detection was evaluated by performing dilution series in E-
BLAST analysis of the amplified target sequence (http:// swab medium.
34 S.E. Leonhard et al. / Journal of Hospital Infection 146 (2024) 31e36
Results
PCR validation
All 12 C. auris strains tested positive with both primer/
probe combinations. All non-auris Candida spp. and formerly
named Candida spp. tested negative. The 50 clinical faeces
samples also tested negative with both primer/probe combi-
nations. In all samples a valid test result was generated, and no
inhibition was observed.
Using our reaction conditions, the first primer/probe com-
bination (amplifying a significantly shorter PCR product) was
slightly more sensitive by a factor of w2 but this was not
statistically evaluated. A series of 10-fold dilutions was per-
formed of a 0.5 McFarland suspension of cultured C. auris,
which contained w5*106 cfu/mL. It was determined that
approximately four cells per PCR can be detected with the
optimized protocol corresponding to w200 cells per collected
E-swab.
Screening in clinical practice
The screening protocol was implemented at the Erasmus MC
on February 15th, 2023. In the eight months thereafter (until
October 18th), a total of 199 patients were screened, and seven
patients were found positive. Three of these patients were
injured soldiers from Ukraine. In Table III the characteristics of
the positive cases and their laboratory results are outlined.
In only one of the positively screened cases were we able to
culture C. auris. In this patient, after three days, growth of one
pink colony and multiple green colonies was seen on the
CHROMagar of the swab from the groin. MALDI-TOF was per-
formed on all colonies and identified the pink colony as C. auris
and the green colonies as C. albicans. The swabs from the nose,
throat, rectum, axilla, and the wounds did not show growth
after 14 days.
In the other patients, C. auris was not cultured, but growth
of other yeasts, including C. albicans, C. tropicalis, and Kluy-
veromyces marxianus was seen on the CHROMagar and SAB-
Genta agar at 40  C. None of the patients colonized with
C. auris developed an infection caused by this pathogen.
Discussion
In this report we describe the development and imple-
mentation of a screening protocol for C. auris using an in-house
developed PCR, combined with specific cultures of PCR-
positive body sites. In the eight months after its introduction,
seven patients were found to be colonized by C. auris. None of
the colonized cases developed an infection due to C. auris. This
highlights the importance of structural C. auris screening
among patients previously admitted to healthcare facilities
abroad to prevent further spread in Dutch hospitals.
In the validation, our PCR showed 100% specificity among
103 samples of other Candida spp. Although our study included
only a small number (N ¼ 12) of C. auris-positive strains, the
sensitivity was 100%. The highest dilution in which C. auris was
still detected showed a limit of detection of four cells per PCR,
similar to other published PCR methods for C. auris, in which
limits of detection varied between 1 and 54 cfu per reaction
[13e15]. Fifty clinical faeces samples all tested negative, and
none showed inhibition. This indicates that the PCR was robust
in clinical samples and faecal carriage of C. auris was not
present in our patient population. As the PCR was developed to
run using our standard LightCycler 480 protocol, the protocol
was easy to implement in our routine diagnostic workflow.
Although recent updates of MALDI-TOF show an increase in
sensitivity and specificity in detecting C. auris, MALDI-TOF
requires growth of C. auris prior to identification [11]. Fur-
thermore, suspected colonies need to be identified based on
morphology before the MALDI-TOF can be used [10]. Culturing
C. auris at standard temperatures of 30e35  C is slow, lacks
sensitivity, and is hampered by the fact that colonies are dif-
ficult to distinguish from other Candida spp. based on mor-
phology. These limitations are only partly avoided when swabs
are incubated at higher temperatures in enriched media with a
high saline percentage before inoculating them on agars [5,11].
Advantages of PCR include rapid test results and high sensi-
tivity and specificity [4,13e15]. Furthermore, when screening
for C. auris by PCR, it is not necessary to use enriched media
and incubation temperatures specific for C. auris for all
screened samples. This makes initial screening with PCR more
efficient. In only one of the seven patients who tested positive
in our screening, C. auris was cultured in just one of the four
PCR-positive body sites. Furthermore, even though samples
were incubated at 40  C, growth of C. albicans and
K. marxianus was also detected. Altogether, this indicates that
culture is less sensitive compared to PCR, and that culture at
high temperatures alone is not sufficient to select for C. auris.
We chose to include swabs of the nose, throat, rectum, axilla,
and groin following data collected during a C. auris outbreak in
the State of New York which showed that the greatest yield is
expected when using a combination of nose, axilla, and groin
swabs when screening for C. auris [4]. We added the axilla and
groin swabs to our standard screening for MDROs. This facili-
tated an easy implementation of this screening protocol in our
hospital. The importance of swabbing several sites is supported
by our finding that one patient only had a positive axilla swab in
our PCR.
Our findings are in contrast with a recently published
screening protocol in a tertiary centre in Germany [20]. They
screened patients with a history of medical treatment abroad
and screened rectal swabs or stool, respiratory samples, and
skin or wound swabs if present. All samples were plated on a
chromogenic Candida agar (CHROMagar Candida) and incu-
bated for 48 h at 37  C. Among 655 patients who were screened
for C. auris upon admission, no colonization was detected.
Several factors can explain the difference in results. First,
C. auris may have further emerged after their study
(2017e2022). Second, they did not include the groins and axilla
as standard screening sites. Third, the culture incubation
temperature and duration were not optimized for growth of
C. auris. Fourth, this may indicate, as we also found in our
study, that culture is not as sensitive as PCR, or that difficulty in
differentiating C. auris from other Candida spp. may have led
to missed cases.
A limitation of our PCR validation is the small number of
C. auris strains used for assay validation. Furthermore, we have
found a relatively low number of clinical cases positive for
C. auris compared to some reported large outbreaks. The low
number of positive clinical cases may be due to the still limited
introduction of C. auris in Dutch hospitals or the limited sen-
sitivity of our screening protocol. Nevertheless, our results
Table III
Characteristics of the positive cases and their laboratory results
Case no. Sexa Transferral Clinical description Month of specimen C. auris PCR: Ct valuesb C. auris culture Antifungal
hospital(s) collection resultsb susceptibility
testing (MIC)
1 Male Hospital in Ukraine Victim of bomb attack. Mar, 2023 Groin: 36 Dry swabs were Fluconazol: >256
and Poland Transferred for orthopaedic Axilla: 36.3 taken of all body mg/mL
surgery, including external Throat: 37.6 sites and 8 wound Micafungin:

S.E. Leonhard et al. / Journal of Hospital Infection 146 (2024) 31e36

fixation device. Nose: 33.5 sites. One groin 0.12 mg/mL
swab showed Anidulafungin:
growth of C. auris 0.06 mg/mL
after 3 days. All Caspofungin:
others remained 0.06 mg/mL
negative after 14 Amphotericin-B:
days. 2 mg/mL
2 Male Hospital in Ukraine Victim of bomb attack. Apr, 2023 Rectum: 37.9 No growth N/A
and other Dutch Transferred for orthopaedic
hospital surgery, including external
fixation device.
3 Male Hospital in Malignancy with recurrent Apr, 2023 Axilla: 35.7 No growth N/A
Germany and pleural effusion. Thoracic drain
other Dutch placed in hospital in Germany.
hospital Drain removed in other Dutch
hospital prior to admission to
Erasmus MC.
4 Male Hospital in Cardiovascular disease Sep, 2023 Throat: 37 No growth N/A
Morocco
5 Male Hospital in Ukraine Military trauma, treated with Oct, 2023 Nose: 37 No growth N/A
external fixation device
6 Male Hospital in Liver disease Oct, 2023 Nose: 35.8 No growth N/A
Curaçao Rectum: 35.2
7 Female Hospital in Pre-admission Oct, 2023 Throat: 35.2 No growthc N/A
Suriname Groin: 35.4
PCR, polymerase chain reaction; MIC, minimum inhibitory concentration.
a
All were adult patients.
b
Both E-swab medium and dry swabs of the nose, throat, axilla, groin and rectum swab, and any wound sites if present, were inoculated on CHROMagar and Sabouraud agar with 4% glucose,
gentamicin and chloramphenicol (SABGenta) and incubated for 14 days at 40  C as per protocol. In this table only the sites that were positive are shown.
c
In this patient only E-swabs were taken.

35
36 S.E. Leonhard et al. / Journal of Hospital Infection 146 (2024) 31e36
indicate that our screening protocol is more sensitive than
culture, as we were able to culture C. auris in only one of seven
PCR-positive cases. To further improve our screening method,
we plan to further improve culture conditions.
In conclusion, we developed, validated, and implemented
in-house an C. auris-specific PCR. In the eight months after its
implementation seven C. auris-positive patients were identi-
fied, of which three originated from Ukraine. As screening for
C. auris was added to our standard screening of MDROs, the
protocol was easy to implement in our hospital. Our findings
reflect the more extensive spread of C. auris among wounded
soldiers from Ukraine or hospitals in Eastern Europe and the
importance of screening for C. auris in hospitals across Europe.
Acknowledgements
C. auris control strains were kindly provided by the
Department of Medical Microbiology & Infectious Diseases,
Canisius Wilhelmina Hospital, Nijmegen, the Netherlands. We
thank the technicians at the Molecular Diagnostics Laboratory
at the Medical Microbiology Department of the Erasmus MC for
expert technical assistance.
Conflict of interest statement
None declared.
Funding sources
None.
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