International Journal of Infectious Diseases 63 (2017) 9598

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International Journal of Infectious Diseases

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

Candida auris: An emerging multidrug-resistant pathogen

David Sears* , Brian S. Schwartz
Division of Infectious Diseases, University of California, San Francisco, USA

A R T I C L E I N F O A B S T R A C T

Article history:
Received 30 August 2017 Candida aurisis an emerging multidrug-resistant pathogen that can be difcult to identify using
Accepted 30 August 2017 traditional biochemical methods. C. auris is capable of causing invasive fungal infections, particularly
Corresponding Editor: Eskild Petersen, Aar- among hospitalized patients with signicant medical comorbidities. Echinocandins are the empiric drugs
hus, Denmark of choice for C. auris, although not all isolates are susceptible and resistance may develop on therapy.
Nosocomial C. auris outbreaks have been reported in a number of countries and aggressive infection
Keywords: control measures are paramount to stopping transmission.
Candida auris 2017 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.
Multidrug-resistance
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
Healthcare-associated
nc-nd/4.0/).
Outbreak
Infection control

Introduction Microbiology and diagnosis

Candida auris was rst identied from samples of external ear
drainage from one Japanese patient (Satoh et al., 2009) and
15 Korean patients in 2009 (Kim et al., 2009). This organism can be
challenging to identify using standard microbiologic techniques
and frequently exhibits multidrug-resistance. In the eight years
since these initial cases, C. auris has become an emerging global
health threat, implicated in a host of invasive infections and
outbreaks in healthcare facilities. To date, cases have now been
identied in India (Sarma et al., 2013; Chowdhary et al., 2013),
South Africa (Magobo et al., 2014), Kuwait (Emara et al., 2015), the
United Kingdom (Schelenz et al., 2016), Venezuela (Calvo et al.,
2016), Brazil (Prakash et al., 2016), the United States (Vallabhaneni
et al., 2016), Colombia (Morales-Lpez et al., 2017), Pakistan
(Lockhart et al., 2017), Spain (Ruiz Gaitn et al., 2017), Germany
(European Centre for Disease Prevention and Control, 2016), Israel
(Ben-Ami et al., 2017), Norway (European Centre for Disease
Prevention and Control, 2016), and Oman (Al-Siyabi et al., 2017).
This review will detail the microbiology, clinical features,
therapeutic options, and infection control measures relevant to
C. auris infection.
* Corresponding author at: 513 Parnassus Ave., Box 0654, San Francisco, CA
94143, USA. Fax: +1 415 476 9364.
E-mail address: david.sears@ucsf.edu (D. Sears).
C. auris is phylogenetically related to Candida haemulonii and
Candida ruelliae (Satoh et al., 2009). Four distinct clades have been
identied from separate geographic origins, suggesting a recent
and nearly simultaneous emergence of different clonal populations
(Lockhart et al., 2017). C. auris grows readily at 3742  C and forms
light pink colonies on chromogenic media (Chowdhary et al., 2014;
Kathuria et al., 2015). Unlike C. haemulonii,C. auris does not form
pseudohyphae. Only some C. auris strains produce the virulence
factors phospholipase and proteinase, which may account for the
variability in pathogenicity demonstrated in a murine model
(Borman et al., 2016; Larkin et al., 2017). C. auris is capable of
forming biolms (Oh et al., 2011) and adhering to catheter
material, although not to the same degree as Candida albicans
(Larkin et al., 2017).
Traditional biochemical methods of identication commonly
misdiagnose C. auris as other yeast. The United States Centers for
Disease Control and Prevention (CDC) recommends further testing
for C. auris whenever C. haemulonii is identied or in a number of
other scenarios depending on the organism reported and the
method of identication (Table 1). Accurate identication can be
performed with VITEK MS and Bruker Biotyper matrix-assisted
laser desorption/ionization time-of-ight (MALDI-TOF) devices
using their research use only databases. Molecular sequencing of
the D1D2 domain of the 28s rDNA can also identify C. auris (CDC,
2017). For laboratories without the capability to perform these
tests, Kumar et al. propose a low-cost alternative that can
accurately distinguish C. auris from C. haemulonii using CHROMa-
gar medium supplemented with Pals medium (Kumar et al., 2017).

http://dx.doi.org/10.1016/j.ijid.2017.08.017
1201-9712/ 2017 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
96 D. Sears, B.S. Schwartz / International Journal of Infectious Diseases 63 (2017) 9598

Table 1 range of healthcare settings and patient populations (Chowdhary

When to suspect Candida auris based on the organism presumptively identied and
the method of identication (CDC, 2017).
Organism reported Method
Candida haemulonii Any
Candida spp. Any validated identication method
Rhodotorula glutinis API 20C if red color is not present
Candida sake API 20C
Candida catenulata BD Phoenix
Candida catenulata MicroScan
Candida famata MicroScan
Candida guilliermondii MicroScan
Candida lusitaniae MicroScan
Source: US Centers for Disease Control and Prevention.
Clinical features
Risk factors for C. auris infection appear to be similar to
infections from Candida in general. These include immunosup-
pressed state, signicant medical comorbidities, central venous
catheters, urinary catheters, recent surgery, parenteral nutrition,
exposure to broad spectrum antimicrobials, intensive care unit
admission, and residence in a high-acuity skilled nursing facility
(Vallabhaneni et al., 2016; Sarma and Upadhyay, 2017). In a case-
control study investigating risk factors for C. auris fungemia
compared to bloodstream infection from other Candida species in
Indian ICUs, those with C. auris fungemia were more likely to have
had longer antecedent hospitalizations, underlying respiratory
conditions, vascular surgery, prior antifungal exposure, and low
APACHE II scores. Patients with C. auris fungemia in this study were
also more frequently from public-sector ICUs from the north of
India (Rudramurthy et al., 2017).
C. auris has been recovered in samples from blood, catheter tips,
cerebrospinal uid, bone, ear discharge, pancreatic uid, pericar-
dial uid, peritoneal uid, pleural uid, respiratory secretions
(including sputum and bronchoalveolar lavage), skin and soft
tissue samples (both tissue and swab cultures), urine, and vaginal
secretions. Clinically, it has been implicated as a causative agent in
fungemia, ventriculitis, osteomyelitis, malignant otitis (including
otomastoiditis), complicated intra-abdominal infections, pericar-
ditis, complicated pleural effusions, and vulvovaginitis (Satoh et al.,
2009; Kim et al., 2009; Sarma et al., 2013; Magobo et al., 2014;
Emara et al., 2015; Schelenz et al., 2016; Calvo et al., 2016;
Vallabhaneni et al., 2016; Morales-Lpez et al., 2017; Lockhart
et al., 2017; Ruiz Gaitn et al., 2017; Ben-Ami et al., 2017; Al-Siyabi
et al., 2017; Borman et al., 2016; Lee et al., 2011; Khillan et al., 2014;
Choi et al., 2017; Chowdhary et al., 2017; Tsay et al., 2017). Much
like other Candida species, there is uncertainty about the ability of
C. auris to cause true respiratory, urinary, and skin and soft tissue
infections despite being isolated from such samples.
While one study reported no C. auris attributable deaths among
nine patients with fungemia, crude mortality rates for C. auris
fungemia have otherwise ranged from 28 to 66% across a wide
et al., 2013; Calvo et al., 2016; Vallabhaneni et al., 2016; Morales-
Lpez et al., 2017; Lockhart et al., 2017; Al-Siyabi et al., 2017;
Chowdhary et al., 2014; Rudramurthy et al., 2017; Lee et al., 2011).
Antifungal therapies
Source control measures, including removal of indwelling
catheters, are likely as important to the successful treatment of
invasive C. auris infections as they are to other forms of invasive
candidiasis. Regarding antifungal therapy, there are no Clinical and
Laboratory Standards Institute (CLSI) or European Committee for
Antimicrobial Susceptibility Testing (EUCAST) dened breakpoints
for C. auris susceptibility. CDC recommends that all C. auris isolates
undergo susceptibility testing and provides guidance for MIC
breakpoints based on related Candida species and expert opinion
(Table 2) (CDC, 2017). Fluconazole (tentative MIC breakpoint 32)
is associated with high minimum inhibitory concentrations (MICs)
and is likely almost always resistant. Susceptibility testing from
four studies involving between 54 and 123 clinical isolates
revealed MIC50 results between 64 and 128 mg/L and
MIC90 results between 64 and 256 mg/L by CLSI microbroth
dilution. Echinocandins (tentative MIC breakpoint 4 for anidu-
lafungin and micafungin, 2 for caspofungin) appear to be most
active in these studies with favorable results for anidulafungin
(MIC50 range 0.1250.5, MIC90 range 0.51), caspofungin (MIC50
0.250.5, MIC90 1), and micafungin (MIC50 0.1250.25, MIC90
0.252). Amphotericin B (tentative MIC breakpoint 2) suscepti-
bility testing exhibits a wider range of MIC results (MIC50 0.51,
MIC90 24) and is likely less reliable as empiric therapy (Prakash
et al., 2016; Lockhart et al., 2017; Kathuria et al., 2015; Arendrup
et al., 2017). Regarding second generation triazole susceptibility,
uconazole susceptibility can be used as a surrogate although
uconazole-resistant isolates may occasionally respond to other
triazole antifungals (CDC, 2017). In comparison to CLSI microbroth
dilution, similar MIC50 and MIC90 results can likely be obtained by
the EUCAST method (Arendrup et al., 2017), although caution
should be used when interpreting Etest and Vitek antifungal
susceptibility testing results (Kathuria et al., 2015).
Based on these results, echinocandins are the empiric drugs of
choice for C.auris infections in adults and children over the age of 2
months. Amphotericin Bwhile less reliableshould be considered
for patients not responding to echinocandin therapy, depending on
MIC results. A mouse model testing antifungal therapy on nine
strains of C. auris suggested that micafungin may be particularly
fungicidal and more active than tentative MIC breakpoints may
suggest (Lepak et al., 2017), however further clinical studies in
humans are needed. It is important to note that resistance may
develop on therapy and close clinical follow-up and potentially
repeat MIC testing may be indicated for patients who are
responding poorly to antifungal therapy.

Table 2
Tentative MIC (mg/L) breakpoints for Candida auris susceptibility (CDC, 2017) and published MIC ranges by CLSI microbroth dilution (Prakash et al., 2016; Lockhart et al., 2017;
Kathuria et al., 2015; Arendrup et al., 2017).

Antifungal drug Tentative MIC breakpoint Published MIC50 range Published MIC90 range
Fluconazole 32 64128 64256
Voriconazolea N/Ab 0.52 48
Amphotericin B 2 0.51 24
Anidulafungin 4 0.1250.5 0.51
Caspofungin 2 0.250.5 1
Micafungin 4 0.1250.25 0.252
a
Also applies to other second generation triazole antifungals.
b
Consider using uconazole susceptibility as a surrogate, although uconazole-resistant isolates may occasionally respond to other triazole antifungals.
 D. Sears, B.S. Schwartz / International Journal of Infectious Diseases 63 (2017) 9598
Much like colonization with other multidrug-resistant species,
CDC does not recommend systemic antifungal therapy for patients
who are colonized with C. auris (CDC, 2017).
Infection control
C. auris can cause widespread and persistent contamination of
environmental surfaces within healthcare facilities and has been
associated with both intra-hospital and inter-hospital transmis-
sion of clonal strains in multiple countries (Kim et al., 2009;
Chowdhary et al., 2013; Schelenz et al., 2016; Calvo et al., 2016;
Morales-Lpez et al., 2017; European Centre for Disease Prevention
and Control, 2016; Ben-Ami et al., 2017; Tsay et al., 2017; Piedrahita
et al., 2017). The largest reported outbreaks to date were in a
cardio-thoracic center in the United Kingdom (22 patients infected
and an additional 28 patients colonized) (Schelenz et al., 2016) and
a surgical intensive care unit in Spain (33 cases of C. auris
fungemia) (European Centre for Disease Prevention and Control,
2016). From 77 clinical cases in the United States, CDC used groin
and axilla swabs to screen an additional 390 close contacts (mainly
patients on the same ward of a known clinical case) and identied
C. auris colonization in another 45 individuals. Patients within
similar geographic regions in this study commonly had over-
lapping stays in the same acute care hospital or long-term care
facility, further supporting healthcare exposure as a key method of
transmission (Tsay et al., 2017).
Given the risk of nosocomial transmission of this multidrug-
resistant pathogen, infection control measures are vital to slowing
the spread of C. auris. CDC recommends that all hospitalized
patients with C. auris infection or colonization be treated using
both Standard Precautions and Contact Precautions (CDC, 2007)
and housed in a private room with daily and terminal cleaning with
a disinfectant agent active against Clostridium difcile spores (US
EPA OCSPP, 2015; Cadnum et al., 2017). Receiving healthcare
facilities should also be notied prior to transfer of an infected or
colonized patient. Infection control precautions should be main-
tained until a patient is no longer infected or colonized with C. auris
although there is uncertainty as to how best to monitor for ongoing
colonization (CDC, 2017). There are no clear data on the efcacy of
decolonization measures for patients colonized with C. auris,
however this has been attempted with chlorhexidine in healthcare
facilities during outbreaks (Schelenz et al., 2016; Calvo et al., 2016;
European Centre for Disease Prevention and Control, 2016).
Future directions
As C. auris cases continue to be found throughout the world,
there is urgent need for improved diagnostics, antifungal thera-
pies, and infection control measures. PCR and real-time PCR assays
to rapidly identify C. auris have shown excellent accuracy in
development and could be performed in laboratories that do not
have the ability to perform MALDI-TOF or molecular sequencing
techniques (Kordalewska et al., 2017). The development of new
antifungal medications with activity against C. auris will be vital to
controlling C. auris as therapeutic options are already limited. SCY-
078, a novel triterpene glucan synthase inhibitor, is currently in
phase III trials for invasive and mucocutaneous candidiasis and has
recently shown promising activity in vitro against C. auris (Larkin
et al., 2017; Berkow et al., 2017). Finally, aggressive infection
control measures are critical to reducing the spread of C. auris.
Antimicrobial stewardship, hand hygiene, and contact precautions
will continue to be of paramount importance. More information is
needed, however, about effective measures to reduce patient
colonization and environmental contamination in healthcare
97
facilities which have served as sites of ongoing transmission of
this emerging pathogen.
Funding sources
This research did not receive any specic grant from funding
agencies in the public, commercial, or not-for-prot sectors.
Conict of interest
The authors report no conicts of interest.
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