pathogens

Review
The Gordian Knot of C. auris: If You Cannot Cut It, Prevent It
Vasiliki Rapti 1, *, Katerina Iliopoulou 2 and Garyfallia Poulakou 1

1 Third Department of Internal Medicine, School of Medicine, National & Kapodistrian University of Athens,
Sotiria General Hospital, 115 27 Athens, Greece; [email protected]
2 Lead Research Nurse, NHS Lothian, Edinburgh EH1 3EG, UK; [email protected]
* Correspondence: [email protected]

Abstract: Since its first description in 2009, Candida auris has, so far, resulted in large hospital out-
breaks worldwide and is considered an emerging global public health threat. Exceptionally for yeast,
it is gifted with a profoundly worrying invasive potential and high inter-patient transmissibility. At
the same time, it is capable of colonizing and persisting in both patients and hospital settings for
prolonged periods of time, thus creating a vicious cycle of acquisition, spreading, and infection. It
exhibits various virulence qualities and thermotolerance, osmotolerance, filamentation, biofilm for-
mation and hydrolytic enzyme production, which are mainly implicated in its pathogenesis. Owing
to its unfavorable profile of resistance to diverse antifungal agents and the lack of effective treatment
options, the implementation of robust infection prevention and control (IPC) practices is crucial for
controlling and minimizing intra-hospital transmission of C. auris. Rapid and accurate microbiologi-
cal identification, adherence to hand hygiene, use of adequate personal protective equipment (PPE),
proper handling of catheters and implantable devices, contact isolation, periodical environmental
decontamination, targeted screening, implementation of antimicrobial stewardship (AMS) programs
and communication between healthcare facilities about residents’ C. auris colonization status are rec-
ognized as coherent strategies for preventing its spread. Current knowledge on C. auris epidemiology,
clinical characteristics, and its mechanisms of pathogenicity are summarized in the present review
and a comprehensive overview of IPC practices ensuring yeast prevention is also provided.

Keywords: Candida auris; epidemiology; colonization; virulence; transmission; risk factors; outcomes;
microbiological identification; infection control practices

Citation: Rapti, V.; Iliopoulou, K.;

Poulakou, G. The Gordian Knot of C.
auris: If You Cannot Cut It, Prevent It.
1. Introduction
Pathogens 2023, 12, 1444. https:// In recent years, the global burden of invasive fungal infections (IFIs) has shown an
doi.org/10.3390/pathogens12121444 upsurge, resulting from both the expansion of the immunocompromised population and
the increase in invasive medical procedures [1]; thus, they embody a serious and growing
Academic Editor: Longzhu Cui
public health threat. Approximately 70% of all IFIs reported annually are attributed to
Received: 1 November 2023 invasive candidiasis (IC), and Candida species have been identified as the predominant
Revised: 30 November 2023 cause of nosocomial fungal infections, as well as the fourth leading cause of all hospital-
Accepted: 11 December 2023 acquired bloodstream infections (BSIs) [2,3]. Although C. albicans is the most commonly
Published: 13 December 2023 encountered pathogen among Candida species [2], we are most concerned about C. auris, a
non-albicans species, which is classified as an urgent public health threat.
C. auris is a notorious cause of insidious hospital outbreaks and deep-seated infec-
Copyright: © 2023 by the authors.
tions [4,5]. It is primarily recovered from hospital environments [6–8], and, due to its
Licensee MDPI, Basel, Switzerland.
unique traits, it is capable of colonizing and persisting in both patients and hospital set-
This article is an open access article
tings for prolonged periods, thus creating a vicious cycle of acquisition, spreading, and
distributed under the terms and infection, particularly in intensive care units (ICUs) [4,5,9]. Generally, it combines all the
conditions of the Creative Commons essential characteristics to be classified as an urgent public health threat [6,10], including
Attribution (CC BY) license (https:// the potentiality to spread rapidly through horizontal transmission, the ability to cause seri-
creativecommons.org/licenses/by/ ous and life-threatening infections in susceptible individuals and the unfavorable profile
4.0/).

Pathogens 2023, 12, 1444. https://doi.org/10.3390/pathogens12121444 https://www.mdpi.com/journal/pathogens

Pathogens 2023, 12, 1444 2 of 14

of resistance to antifungal agents, alongside the lack of effective treatment options and
standardized measures for prevention and control [4,5].
The aim of the present review is to summarize current knowledge on C. auris epi-
demiology, its clinical characteristics and mechanisms of pathogenicity, and provide a
comprehensive overview of IPC measures and strategies.

2. Epidemiology
C. auris is a newly emerging multidrug-resistant yeast pathogen that has garnered
the attention of the scientific and healthcare community. Whole-genome sequencing and
phylogenetic analyses have revealed >4 major clades of C. auris with each one covering a
distinct geographic area that emerged independently and nearly simultaneously at different
locations across three continents [4,11–13].
Since its first description as a novel Candida species in 2009 in Japan, C. auris has, so far,
been isolated in over 40 countries across six continents [4]. It is considered endemic in many
regions of Africa and Asia [4,14–16], whereas prolonged and difficult-to-contain large-scale
outbreaks, especially in ICUs, have been reported in Europe and the United States of
America (USA) [4,5,17–25]. According to the European Centre for Disease Prevention
and Control (ECDC), in a 4-year period (2013–2017), 620 C. auris cases were recorded in
the European Union and European Economic Area, the vast majority of which derived
from four large outbreaks in Spain and the United Kingdom [18,19,26–28]. Currently,
the European burden of C. auris is steadily increasing; several sporadic cases have been
observed all over Europe [26,29], and Spain turns out to be the only European country
reporting regional endemicity [18]. In the USA, the Centers for Disease Control and
Prevention (CDC) announced that clinical cases have increased each year since 2016, with
the most rapid rise occurring during 2020–2021, and 17 states identified their first C. auris
case during 2019–2021 [24,25].
The coronavirus disease 2019 (COVID-19) pandemic has further shaped the landscape
of C. auris disease with a sharp rise in new cases of colonization and infection being
observed [30,31], mainly attributed to the overload of the healthcare systems worldwide and
the consequent compromised IPC practices [32–34], alongside the inability to implement
adequate AMS programs. Concurrently, considering that critically ill COVID-19 patients
tend to share risk factors, medications and underlying comorbidities with C. auris-infected
patients [34], preventing the spread of this superbug in the ICU is challenging.
The prevalence and geographic extent of C. auris disease are possibly underestimated,
mostly in low- and middle-income countries. The paucity of data arises from both the
absence of a global identification strategy and the limited accuracy of available conventional
diagnostic tools [35], since there is no widely used molecular method for rapid identification.
Simultaneously, as a result of its low incidence, no large-scale epidemiology studies have
been reported until now.

3. Colonization and Virulence Factors

The pathogenicity and virulence of C. auris are profoundly worrying, since it possesses
its own unique characteristics that enhance invasive potential, favor antifungal tolerance
and offer a growing advantage in natural and host niches. Thermotolerance, osmotolerance,
filamentation, biofilm formation and hydrolytic enzyme production have been recognized
as key components of C. auris pathogenesis.
Unlike most fungi that are unable to survive at human physiological temperatures,
C. auris exhibits thermotolerance, allowing its growth at high temperatures, optimally at
37 ◦ C, and maintaining viability up to 42 ◦ C [4,36–38]. Of note, this new fungal disease was
hypothesized to have originated from climate change, specifically global warming, based
on phylogenetic analysis findings [39]. Another major trait is tolerance to osmotic stresses
and high-saline environments (>10% NaCl, wt/vol) [4,36–38,40]. Notably, thermotolerance
and osmotolerance, alongside limited susceptibility to commonly used disinfectants, are
three cardinal characteristics of C. auris that permit its survival for days to weeks in diverse
Pathogens 2023, 12, 1444 3 of 14

moist and dry surfaces [37,41–44]. It endures seven days on steel and porous surfaces [43],
while on plastics, it persists for at least two weeks and can further survive in a-non
culturable state for up to a month [37]. Consequently, persistence in harsh environmental
conditions, a hallmark feature of C. auris that distinguishes it from the majority of other
human fungal pathogens, leads to the observed high intra-hospital transmissibility and
protracted outbreaks within healthcare settings [20,37,43].
Similar to other Candida species, it can undergo filamentation, a critical step in the
fungal invasion of host tissues, both as pseudohyphae [28] and true hyphae [4]. Low
temperatures were found to stimulate filamentous phenotype, whereas the human physio-
logical temperature suppresses filamentous growth [45–47], leading to the conclusion that
filamentous morphologies of C. auris may survive in the environment and on the host skin
surface where the temperature is lower than inside the host. Additionally, a portion of C.
auris isolates are capable of producing aggregates of pseudohyphal-like cells under high
salt stress conditions or in biofilms [4,36,48]. The aggregating cells are known to display
reduced virulence, but better survival capacity [28], selective tolerance to biocides and
unique transferability to new, sterile surfaces after treatment [49,50].
Biofilm formation represents one of the main pathogenic traits. The majority of C. auris
colonizing and clinical isolates exhibit an equal or even greater biofilm formation than C. al-
bicans [48,51–54]. Singh and colleagues demonstrated that aggregated and non-aggregated
phenotypes are predominantly associated with colonizing and clinical isolates, respectively,
with the latter forming more robust biofilms [48]. Dense biofilms with up to 30-fold higher
cellular burden than C. albicans are produced in contaminated with dried-up sweat and
fatty acids surfaces, as might be the case during contact transmission from a colonized
patient [51,55]. Besides, multilayer biofilms are rapidly formed in regions like the axilla and
groin, while robust ones have been implicated in a variety of implant-associated infections,
including BSIs and urinary tract infections (UTIs) [56,57]; hence, removal of central venous
catheters (CVCs), other type of catheters and medical devices, where possible, should
be advocated as an adjunctive treatment strategy [19,34]. Resistance to desiccation, os-
motic stress [55,56] and various antifungals (e.g., fluconazole, voriconazole, echinocandins,
amphotericin B) [51], as well as reduced susceptibility to potent skin disinfection agents,
such as hydrogen peroxide and chlorhexidine [58], are other well-known characteristics
of C. auris biofilms. Lastly, Kean and colleagues shed light on C. auris biofilm-mediated
resistance [59]. During biofilm formation, C. auris induces the expression of a wide array of
genes encoding cell-wall proteins and adhesins that favor biofilm adherence and persis-
tence on biotic and abiotic surfaces. At the same time, genes encoding extracellular matrix
proteins are upregulated and the produced matrix provides both structural integrity to the
biofilm and yeast protection from environmental stressors, such as chemicals and disinfec-
tants. Finally, a plethora of transporters and efflux-pumps are activated and resistance to
antifungals and toxic chemicals is further promoted [59].
As far as virulence is concerned, C. auris expresses several virulence factors to degrade
and invade host tissues [40,47]. Once in the environment, it activates the stress-activated
protein kinase Hog1 for its adaptation to the dry abiotic milieu [55,56,60]. During this
transition, phospholipases and proteinases are secreted in a strain-dependent manner and
contribute to C. auris pathogenesis [52]. C. auris also stimulates hemolysin secretion to
accelerate iron assimilation from the hemoglobin–heme group and eventually enhance its
survival within the host [61,62].

4. Predisposing Factors for C. auris Infection, Clinical Spectrum and Outcomes

The predisposing risk factors for C. auris infection (Table 1) are similar to other Can-
dida species, since they are opportunistic pathogens that primarily affect critically ill and
immunocompromised patients [63].
Pathogens 2023, 12, 1444 4 of 14

Table 1. Predisposing factors for C. auris infection.

Predisposing Factors Reference

Chronic Disease
(e.g., cardiovascular, respiratory and renal disease, diabetes [4,11,17,30,64–68]
mellitus)
Immunosuppression
(e.g., malignancy, AIDS, organ transplantation, [4,11,30,64,65,67,69]
immunosuppressive agents)
Catheters and Indwelling Medical Devices [4,11,17,30,41,64–67,70–73]
Mechanical Ventilation [4,30,64,66,70,73]
Prolonged Hospital and ICU stay [30,65,67,70]
Broad-spectrum Antimicrobial and Antifungal Therapy [11,19,30,64–68,70,73]
Parenteral Nutrition [19,30,65]
Recently Performed Invasive Medical Procedures
[11,19,30,65,67,68,70]
(e.g., surgery)
Age
[65,67]
(e.g., preterm infants and elderly)
Male sex and country-specific health factors [65,67]
Diarrhea [74]
Tetracyclines consumption (minocycline and tigecycline) [74]
AIDS: Acquired immunodeficiency syndrome; ICU: Intensive care unit.

Clinical manifestations of C. auris are diverse and range from colonization and mild,
superficial skin infections to invasive disease and deep-seated infections [4,5]. Common sites
of colonization include the skin, mostly the groin and axilla areas, rectum and mucosal surfaces
of the urinary and respiratory tract (e.g., nares, and oropharynx) [9,15,19,30,41,70,75–77]. It
is suggested that C. auris is incapable of colonizing anaerobic environments [5], like the
gut, and the salivary antimicrobial peptide histatin 5 exerts a potent candidacidal effect
on C. auris [71]. Therefore, unlike C. albicans, the colonization of the gastrointestinal tract
is rare. Infection can occur at multiple body sites and C. auris has been isolated from
both sterile (e.g., blood, cerebrospinal fluid, and bile) and non-sterile samples (e.g., urine,
sputum, tissue, wound swabs, and catheter tips) [4,5,36,76]. Progression from colonization
to invasive infections is estimated to occur in up to one fourth of affected patients [30,72],
and candidemia is the predominant type of C. auris infection, followed by urinary tract,
wound and ear infections, and rarely by respiratory tract or intra-abdominal infections,
skin abscesses, myocarditis, meningitis and osteomyelitis [5]. It is noteworthy that C. auris
candidemia usually follows colonization and multisite colonization is an independent
risk factor for the development of candidemia [30]. Hence, the prompt identification
of colonized patients at greater risk for developing candidemia may be beneficial for
improving early diagnosis and preventing invasive infection through interventions on
modifiable predictors. Lastly, the risk of infection of implantable devices (e.g., defibrillators,
pacemakers, prosthetic joints, etc.) when the candidate is already colonized by C. auris
has not yet been addressed in the literature, but according to the authors’ opinion, it is not
negligible.
Invasive infections caused by C. auris are potentially life-threatening and increased
mortality rates with significant geographic variation have been reported. In the literature,
crude mortality ranges from 27% to 70% [11,30,64–66,68,70,73], whereas attributable mor-
tality has not been adequately explored. Notably, a recent meta-analysis of 4733 C. auris
cases, recorded from 2009 to 2019 in 33 countries worldwide, estimated a crude mortality
of 39% and suggested a lower mortality in the European compared to the Asian continent
(20% vs. 44%) [78]. Furthermore, as expected, BSIs incur a significant mortality toll, which
can be as high as 70% [11,64,70,73], yet a crude mortality of 45% was documented in the
aforementioned meta-analysis [78]. Additionally, crude 30-day mortality, reaching almost
60%, was revealed in case of recurrent candidemia in a study of 157 critically ill and C.
auris-colonized patients, of whom 27 patients developed candidemia and 7 had a late
recurrent episode [30]. This finding, however, should be interpreted with caution as it
 toll, which can be as high as 70% [11,64,70,73], yet a crude mortality of 45% was docu-
mented in the aforementioned meta-analysis [78]. Additionally, crude 30-day mortality,
reaching almost 60%, was revealed in case of recurrent candidemia in a study of 157
critically ill and C. auris-colonized patients, of whom 27 patients developed candidemia
and 7 had a late recurrent episode [30]. This finding, however, should be interpreted with
Pathogens 2023, 12, 1444 5 of 14
caution as it may reflect the severity of underlying noninfectious conditions in patients
with prolonged ICU stay [79]. In co-infected COVID-19 patients, the estimated mortality
is 44.4% and candidemia engenders a mortality of 64.7% [80]. Regarding the specific
may reflect the
factors that are associated withseverity of underlying
unfavorable noninfectious
prognosis, advanced conditions
age, andinpresence
patients with
of prolonged
ICU stay [79]. In co-infected COVID-19 patients, the estimated mortality is 44.4% and
comorbidities, C. auris infection and particularly candidemia, as well as prolonged hos-
candidemia engenders a mortality of 64.7% [80]. Regarding the specific factors that are as-
pitalization, were identified in the survival analysis of a study that analyzed outcomes of
sociated with unfavorable prognosis, advanced age, and presence of comorbidities, C. auris
108 patients either infected or colonized by C. auris [66]. Similarly, in a retrospective
infection and particularly candidemia, as well as prolonged hospitalization, were identified
analysis of 92 C.inauris-affected patients,ofonly
the survival analysis candidemia
a study was outcomes
that analyzed causally linked to greater
of 108 patients either infected
mortality, while orboth infected and colonized cases shared comparable mortality [70].
colonized by C. auris [66]. Similarly, in a retrospective analysis of 92 C. auris-affected
patients, only candidemia was causally linked to greater mortality, while both infected and
5. Infection Prevention and
colonized Control
cases sharedStrategies
comparable mortality [70].
Prompt and accurate microbiological identification, as well as robust implementa-
5. Infection Prevention and Control Strategies
tion of evidence-based IPC strategies are crucial for controlling and preventing C. auris
outbreaks in healthcarePrompt and accurate
settings. microbiological
It is worth mentioning identification, as well
that C. auris as robust implementation
is transmissible
whether a patient is colonized or infected; thus, IPC measures are the same for bothC.pa-
of evidence-based IPC strategies are crucial for controlling and preventing auris outbreaks
in healthcare settings. It is worth mentioning that C. auris is transmissible whether a patient
tient groups.
is colonized or infected; thus, IPC measures are the same for both patient groups.
The IPC strategies which have, so far, been successfully implemented in diverse
The IPC strategies which have, so far, been successfully implemented in diverse health-
healthcare settings worldwide [19,20,81–89] are illustrated in Figure 1 and they are dis-
care settings worldwide [19,20,81–89] are illustrated in Figure 1 and they are discussed in
cussed in the following paragraphs.
the following paragraphs.

Figure 1. Optimal strategies for controlling and minimizing intra-hospital transmission of C. auris.
Figure 1. Optimal strategies for controlling and minimizing intra-hospital transmission of C. auris.
AMS: antimicrobial stewardship; PPE: personal protective equipment.
AMS: antimicrobial stewardship; PPE: personal protective equipment.
5.1. Rapid and Accurate Identification
5.1. Rapid and AccurateC.Identification
auris has overlapping phenotypic characteristics with other closely related species,
C. auris hassuch
overlapping phenotypic
as C. haemulonii, C. sakecharacteristics with other
and R. glutinis, which closelyits
compromise related spe-accurate iden-
rapid and
tification [90].
cies, such as C. haemulonii, Due and
C. sake to misidentification
R. glutinis, which issues, it is essential
compromise its that microbiology
rapid and accu- laboratories
update
rate identification [90]. their
Due tocommercial identification
misidentification software
issues, to enable
it is essential them
that to easily and efficiently
microbiology
identify C. auris cases [67], while the need for full identification
laboratories update their commercial identification software to enable them to easily in patients
andat greater risk
for C. auris colonization or infection should be communicated.
efficiently identify C. auris cases [67], while the need for full identification in patients at
greater risk for C. aurisA colonization
substantial progress has been
or infection shouldmade to improve C. auris identification methods.
be communicated.
The first step included the development of a high-salt, high-temperature enrichment
A substantial progress has been made to improve C. auris identification methods.
culture-based method that enables the accurate isolation of C. auris [37]. Once an isolate is
The first step included the development of a high-salt, high-temperature enrichment
obtained, matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass
culture-based method that enables the accurate isolation of C. auris [37]. Once an isolate is
spectrometry can be successfully applied for yeast identification, provided that the reference
obtained, matrix-assisted laser desorption/ionization
database contains the necessary information time-of-flight
[6,91]. In case(MALDI-TOF)
that MALDI-TOF massis not available,
spectrometry cansequence
be successfully applied for yeast identification, provided
analysis of the internal transcribed spacer and D1/D2 region of thethat the ref-
28 s ribosomal
erence database contains the necessary
deoxyribonucleic information
acid (DNA) can be[6,91]. In case
performed that MALDI-TOF
[6,10]. Nevertheless,isDNA not sequencing
available, sequence
is aanalysis of the internal
time-consuming, expensivetranscribed spacer
and is not and D1/D2
available region of the
in all diagnostic lab28methods, and
s ribosomal deoxyribonucleic acid (DNA) can be performed [6,10]. Nevertheless, DNA
its applicability may be limited, at least in developing countries [91]. For this reason,
sequencing is a various
time-consuming, expensive and
sequencing-independent is not available
DNA-based methods, inincluding
all diagnostic lab or multiplex
end-point
methods, and itspolymerase
applicabilitychain
mayreaction (PCR) assays,
be limited, at leasthave been designed;
in developing they are
countries highly
[91]. Forsensitive and
some of them were successfully validated for the direct detection of C. auris in clinical and
environmental samples [91].
Lately, other culture-independent methods, such as PCR-restriction fragment length poly-
morphism (RFLP) [92], Taqman quantitative PCR (qPCR) [93,94], SYBR green qPCR [95], GPS™
MONODOSE CanAur dtec-qPCR (Genetic PCR Solutions™, Elche, Alicante, Spain) [96]
and T2 Magnetic Resonance assay [97], have emerged as an attractive alternative approach
for rapid detection, mostly in surveillance samples, as they are accompanied by accurate
and reproducible identification of C. auris with a significantly reduced turnaround time
compared to culture/MALDI-TOF-based methods.
Pathogens 2023, 12, 1444 6 of 14

5.2. Transmission
An alarming characteristic of C. auris is its inter-patient transmissibility and the fact
that even colonized patients can serve as a reservoir for nosocomial spread. Specifically,
it is efficiently transmitted from patient to patient, either directly or indirectly by sharing
the same room or contaminated items, and by the colonized hands of healthcare workers
(HCWs) [75]. Notably, contact with contaminated items is by far the most common method
of colonization [20,37,43,44,64], and close contact of cases (e.g., current or past room con-
tacts within a prior month) has a documented colonization rate of 12–21% [22,64]. The
minimum contact period for the acquisition of C. auris from an infected person or surface is
estimated to be 4 h [21], and invasive infections have occurred in patients within 48 h of
ICU admission [98].
Sources of contamination have been found within the patient’s room, including bed-
ding materials (e.g., bed rails and pans, mattress, linen, and pillows), furniture, door
handles, flooring, walls, radiators, window sills, faucets and sinks [5,6,36,42,64,98,99]. It
has also been isolated from high-touch surfaces and medical equipment, such as oxy-
gen masks, axillary temperature probes, sphygmomanometer cuffs, pulse oxygen meters,
electrocardiograph leads, catheter tips, infusion pumps and ventilators, particularly in
outbreak settings [6,10,17,20–22,36,44,64,98–100]. For instance, following the identification
of a cluster of C. auris infections in the neurosciences ICU, Eyre and colleagues concluded
that patients exposed to reusable skin-surface axillary temperature probes had a sevenfold
risk of infection or colonization [44].

Transmission-Based Precautions
In a systematic review of 17 studies reporting multidrug-resistant (MDR) outbreaks in
ICUs, mainly caused by C. auris (n = 6), during the COVID-19 pandemic, the most com-
monly identified factors contributing to the outbreaks were inadequate PPE or a shortage
of PPE, hand hygiene non-adherence, and high antibiotic use, followed by environmental
contamination, prolonged critical illness and lack of trained HCWs [101]. Therefore, all
HCWs attending C. auris-infected or -colonized patients should apply standard hand hy-
giene practices and perform adequate hand hygiene with soap and water, alcohol-based
hand sanitizers, or chlorhexidine hand rubs [6,10,20,22,90,102–104]. Sharing of medical
supplies and equipment is prohibited and use of disposable PPE (e.g., gloves, aprons, and
gowns) is recommended [6,10,90,102,104]. Hospital infection control teams should raise
awareness about C. auris, ensure that enough quantities of hand hygiene materials are
available and monitor HCW adherence with recommended hand hygiene practices and
PPE use, as well as train the personnel and retrain them at regular intervals. Additionally,
as a low HCW/patient ratio is a well-established risk factor for MDR-organism (MDRO)
transmission [105], a minimum number of HCWs should be designated for C. auris cases.
Strict isolation of patients harboring C. auris is recommended by the CDC and ECDC
in order to prevent horizontal transfer to other patients [6,10]. Ideally, they should be
placed in single-occupancy rooms with designated medical equipment and attached toilet
facilities and be restricted there, except for medically necessary procedures [6,104]. Their
rooms should be clearly marked and limited contact with visitors should be allowed. In
case the number of single rooms is limited, they should be reserved for patients at the
highest risk for transmission, such as those with uncontained secretions or diarrhea [90].
C. auris patients can also be cohorted [90,104], taking into account that these patients are
usually co-infected with other MDROs. Strict isolation measures should not be an excuse
for suboptimal patient care or result in the subject’s stigmatization [106]. Safety indicators
and tools should be developed to avoid rupture in the flow of care as well as isolated
patients’ emotional stress.

5.3. Decontamination and Disinfection Procedures

Extensive contamination of the healthcare environment has been described in facilities
with C. auris outbreaks, highlighting the crucial role of enhanced daily and terminal
Pathogens 2023, 12, 1444 7 of 14

disinfection in spread prevention [6,10]. Nevertheless, there are currently no standardized

cleaning or disinfection procedures. Prior to decontamination, visible organic materials
(e.g., body fluids) from the patient care area should be removed and cleaned [90], and the
frequency of cleaning and disinfection is recommended to be at least twice daily, up to
three times during outbreaks, and at least on all high-touch surfaces, such as bedrails and
bedside tables [6]. Moreover, in case of patient discharge or transfer, terminal cleaning and
disinfection should be carried out with great diligence and environmental sampling for C.
auris culture should be performed in an outbreak setting [6,10,90,104]. To date, only sodium
hypochlorite of 100 ppm concentration and topical hydrogen peroxide-based disinfectants
are widely recommended for use [6,20,107,108], since commercially available products have
been proven ineffective in eradicating C. auris [109]. For this reason, the US Environmental
Protection Agency (EPA) has registered a list of qualified products for use and released
a standardized quantitative disk carrier method, with the acronym SOP-MB-35-00, for
evaluating the efficacy of antimicrobials against C. auris on hard, non-porous surfaces [110].
It is worth mentioning that disinfectant selection should be made weighting toxicity.
For instance, exceptionally toxic disinfectants, like high-strength sodium hypochlorite
agents of 5000 ppm concentration, should be reserved for terminal cleaning and not used
on a regular basis. In addition to routine cleaning with disinfectants, peracetic acid [111],
hydrogen peroxide < 1% [112], vaporized hydrogen peroxide [113], and ultraviolet subtype-
C (UV-C) are other measures that can be used for optimal decontamination [114,115]. For
example, UV-C is sufficient to prevent biofilm formation [115], and repeated flushing of
colonized sinks in the patient’s room with ozonated water (2.5 ppm) (cycles of 30 s every
4 h) resulted in yeast elimination within 2 days [116]. Recently, silver nanoparticles are
recognized as promising antifungal agents, as they exhibited both inhibitory effects on the
growth of C. auris and antibiofilm formation activity [117]. Finally, as already mentioned,
dedicated and single-use items (e.g., pillows, and bedding material) and equipment (e.g.,
thermometers, and blood pressure cuffs) should be used and, for equipment that cannot be
dedicated to patients harboring C. auris, it is mandatory for it to be thoroughly disinfected
after use [90,104].

5.4. Decolonization Protocols

The efficacy of decolonization protocols is still under investigation and not supported
by regulatory bodies. Schelenz and colleagues suggest oral nystatin use, bathing with single-
use wipes of 2% chlorhexidine gluconate twice daily and mouth washing with chlorhexidine
0.2% or chlorhexidine 1% dental gel in oropharyngeal-colonized, skin-colonized and ven-
tilated patients, respectively [21]. However, if transient decolonization is achieved, the
occurrence of recolonization is a potent scenario and high-touch areas may be the source
of contamination where C. auris persists for long periods of time [20,21]. For this reason,
patients with a history of colonization/infection by C. auris in the past should be considered
as potentially colonized for at least one year in case of readmission, until surveillance
cultures prove negative.

5.5. Targeted Screening and Labelling of the Patients

Targeted screening serves as a useful tool to prevent hospital transmission by rapidly
implementing IPC practices. Once a C. auris-positive case has been identified, the infection
control team should be immediately informed in order to trace the contact of origin and
identify other potential patients who may have been exposed to the fungi. Moreover, C.
auris cases should be followed until discharge and flagged for at least one year after the
first negative screening culture [102], whereas HCWs and persons in close contact with
them should be placed under strict contact precautions [21].
The CDC recommends that screening should be considered for close healthcare con-
tacts with newly identified C. auris cases (colonized and/or infected) and patients reporting
an overnight healthcare facility stay in a country outside the US in the previous year, espe-
cially if the country has documented C. auris cases [6]; pre-emptive screening of patients
Pathogens 2023, 12, 1444 8 of 14

with international exposure is based on the finding that patients with a history of abroad
hospitalization are at higher risk of MDRO carriage during ICU admission [118], and
approximately 1 in 2 are estimated to be positive [119]. Notably, similar recommendations
are supported by the ECDC [10].
Collection of one or more swabs of the patient’s axilla and groin regions is the screening
method of choice [6], as they are thought to be consistent sites of colonization, albeit other
body sites and specimens (e.g., nares, external ear canals, urine, wounds, and rectum) can
be sampled, if indicated [10]. Initial screening and active surveillance may be conducted
with one of the rapid microbial-detection methods mentioned above, followed by culture
and molecular typing for epidemiological investigation. In the literature, there are several
paradigms of successful screening programs [109,120,121], hence emphasizing the need
and utility of a rapid and automated molecular surveillance admission screening, primarily
in endemic regions.

5.6. Handling of Catheters and Implantable Devices

In the context of infection source control, urinary catheter or CVC removal in C.
auris-infected patients is crucial [17,19,122–124]. Strict adherence to central, peripheral,
and urinary catheter care bundles and proper care of the tracheostomy site are essential
preventive measures [6], and placing chlorhexidine-impregnated protective disks in all
CVC exit sites may result in the reduction of central line-associated BSIs [21]. As previously
discussed, the risk of infection of implantable devices in C. auris colonized patients does
not seem negligible. Therefore, although there are no specific recommendations to our
knowledge, we would suggest rigorous skin preparation before the implantation and a
single dose of an antifungal agent preoperatively, according to the antibiogram, prioritizing
agents acting in the presence of biofilm.

5.7. AMS Programs Implementation

Antifungal stewardship (AFS) programs are recognized as an essential tool for min-
imizing antifungal overuse or misuse [122,123], and C. auris emergence provided the
impetus for their broad implementation. For instance, in the past, AFS was less attrac-
tive and in a survey of AFS initiatives in English acute hospitals, only a minority (11%)
conducted a dedicated AFS program [125]. Considering that antifungal drug classes are
limited compared with antibacterial classes and the fact that C. auris presents reduced
susceptibility to azoles, polyenes, and echinocandins, in a clade-dependent manner [126],
judicious use of antifungals is necessary. Therefore, intensification of AFS within the AMS
programs is of great importance. Decreasing empiric antifungal treatment as much as pos-
sible and performing de-escalation that includes antifungal agents are important elements
of AFS programs, along with curtailing unnecessary prolongation of antifungal courses.
Specific training and feedback of all stakeholders is warranted, as in the case of antibiotic
stewardship strategies.
Prior or continual exposure to broad-spectrum antimicrobial therapy, a well-established
risk factor for C. auris acquisition, has a long-lasting effect on skin microbiota [125]. Interest-
ingly, C. auris-positive individuals were shown to harbor different commensal bacteria and
fungi communities [126], although it should be clarified whether dysbiosis contributes to C.
auris colonization or C. auris colonization promotes the alteration of microbial communities.
Therefore, the conduction of studies investigating the intersection of skin microbiota and C.
auris skin colonization is needed.

6. Conclusions
C. auris is considered an emerging health threat with reports of both sporadic cases
and outbreaks in healthcare facilities from diverse countries across six continents. It is
implicated in a variety of invasive, potentially life-threatening infections and the patients
most commonly affected include the elderly with debilitating comorbidities, catheters or
indwelling medical devices, and prolonged ICU stay that have been exposed to broad-
Pathogens 2023, 12, 1444 9 of 14

spectrum antimicrobial agents, administered parenteral nutrition or recently undergone

invasive medical procedures. Faulty and delayed detection by conventional diagnostic
tools, high inter-patient transmissibility, intrinsic or acquired resistance to one or more
antifungal drugs, and limited susceptibility to commonly used disinfectants are the main
reasons hindering the adequate management of C. auris outbreaks. Hence, establishing a
multidisciplinary model and bundling of practices for controlling and preventing its spread
are of utmost importance.

Author Contributions: Conceptualization, V.R. and G.P.; writing—original draft preparation, V.R.;
writing—review and editing, V.R., K.I. and G.P.; supervision, G.P. All authors have read and agreed
to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare no conflict of interest.

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