Next Article in Journal
Central Carbon Metabolism in Candida albicans Biofilms Is Altered by Dimethyl Sulfoxide
Next Article in Special Issue
A Mini-Review of In Vitro Data for Candida Species, Including C. auris, Isolated during Clinical Trials of Three New Antifungals: Fosmanogepix, Ibrexafungerp, and Rezafungin
Previous Article in Journal
Chronic Pulmonary Aspergillosis after Surgical Treatment for Non-Small Cell Lung Cancer—An Analysis of Risk Factors and Clinical Outcomes
Previous Article in Special Issue
Virulence Traits and Azole Resistance in Korean Candida auris Isolates
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Systematic Review

Potential Environmental Reservoirs of Candida auris: A Systematic Review

by
Isabel Silva
1,
Isabel M. Miranda
2 and
Sofia Costa-de-Oliveira
3,4,*
1
Faculty of Medicine, University of Porto, 4200-319 Porto, Portugal
2
Cardiovascular R&D Centre UnIC@RISE, Department of Surgery and Physiology, Faculty of Medicine, University of Porto, 4200-319 Porto, Portugal
3
Division of Microbiology, Department of Pathology, Faculty of Medicine, University of Porto, 4200-319 Porto, Portugal
4
Center for Health Technology and Services Research—CINTESIS@RISE, Faculty of Medicine, University of Porto, 4200-319 Porto, Portugal
*
Author to whom correspondence should be addressed.
J. Fungi 2024, 10(5), 336; https://doi.org/10.3390/jof10050336
Submission received: 1 April 2024 / Revised: 28 April 2024 / Accepted: 4 May 2024 / Published: 8 May 2024
(This article belongs to the Collection Invasive Candidiasis)

Abstract

:
Candida auris, a multidrug-resistant yeast, poses significant challenges in healthcare settings worldwide. Understanding its environmental reservoirs is crucial for effective control strategies. This systematic review aimed to review the literature regarding the natural and environmental reservoirs of C. auris. Following the PRISMA guidelines, published studies until October 2023 were searched in three databases: PubMed, Web of Science, and Scopus. Information regarding the origin, sampling procedure, methods for laboratory identification, and antifungal susceptibility was collected and analyzed. Thirty-three studies published between 2016 and 2023 in 15 countries were included and analyzed. C. auris was detected in various environments, including wastewater treatment plants, hospital patient care surfaces, and natural environments such as salt marshes, sand, seawater, estuaries, apples, and dogs. Detection methods varied, with molecular techniques often used alongside culture. Susceptibility profiles revealed resistance patterns. Phylogenetic studies highlight the potential of environmental strains to influence clinical infections. Despite methodological heterogeneity, this review provides valuable information for future research and highlights the need for standardized sampling and detection protocols to mitigate C. auris transmission.

Graphical Abstract

1. Introduction

Candida auris is a multidrug-resistant yeast first identified in the ear of a Japanese patient in 2009 [1]. A member of the Candida/Clavispora clade, closely related to Candida lusitaniae and Candida haemulonii, it has emerged in recent years as a cause for healthcare-related infections, complicating treatment protocols and increasing patient morbidity and mortality rates [2]. It has been identified in more than 40 countries, with outbreaks reported on multiple continents, with notable impacts in countries such as the United States, India, South Africa, and several European nations, including the United Kingdom Spain, France, and Italy (Figure 1) [3,4]. In 2022, the World Health Organization designated this fungal pathogen as a priority due to its rapid transmission in healthcare settings and high mortality rate [5,6].
C. auris is implicated in a range of serious conditions including bloodstream and urinary tract infections, otitis, post-surgical complications, skin abscesses often related to catheter use, myocarditis, meningitis, osteomyelitis, and various wound infections [19]. However, it can also colonize noninvasive body sites, like skin, without causing active infection. Invasive infections caused by C. auris pose a significant mortality risk in hospital settings, with death rates varying between 30% and 60% [20]. Certain factors increase the likelihood of C. auris infection, including male gender, premature birth history in infants, underlying health conditions such as diabetes, kidney or hearing impairments, physical injuries, previous central venous catheter insertions, and extensive use of broad-spectrum antibiotics [21].
Phylogenetic studies obtained by whole-genome sequencing (WGS) techniques have identified four distinct clades, namely, clades I, II, III, and IV (South Asia, East Asia, Africa, and South America, respectively) [22]. A fifth and a sixth clade, separated from the others by more than 36,000 single-nucleotide polymorphisms (SNPs), were confirmed to have appeared in patients from Iran and Singapore, respectively [23,24].
C. auris has become a significant concern due to its multidrug-resistant nature. Of C. auris isolates, 44.29% are resistant to fluconazole, followed by 15.46% to amphotericin B, 12.67% to voriconazole, 3.48% to caspofungin, and 1.95% to flucytosine [25]. In the United States, the prevalence of resistance among these fungal pathogens has been observed to be 90% against fluconazole, 30% against amphotericin B, and 5% against echinocandins, with a tendency to rise over time [26,27]. Although resistance rates vary depending on the clade, country, and healthcare setting, C. auris has shown resistance to fluconazole, amphotericin B, and echinocandins [6,28].
Identifying C. auris isolates through conventional laboratory methods has proven to be challenging, often leading to its misidentification [4]. As a result, matrix-assisted laser desorption/ionization–time of flight (MALDI-TOF) and molecular identification via sequencing the ITS and/or D1/D2 DNA sequence seem to be good options for its identification [25].
C. auris thrives in environments with elevated salinity and high temperature, ideally between 37 °C and 40 °C [29,30]. Yeasts typically possess a keen sensitivity to ambient temperatures, often displaying a diminished ability to survive at the elevated temperatures in the human body [31]. The rise in global temperatures may have caused certain species, such as C. auris, to evolve and thrive in warmer climates [32]. This evolutionary development has allowed for C. auris to overcome the human body’s innate temperature defenses, thereby enabling colonization and leading to subsequent infection.
C. auris can exhibit the capacity to persist for extended periods on various surfaces due to its ability to form biofilms, like glass, fabric, plastic, wood, and steel, tending to flourish in moist environments [33]. Consequently, these materials pose a potential source of infection within hospital settings, emphasizing the importance of thorough disinfection protocols to interrupt the transmission of C. auris [4]. The significance of microbiological sampling of healthcare environment surfaces is emphasized in the literature, as it aids in understanding contamination levels and informs cleaning protocols. General recommendations have been proposed for designing routine protocols for surface sampling in healthcare environments [34].
The aim of this paper was to undertake a thorough systematic review to clarify the environmental reservoirs of C. auris in natural and hospital settings. Recognizing the environmental reservoirs of C. auris is a crucial aspect of comprehending pathogen transmission and will contribute to understanding the dynamics of the disease, leading to the development of more effective control strategies.

2. Materials and Methods

This systematic review was carried out in strict accordance with the Cochrane Handbook for Systematic Reviews of Interventions [35] and the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [36] checklist of the review was followed (Supplementary Material—S1).

2.1. Data Source and Search Strategy

The electronic bibliographic databases of PubMed, Scopus, and Web of Science were searched using a combination of MeSH terms and keywords: (“Candida auris” OR “C. auris”) AND (“environment” OR “environmental” OR “globalization” OR vector* OR “travel” OR “imported” OR “ecological” OR reservoir* OR “One Health” OR Ecosystem* OR “Climate Change” OR “Global warming” OR Niche*)
Studies were selected and screened until October 2023. The search included all publication types except reviews or systematic reviews, and no language restrictions were applied.

2.2. Eligibility Criteria

Studies were included in this review if they met the following criteria: (1) C. auris detected and isolated from natural environments or animals; (2) studies identified the presence of C. auris in urban environments outside of a hospital setting; (3) studies reporting the presence of C. auris from hospital environmental surfaces or materials. The exclusion criteria were (1) studies regarding hospital disinfection procedures or surface decontamination efficacy, (2) studies not addressing the detection of C. auris, and (3) systematic reviews, editorials, and grey literature.

2.3. Data Extraction and Synthesis

A total of 929 references were obtained in the three databases. The extracted studies were uploaded to EndNote and Rayyan software [37] for duplicate removal, quality assessment, and further selection. In a blinded, standardized manner, a screening of the title, abstract, and full text was performed and guided based on inclusion and exclusion criteria by two independent reviewers (IS and SCO). Thirty-three studies were included in the systematic review (Figure 2).
A protocol was defined to synthesize the data collected from the selected studies uniformly and consistently. Data such as year of publication, country, study time frame, sample type, collecting procedure, laboratory methods for strain identification, clade determination, and susceptibility profile were extracted from the included publications. IS and SCO extracted the above information independently.

2.4. Risk of Bias (ROB) Assessment

To evaluate the risk of bias in the studies included in this review, the National Institute of Health (NIH) Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies was used [38]. A 3-point scale was used to grade the potential source of bias as good, fair, or poor. No studies were excluded based on quality. ROB assessment was performed independently by SCO and IMM.

3. Results

Table 1 and Table 2 show the characteristics of the 33 studies included in this analysis, spanning the publication years from 2016 to 2023 and conducted within a sampling timeframe extending from 2013 to 2022. These studies were carried out across 15 countries, namely, the United Kingdom, the United States of America, Qatar, South Africa, Colombia, Spain, Kuwait, Oman, India, France, Hong Kong, Greece, China, the Netherlands, and the Republic of Korea.
Among the 33 studies included, 4 centered on natural environments, 3 examined urban non-hospital environments, 1 centered on both (Table 1), and 25 focused on isolation of C. auris within hospital settings (Table 2).

3.1. Potential Natural Environmental Reservoirs

Regarding the five studies that investigated C. auris in natural environments, four of these articles employed a similar approach for strain identification, beginning with its isolation through culture techniques and subsequent confirmation through genomic amplification [39,40,41,42]. The only study that deviated from this method attempted to identify previously misidentified C. auris strains from the Sequence Read Archive at the National Center for Biotechnology Information [43]. Generally, the collected samples were inoculated in Sabouraud Dextrose Agar, CHROMagar Candida, Yeast nitrogen, and Malt Extract agar at 24–42 °C.
C. auris was detected in diverse environmental substrates, including ears and skin from dogs [39], stored apples purchased from vendors [40], soil from a salt marsh, beach sand, and seawater in India [41], as well as water from estuaries in Colombia [42]. Genomic amplification alone enabled the identification of C. auris in unique contexts, such as on the skin of Lissotriron vulgaris and Triturus cristatus in a natural reserve in the UK, in the ear of a dog with otitis in Spain, and in airborne dust from Kuwait [43]. Among the reviewed studies, only the three conducted in India identified the clade of C. auris (South Asian clade) [39,40,41].

3.2. Potential Urban Non-Hospital Environmental Reservoirs

Out of the 33 articles included, only 4 reported the identification of C. auris in urban non-hospital environments [43,44,45,46]. Two of these studies solely relied on genomic amplification for identification, without performing culture [43,44]. The remaining two studies combined culture and PCR techniques [45,46]. They utilized CHROMagar medium at 42 °C, Sabouraud Dextrose Agar at 24 °C, and Malt Extract Agar at 24 °C for culture, successfully identifying C. auris in wastewater from various sources in Florida [45] and swimming pools in the Netherlands [46]. The other two studies identified C. auris solely through PCR, detecting its presence in activated sludge and membrane biofilm from a wastewater treatment plant in the Republic of Korea [43] and in pelleted solids from wastewater in the state of South Nevada, USA [44].
Table 1. Potential non-hospital environmental reservoirs of C. auris.
Table 1. Potential non-hospital environmental reservoirs of C. auris.
First Author and YearCountryTime of the YearPositive Type of SamplesHarvesting MethodCulture and TemperatureGenomic AmplificationProteomicClade
Yadav, 2022 [40]IndiaMarch–April 2020; June–July 2021Stored apples (epicarp)Sterile Swabs SweptSabouraud dextrose with chloramphenicol and gentamicin, CHROMagar Candida, and Yeast nitrogen broth at 37 °CIllumina Hiseq 4000MALDI-TOF MS I
Epicard homogenizes in saline
Yadav, 2023 [39]India-Ear and skin of dogsSwab samplesYeast nitrogen broth with 10% NaCl at 37 °C for 4 daysIllumina HiSeq 4000MALDI-TOF MS I
Arora, 2021 [41]IndiaFebruary–March 2020Salt march soil and sandy beach sediment2 g sediment suspended in 8 mL of 0.85% NaClSabouraud dextrose agar plates with chloramphenicol and gentamicin at 28 °C up to 7 daysIllumina Hiseq 4000MALDI-TOF MSI
Seawater from the sandy beachfiltered with 0.45 um filters in 50 mL sterile bottles
Membrane biofilm
Escandón, 2022 [42]Colombia2018Water from Estuaries100 mL of water from a depth of 30 cmSalt Sabouraud Dextrose selective broth at 40 °C for 48 hPCR MALDI-TOF MS-
Irinyi, 2022 [43]UK2019Skin of Lissotriron vulgaris and Triturus cristatusSterile Swabs-Illumina Miseq--
Spain2019Ear of dog--PCR--
Kuwait2017–2018Airborne dustDust-laden filter paper from a high-volume air sampler-Illumina HiSeq 2500--
Republic of Korea2016Activated sludge50 mL of a sterilized conical tube-Illumina MiSeq--
Barber, 2023 [44]USA June–September 2022Pelleted wastewater solids--qPCR --
Babler, 2023 [45]USA2021–2022Wastewater from the central district plantSterile HDPE bottle containing 0.1 g sodium thiosulfateCHROMagar
at 42 °C for 48 h
qPCR--
Wastewater from sewer cleanout from the hospital
Ekowati, 2018 [46]Netherlands-Water samples from two poolsPlastic containersSabouraud Dextrose Agar and Malt Extract Agar at 24 °C for 7 daysPCR--
Polymerase chain reaction (PCR), quantitative polymerase chain reaction (qPCR).
Table 2. Sites of detection of C. auris in hospital environment.
Table 2. Sites of detection of C. auris in hospital environment.
First Author and YearCountryTime of the YearSample Type Sampling MethodCulture and DetectionPositive Samples/Total Samples CollectedMolecular IdentificationClade and Clinical IdenticalConclusion
Katsiari, 2023 [13]GreeceOctober 2020–January 2022 Environmental screening process -Sabouraud Dextrose Agar at 35 °C and 42 °C3/NAPCR
MALDI-TOF
Clade I and identical sequences to clinical samplesOnly beds and a side table near infected patients were positive.
Tian, 2021 [47]China March 2018Environmental screening process -Yeast Extract–Peptone–Dextrose Medium at 37 °C for 16 h1/1Illumina NovaSeq platform
MALDI-TOF
Clade III clade and clinically relatedOnly the bedrails of a patient infected were positive.
Didik, 2023 [48]Hong KongSeptember–October 2022Frequently touched items of ward communal
area returned air grilles and high-level supply air grilles.
Flexible pre-moistened sterile poly wipe
sponge swabs
Sabouraud dextrose broth with 10% NaCl, chloramphenicol and
colistin for 7 days at 40°
32/249Illumina iSeq or MiSeq
MALDI-TOF
Clade I29 positive samples were from frequently touched items and 3 from returned air grilles and supply air grilles.
Alanio, 2022 [49]FranceJanuary 2021Investigation of the environment after bio-cleaning (sodium hypochlorite and sporicide)Sterile pre-moistened cotton swabs unloaded in water.Sabouraud Dextrose Agar0/NAqPCR Clade IOnly the mattresses, bed fences, and trolleys of infected patients were positive.
qPCR NA/NA
Yadav, 2021 [50]IndiaDecember 2019–May 2020Near each patient’s bed (bed railing, bed sheet, pillow, bedside
trolly, floor, and air conditioner air wings), medical equipment (thermometer, B.P. cuffs, ECG clip and sucker, oxygen mask, and nebulizer), and portable devices (mobile, wheelchair, and intravenous pole).
Premoistened swabs Sabouraud Dextrose Agar containing chloramphenicol and gentamicin
at 37 °C for 48–72 h
15/148Illumina Hiseq 4000
MALDI-TOF
Clade I
and
SNP difference
Between 1–160 among clinical and environmental isolates.
Recovered from near-patient sites (floor, bed railing, bedside trollies, pillow, and bed sheet). It was also recovered from air conditioner air wings, a mobile phone, and two medical equipment: an oxygen mask and
intravenous pole.
Yeast nitrogen enrichment
broth containing 10% NaCl and 2% mannitol as a carbon source, and vortexed
and incubated at 37 °C for 72–96 h
Umamheshwari, 2021 [51]IndiaDecember 2018–March 2019Beds, bed rails, bedside tables/cardiac
tables, and nursing cart.
Sterile pre-moistened in saline cotton swabs Sabouraud Dextrose Agar plates for 7 days at 37 °C2/46PCR
VITEK 2
MALDI TOF MS
Clade I and
>90% similarity between clinical and environmental isolates
Only the bed railings around an infected patient were positive
Taori, 2019 [52]UKJuly 2016–February 2017High touch point areasSterile pre-moistened in saline cotton swabsBrilliance Candida agar for 48 h at 37 °C2/48PCR
VITEK 2
MALDI TOF MS
Clade IOnly the bed railings and dining trolleys around an infected patient were positive
Biswal, 2017 [53]IndiaJanuary–March 2017Environmental sampling of surfaces of objects or fomites in ICUCotton swabs pre-moistened in salineSabouraud dextrose agar for 48 h at 37 °C24/304Sequencing of
ITS and D1/D2 regions of ribosomal DNA
MALDI TOF
-Recovered from near-patient sites (beds) and medical equipment: expiratory end of the ventilator, ECG leads, cuffs blood pressure, and temperature probes.
Ruiz-Gaitan, 2019 [54]Spain2016–2018Patients’ environment (bed rails, table, infusion pumps, keyboards, and walls) after cleaning, faucets, benches, and reusable medical devices. Cotton gauzes soaked in saline Sabouraud dextrose broth with chloramphenicol at 35 °C for 72 h61/738Sequencing ITS
VITEK MS IVD
-Isolated from Blood pressure cuffs, patient tables, keyboards, infusion pumps
Adams, 2018 [55]USA (New York)2013–2017Environmental samples were collected from rooms belonging to infected patients on near-patient surfaces, equipment, and other objects. They were also collected from objects outside these rooms. Sponge sticks with 45 mL of phosphate-buffered saline with 0.02% Tween 80Sponge suspension on different agar media or Sponge suspension in 5 mL of SDB-AS broth at 40 °C for 2 weeks62/781Real-time PCR
MALDI-TOF
Clade IIsolated from near-patient surfaces and other surfaces inside patients’ rooms, like floors, curtains, and others. It was also isolated from equipment outside these rooms, like vital sign machines, thermometers, and others.
Real-time PCR19/781 (culture negative)
Al Maani, 2019 [56]OmanOctober 2018Collected from high touch areas and re-useable devicesSterile swabs pre-moistened in sterile salineSabouraud dextrose agar and incubated at 37 °C for 48 h.2/140PCR
MALDI-TOF MS
Clade I Isolated from the ventilator end and trolley belonging to the patient’s rooms.
Alfouzan, 2020 [57]KuwaitJanuary 2018–2019Collected from infected patients’ rooms. Swab samplesSabouraud dextrose agar with gentamicin for 24–48 h at 37 °C7/261PCR
VITEK 2
MALDI TOF MS
Clade I and genetically identical to clinical strainsIsolated from the Bedrail, bedside drawer, toilet flush handle, toilet faucet handle, and wall
Kumar, 2019 [58] USAApril–June 2017Patients’ room objects <3 feet from the patient, >3 feet away, and bathrooms. As well as portable medical equipment. Sponge sticks pre-moistened with neutralizing bufferSabouraud dextrose agar and incubated at 37 °C for 96 h.8/204MALDI-TOF-Isolated from the Bedrail, bedside table, call button, and sink drain
Ruiz-Gaitán, 2018 [59]SpainApril 2016–January 2017Environmental surveillance on various surfaces and objects. Cotton gauze moistened with salineSabouraud dextrose agar with chloramphenicol
For 72 h at 35 °C
-PCR
Vitek MS Ruo
-Isolated from Beds, tables, floors, walls, keyboards blood pressure cuffs, and hemodialysis drains
Escandón, 2019 [60]ColombiaFebruary 2015–August 2016Samples were collected from surfaces and objects belonging to four zones in patients’ rooms: zone 1 being near bed, zone 2 being infrequent patient contact, zone 3 with almost no contact, and zone 4 being bathrooms adjects to patients’ rooms. 3M Sponge sticks and EnviroMax Plus swabsSalt Sabouraud dextrose broth37/322Illumina Hiseq 2500
MALDI-TOF
Genetically identical to clinical strainsFrom zone 1 it was isolated from bedrails, cellular phones, hand controllers, and floors. From zone 2, chairs, bed trays, and medical equipment. From zone 3, closets, door handles, and alcohol gel dispensers, and zone 4 sink basins, bedpans, and mop buckets.
Eyre, 2018 [61]UKNovember 2016–April 2017Environmental screeningBacterial swabs in a liquid transport medium (Sigma Transwab) and sponges to sample larger surface areas (Polywipe) and Sabouraud dextrose agar contact
plates
Sabouraud
Dextrose Agar with chloramphenicol at 37 °C
NA/128Illumina miseq
MALDI-TOF
Clade III and clinical and environmental samples were closely related. Isolated from a pulse oximeter, temperature probes, and patient mobile hoist.
Rhodes, 2018 [62]UKApril 2015–November 2016Environmental screening of a room of a colonized patient.-Sabouraud
Dextrose Agar at 35 °C for 18–48 h
2/2Illumina hiseq 2500
MALDI-TOF
Clade IIsolated from Beds and trolleys
Lesho, 2018 [63]USA-3/132
(outside)
Sponge sticks and premoistened rayon-tipped swabsSabouraud
Dextrose Agar with gentamycin and chloramphenicol
5 days
3/ 132WGS
MALDI-TOF
Clade I
and genetically identical to clinical strains
Isolated from reclining chairs inside the patient room and sink outside the room.
Naicker, 2021 [64]South Africa2017Hight touch surfaces and objects and other surfaces in patient care are SwabSabourad agar 10/NAWGS
MALDI-TOF
Clade III and there were a maximum of 27 SNP differences between environmental to clinical strains.Isolated from handwashing basin, bed linen, bed rails, window-sill, a curtain, drying rack, and the floor.
Pacilli, 2020 [65]USAMay 2016–December 2018Hight touch surfaces in patient care environments, multiuse patient care items, and mobile equipment. 3M Sponge sticks with neutralizing buffer,
homogenized in 40 mL of phosphate-buffered saline with 0.02% Tween 80
CHROMagar Candida plates for 7 days73/191MALDI-TOF-Isolated from glucometers, temperature probes, mobile ultrasounds, pulse-oximeters, blood pressure cuffs, stethoscopes, over-bed tables, bedside chairs, nursing carts, doorknobs, bedrails, and windowsills
Salah, 2021 [66]QatarApril 2018–November 2020Environmental screening-CHROMagar Candida for 5 days at 42 °C-Illumina NextSeq 550 or Illumina Miseq
MALDI-TOF
Clade I and genetically identical to clinical isolatesIsolated from a bedside table, bed, couch, and cabinet inside patients’ rooms.
Schelenz, 2016 [67]UKApril 2015–July 2016Environmental screening of the area surrounding colonized patients-Sabouraud
Dextrose Agar plates
-MALDI-TOF-Isolated from the Floor around bedsites, trollies, radiators, windowsills, equipment monitors, keypads
Sexton, 2021 [68]USA (Chicago)October 2018Environmental screening of patients’ rooms windowsills, doorknobs, and handrails.3M Sponge sticks with neutralizing buffer, homogenized in 40 mL of phosphate-buffered saline with 0.02% Tween 80CHROMagar Candida plates at 40 °C for 72 h50/100qPCR
MALDI-TOF
-Isolated from
window, indoor knob, outdoor knob, left handrail and right handrail
qPCR 70/100
Zhu, 2020 [69]USA2016–2018Environmental sampling of porous and nonporous surfaces.3M sponge sticks, vortexed with 1 mL modified liquid amies mediumSabouraud
Dextrose Agar with chloramphenicol, gentamicin, penicillin and streptomycin,
and
Sabouraud ulcitol agar containing the above antibacterial with 10 salt
109/3672PCR
MALDI-TOF
Clade I Isolated from near-patient environments (floors, beds, walls, etc.), from mobile medical equipment (lifter, blood pressure cuff, etc.), and outside rooms (computer keyboard). Degrees of colonization were significantly higher on nonporous than porous surfaces.
PCR434/3672
Patterson, 2021 [70]UK--3M Sponge sticks with neutralizing buffer
----A patient’s bed space and staff lanyards were infected.
Whole-genome sequencing (WGS), polymerase chain reaction (PCR), quantitative polymerase chain reaction (qPCR).

3.3. Potential Hospital Environmental Reservoirs

The other 25 papers focused on hospital environmental sources of C. auris, mostly during outbreaks of this fungal infection. As shown in Table 2, the studies employed various techniques for obtaining the samples. Sixteen studies used swabs [48,49,50,51,52,53,55,56,57,58,60,63,65,68,69,70], while two used gauze [54,59], and one used both direct contact plates and swab techniques [61]. Six studies did not report the methods of sample collection [13,47,62,64,66,67]. Among the studies that employed swabs, only 12 reported the material, of which 9 were sponges [48,55,58,60,63,65,68,69,70] and 3 were cotton [49,51,53]. All of the studies performed culture and subsequent confirmation through genomic amplification. The collected samples were inoculated in some Yeast Extract–Peptone–DextroseMedium, Yeast nitrogen enrichment, Sabouraud Dextrose agar or broth, Brilliance Candida agar, CHROMagar Candida, and Sabouraud ulcitol agar at 35–42 ºC. Only one study did not have culture-positive samples, having only identified C. auris by qPCR [49]. All of the studies included revealed that C. auris was frequently detected on surfaces near the patient’s bed area or in high-touch objects. Mobile medical devices, such as thermometers and stethoscopes, were contaminated with C. auris in 10 studies [48,50,53,54,55,59,60,61,65,69]. Additionally, 13 studies reported the presence of this yeast in areas outside the patient’s rooms, such as keyboards, sinks, and air vents [48,50,53,54,55,57,58,59,60,64,65,69,70]. The clade of C. auris was determined by WGS and analyzed by fifteen studies, of which twelve studies found the South Asian clade [13,48,49,50,51,52,55,56,57,62,63,66] and three studies detected the African clade [47,61,64].
Eleven studies tried to understand the relationship between clinical and environmental samples [13,47,48,50,51,57,60,61,63,64,66]. Five studies proved that they were similar [13,57,60,63,66], four that there was a close relationship between them [47,48,51,61], and two mentioned that there was a difference of between 1 and 160 SNPs between clinical and environmental samples [50,64].

3.4. Susceptibility of Natural and Hospital Environmental Samples

Table 3 presents the susceptibility profiles to various antifungal agents commonly used and gene mutations responsible for reduced susceptibility in all studies included in this analysis. Among the studies included, eleven tested the susceptibility profiles for antifungals, with four conducted in natural environments [39,40,41,42] and seven in hospital settings [47,50,51,56,57,60,69]. Of these, nine studies utilized the Clinical & Laboratory Standards Institute broth microdilution method to estimate minimum inhibitory concentrations [39,40,41,42,50,51,56,69], one employed the MICRONAUT-AM broth microdilution procedure [57], one used Sensititre YeastOne plates [47], and one did not specify the method used [60]. Although there are currently no established susceptibility breakpoints specific for C. auris, and there is still no clear correlation between microbiologic breakpoints and clinical outcomes, the CDC has proposed tentative minimal inhibitory concentration (MIC) breakpoints for fluconazole (≥32 mg/L), amphotericin B (≥2.0 mg/L), and anidulafungin (≥4 mg/L) based on closely related Candida species and expert opinion [71].
The susceptibility profile of the strains isolated from natural environmental samples to antifungal drugs was tested in four studies. Arora and colleagues found that sand/beach samples had high MIC values for fluconazole (MIC > 32 mg/L) and amphotericin B (>2 mg/L), but soil samples from the salt marsh had low MIC values for both drugs [41]. Salt marsh samples also grew slower and preferred lower temperatures than the others. Apple samples stored in a warehouse showed low MIC values for amphotericin B (<2 mg/L), but fluconazole MIC values varied [40]. Water samples from Colombian estuaries had low MIC values for fluconazole and amphotericin B [42]. Samples from dog’s ears and skin showed high MIC values for fluconazole and low for amphotericin [39]. All samples showed low MICs to anidulafungin across all studies.
Three studies investigated genetic mutations linked to antifungal resistance [39,40,41]. These studies identified mutations in the CDR1, ERG11, and TAC1B genes. Specifically, the CDR1 gene revealed V704L and E709D mutations [40], the TAC1B gene showed an A640V mutation [39], and the ERG11 gene exhibited K143R [39,40] and Y132F mutations [40,41].
Seven studies tested the susceptibility of hospital environmental samples and found that all samples tested showed low MIC values to anidulafungin [47,50,51,56,57,60,63,69]. Except for Al Maani et al.’s study [56], all the other articles had samples that showed high MIC values for fluconazole (MIC ≥ 32 mg/L). Out of these, only one contained samples with elevated MIC values exclusively [47]. Only one study included samples that exclusively exhibited low MIC values for amphotericin B [47]. Five studies reported samples with high MIC values of amphotericin B (MIC ≥ 2.0 mg/L) [50,51,56,60,69]. In one study, MIC values for fluconazole and amphotericin B were not provided; instead, they were classified as resistant and susceptible, respectively [57]. Five studies examined genetic mutations associated with resistance to certain antifungals [47,50,51,57,63]. Mutations in the ERG11 gene were identified, particularly VF125AL (I74L) [47], Y132F [50,51,57], and K143R [63].

3.5. Risk of Bias—Quality Assessment

Due to the heterogenicity of the studies regarding natural environments, quality assessment was performed only in hospital environmental studies. All analyzed studies were classified as “Good”, being methodologically robust, with clear objectives, thorough methods for sample collection and analysis, and significant contributions to understanding the molecular epidemiology and drug resistance (Supplementary Material—S2).

4. Discussion

The present systematic review, conducted per PRISMA guidelines, provides an update on potential environmental reservoirs of C. auris. This is necessary to understand the disease’s epidemiology and important niches, which in turn helps with its prevention and management.

4.1. Sampling and Detection

Our study’s findings highlight the differences concerning environmental sampling procedures found both within and across nations. Few studies have compared the most efficient method for environmental sampling recovery for Candida auris. One study found that culture recovery is best with swabs instead of sponges, with 8.4% and >0.1% in culture recovery, respectively [72]. Additionally, using a polyurethane sponge seems to be better for C. auris recovery than cellulose sponges. Another article has proven that inoculating C. auris samples in Salt Sabouraud Enrichment Broth is better for C. auris isolation than directly plating it in CHROMagar [30]. The enrichment broth procedure inhibits the growth of another organism by creating a high-temperature and high-salinity environment, so it should only be used when trying to isolate C. auris specifically. Most studies in this review used both culture and molecular/proteomic techniques to detect and identify C. auris in the environment. One of the most effective identification methods used for detecting C. auris in cultured isolates is MALDI-TOF MS, which reduces the processing period to less than three hours compared to traditional and DNA-based methods [73]. Researchers can use the Bruker and Vitek MALDI-TOF MS systems to correctly identify C. auris [74]. Vitek 2 technology, with software version 8.01, may misidentify C. auris as C. duobushaemulonii [74]. Therefore, additional testing is necessary to rule out C. auris when using this technology. A reliable way to distinguish C. auris from other yeast species is to sequence the rDNA regions (internal transcribed spacer and D1/D2 region of large subunit) [75]. PCR/real-time PCR assays are a dependable method to rule out negative samples when additional analysis is required for further investigation [76].

4.2. Potential Natural Environmental Reservoirs

As shown in Table 1, C. auris was isolated from a wide range of natural habitats, indicating a potential reservoir of C. auris in the environment and/or intermediate host. According to reports from two countries located on separate continents at the time of this analysis, aquatic environments appear to be a source of C. auris. Furthermore, amphibians known to live in aquatic environments have been shown to contain this yeast’s DNA. These findings imply that numerous hosts can become contaminated by the aquatic environment and may play a role in C. auris’ persistence in this habitat, like other yeasts.
This analysis reports the occurrence of C. auris infections in animals, which is consistent with the literature documenting similar cases caused by other Candida species [77]. In humans, the majority of Candida infections arise from colonizing strains rather than through transmission, rendering the likelihood of zoonotic disease minimal [78]. Even with the diminished likelihood of zoonotic transmission, animals could still play a role in disseminating C. auris within the environment, which may subsequently result in human colonization.
Researchers have found C. auris on the surfaces of apples bought in local food markets in India, but not on freshly harvested apples from orchards [79]. This indicates that contamination with C. auris may occur during transportation or storage. Identifying the stage at which contamination occurs may be important in understanding its impact and risk to human contamination and subsequent infection.
Finding C. auris in aquatic environments supports the hypothesis that it may have natural reservoirs outside human-made environments. The presence of C. auris in these settings suggests that it might have adapted to survive or even thrive in aquatic conditions. Notably, isolation of the drug-susceptible C. auris strain from aquatic habitat with no known human activity probably indicates that C. auris existed as a drug-susceptible pathogen and developed multidrug-resistant traits after its adaptation in humans [41].

4.3. Potential Urban Non-Hospital Environmental Reservoirs

C. auris, known to colonize the skin and found in human excrement, has the potential to infiltrate plumbing systems via skin shedding and fecal disposal, eventually arriving at wastewater treatment facilities [80]. It is, therefore, unsurprising that it has been identified in such facilities and sewage systems across multiple countries. This situation, however, presents certain challenges. Firstly, sewage discharge can facilitate the propagation of microbes, including C. auris, into marine ecosystems due to the coastal and estuarine outflows of wastewater treatment plants and sewer overflow [81,82]. Secondly, in the face of water shortages, the prospect of utilizing wastewater effluents for irrigation and drinking water production is being explored [83]. This could potentially amplify the spread of microbiological agent into the environment, thus requiring careful management strategies [84].
One study reported finding C. auris in air dust samples from Kuwait. Previous research showed that airborne microorganisms can travel far and settle on human skin, affecting human health and causing diseases [85,86]. C. auris was also found in swimming pools in Netherlands; it is known that recreational swimming pools can also pose the threat of water-borne yeast infection, particularly in immunocompromised patients [87].

4.4. Potential Hospital Environmental Reservoirs

The role of hospital surfaces in the transmission of healthcare-associated infection has been highlighted by several authors [88]. Environmental surfaces that are close to or frequently touched by colonized patients are more likely to harbor these organisms [89]. Nevertheless, we should be aware that most of the studies included were conducted in the context of outbreak investigations, and the level of contamination in non-outbreak situations remains uncertain. While it is true that five studies found that the environmental samples were identical to the clinical samples, it is important to note that they did not establish a correlation between this contamination of the environment and the transmission of C. auris to other patients. Only one study explicitly correlated the contamination of the environment (temperature probes) as a source of transmission of C. auris, leading to an outbreak [61]. Therefore, it is essential to apply strict hygiene measures and disinfect the environment using an Environmental Protection Agency-registered hospital-grade disinfectant proven effective against C. auris or disinfectants known to be effective against Clostridium difficile spores to avoid transmission [90,91,92].
This yeast was also detected in areas not within reach by humans, such as air vents and very high curtains. Like Acinetobacter and Staphylococcus aureus, C. auris may disperse through the air by shedding skin flakes that contain the fungus and are carried by air currents [93,94]. It was also found outside patients’ rooms, and on computer keyboards and medical carts, which may suggest that the medical staff are not sanitizing their hands properly [89,90].

4.5. Susceptibility and Phylogeny

C. auris poses a significant challenge within the domain of mycotic diseases due to its resistance to multiple drugs and complicating therapeutic approaches [20]. Echinocandin treatment is considered the first-line option [95]. However, in cases of echinocandin resistance, treating C. auris infections often involves combination antifungal therapy. Combining echinocandins with other antifungal agents such as triazoles or polyenes may enhance efficacy, broaden the antifungal spectrum, and reduce the potential for resistance development [20]. To ensure effective control of C. auris infections, diligent patient monitoring must be observed for signs of clinical recovery during antifungal therapy.
Of the included studies in this review, gene sequencing for various isolates showed mutations in ERG11 and TAC1B, known to contribute to reduced azole susceptibility [96,97], and showed mutations in the CDR1 gene: these changes are known to contribute to antifungal resistance [98]. In addition to the mutations identified in the included studies, other relevant ones are highlighted in the literature. Mutations in the ERG3 and ERG5 genes have been found to impact susceptibility to amphotericin B, while mutations in the FKS1 gene affect susceptibility to echinocandins [20].
Clades I, III, and IV are associated with outbreaks of invasive and multidrug-resistant infections [99]. Clade II frequently exhibits susceptibility to all antifungal medications, with the majority of instances presenting as ear infections. To date, there have been no associations with outbreaks. Clade II strains exhibit a different karyotype, with large sub-telomeric deletions and rearrangements, and are less commonly linked to invasive infections. Clade V and VI isolates have not been extensively studied, and their clinical implications remain to be fully understood [23,24].

4.6. Strategic Surveillance Approach

Based on our findings, it is evident that C. auris frequently contaminate areas surrounding the patient’s bed. Therefore, to assess effective disinfection, priority should be given to these zones, with particular attention to bedside tables and hand-rails. Additionally, mobile medical devices should be included in routine investigations due to their potential for cross-contamination between patients [61]. Ensuring proper disinfection protocols for these devices with proper hand hygiene measures is essential in minimizing the risk of transmission of pathogens, including C. auris [100].
In terms of environmental sampling for C. auris, an effective method would involve swabbing surfaces [72] and inoculating them in Salt Sabouraud Enrichment Broth [30], followed by MALDI-TOF MS or PCR analysis [76]. Positive samples should then undergo culture to confirm viability and perform antifungal susceptibility testing. This comprehensive approach allows for the detection of viable fungal organisms and ensures an accurate assessment of environmental contamination levels.

4.7. Limitations

This study has some important limitations that should be noted. A limited number of studies has been conducted on isolation in natural settings, and therefore, this review can only offer a snapshot of the potential reality. Choosing where to collect samples in an environment can significantly impact the relevance and applicability of the data obtained. Another limitation is the heterogeneity of the methods used in the articles that were reviewed, such as the study design and the environmental sampling techniques for C. auris detection. Also, these differences could affect the consistency and validity of the results and the implications derived from them. Furthermore, the research had some limitations that prevented a comprehensive understanding of the reservoir behavior, such as the inability to identify the strain involved and not performing susceptibility assays. It is important to emphasize that only studies regarding the hospital environmental detection of C. auris in the context of an outbreak were considered.

5. Conclusions

Despite these limitations, the present review demonstrates potential environmental reservoirs of C. auris in clinical and non-clinical environments. In addition, it offers a broad perspective on various aspects that need more research, providing guidance for future studies on C. auris.
It is worth mentioning that global warming may pose a substantial health risks concerning the proliferation of fungal infections [101]. The gradual increase in temperature promotes an environment that favors the evolution of yeasts, allowing for them to acquire thermotolerance [102]. This adaptation allows for a broader geographic distribution of pathogenic yeasts and their carriers since warmer climates make previously inhospitable regions susceptible to fungal diseases [101]. Climate-induced phenomena such as floods, storms, and hurricanes increase the risk of fungal infections. These events have the potential to spread fungal spores on a large scale and aerosolize them, which increases the possibility of human contact. In addition, the injuries caused by these disasters serve as a gateway for fungal pathogens, introducing new or uncommon species into humans [101]. Therefore, the continued rise in global temperatures may lead to an expansion of the natural habitat of C. auris, further increasing the risk of this infection in humans [103]. Tackling the interplay between climate change and fungal infections, including C. auris, requires proactive measures to mitigate climate change and improve surveillance, prevention, and control strategies for emerging fungal pathogens.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jof10050336/s1. Table S1. PRISMA checklist of the systematic search of the relevant studies. Table S2. Risk of Bias assessment of the included studies by NIH Quality Assessment Tool for Observational Cohort and Cross-Sectional Studies.

Author Contributions

Conceptualization, I.S. and S.C.-d.-O.; Methodology, I.S. and S.C.-d.-O.; Validation, I.S., I.M.M. and S.C.-d.-O.; Data Analysis, I.S. and S.C.-d.-O.; Original Draft Preparation, I.S.; Review and Editing, S.C.-d.-O. and I.M.M.; Supervision, S.C.-d.-O. All authors have read and agreed to the published version of the manuscript.

Funding

S.C.-d.-O. acknowledges national funds through the FCT, IP, within the scope of the project RISE-LA/P/0053/2020.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Conflicts of Interest

The authors declare no conflicts of interest.

Correction Statement

This article has been republished with a minor correction to the Introduction. This change does not affect the scientific content of the article.

References

  1. Satoh, K.; Makimura, K.; Hasumi, Y.; Nishiyama, Y.; Uchida, K.; Yamaguchi, H. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol. Immunol. 2009, 53, 41–44. [Google Scholar] [CrossRef] [PubMed]
  2. Sharma, C.; Kumar, N.; Pandey, R.; Meis, J.F.; Chowdhary, A. Whole genome sequencing of emerging multidrug resistant Candida auris isolates in India demonstrates low genetic variation. New Microbes New Infect. 2016, 13, 77–82. [Google Scholar] [CrossRef] [PubMed]
  3. Kohlenberg, A.; Monnet, D.L.; Plachouras, D. Increasing number of cases and outbreaks caused by Candida auris in the EU/EEA, 2020 to 2021. Eurosurveill 2022, 27, 2200846. [Google Scholar] [CrossRef] [PubMed]
  4. Centers for Disease Control and Prevention. Tracking Candida auris. Available online: https://stacks.cdc.gov/view/cdc/100943 (accessed on 16 January 2024).
  5. Lockhart, S.R.; Etienne, K.A.; Vallabhaneni, S.; Farooqi, J.; Chowdhary, A.; Govender, N.P.; Colombo, A.L.; Calvo, B.; Cuomo, C.A.; Desjardins, C.A.; et al. Simultaneous Emergence of Multidrug-Resistant Candida auris on 3 Continents Confirmed by Whole-Genome Sequencing and Epidemiological Analyses. Clin. Infect. Dis. 2017, 64, 134–140. [Google Scholar] [CrossRef] [PubMed]
  6. World Health Organization. WHO Fungal Priority Pathogens List to Guide Research, Development and Public Health Action; World Health Organization: Geneva, Switzerland, 2022. [Google Scholar]
  7. Kömeç, S.; Karabıçak, N.; Ceylan, A.N.; Gülmez, A.; Özalp, O. Three Candida auris Case Reports from Istanbul, Turkey. Mikrobiyol. Bul. 2021, 55, 452–460. [Google Scholar] [CrossRef] [PubMed]
  8. Wong, S.C.; Yuen, L.L.; Li, C.K.; Kwok, M.O.; Chen, J.H.; Cheng, V.C. Proactive infection control measures to prevent nosocomial transmission of Candida auris in Hong Kong. J. Hosp. Infect. 2023, 134, 166–168. [Google Scholar] [CrossRef]
  9. Codda, G.; Willison, E.; Magnasco, L.; Morici, P.; Giacobbe, D.R.; Mencacci, A.; Marini, D.; Mikulska, M.; Bassetti, M.; Marchese, A.; et al. In vivo evolution to echinocandin resistance and increasing clonal heterogeneity in Candida auris during a difficult-to-control hospital outbreak, Italy, 2019 to 2022. Eurosurveill 2023, 28, 2300161. [Google Scholar] [CrossRef]
  10. Theut, M.; Antsupova, V.; Andreasen, A.S.; Buhl, D.; Midttun, M.; Knudsen, J.D.; Arendrup, M.C.; Hare, R.K.; Astvad, K.; Bangsborg, J. The first two cases of Candida auris in Denmark. Ugeskr. Laeger 2022, 184, V10210768. [Google Scholar] [PubMed]
  11. Stanciu, A.M.; Florea, D.; Surleac, M.; Paraschiv, S.; Oțelea, D.; Tălăpan, D.; Popescu, G.A. First report of Candida auris in Romania: Clinical and molecular aspects. Antimicrob. Resist. Infect. Control 2023, 12, 91. [Google Scholar] [CrossRef]
  12. Allaw, F.; Kara Zahreddine, N.; Ibrahim, A.; Tannous, J.; Taleb, H.; Bizri, A.R.; Dbaibo, G.; Kanj, S.S. First Candida auris Outbreak during a COVID-19 Pandemic in a Tertiary-Care Center in Lebanon. Pathogens 2021, 10, 157. [Google Scholar] [CrossRef]
  13. Katsiari, M.; Mavroidi, A.; Kesesidis, N.; Palla, E.; Zourla, K.; Ntorlis, K.; Konstantinidis, K.; Laskou, M.; Strigklis, K.; Sakkalis, A.; et al. Emergence of Clonally-Related South Asian Clade I Clinical Isolates of Candida auris in a Greek COVID-19 Intensive Care Unit. J. Fungi 2023, 9, 243. [Google Scholar] [CrossRef] [PubMed]
  14. Zerrouki, H.; Ibrahim, A.; Rebiahi, S.A.; Elhabiri, Y.; Benhaddouche, D.E.; de Groot, T.; Meis, J.F.; Rolain, J.M.; Bittar, F. Emergence of Candida auris in intensive care units in Algeria. Mycoses 2022, 65, 753–759. [Google Scholar] [CrossRef] [PubMed]
  15. Oladele, R.; Uwanibe, J.N.; Olawoye, I.B.; Ettu, A.O.; Meis, J.F.; Happi, C.T. Emergence and Genomic Characterization of Multidrug Resistant Candida auris in Nigeria, West Africa. J. Fungi 2022, 8, 787. [Google Scholar] [CrossRef] [PubMed]
  16. de Melo, C.C.; de Sousa, B.R.; da Costa, G.L.; Oliveira, M.M.E.; de Lima-Neto, R.G. Colonized patients by Candida auris: Third and largest outbreak in Brazil and impact of biofilm formation. Front. Cell Infect. Microbiol. 2023, 13, 1033707. [Google Scholar] [CrossRef] [PubMed]
  17. Fox-Lewis, S.; Buckwell, L.; McKinney, W.; Tang, R.; Upton, G.; Francis, B.; Roberts, S. Candida auris: Lessons learnt from the first detected case in Aotearoa New Zealand. N. Z. Med. J. 2023, 136, 78–80. [Google Scholar] [PubMed]
  18. Henriques, J.; Mixao, V.; Cabrita, J.; Duarte, T.I.; Sequeira, T.; Cardoso, S.; Germano, N.; Dias, L.; Bento, L.; Duarte, S.; et al. Candida auris in Intensive Care Setting: The First Case Reported in Portugal. J. Fungi 2023, 9, 837. [Google Scholar] [CrossRef] [PubMed]
  19. Cortegiani, A.; Misseri, G.; Fasciana, T.; Giammanco, A.; Giarratano, A.; Chowdhary, A. Epidemiology, clinical characteristics, resistance, and treatment of infections by Candida auris. J. Intensive Care 2018, 6, 69. [Google Scholar] [CrossRef] [PubMed]
  20. Du, H.; Bing, J.; Hu, T.; Ennis, C.L.; Nobile, C.J.; Huang, G. Candida auris: Epidemiology, biology, antifungal resistance, and virulence. PLoS Pathog. 2020, 16, e1008921. [Google Scholar] [CrossRef]
  21. Hu, S.; Zhu, F.; Jiang, W.; Wang, Y.; Quan, Y.; Zhang, G.; Gu, F.; Yang, Y. Retrospective Analysis of the Clinical Characteristics of Candida auris Infection Worldwide From 2009 to 2020. Front. Microbiol. 2021, 12, 658329. [Google Scholar] [CrossRef]
  22. Chakrabarti, A.; Sood, P. On the emergence, spread and resistance of Candida auris: Host, pathogen and environmental tipping points. J. Med. Microbiol. 2021, 70, 001318. [Google Scholar] [CrossRef]
  23. Spruijtenburg, B.; Badali, H.; Abastabar, M.; Mirhendi, H.; Khodavaisy, S.; Sharifisooraki, J.; Taghizadeh Armaki, M.; de Groot, T.; Meis, J.F. Confirmation of fifth Candida auris clade by whole genome sequencing. Emerg Microbes Infect. 2022, 11, 2405–2411. [Google Scholar] [CrossRef]
  24. Chayaporn, S.; Karrie Kwan Ki, K.; Kar Mun, L.; Mei Gie, T.; Patipan, B.; Joash Jun Keat, C.; Sui Sin, G.; Prevena, R.; Lai Chee, L.; Kwee Yuen, T.; et al. Discovery of the sixth Candida auris clade in Singapore. medRxiv 2023. [Google Scholar] [CrossRef]
  25. Osei Sekyere, J. Candida auris: A systematic review and meta-analysis of current updates on an emerging multidrug-resistant pathogen. Microbiologyopen 2018, 7, e00578. [Google Scholar] [CrossRef] [PubMed]
  26. Lyman, M.; Forsberg, K.; Sexton, D.J.; Chow, N.A.; Lockhart, S.R.; Jackson, B.R.; Chiller, T. Worsening Spread of Candida auris in the United States, 2019 to 2021. Ann. Intern. Med. 2023, 176, 489–495. [Google Scholar] [CrossRef] [PubMed]
  27. Bidaud, A.L.; Botterel, F.; Chowdhary, A.; Dannaoui, E. In vitro antifungal combination of flucytosine with amphotericin B, voriconazole, or micafungin against Candida auris shows no antagonism. Antimicrob. Agents Chemother. 2019, 63, e01393-19. [Google Scholar] [CrossRef]
  28. Ahmad, S.; Asadzadeh, M. Strategies to Prevent Transmission of Candida auris in Healthcare Settings. Curr. Fungal. Infect. Rep. 2023, 17, 36–48. [Google Scholar] [CrossRef] [PubMed]
  29. Allert, S.; Schulz, D.; Kämmer, P.; Großmann, P.; Wolf, T.; Schäuble, S.; Panagiotou, G.; Brunke, S.; Hube, B. From environmental adaptation to host survival: Attributes that mediate pathogenicity of Candida auris. Virulence 2022, 13, 191–214. [Google Scholar] [CrossRef]
  30. Welsh, R.M.; Bentz, M.L.; Shams, A.; Houston, H.; Lyons, A.; Rose, L.J.; Litvintseva, A.P. Survival, Persistence, and Isolation of the Emerging Multidrug-Resistant Pathogenic Yeast Candida auris on a Plastic Health Care Surface. J. Clin. Microbiol. 2017, 55, 2996–3005. [Google Scholar] [CrossRef]
  31. Robert, V.; Cardinali, G.; Casadevall, A. Distribution and impact of yeast thermal tolerance permissive for mammalian infection. BMC Biol. 2015, 13, 18. [Google Scholar] [CrossRef]
  32. Casadevall, A.; Kontoyiannis, D.P.; Robert, V. Environmental Candida auris and the Global Warming Emergence Hypothesis. mBio 2021, 12, e00360-21. [Google Scholar] [CrossRef]
  33. Dire, O.; Ahmad, A.; Duze, S.; Patel, M. Survival of Candida auris on environmental surface materials and low-level resistance to disinfectant. J. Hosp. Infect. 2023, 137, 17–23. [Google Scholar] [CrossRef]
  34. Rawlinson, S.; Ciric, L.; Cloutman-Green, E. How to carry out microbiological sampling of healthcare environment surfaces? A review of current evidence. J. Hosp. Infect. 2019, 103, 363–374. [Google Scholar] [CrossRef] [PubMed]
  35. Higgins, J.P.T.; Thomas, J.; Chandler, J.; Cumpston, M.; Li, T.; Page, M.J.; Welch, V.A. Cochrane Handbook for Systematic Reviews of Interventions Version 6.4 (Updated August 2023). Available online: www.training.cochrane.org/handbook (accessed on 3 March 2024).
  36. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Bmj 2021, 372, n71. [Google Scholar] [CrossRef]
  37. Ouzzani, M.; Hammady, H.; Fedorowicz, Z.; Elmagarmid, A. Rayyan—A web and mobile app for systematic reviews. Syst. Rev. 2016, 5, 210. [Google Scholar] [CrossRef]
  38. Study Quality Assessment Tools. Available online: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools (accessed on 3 March 2024).
  39. Yadav, A.; Wang, Y.; Jain, K.; Panwar, V.A.R.; Kaur, H.; Kasana, V.; Xu, J.; Chowdhary, A. Candida auris in Dog Ears. J. Fungi 2023, 9, 720. [Google Scholar] [CrossRef] [PubMed]
  40. Yadav, A.; Jain, K.; Wang, Y.; Pawar, K.; Kaur, H.; Sharma, K.K.; Tripathy, V.; Singh, A.; Xu, J.; Chowdhary, A. Candida auris on Apples: Diversity and Clinical Significance. mBio 2022, 13, e00518-22. [Google Scholar] [CrossRef]
  41. Arora, P.; Singh, P.; Wang, Y.; Yadav, A.; Pawar, K.; Singh, A.; Padmavati, G.; Xu, J.; Chowdhary, A. Environmental Isolation of Candida auris from the Coastal Wetlands of Andaman Islands, India. mBio 2021, 12, e03181-20. [Google Scholar] [CrossRef] [PubMed]
  42. Escandón, P. Novel Environmental Niches for Candida auris: Isolation from a Coastal Habitat in Colombia. J. Fungi 2022, 8, 748. [Google Scholar] [CrossRef]
  43. Irinyi, L.; Roper, M.; Malik, R.; Meyer, W. Finding a Needle in a Haystack–In Silico Search for Environmental Traces of Candida auris. Jpn. J. Infect. Dis. 2022, 75, 490–495. [Google Scholar] [CrossRef]
  44. Barber, C.; Crank, K.; Papp, K.; Innes, G.K.; Schmitz, B.W.; Chavez, J.; Rossi, A.; Gerrity, D. Community-Scale Wastewater Surveillance of Candida auris during an Ongoing Outbreak in Southern Nevada. Environ. Sci. Technol. 2023, 57, 1755–1763. [Google Scholar] [CrossRef]
  45. Babler, K.; Sharkey, M.; Arenas, S.; Amirali, A.; Beaver, C.; Comerford, S.; Goodman, K.; Grills, G.; Holung, M.; Kobetz, E.; et al. Detection of the clinically persistent, pathogenic yeast spp. Candida auris from hospital and municipal wastewater in Miami-Dade County, Florida. Sci. Total Environ. 2023, 898, 165459. [Google Scholar] [CrossRef] [PubMed]
  46. Ekowati, Y.; Ferrero, G.; Kennedy, M.D.; de Roda Husman, A.M.; Schets, F.M. Potential transmission pathways of clinically relevant fungi in indoor swimming pool facilities. Int. J. Hyg. Environ. Health 2018, 221, 1107–1115. [Google Scholar] [CrossRef]
  47. Tian, S.; Bing, J.; Chu, Y.; Chen, J.; Cheng, S.; Wang, Q.; Zhang, J.; Ma, X.; Zhou, B.; Liu, L.; et al. Genomic epidemiology of Candida auris in a general hospital in Shenyang, China: A three-year surveillance study. Emerg. Microbes Infect. 2021, 10, 1088–1096. [Google Scholar] [CrossRef]
  48. Didik, T.; Pak-Yuen Yau, A.; Leong Cheung, H.; Suet-Yi, L.; Nga-Han, C.; Yuen-Ting, W.A.H.; Kam-Hei Luk, H.; Kwan-Yue Choi, G.; Hua-Yin Cheng, N.; Tse, H.; et al. Long-range air dispersion of Candida auris in a Cardiothoracic unit outbreak in Hong Kong. J. Hosp. Infect. 2023, 142, 105–114. [Google Scholar] [CrossRef] [PubMed]
  49. Alanio, A.; Snell, H.M.; Cordier, C.; Desnos-Olivier, M.; Dellière, S.; Aissaoui, N.; Sturny-Leclère, A.; Da Silva, E.; Eblé, C.; Rouveau, M.; et al. First Patient-to-Patient Intrahospital Transmission of Clade I Candida auris in France Revealed after a Two-Month Incubation Period. Microbiol. Spectr. 2022, 10, e0183322. [Google Scholar] [CrossRef]
  50. Yadav, A.; Singh, A.; Wang, Y.; Haren, M.H.V.; Singh, A.; De Groot, T.; Meis, J.F.; Xu, J.; Chowdhary, A. Colonisation and transmission dynamics of Candida auris among chronic respiratory diseases patients hospitalised in a chest hospital, Delhi, India: A comparative analysis of whole genome sequencing and microsatellite typing. J. Fungi 2021, 7, 81. [Google Scholar] [CrossRef]
  51. Umamaheshwari, S.; Neelambike, S.M.; Shankarnarayan, S.A.; Kumarswamy, K.S.; Gopal, S.; Prakash, H.; Rudramurthy, S.M. Clinical profile, antifungal susceptibility, and molecular characterization of Candida auris isolated from patients in a South Indian surgical ICU. J. Med. Mycol. 2021, 31, 101176. [Google Scholar] [CrossRef] [PubMed]
  52. Taori, S.K.; Khonyongwa, K.; Hayden, I.; Athukorala, G.D.A.; Letters, A.; Fife, A.; Desai, N.; Borman, A.M. Candida auris outbreak: Mortality, interventions and cost of sustaining control. J. Infect. 2019, 79, 601–611. [Google Scholar] [CrossRef]
  53. Biswal, M.; Rudramurthy, S.M.; Jain, N.; Shamanth, A.S.; Sharma, D.; Jain, K.; Yaddanapudi, L.N.; Chakrabarti, A. Controlling a possible outbreak of Candida auris infection: Lessons learnt from multiple interventions. J. Hosp. Infect. 2017, 97, 363–370. [Google Scholar] [CrossRef]
  54. Ruiz-Gaitán, A.; Martínez, H.; Moret, A.M.; Calabuig, E.; Tasias, M.; Alastruey-Izquierdo, A.; Zaragoza, Ó.; Mollar, J.; Frasquet, J.; Salavert-Lletí, M.; et al. Detection and treatment of Candida auris in an outbreak situation: Risk factors for developing colonization and candidemia by this new species in critically ill patients. Expert. Rev. Anti-Infect. Ther. 2019, 17, 295–305. [Google Scholar] [CrossRef]
  55. Adams, E.; Quinn, M.; Tsay, S.; Poirot, E.; Chaturvedi, S.; Southwick, K.; Greenko, J.; Fernandez, R.; Kallen, A.; Vallabhaneni, S.; et al. Candida auris in Healthcare Facilities, New York, USA, 2013–2017. Emerg. Infect. Dis. 2018, 24, 1816–1824. [Google Scholar] [CrossRef] [PubMed]
  56. Al Maani, A.; Paul, H.; Al-Rashdi, A.; Al Wahaibi, A.; Al-Jardani, A.; Al Abri, A.M.A.; Al Balushi, M.A.H.; Al Abri, S.; Al Reesi, M.; Al Maqbali, A.; et al. Ongoing challenges with healthcare-associated Candida auris outbreaks in Oman. J. Fungi 2019, 5, 101. [Google Scholar] [CrossRef] [PubMed]
  57. Alfouzan, W.; Ahmad, S.; Dhar, R.; Asadzadeh, M.; Almerdasi, N.; Abdo, N.M.; Joseph, L.; de Groot, T.; Alali, W.Q.; Khan, Z.; et al. Molecular Epidemiology of Candida auris Outbreak in a Major Secondary-Care Hospital in Kuwait. J. Fungi 2020, 6, 307. [Google Scholar] [CrossRef]
  58. Kumar, J.; Eilertson, B.; Cadnum, J.L.; Whitlow, C.S.; Jencson, A.L.; Safdar, N.; Krein, S.L.; Tanner, W.D.; Mayer, J.; Samore, M.H.; et al. Environmental contamination with candida species in multiple hospitals including a tertiary care hospital with a Candida auris outbreak. Pathog. Immun. 2019, 4, 260–270. [Google Scholar] [CrossRef] [PubMed]
  59. Ruiz-Gaitán, A.; Moret, A.M.; Tasias-Pitarch, M.; Aleixandre-López, A.I.; Martínez-Morel, H.; Calabuig, E.; Salavert-Lletí, M.; Ramírez, P.; López-Hontangas, J.L.; Hagen, F.; et al. An outbreak due to Candida auris with prolonged colonisation and candidaemia in a tertiary care European hospital. Mycoses 2018, 61, 498–505. [Google Scholar] [CrossRef] [PubMed]
  60. Escandón, P.; Chow, N.A.; Caceres, D.H.; Gade, L.; Berkow, E.L.; Armstrong, P.; Rivera, S.; Misas, E.; Duarte, C.; Moulton-Meissner, H.; et al. Molecular Epidemiology of Candida auris in Colombia Reveals a Highly Related, Countrywide Colonization With Regional Patterns in Amphotericin B Resistance. Clin. Infect. Dis. 2019, 68, 15–21. [Google Scholar] [CrossRef] [PubMed]
  61. Eyre, D.W.; Sheppard, A.E.; Madder, H.; Moir, I.; Moroney, R.; Quan, T.P.; Griffiths, D.; George, S.; Butcher, L.; Morgan, M.; et al. A Candida auris Outbreak and Its Control in an Intensive Care Setting. N. Engl. J. Med. 2018, 379, 1322–1331. [Google Scholar] [CrossRef] [PubMed]
  62. Rhodes, J.; Abdolrasouli, A.; Farrer, R.A.; Cuomo, C.A.; Aanensen, D.M.; Armstrong-James, D.; Fisher, M.C.; Schelenz, S. Genomic epidemiology of the UK outbreak of the emerging human fungal pathogen Candida auris. Emerg. Microbes Infect. 2018, 7, 43. [Google Scholar] [CrossRef] [PubMed]
  63. Lesho, E.P.; Bronstein, M.Z.; McGann, P.; Stam, J.; Kwak, Y.; Maybank, R.; McNamara, J.; Callahan, M.; Campbell, J.; Hinkle, M.K.; et al. Importation, Mitigation, and Genomic Epidemiology of Candida auris at a Large Teaching Hospital. Infect. Control Hosp. Epidemiol. 2018, 39, 53–57. [Google Scholar] [CrossRef]
  64. Naicker, S.D.; Maphanga, T.G.; Chow, N.A.; Allam, M.; Kwenda, S.; Ismail, A.; Govender, N.P. Clade distribution of Candida auris in South Africa using whole genome sequencing of clinical and environmental isolates. Emerg. Microbes Infect. 2021, 10, 1300–1308. [Google Scholar] [CrossRef]
  65. Pacilli, M.; Kerins, J.L.; Clegg, W.J.; Walblay, K.A.; Adil, H.; Kemble, S.K.; Xydis, S.; McPherson, T.D.; Lin, M.Y.; Hayden, M.K.; et al. Regional emergence of Candida auris in Chicago and lessons learned from intensive follow-up at 1 ventilator-capable skilled nursing facility. Clin. Infect. Dis. 2020, 71, E718–E725. [Google Scholar] [CrossRef] [PubMed]
  66. Salah, H.; Sundararaju, S.; Dalil, L.; Salameh, S.; Al-Wali, W.; Tang, P.T.; Ben Abid, F.; Tsui, C.K.M. Genomic Epidemiology of Candida auris in Qatar Reveals Hospital Transmission Dynamics and a South Asian Origin. J. Fungi 2021, 7, 240. [Google Scholar] [CrossRef] [PubMed]
  67. Schelenz, S.; Hagen, F.; Rhodes, J.L.; Abdolrasouli, A.; Chowdhary, A.; Hall, A.; Ryan, L.; Shackleton, J.; Trimlett, R.; Meis, J.F.; et al. First hospital outbreak of the globally emerging Candida auris in a European hospital. Antimicrob. Resist. Infect. Control. 2016, 5, 35. [Google Scholar] [CrossRef] [PubMed]
  68. Sexton, D.J.; Bentz, M.L.; Welsh, R.M.; Derado, G.; Furin, W.; Rose, L.J.; Noble-Wang, J.; Pacilli, M.; McPherson, T.D.; Black, S.; et al. Positive Correlation between Candida auris Skin-Colonization Burden and Environmental Contamination at a Ventilator-Capable Skilled Nursing Facility in Chicago. Clin. Infect. Dis. 2021, 73, 1142–1148. [Google Scholar] [CrossRef]
  69. Zhu, Y.; O’Brien, B.; Leach, L.; Clarke, A.; Bates, M.; Adams, E.; Ostrowsky, B.; Quinn, M.; Dufort, E.; Southwick, K.; et al. Laboratory Analysis of an Outbreak of Candida auris in New York from 2016 to 2018: Impact and lessons learned. J. Clin. Microbiol. 2020, 58, e01503-19. [Google Scholar] [CrossRef] [PubMed]
  70. Patterson, C.A.; Wyncoll, D.; Patel, A.; Ceesay, Y.; Newsholme, W.; Chand, M.; Mitchell, H.; Tan, M.; Edgeworth, J.D. Cloth Lanyards as a Source of Intermittent Transmission of Candida auris on an ICU. Crit. Care Med. 2021, 49, 697–701. [Google Scholar] [CrossRef]
  71. CDC. Candida auris—Antifungal Susceptibility Testing and Interpretation. Available online: https://www.cdc.gov/fungal/candida-auris/c-auris-antifungal.html (accessed on 4 March 2024).
  72. Furin, W.A.; Tran, L.H.; Chan, M.Y.; Lyons, A.K.; Noble-Wang, J.; Rose, L.J. Sampling efficiency of Candida auris from healthcare surfaces: Culture and nonculture detection methods. Infect. Control Hosp. Epidemiol. 2022, 43, 1492–1494. [Google Scholar] [CrossRef] [PubMed]
  73. Ghosh, A.K.; Paul, S.; Sood, P.; Rudramurthy, S.M.; Rajbanshi, A.; Jillwin, T.J.; Chakrabarti, A. Matrix-assisted laser desorption ionization time-of-flight mass spectrometry for the rapid identification of yeasts causing bloodstream infections. Clin. Microbiol. Infect. 2015, 21, 372–378. [Google Scholar] [CrossRef]
  74. Ambaraghassi, G.; Dufresne, P.J.; Dufresne, S.F.; Vallières, É.; Muñoz, J.F.; Cuomo, C.A.; Berkow, E.L.; Lockhart, S.R.; Luong, M.L. Identification of Candida auris by Use of the Updated Vitek 2 Yeast Identification System, Version 8.01: A Multilaboratory Evaluation Study. J. Clin. Microbiol. 2019, 57, e00884-19. [Google Scholar] [CrossRef]
  75. Jeffery-Smith, A.; Taori, S.K.; Schelenz, S.; Jeffery, K.; Johnson, E.M.; Borman, A.; Manuel, R.; Brown, C.S. Candida auris: A Review of the Literature. Clin. Microbiol. Rev. 2018, 31, e00029-17. [Google Scholar] [CrossRef]
  76. Kordalewska, M.; Perlin, D.S. Molecular Diagnostics in the Times of Surveillance for Candida auris. J. Fungi 2019, 5, 77. [Google Scholar] [CrossRef] [PubMed]
  77. Seyedmousavi, S.; Bosco, S.M.G.; de Hoog, S.; Ebel, F.; Elad, D.; Gomes, R.R.; Jacobsen, I.D.; Jensen, H.E.; Martel, A.; Mignon, B.; et al. Fungal infections in animals: A patchwork of different situations. Med. Mycol. 2018, 56, 165–187. [Google Scholar] [CrossRef] [PubMed]
  78. Odds, F.C.; Davidson, A.D.; Jacobsen, M.D.; Tavanti, A.; Whyte, J.A.; Kibbler, C.C.; Ellis, D.H.; Maiden, M.C.; Shaw, D.J.; Gow, N.A. Candida albicans strain maintenance, replacement, and microvariation demonstrated by multilocus sequence typing. J. Clin. Microbiol. 2006, 44, 3647–3658. [Google Scholar] [CrossRef] [PubMed]
  79. Benedict, K.; Chiller, T.M.; Mody, R.K. Invasive Fungal Infections Acquired from Contaminated Food or Nutritional Supplements: A Review of the Literature. Foodborne Pathog. Dis. 2016, 13, 343–349. [Google Scholar] [CrossRef] [PubMed]
  80. Das, D.; HogenEsch, H.; Thangamani, S. Intestinal colonization with Candida auris and mucosal immune response in mice treated with cefoperazone oral antibiotic. Front. Immunol. 2023, 14, 1123200. [Google Scholar] [CrossRef] [PubMed]
  81. Lara-Martín, P.A.; González-Mazo, E.; Petrovic, M.; Barceló, D.; Brownawell, B.J. Occurrence, distribution and partitioning of nonionic surfactants and pharmaceuticals in the urbanized Long Island Sound Estuary (NY). Mar. Pollut. Bull 2014, 85, 710–719. [Google Scholar] [CrossRef] [PubMed]
  82. Brandão, J.; Albergaria, I.; Albuquerque, J.; José, S.; Grossinho, J.; Ferreira, F.C.; Raposo, A.; Rodrigues, R.; Silva, C.; Jordao, L.; et al. Untreated sewage contamination of beach sand from a leaking underground sewage system. Sci. Total Environ. 2020, 740, 140237. [Google Scholar] [CrossRef] [PubMed]
  83. Garcia, X.; Pargament, D. Reusing wastewater to cope with water scarcity: Economic, social and environmental considerations for decision-making. Resour. Conserv. Recycl. 2015, 101, 154–166. [Google Scholar] [CrossRef]
  84. Farhadkhani, M.; Nikaeen, M.; Hadi, M.; Gholipour, S.; Yadegarfar, G. Campylobacter risk for the consumers of wastewater-irrigated vegetables based on field experiments. Chemosphere 2020, 251, 126408. [Google Scholar] [CrossRef]
  85. Barberán, A.; Dunn, R.R.; Reich, B.J.; Pacifici, K.; Laber, E.B.; Menninger, H.L.; Morton, J.M.; Henley, J.B.; Leff, J.W.; Miller, S.L.; et al. The ecology of microscopic life in household dust. Proc. Biol. Sci. 2015, 282, 20151139. [Google Scholar] [CrossRef]
  86. Dögen, A.; Sav, H.; Gonca, S.; Kaplan, E.; Ilkit, M.; Novak Babic, M.; Gunde-Cimerman, N.; de Hoog, G.S. Candida parapsilosis in domestic laundry machines. Med. Mycol. 2017, 55, 813–819. [Google Scholar] [CrossRef] [PubMed]
  87. Góralska, K.; Błaszkowska, J.; Dzikowiec, M. The occurrence of potentially pathogenic filamentous fungi in recreational surface water as a public health risk. J. Water Health 2020, 18, 127–144. [Google Scholar] [CrossRef] [PubMed]
  88. Siani, H.; Wesgate, R.; Maillard, J.Y. Impact of antimicrobial wipes compared with hypochlorite solution on environmental surface contamination in a health care setting: A double-crossover study. Am. J. Infect. Control 2018, 46, 1180–1187. [Google Scholar] [CrossRef] [PubMed]
  89. Caliman Sato, M.; Izu Nakamura Pietro, E.C.; Marques da Costa Alves, L.; Kramer, A.; da Silva Santos, P.S. Candida auris: A novel emerging nosocomial pathogen-properties, epidemiological situation and infection control. GMS Hyg. Infect. Control 2023, 18, Doc18. [Google Scholar] [CrossRef] [PubMed]
  90. Thoma, R.; Seneghini, M.; Seiffert, S.N.; Vuichard Gysin, D.; Scanferla, G.; Haller, S.; Flury, D.; Boggian, K.; Kleger, G.R.; Filipovic, M.; et al. The challenge of preventing and containing outbreaks of multidrug-resistant organisms and Candida auris during the coronavirus disease 2019 pandemic: Report of a carbapenem-resistant Acinetobacter baumannii outbreak and a systematic review of the literature. Antimicrob. Resist. Infect. Control 2022, 11, 12. [Google Scholar] [CrossRef] [PubMed]
  91. Haq, M.F.; Pearlmutter, B.S.; Cadnum, J.L.; Donskey, C.J. Efficacy of 23 commonly used liquid disinfectants against Candida auris isolates from the 4 major clades. Infect. Control. Hosp. Epidemiol. 2024, 45, 127–131. [Google Scholar] [CrossRef] [PubMed]
  92. Infection Prevention and Control for Candida auris. Available online: https://www.cdc.gov/fungal/candida-auris/c-auris-infection-control.html (accessed on 18 March 2024).
  93. Wong, S.C.; Lam, G.K.; Chen, J.H.; Li, X.; Ip, F.T.; Yuen, L.L.; Chan, V.W.; AuYeung, C.H.; So, S.Y.; Ho, P.L.; et al. Air dispersal of multidrug-resistant Acinetobacter baumannii: Implications for nosocomial transmission during the COVID-19 pandemic. J. Hosp. Infect. 2021, 116, 78–86. [Google Scholar] [CrossRef] [PubMed]
  94. Wong, S.C.; Chen, J.H.; Yuen, L.L.; Chan, V.W.; AuYeung, C.H.; Leung, S.S.; So, S.Y.; Chan, B.W.; Li, X.; Leung, J.O.; et al. Air dispersal of meticillin-resistant Staphylococcus aureus in residential care homes for the elderly: Implications for transmission during the COVID-19 pandemic. J. Hosp. Infect. 2022, 123, 52–60. [Google Scholar] [CrossRef] [PubMed]
  95. CDC. Candida auris—Treatment and Management. Available online: https://www.cdc.gov/fungal/candida-auris/c-auris-treatment.html (accessed on 4 March 2024).
  96. Sionov, E.; Chang, Y.C.; Garraffo, H.M.; Dolan, M.A.; Ghannoum, M.A.; Kwon-Chung, K.J. Identification of a Cryptococcus neoformans cytochrome P450 lanosterol 14α-demethylase (Erg11) residue critical for differential susceptibility between fluconazole/voriconazole and itraconazole/posaconazole. Antimicrob. Agents Chemother. 2012, 56, 1162–1169. [Google Scholar] [CrossRef]
  97. Rybak, J.M.; Muñoz, J.F.; Barker, K.S.; Parker, J.E.; Esquivel, B.D.; Berkow, E.L.; Lockhart, S.R.; Gade, L.; Palmer, G.E.; White, T.C.; et al. Mutations in TAC1B: A Novel Genetic Determinant of Clinical Fluconazole Resistance in Candida auris. mBio 2020, 11, e00365-20. [Google Scholar] [CrossRef]
  98. Coste, A.; Turner, V.; Ischer, F.o.; Morschhäuser, J.; Forche, A.; Selmecki, A.; Berman, J.; Bille, J.; Sanglard, D. A Mutation in Tac1p, a Transcription Factor Regulating CDR1 and CDR2, Is Coupled With Loss of Heterozygosity at Chromosome 5 to Mediate Antifungal Resistance in Candida albicans. Genetics 2006, 172, 2139–2156. [Google Scholar] [CrossRef]
  99. Muñoz, J.F.; Welsh, R.M.; Shea, T.; Batra, D.; Gade, L.; Howard, D.; Rowe, L.A.; Meis, J.F.; Litvintseva, A.P.; Cuomo, C.A. Clade-specific chromosomal rearrangements and loss of subtelomeric adhesins in Candida auris. Genetics 2021, 218, iyab029. [Google Scholar] [CrossRef]
  100. Queiroz Júnior, J.R.A.d.; Melo, I.O.; Calado, G.H.d.S.; Cavalcanti, L.R.C.; Sobrinho, C.R.W. Identification and resistance profile of bacteria isolated on stethoscopes by health careprofessionals: Systematic review. Am. J. Infect. Control 2021, 49, 229–237. [Google Scholar] [CrossRef]
  101. Nnadi, N.E.; Carter, D.A. Climate change and the emergence of fungal pathogens. PLoS Pathog. 2021, 17, e1009503. [Google Scholar] [CrossRef]
  102. Fisher, M.C.; Henk, D.A.; Briggs, C.J.; Brownstein, J.S.; Madoff, L.C.; McCraw, S.L.; Gurr, S.J. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484, 186–194. [Google Scholar] [CrossRef]
  103. Chowdhary, A.; Voss, A.; Meis, J.F. Multidrug-resistant Candida auris: ‘new kid on the block’ in hospital-associated infections? J. Hosp. Infect. 2016, 94, 209–212. [Google Scholar] [CrossRef]
Figure 1. Global epidemiology of Candida auris until October 2023 [3,4,7,8,9,10,11,12,13,14,15,16,17,18]. The grey color represents countries with no C. auris cases published in the literature.
Figure 1. Global epidemiology of Candida auris until October 2023 [3,4,7,8,9,10,11,12,13,14,15,16,17,18]. The grey color represents countries with no C. auris cases published in the literature.
Jof 10 00336 g001
Figure 2. PRISMA flow chart representing the systematic identification of studies search via databases and registers.
Figure 2. PRISMA flow chart representing the systematic identification of studies search via databases and registers.
Jof 10 00336 g002
Table 3. Results of antifungal susceptibility testing and gene mutations.
Table 3. Results of antifungal susceptibility testing and gene mutations.
First Author, YearGene MutationMIC (mg/L)/Phenotype
CDR1TAC1BERG11FCZAmBAND
Natural EnvironmentYadav, 2023 [39]-A640V (2/6)K143R (2/6)32–1280.25–0.50.01–0.06
Yadav, 2022 [40]V704L (13/19)
E709D (3/19)
-K143R (13/19)
Y132F (3/19)
16–1280.25-
Escadón, 2022 [42]---2.0 0.50.25
Arora, 2021 [41]--Y132F8–256 1–40.125
Hospital EnvironmentTian, 2021 [47]--VF125AL
(I74L)
25610.5
Yadav, 2021 [50]--Y132F16–1280.25–40.125–0.5
Umamaheshwari, 2021 [51] --Y132F16–3220.25–0.5
Alfouzan, 2020 [57]--Y132FR *S **-
Al Maani, 2019 [56]---8–161–20.031
Escadón, 2019 [60]---2–640.38–40.03–0.125
Zhu, 2019 [69]---8–2560.25–3.00.08–1
Lesho, 2018 [63]--K143R (1/1)--
Minimum concentration inhibition (MIC); fluconazole (FCZ); anidulafungin (AND); amphotericin B (AmB); * resistance (R) to FCZ was set at MIC of ≥32 mg/L, AmB at ≥2.0 mg/L, AND at ≥4 mg/L [71]. ** Susceptible (S).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Silva, I.; Miranda, I.M.; Costa-de-Oliveira, S. Potential Environmental Reservoirs of Candida auris: A Systematic Review. J. Fungi 2024, 10, 336. https://doi.org/10.3390/jof10050336

AMA Style

Silva I, Miranda IM, Costa-de-Oliveira S. Potential Environmental Reservoirs of Candida auris: A Systematic Review. Journal of Fungi. 2024; 10(5):336. https://doi.org/10.3390/jof10050336

Chicago/Turabian Style

Silva, Isabel, Isabel M. Miranda, and Sofia Costa-de-Oliveira. 2024. "Potential Environmental Reservoirs of Candida auris: A Systematic Review" Journal of Fungi 10, no. 5: 336. https://doi.org/10.3390/jof10050336

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop