Candida auris – recommendations on infection prevention and control measures in Switzerland

DOI: https://doi.org/10.4414/smw.2020.20297

Danielle Vuichard-Gysina, Rami Sommersteinb, Romain Martischangc, Stephan Harbarthc, Stefan P. Kusterd, Laurence Senne, Andreas Widmerf

on behalf of Swissnoso

aDepartment of Internal Medicine, Division of Infectious Diseases,

bDepartment of Infectious Diseases, Bern University Hospital,

cInfection Control Programme,

dDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich,

eService of Hospital Preventive Medicine,

fDivision of Infectious Diseases and Hospital Epidemiology, University Hospital Basel,

Candida auris – recommendations on infection prevention and control measures in Switzerland

Summary

Candida auris, a globally emerging pathogen, has been repeatedly introduced into European healthcare settings, leading to large and long-lasting nosocomial outbreaks. The pathogen has already been isolated in Switzerland, requiring clinicians and microbiologists to become alert. This is the first comprehensive guidance document on prevention and control of C. auris in Swiss acute care hospitals. It brings to light the most recent evidence from published original articles and reviews. We emphasise the importance of quickly identifying this yeast by means of screening in order to prevent an outbreak that could be difficult to contain. Key containment strategies include reinforcing early detection, hand hygiene, application of strict contact precautions for colonised and infected patients, and thorough specific environmental cleaning and disinfection.

Introduction

Candida auris was unknown before 2009. After its first isolation from a Japanese patient’s external ear discharge [1], it rapidly spread worldwide [2] and hit several healthcare settings, producing large nosocomial outbreaks that were difficult to contain [3–5]. In clinical studies, C. auris has been isolated from various materials [3, 6], and experiments have shown growth on dry and moist surfaces for several days [7, 8]. Its particular ability to persist in the hospital environment apparently forced one hospital in New York to rip out some ceiling and floor tiles in order to eradicate this tenacious yeast [9]. Most C. auris isolates are resistant to fluconazole and voriconazole, and exhibit variable non-susceptibility rates to other antifungal classes such as amphotericin and echinocandins [2]. Most worrying, however, is that there are already reports of pan-resistant C. auris [10, 11]. This is of major concern since treatment options in the event of invasive infection will be extremely limited. C. auris is more likely to cause invasive infections, including candidaemia, than other species of Candida. Serious infections are observed especially in patients with severe underlying diseases or immunosuppression and in neonates. Case-fatality rates for C. auris bloodstream infections may exceed 30% [12]. However, attributable mortality is difficult to determine since invasive infections usually occur in severely ill patients with multiple comorbidities [13].

Since the detection of the first case of C. auris in Switzerland in 2018 [14], Swissnoso has become aware through personal communication of two other cases in Switzerland, indicating that this emerging fungus has definitively arrived in Switzerland. Lack of awareness could quickly result in an outbreak if C. auris remains unnoticed or is detected only once a patient has developed invasive infection. Clinicians, hospital epidemiologists and microbiologists therefore need to be prepared for their first case. In this document, we aim to provide a guidance for infection prevention and control of C. auris in Swiss healthcare settings.

Methods

Recommendations issued by the US Centers for Disease Control (CDC) [15], the European Centre for Disease Prevention and Control (ECDC) [16], Public Health England [17], Pan-American Health Organization / World Health Organization [18] and Public Health Ontario [19] were reviewed and, where available, updated with more recent published literature. Eventually, since these guidelines are not harmonised in all aspects, some of the current recommendations rely on consensus opinions from Swissnoso experts, based on their experience and strategies that have proven effective in controlling transmission of other multi-resistant pathogens in the hospital setting (e.g., vancomycin-resistant enterococci, methicillin-resistant Staphylococcus aureus).

Epidemiology

C. auris is spreading around the world and has already been reported from five continents [20]. In Europe, the highest number of cases have been reported in outbreaks in Spain and the UK (table 1). However, sporadic cases have occurred in several other countries, including our neighbours France, Germany, Austria and Italy [22]. In view of the fact that some countries still have difficulties in establishing reliable data, either due to problems with microbiological identification or due to the absence of mandatory notification, the actual prevalence in some countries may be underestimated [23].

Table 1 Countries from which C. auris cases have been reported (data as of 31 December 2019 [21]).

Single cases Transmissions or multiple cases
Europe Austria, Belgium, Greece, Italy, Poland, Norway, Switzerland, The Netherlands France, Germany, Spain, the United Kingdom
Asia and the pacific region Iran, United Arab Emirates, Taiwan, Thailand Australia, Bangladesh, China, India, Israel, Japan, Kuwait, Malaysia, Oman, Pakistan, Russia, Saudi Arabia, Singapore, South Korea
Africa Egypt Kenya, South Africa
North America Canada, United States (New York City area, New Jersey, Chicago area)
South America Chile, Costa Rica Colombia, Panama, Venezuela

The information in this table has mainly been derived from a Centers for Disease Control and Prevention (CDC) website, which is available free of charge. Please note that the content on the CDC website may be subject to change and its re-use does not imply endorsement by CDC. Other countries not listed in this table may also have undetected or unreported C. auris cases.

Mode of transmission

Experience from outbreaks showed that C. auris substantially contaminates mobile equipment and the immediate environment of colonised or infected patients [5]. Direct transmission from fomites (such as blood pressure cuffs, axillary temperature probes, ultrasound machines, physical therapy equipment and other utensils in contact with the patient) is a particular risk [17]. Contamination of healthcare workers’ hands with Candida sp. is common [24–26], but it has proved difficult to show that hand contamination is a relevant source of transmission in C. auris outbreaks [3, 4, 6].

Early detection and vigilance

Acute care facilities should have in place a screening policy for early detection of multidrug resistant organisms, including C. auris, in order to rapidly identify cases, implement precautionary measures and prevent further transmission within the healthcare facility. Delays in identification, through lack of either screening or availability of a microbiology laboratory on site, can easily lead to clusters or epidemics.

Admission screening

Screening of high-risk patients transferred from a hospital abroad with recent C. auris transmission or with endemic C. auris is strongly encouraged. According to the recent recommendation issued by the International Society for Antimicrobial Chemotherapy (ISAC) Working Group on Infection Prevention and Control (IPC), patients with a recent stay in an intensive care unit in an endemic country and transfers from hospitals known to have C. auris should routinely be investigated [27]. Countries reporting C. auris cases are listed in table 1. The epidemiological profile of C. auris, however, is evolving. We therefore recommend checking the CDC’s report on the global tracking of C.auris cases on a regular basis [21].

In view of the global spread, the uncertainty in the identification of laboratories and possible delays in communication, virtually any healthcare facility abroad could be affected without knowing it. Therefore, hospitals may even consider examining all patients referred from a healthcare facility abroad.

In-hospital screening

Patients

Detection of C. auris in a non-isolated patient from a healthcare facility should trigger screening of close contacts, including those who had been sharing the room or equipment. In the absence of firm evidence on the duration (hours/days) of required overlapping exposure between index case and close contacts, screening all close contacts since hospital admission of the index case should be considered. The screening should include all current ward mates if detection was in a non-isolated patient during an intensive care stay or if secondary cases are detected among roommates. All close contacts should be placed under pre-emptive contact precautions either in a single room or grouped together in a multi-bed room. Pre-emptive contact precautions can be discontinued after three consecutive negative screenings at a minimum interval of 24 hours are available [17]. However, the 24-hour interval seems relatively short to safely rule out C. auris colonisation and de-isolated contact patients staying at the hospital should therefore be screened on a weekly basis until their discharge [27].

More intensive actions are required if two or more cases are identified: all current and previous roommates should be tested, and ward-wide screening should include any other patient who had a significant exposure such as sharing the same equipment [19, 27, 28]. We recommend weekly point prevalence screenings on affected wards for at least 3 weeks in a row after the last positive case was detected.

Healthcare workers

Contamination of healthcare workers’ hands with Candida sp. is common [24–26]. However, whether there is chronic C. auris colonisation in healthcare workers that could pose a risk for transmission remains unclear. Screening of healthcare workers is therefore not recommended unless there is substantial evidence suggesting healthcare workers as potential source or if ongoing transmission is identified despite adherence to recommended infection control measures.

Body sites to test for colonisation

Axilla and groin are the body sites most frequently colonised with C. auris. The nares, if found positive, usually have a higher load than other sites. Combining these three sites has been shown to have the highest sensitivity [11]. The sites most frequently considered in targeted multidrug-resistant organisms in Switzerland are nose, throat and groin for multi-resistant Staphylococcus aureus, and rectum or perianal site for gram-negative multidrug-resistant organisms and vancomycin resistant enterococci [29]. Relying solely on these anatomical sites, however, may not be sufficient for detection of C. auris [30].

Since admission screening would ideally be combined with screening for other multidrug-resistant organisms, a reasonable approach – on the basis of sensitivity and logistical aspects – includes a composite bilateral swab of axilla and groin and a swab from both nostrils (table 2). Sampling of other sites (throat, rectum, urine from catheterised patients, wounds or catheter exit sites) increases the test yield and can be performed in addition if part of targeted admission screening for other multidrug-resistant organisms or if clinically indicated [17, 27, 31].

Table 2 Recommended body sites for C. auris screening [15, 17].

Minimum standard
Axilla and groin bilaterally, a composite (pooled) swab is acceptable
Nose (both nostrils)
Consider additional sites if clinically relevant
Wounds
Catheter entry site
Sputum / endotracheal secretions
Throat
Drain fluid
Rectum or stool sample
Urine, if catheterised
Vaginal swab

Microbiological diagnostics

Laboratories should identify isolates of non-albicans Candida species from invasive infections to the species level. Identification of Candida to species level from non-sterile sites should be considered if a C. auris case has been detected in the healthcare facility or if a patient had an overnight stay within the last 12 months in a healthcare facility in a country with documented C. auris transmission [32]. In a previous review [14], our colleagues discussed the diagnostic challenges and the risk of misidentification due to similarity with other Candida spp. such as Candida of the haemulonii complex. In brief, C. auris cannot be identified reliably based on microscopy or growth on chromogenic agar [33]. Matrix assisted laser desorption ionisations time of flight mass spectrometry (MALDI-TOF MS) is a reliable identification method. Frequently used MALDI-TOF platforms are MALDI Biotyper (Bruker-Daltonics) and Vitek MS (bioMérieux) [3–5, 34]. Importantly, it must be assured that different C. auris spectra are included in the library and laboratories use the most updated versions [34]. Laboratories performing MALDI-TOF should follow the enrichment broth protocol described in Welsh et al. [7] which is intended for facilitated isolation of C. auris from various clinical specimens.

Molecular-based methods that can rapidly and accurately identify C. auris include conventional or real-time PCR assays [35–37]. These assays can be performed directly from the clinical specimen and do not require prior culture, which is very useful when investigating larger outbreaks.

We are aware that not all laboratories serving healthcare facilities have the means to reliably identify C. auris and test its susceptibility to the whole panel of antifungal agents. It is therefore essential to set up a collaboration with a central laboratory that can provide rapid assistance. All suspicious isolates should be stored, preferably at −80°C, for further analysis.

Case management

The suspicion of a microbiological sample being positive for C. auris should trigger immediate reporting to the infection prevention and control team, in order to implement adequate measures aiming at identifying and interrupting transmission (table 3).

Table 3 Overview of infection prevention and control measures for C. auris single cases and outbreaks. Adapted from Kenters et al. [27]*.

Single/sporadic case(s) Outbreak
Hand hygiene Use an alcohol based compound Use an alcohol based compound
Contact isolation
Gloves Single-use, non-sterile
Use per patient when entering the room
Discard when visibly soiled or when leaving the patient and immediately perform hand hygiene
Single-use, non-sterile
Use per patient when entering the room
Discard when visibly soiled or when leaving the patient and immediately perform hand hygiene
Gown Staff wears a gown for any direct patient contact
Discard when leaving the patient and immediately perform hand hygiene
Staff wears a gown for any direct patient contact and per patient in cohort
Discard when leaving the patient and immediately perform hand hygiene
Surgical mask Staff wear a mask for any direct patient contact
Required for the patient when exiting the room
Staff wear a mask for any direct patient contact
Required for the patient when exiting the room
Room Single room Single room or cohort positive cases in an area clearly separated from confirmed negative patients
Ventilation Normal Normal
Toilet / commode / bedpan Dedicated toilet, commode and/or bedpan
En-suite bathroom (if available)
Dedicated toilet, commode, bedpan or en-suite bathroom (if available)
Bathroom can be shared with other cases if cohort area
Bathroom/washbasin Dedicated Dedicated/shared with other cases
Bedding Check pillow and mattresses (when linen is removed) for damage and discard if damaged Single use pillows or check pillows and mattresses (when linen is removed) for damage and discard if damaged
Cleaning and disinfection
Cleaning material Single use cloths Single use (microfibre) cloths
Frequency of environmental decontamination Twice daily (affected rooms, at least high-touch surfaces) Twice daily (wards, at least high-touch surfaces)
Small surfaces 70% ethanol or alcohol-based disinfectants and follow manufacturers’ direction 70% ethanol or alcohol-based disinfectants and follow manufacturers’ direction
Alcohol-sensitive or large surfaces Use disinfectant compound with fungicidal activity
Follow all manufacturers’ direction
Use disinfectant compound with fungicidal activity
Follow all manufacturers’ direction
Surveillance
Index case was not isolated Test current and previous roommates (since hospital admission of the index case), extend screening to all current ward mates if secondary cases are identified Not applicable
Screening frequency Weekly point prevalence testing on intensive care units (other units, e.g., oncology, to be considered in individual risk assessment) Perform weekly point prevalence testing on outbreak wards
In case of ongoing transmission increase frequency from weekly to twice or thrice weekly point prevalence testing
Alternatively continue weekly prevalence testing and perform additional screening on admission and at discharge
Inter-hospital transfers
Communication Notify receiving hospital in advance if a C. auris-positive patient is transferred
Inform healthcare institutions where a patient has stayed before being transferred
Notify receiving hospitals in advance about the current epidemiological situation and the perceived risk of any transferred patient of being colonised or infected with C. auris (room-/ward-mates of a C. auris positive patient) and any (pending) screening result

* Written permission for re-use was obtained from the responsible author of the original publication. † The product needs to meet the EN1500 testing standard.

Measures upon detection of an incident case in a hospital

Ideally, enforced contact isolation is applied as soon as C. auris is suspected in a patient. Upon confirmation of the identification at the latest, the following actions should be taken (adapted from [28]):

Contact precautions and isolation

Contact isolation is recommended for all microbiologically confirmed cases and close contacts. Single rooms should have a dedicated or en-suite bathroom. We recommend using dedicated items, preferably single-use items or equipment and discarding them immediately after use. Proper re-processing according to the manufacturer’s instructions is crucial for any re-usable item; for example, we strongly discourage using wipes containing disinfectants if the re-usable item is in fact difficult to clean with wipes.

Staff and visitors should wear gowns, gloves and surgical masks upon entry to the room. Swissnoso is aware that many Swiss hospitals have dropped this procedure for other multidrug resistant organisms and apply personnel protective equipment as for standard precautions. However, due to the high environmental burden of C. auris, this approach might be insufficient. Importantly, the infection prevention and control team must ensure regular training on correct donning and doffing of personal protective equipment.

Data on transmission by droplets is not known, but C. auris has been isolated from patients’ nostrils [38]. Wearing a surgical mask is therefore recommended for staff and visitors when entering a patient’s room and is required for the patient when exiting the room for a medical procedure. Medical personnel should inform the patient about not leaving the room otherwise and communicate any medically necessary movement outside the room to the infection control team.

Clearly, proper hand hygiene as recommended by the World Health Organization remains the most important measure to prevent transmission of known or unrecognised pathogens. After leaving the patient’s room it is of utmost importance to carry out thorough hand hygiene using alcoholic hand-rub immediately after removing gowns and gloves.

Transmission via droplets is unlikely unless a patient has symptoms of respiratory tract infection and presence of C. auris in the respiratory tract. After contact with potentially contaminated respiratory secretions, correct hand hygiene must be carried out as for standard precautions. To the extent possible, the number of healthcare workers and other personnel who care for the C. auris patient should be kept to a minimum. Since the duration of colonisation remains largely unknown but can last several months, and no effective decolonisation scheme is available, colonised or infected patients should be placed under contact isolation for the duration of the entire hospital stay. After discharge, patients should remain labelled in an electronic alert system for early detection and immediate contact isolation upon readmission.

Five consecutive negative screenings at least one week apart may allow discontinuation of contact precautions and isolation. However, we advise the first control swabs to be taken only after a period of 3–6 months and to maintain flagging of patients for at least 1 year after the first negative culture [27].

Communication

Microbiologists should inform the local infection and control team as soon as C. auris is suspected (e.g., when non-C. albicans isolates with fluconazole resistance are found) to allow rapid implementation of necessary infection control measures. Colonised and infected patients, as well as close contacts, without at least three consecutive negative screenings 1 week apart should be (electronically) labelled in their patient file. Patients and their family should be informed about the importance of contact isolation measures and what they can do to prevent C. auris from spreading. A communication standard for inter-facility transfers must be in place. After discharge the general practitioner must be informed. Since reporting of a single C. auris case to the Federal Office of Public Health is not mandatory, we strongly advise at least informing colleagues and collaborators about such an epidemiologically important finding.

Environmental decontamination

Survival in the hospital environment, particularly on plastic [7] and moist surfaces [8] facilitates persistence of C. auris. However, it is not commonly found in the general environment or air [5]. Thorough cleaning and disinfection of patient equipment and the surrounding area is critical to prevent spreading of this organism and to break the chain of transmission. Daily environmental cleaning and disinfection should be intensified to a minimum twice daily for at least all high-touch surfaces on wards with C. auris positive patients [27]. Thoroughness of terminal environmental decontamination after discharge of a C. auris positive patient should be reinforced using a compound with adequate fungicidal efficacy. International guidelines recommend using high-strength (1000 ppm) chlorine-based or hydrogen-peroxide-containing disinfectants. However, any surface disinfectant with approved fungicidal and sporicidal activity (e.g., effective against Clostridioides difficile) is effective provided the recommended contact time is followed [3, 6]. The exception are water-based quaternary ammonium compounds, which seem to have poor activity against C. auris, and their use is therefore discouraged [39, 40]. Efficacy of no-touch disinfectant technologies such as ultraviolet light on killing of C. auris on surfaces depends largely on contact time and distance of the surfaces from the light source, but data are still limited. Ultraviolet light disinfection is recommended as an adjunctive disinfecting method for terminal cleaning if available, after the surface has been thoroughly cleaned and disinfected [41, 42]. Everything that cannot be cleaned must be discarded (e.g., porous materials, etc.).

Waste management

Bedding, towels and cloths should be replaced when visibly soiled and/or after patient discharge, and machine washed. We recommend following the “Minimum standards for handling contaminated laundry in the healthcare sector” issued by the Swiss Society of Hospital Hygiene [43].

Decolonisation of patients

There is no established decolonisation regimen. Chlorhexidine gluconate and povidone iodine are effective in killing C. auris in vitro [44, 45]. Chlorhexidine gluconate combined with topical mupirocin have shown some effect on reducing candiduria in patients in intensive care when universally applied [46]. However, the prolonged C. auris outbreaks in the UK and Spain showed that despite decolonisation efforts using daily chlorhexidine gluconate washes patients continued to be colonised or developed new candidaemia episodes [3, 4]. This may be explained by re-colonisation from the contaminated environment (e.g., bedlinen, mattresses), insufficient contact time and the relatively low chlorhexidine gluconate concentration of 2% commonly used in clinical practice [44]. Therefore, as a validated and published decolonisation regimen is lacking, no firm recommendation can be made until further studies are available.

Additional measures for outbreaks

When to declare an outbreak terminated

An outbreak can be considered over if no new patient has been identified on clinical or screening specimens over a 3-week period, and at least three unit-wide point prevalence studies are negative [19].

Summary

Why C. auris is a problem

What can we do?

Acknowledgment

We thank Andreas Voss for kindly providing permission for re-use of their published table.

Notes

Financial disclosure

Swissnoso receives financial support from the Federal Office of Public Health in order to produce guidelines on infection prevention and control of multidrug resistant and epidemiologically important organisms.

Potential competing interests

All authors declare to have no conflict of interest with respect to this 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(1):41–4. doi:.https://doi.org/10.1111/j.1348-0421.2008.00083.x

2 Lockhart SR , Etienne KA , Vallabhaneni S , Farooqi J , Chowdhary A , Govender NP , 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(2):134–40. doi:.https://doi.org/10.1093/cid/ciw691

3 Schelenz S , Hagen F , Rhodes JL , Abdolrasouli A , Chowdhary A , Hall A , et al. First hospital outbreak of the globally emerging Candida auris in a European hospital. Antimicrob Resist Infect Control. 2016;5(35):35. doi:.https://doi.org/10.1186/s13756-016-0132-5

4 Ruiz-Gaitán A , Moret AM , Tasias-Pitarch M , Aleixandre-López AI , Martínez-Morel H , Calabuig E , et al. An outbreak due to Candida auris with prolonged colonisation and candidaemia in a tertiary care European hospital. Mycoses. 2018;61(7):498–505. doi:.https://doi.org/10.1111/myc.12781

5 Eyre DW , Sheppard AE , Madder H , Moir I , Moroney R , Quan TP , et al. A Candida auris Outbreak and Its Control in an Intensive Care Setting. N Engl J Med. 2018;379(14):1322–31. doi:.https://doi.org/10.1056/NEJMoa1714373

6 Biswal M , Rudramurthy SM , Jain N , Shamanth AS , Sharma D , Jain K , et al. Controlling a possible outbreak of Candida auris infection: lessons learnt from multiple interventions. J Hosp Infect. 2017;97(4):363–70. doi:.https://doi.org/10.1016/j.jhin.2017.09.009

7 Welsh RM , Bentz ML , Shams A , Houston H , Lyons A , Rose LJ , et al. Survival, Persistence, and Isolation of the Emerging Multidrug-Resistant Pathogenic Yeast Candida auris on a Plastic Health Care Surface. J Clin Microbiol. 2017;55(10):2996–3005. doi:.https://doi.org/10.1128/JCM.00921-17

8 Piedrahita CT , Cadnum JL , Jencson AL , Shaikh AA , Ghannoum MA , Donskey CJ . Environmental Surfaces in Healthcare Facilities are a Potential Source for Transmission of Candida auris and Other Candida Species. Infect Control Hosp Epidemiol. 2017;38(9):1107–9. doi:.https://doi.org/10.1017/ice.2017.127

9A misterious infection, spanning the globe in a climate of secrecy. New York Times. [Internet]. Available at: https://www.nytimes.com/2019/04/06/health/drug-resistant-candida-auris.html. Accessed 2019 June 11. 

10 Chowdhary A , Prakash A , Sharma C , Kordalewska M , Kumar A , Sarma S , et al. A multicentre study of antifungal susceptibility patterns among 350 Candida auris isolates (2009-17) in India: role of the ERG11 and FKS1 genes in azole and echinocandin resistance. J Antimicrob Chemother. 2018;73(4):891–9. doi:.https://doi.org/10.1093/jac/dkx480

11 Zhu Y , O’Brien B , Leach L , Clarke A , Bates M , Adams E , 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(4):e01503-19. doi:.https://doi.org/10.1128/JCM.01503-19

12 Chowdhary A , Sharma C , Duggal S , Agarwal K , Prakash A , Singh PK , et al. New clonal strain of Candida auris, Delhi, India. Emerg Infect Dis. 2013;19(10):1670–3. doi:.https://doi.org/10.3201/eid1910.130393

13 Jeffery-Smith A , Taori SK , Schelenz S , Jeffery K , Johnson EM , Borman A , et al.; Candida auris Incident Management Team. Candida auris: a Review of the Literature. Clin Microbiol Rev. 2017;31(1):e00029-17. doi:.https://doi.org/10.1128/CMR.00029-17

14 Riat A , Neofytos D , Coste A , Harbarth S , Bizzini A , Grandbastien B , et al. First case of Candida auris in Switzerland: discussion about preventive strategies. Swiss Med Wkly. 2018;148:w14622.  

15Centers for Disease Control and Prevention (CDC). Clinical alert to U.S. healthcare facilities: global emergence of invasive infections caused by the multidrug-resistant yeast Candida auris. Atlanta: CDC; Update September 18 2017. Available at: https://www.cdc.gov/fungal/candida-auris/c-auris-alert-09-17.html. 

16European Centre for Disease Prevention and Control (ECDC). Candida auris in healthcare settings -Europe. Stockholm: ECDC; 2016. Available from: https://ecdc.europa.eu/sites/portal/files/media/en/publications/Publications/Candida-in-healthcaresettings_19-Dec-2016.pdf. 

17Public Health England (PHE). Candida auris within the United Kingdom: updated guidance published. Updated 11 August 2017. Available from https://www.gov.uk/government/publications/candida-auris-emergence-in-england/candida-auris-within-the-united-kingdom-updated-guidance-published. Accessed 2020 May 7. 

18Pan American Health Organization / World Health Organization. Epidemiological Alert: Candida auris outbreaks in health care services. 3 October, Washington, D.C.: PAHO/WHO; 2016; available at www.paho.org. Accessed 2019 June 14. 

19Ontario Agency for Health Protection and Promotion (Public Health Ontario), Provincial Infectious Diseases Advisory Committee. Interim guide for infection prevention and control of Candida auris. Toronto, ON: Queen's Printer for Ontario; 2019. Available from: www.publichealthontario.ca. Accessed 2019 June 14. 

20 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(1):69. doi:.https://doi.org/10.1186/s40560-018-0342-4

21Centers for Disease Control and Prevention (CDC). Atlanta. Tracking C. auris. Available from: https://www.cdc.gov/fungal/diseases/candidiasis/tracking-c-auris.html. Accessed 2020 May 7. 

22 Kohlenberg A , Struelens MJ , Monnet DL , Plachouras D ; The Candida Auris Survey Collaborative Group. Candida auris: epidemiological situation, laboratory capacity and preparedness in European Union and European Economic Area countries, 2013 to 2017. Euro Surveill. 2018;23(13):pii=18-00136. doi:.https://doi.org/10.2807/1560-7917.ES.2018.23.13.18-00136

23 Plachouras D , Lötsch F , Kohlenberg A , Monnet DL ; Candida auris survey collaborative group. Candida auris: epidemiological situation, laboratory capacity and preparedness in the European Union and European Economic Area*, January 2018 to May 2019. Euro Surveill. 2020;25(12):pii=2000240. doi:.https://doi.org/10.2807/1560-7917.ES.2020.25.12.2000240

24WHO Guidelines on Hand Hygiene in Health. Care First Global Patient Safety Challenge Clean Care is Safer Care, 2009. Available from: https://www.who.int/gpsc/5may/background/5moments/en/. Accessed 2019 Feb 15. 

25 Vazquez JA , Dembry LM , Sanchez V , Vazquez MA , Sobel JD , Dmuchowski C , et al. Nosocomial Candida glabrata colonization: an epidemiologic study. J Clin Microbiol. 1998;36(2):421–6. doi:.https://doi.org/10.1128/JCM.36.2.421-426.1998

26 Strausbaugh LJ , Sewell DL , Ward TT , Pfaller MA , Heitzman T , Tjoelker R . High frequency of yeast carriage on hands of hospital personnel. J Clin Microbiol. 1994;32(9):2299–300. doi:.https://doi.org/10.1128/JCM.32.9.2299-2300.1994

27 Kenters N , Kiernan M , Chowdhary A , Denning DW , Pemán J , Saris K , et al. Control of Candida auris in healthcare institutions. Outcome of an International Society for Antimicrobial Chemotherapy expert meeting. Int J Antimicrob Agents. 2019;54(4):400–6. doi:.https://doi.org/10.1016/j.ijantimicag.2019.08.013

28 Tsay S , Kallen A , Jackson BR , Chiller TM , Vallabhaneni S . Approach to the Investigation and Management of Patients With Candida auris, an Emerging Multidrug-Resistant Yeast. Clin Infect Dis. 2018;66(2):306–11. doi:.https://doi.org/10.1093/cid/cix744

29 Martischang R , Buetti N , Balmelli C , Saam M , Widmer A , Harbarth S . Nation-wide survey of screening practices to detect carriers of multi-drug resistant organisms upon admission to Swiss healthcare institutions. Antimicrob Resist Infect Control. 2019;8(1):37. doi:.https://doi.org/10.1186/s13756-019-0479-5

30 Vogelzang EH , Weersink AJL , van Mansfeld R , Chow NA , Meis JF , van Dijk K . The First Two Cases of Candida auris in The Netherlands. J Fungi (Basel). 2019;5(4):91. doi:.https://doi.org/10.3390/jof5040091

31European Centre for Disease Prevention and Control. Candida auris in healthcare settings – Europe – first update, 23 April 2018. Stockholm: ECDC; 2018. 

32Centers for Disease Control and Prevention. Surveillance for Candida auris. December 21, 2018. Available from: https://www.cdc.gov/fungal/candida-auris/c-auris-surveillance.html. Accessed 2019 August 30. 

33 Dewaele K , Lagrou K , Frans J , Hayette MP , Vernelen K . Hospital Laboratory Survey for Identification of Candida auris in Belgium. J Fungi (Basel). 2019;5(3):84. doi:.https://doi.org/10.3390/jof5030084

34 Buil JB , van der Lee HAL , Curfs-Breuker I , Verweij PE , Meis JF . External Quality Assessment Evaluating the Ability of Dutch Clinical Microbiological Laboratories to Identify Candida auris . J Fungi (Basel). 2019;5(4):94. doi:.https://doi.org/10.3390/jof5040094

35 Chowdhary A , Sharma C , Meis JF . Candida auris: A rapidly emerging cause of hospital-acquired multidrug-resistant fungal infections globally. PLoS Pathog. 2017;13(5):e1006290. doi:.https://doi.org/10.1371/journal.ppat.1006290

36 Kordalewska M , Zhao Y , Lockhart SR , Chowdhary A , Berrio I , Perlin DS . Rapid and Accurate Molecular Identification of the Emerging Multidrug-Resistant Pathogen Candida auris. J Clin Microbiol. 2017;55(8):2445–52. doi:.https://doi.org/10.1128/JCM.00630-17

37 Leach L , Zhu Y , Chaturvedi S . Development and Validation of a Real-Time PCR Assay for Rapid Detection of Candida auris from Surveillance Samples. J Clin Microbiol. 2018;56(2):e01223-17. doi:.https://doi.org/10.1128/JCM.01223-17

38 Tsay S , Welsh RM , Adams EH , Chow NA , Gade L , Berkow EL , et al.; MSD. Notes from the Field: Ongoing Transmission of Candida auris in Health Care Facilities - United States, June 2016-May 2017. MMWR Morb Mortal Wkly Rep. 2017;66(19):514–5. doi:.https://doi.org/10.15585/mmwr.mm6619a7

39 Cadnum JL , Shaikh AA , Piedrahita CT , Sankar T , Jencson AL , Larkin EL , et al. Effectiveness of disinfectants against candida auris and other candida species. Infect Control Hosp Epidemiol. 2017;38(10):1240–3. doi:.https://doi.org/10.1017/ice.2017.162

40 Rutala WA , Kanamori H , Gergen MF , Sickbert-Bennett EE , Weber DJ . Susceptibility of Candida auris and Candida albicans to 21 germicides used in healthcare facilities. Infect Control Hosp Epidemiol. 2019;40(3):380–2. doi:.https://doi.org/10.1017/ice.2019.1

41 Cadnum JL , Shaikh AA , Piedrahita CT , Jencson AL , Larkin EL , Ghannoum MA , et al. Relative resistance of the emerging fungal pathogen Candida auris and other Candida species to killing by ultraviolet light. Infect Control Hosp Epidemiol. 2018;39(1):94–6. doi:.https://doi.org/10.1017/ice.2017.239

42 de Groot T , Chowdhary A , Meis JF , Voss A . Killing of Candida auris by UV-C: Importance of exposure time and distance. Mycoses. 2019;62(5):408–12. doi:.https://doi.org/10.1111/myc.12903

43Schlegel M, Oswald E. Minimale Standards für den Umgang mit Schmutzwäsche im Gesundheitswesen. Available from: https://www.sgsh.ch/fileadmin/user_upload/Fachwissen/Dokumente/17-04_SGSH_VTS_Empfehlung_zum_Umgang_mit_Schmutzwaesche_def.pdf. Accessed, 2019 September 27. 

44 Abdolrasouli A , Armstrong-James D , Ryan L , Schelenz S . In vitro efficacy of disinfectants utilised for skin decolonisation and environmental decontamination during a hospital outbreak with Candida auris. Mycoses. 2017;60(11):758–63. doi:.https://doi.org/10.1111/myc.12699

45 Moore G , Schelenz S , Borman AM , Johnson EM , Brown CS . Yeasticidal activity of chemical disinfectants and antiseptics against Candida auris. J Hosp Infect. 2017;97(4):371–5. doi:.https://doi.org/10.1016/j.jhin.2017.08.019

46 Huang SS , Septimus E , Hayden MK , Kleinman K , Sturtevant J , Avery TR , et al.; Agency for Healthcare Research and Quality (AHRQ) DEcIDE Network and Healthcare-Associated Infections Program, and the CDC Prevention Epicenters Program. Effect of body surface decolonisation on bacteriuria and candiduria in intensive care units: an analysis of a cluster-randomised trial. Lancet Infect Dis. 2016;16(1):70–9. doi:.https://doi.org/10.1016/S1473-3099(15)00238-8

Notes

Financial disclosure

Swissnoso receives financial support from the Federal Office of Public Health in order to produce guidelines on infection prevention and control of multidrug resistant and epidemiologically important organisms.

Potential competing interests

All authors declare to have no conflict of interest with respect to this article.