Abstract
Candida aurisis an emerging multidrug-resistant pathogen that can be difficult to identify using traditional biochemical methods. C. auris is capable of causing invasive fungal infections, particularly among hospitalized patients with significant medical comorbidities. Echinocandins are the empiric drugs of choice for C. auris, although not all isolates are susceptible and resistance may develop on therapy. Nosocomial C. auris outbreaks have been reported in a number of countries and aggressive infection control measures are paramount to stopping transmission.
Keywords
Introduction
Candida auris was first identified from samples of external ear drainage from one Japanese patient (
Satoh et al., 2009
) and 15 Korean patients in 2009 (Kim et al., 2009
). This organism can be challenging to identify using standard microbiologic techniques and frequently exhibits multidrug-resistance. In the eight years since these initial cases, C. auris has become an emerging global health threat, implicated in a host of invasive infections and outbreaks in healthcare facilities. To date, cases have now been identified in India (Sarma et al., 2013
, Chowdhary et al., 2013
), South Africa (Magobo et al., 2014
), Kuwait (Emara et al., 2015
), the United Kingdom (Schelenz et al., 2016
), Venezuela (Calvo et al., 2016
), Brazil (Prakash et al., 2016
), the United States (- Prakash A.
- Sharma C.
- Singh A.
- Kumar Singh P.
- Kumar A.
- Hagen F.
- et al.
Evidence of genotypic diversity among Candida auris isolates by multilocus sequence typing, matrix-assisted laser desorption ionization time-of-flight mass spectrometry and amplified fragment length polymorphism.
Clin Microbiol Infect. 2016; 22 (277.e1-277.e9)https://doi.org/10.1016/j.cmi.2015.10.022
Vallabhaneni et al., 2016
), Colombia (Morales-López et al., 2017
), Pakistan (Lockhart et al., 2017
), Spain (Ruiz Gaitán et al., 2017
), Germany (European Centre for Disease Prevention and Control, 2016
), Israel (Ben-Ami et al., 2017
), Norway (European Centre for Disease Prevention and Control, 2016
), and Oman (Al-Siyabi et al., 2017
). This review will detail the microbiology, clinical features, therapeutic options, and infection control measures relevant to C. auris infection.- Al-Siyabi Turkiya
- Al Busaidi Ibrahim
- Balkhair Abdullah
- Al-Muharrmi Zakariya
- Al-Salti Maya
- Al’Adawi Badriya
First report of Candida auris in Oman: clinical and microbiological description of five candidemia cases.
J Infect. 2017; (Available at: http://dx.doi.org/10.1016/j.jinf.2017.05.016. [Accessed June 30, 2017])
Microbiology and diagnosis
C. auris is phylogenetically related to Candida haemulonii and Candida ruelliae (
Satoh et al., 2009
). Four distinct clades have been identified from separate geographic origins, suggesting a recent and nearly simultaneous emergence of different clonal populations (Lockhart et al., 2017
). C. auris grows readily at 37–42 °C and forms light pink colonies on chromogenic media (Chowdhary et al., 2014
, Kathuria et al., 2015
). Unlike C. haemulonii, C. auris does not form pseudohyphae. Only some C. auris strains produce the virulence factors phospholipase and proteinase, which may account for the variability in pathogenicity demonstrated in a murine model (- Kathuria Shallu
- Singh Pradeep K.
- Sharma Cheshta
- Prakash Anupam
- Masih Aradhana
- Kumar Anil
- et al.
Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization–time of flight mass spectrometry and DNA sequencing and its antifungal susceptibility profile variability by vitek 2, CLSI broth microdilution, and etest method.
Borman et al., 2016
, - Borman Andrew M.
- Szekely Adrien
- Johnson Elizabeth M.
Comparative pathogenicity of United Kingdom isolates of the emerging pathogen Candida auris and other key pathogenic Candida Species.
mSphere. 2016; 1 (e00189-16)https://doi.org/10.1128/mSphere.00189-16
Larkin et al., 2017
). C. auris is capable of forming biofilms (- Larkin Emily
- Hager Christopher
- Chandra Jyotsna
- Mukherjee Pranab K.
- Retuerto Mauricio
- Salem Iman
- et al.
The emerging pathogen Candida auris: growth phenotype, virulence factors, activity of antifungals, and effect of SCY-078, a novel glucan synthesis inhibitor, on growth morphology and biofilm formation.
Antimicrob Agents Chemother. 2017; 61 (e02396-16)https://doi.org/10.1128/AAC.02396-16
Oh et al., 2011
) and adhering to catheter material, although not to the same degree as Candida albicans (Larkin et al., 2017
).- Larkin Emily
- Hager Christopher
- Chandra Jyotsna
- Mukherjee Pranab K.
- Retuerto Mauricio
- Salem Iman
- et al.
The emerging pathogen Candida auris: growth phenotype, virulence factors, activity of antifungals, and effect of SCY-078, a novel glucan synthesis inhibitor, on growth morphology and biofilm formation.
Antimicrob Agents Chemother. 2017; 61 (e02396-16)https://doi.org/10.1128/AAC.02396-16
Traditional biochemical methods of identification commonly misdiagnose C. auris as other yeast. The United States Centers for Disease Control and Prevention (CDC) recommends further testing for C. auris whenever C. haemulonii is identified or in a number of other scenarios depending on the organism reported and the method of identification (Table 1). Accurate identification can be performed with VITEK MS and Bruker Biotyper matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) devices using their “research use only” databases. Molecular sequencing of the D1–D2 domain of the 28s rDNA can also identify C. auris (
CDC, 2017
). For laboratories without the capability to perform these tests, Kumar et al. propose a low-cost alternative that can accurately distinguish C. auris from C. haemulonii using CHROMagar medium supplemented with Pal’s medium (Kumar et al., 2017
).Table 1When to suspect Candida auris based on the organism presumptively identified and the method of identification (
CDC, 2017
).Source: US Centers for Disease Control and Prevention.
| Organism reported | Method |
|---|---|
| Candida haemulonii | Any |
| Candida spp. | Any validated identification method |
| Rhodotorula glutinis | API 20C if red color is not present |
| Candida sake | API 20C |
| Candida catenulata | BD Phoenix |
| Candida catenulata | MicroScan |
| Candida famata | MicroScan |
| Candida guilliermondii | MicroScan |
| Candida lusitaniae | MicroScan |
Clinical features
Risk factors for C. auris infection appear to be similar to infections from Candida in general. These include immunosuppressed state, significant medical comorbidities, central venous catheters, urinary catheters, recent surgery, parenteral nutrition, exposure to broad spectrum antimicrobials, intensive care unit admission, and residence in a high-acuity skilled nursing facility (
Vallabhaneni et al., 2016
, Sarma and Upadhyay, 2017
). In a case-control study investigating risk factors for C. auris fungemia compared to bloodstream infection from other Candida species in Indian ICUs, those with C. auris fungemia were more likely to have had longer antecedent hospitalizations, underlying respiratory conditions, vascular surgery, prior antifungal exposure, and low APACHE II scores. Patients with C. auris fungemia in this study were also more frequently from public-sector ICUs from the north of India (Rudramurthy et al., 2017
).C. auris has been recovered in samples from blood, catheter tips, cerebrospinal fluid, bone, ear discharge, pancreatic fluid, pericardial fluid, peritoneal fluid, pleural fluid, respiratory secretions (including sputum and bronchoalveolar lavage), skin and soft tissue samples (both tissue and swab cultures), urine, and vaginal secretions. Clinically, it has been implicated as a causative agent in fungemia, ventriculitis, osteomyelitis, malignant otitis (including otomastoiditis), complicated intra-abdominal infections, pericarditis, complicated pleural effusions, and vulvovaginitis (
Satoh et al., 2009
, Kim et al., 2009
, Sarma et al., 2013
, Magobo et al., 2014
, Emara et al., 2015
, Schelenz et al., 2016
, Calvo et al., 2016
, Vallabhaneni et al., 2016
, Morales-López et al., 2017
, Lockhart et al., 2017
, Ruiz Gaitán et al., 2017
, Ben-Ami et al., 2017
, Al-Siyabi et al., 2017
, - Al-Siyabi Turkiya
- Al Busaidi Ibrahim
- Balkhair Abdullah
- Al-Muharrmi Zakariya
- Al-Salti Maya
- Al’Adawi Badriya
First report of Candida auris in Oman: clinical and microbiological description of five candidemia cases.
J Infect. 2017; (Available at: http://dx.doi.org/10.1016/j.jinf.2017.05.016. [Accessed June 30, 2017])
Borman et al., 2016
, - Borman Andrew M.
- Szekely Adrien
- Johnson Elizabeth M.
Comparative pathogenicity of United Kingdom isolates of the emerging pathogen Candida auris and other key pathogenic Candida Species.
mSphere. 2016; 1 (e00189-16)https://doi.org/10.1128/mSphere.00189-16
Lee et al., 2011
, Khillan et al., 2014
, - Khillan Vikas
- Rathore Neha
- Kathuria Shallu
- Chowdhary Anuradha
A rare case of breakthrough fungal pericarditis due to fluconazole-resistant Candida auris in a patient with chronic liver disease.
JMM Case Rep. 2014; 1https://doi.org/10.1099/jmmcr.0.T00018
Choi et al., 2017
, - Choi Hyoung I.
- An Jin
- Hwang Jae Joon
- Moon Soo-youn
- Son Jun Seong
Otomastoiditis caused by Candida auris: case report and literature review.
Mycoses. 2017; https://doi.org/10.1111/myc.12617
Chowdhary et al., 2017
, Tsay et al., 2017
). Much like other Candida species, there is uncertainty about the ability of C. auris to cause true respiratory, urinary, and skin and soft tissue infections despite being isolated from such samples.While one study reported no C. auris attributable deaths among nine patients with fungemia, crude mortality rates for C. auris fungemia have otherwise ranged from 28 to 66% across a wide range of healthcare settings and patient populations (
Chowdhary et al., 2013
, Calvo et al., 2016
, Vallabhaneni et al., 2016
, Morales-López et al., 2017
, Lockhart et al., 2017
, Al-Siyabi et al., 2017
, - Al-Siyabi Turkiya
- Al Busaidi Ibrahim
- Balkhair Abdullah
- Al-Muharrmi Zakariya
- Al-Salti Maya
- Al’Adawi Badriya
First report of Candida auris in Oman: clinical and microbiological description of five candidemia cases.
J Infect. 2017; (Available at: http://dx.doi.org/10.1016/j.jinf.2017.05.016. [Accessed June 30, 2017])
Chowdhary et al., 2014
, Rudramurthy et al., 2017
, Lee et al., 2011
).Antifungal therapies
Source control measures, including removal of indwelling catheters, are likely as important to the successful treatment of invasive C. auris infections as they are to other forms of invasive candidiasis. Regarding antifungal therapy, there are no Clinical and Laboratory Standards Institute (CLSI) or European Committee for Antimicrobial Susceptibility Testing (EUCAST) defined breakpoints for C. auris susceptibility. CDC recommends that all C. auris isolates undergo susceptibility testing and provides guidance for MIC breakpoints based on related Candida species and expert opinion (Table 2) (
CDC, 2017
). Fluconazole (tentative MIC breakpoint ≥32) is associated with high minimum inhibitory concentrations (MICs) and is likely almost always resistant. Susceptibility testing from four studies involving between 54 and 123 clinical isolates revealed MIC50 results between 64 and 128 mg/L and MIC90 results between 64 and 256 mg/L by CLSI microbroth dilution. Echinocandins (tentative MIC breakpoint ≥4 for anidulafungin and micafungin, ≥2 for caspofungin) appear to be most active in these studies with favorable results for anidulafungin (MIC50 range 0.125–0.5, MIC90 range 0.5–1), caspofungin (MIC50 0.25–0.5, MIC90 1), and micafungin (MIC50 0.125–0.25, MIC90 0.25–2). Amphotericin B (tentative MIC breakpoint ≥2) susceptibility testing exhibits a wider range of MIC results (MIC50 0.5–1, MIC90 2–4) and is likely less reliable as empiric therapy (Prakash et al., 2016
, - Prakash A.
- Sharma C.
- Singh A.
- Kumar Singh P.
- Kumar A.
- Hagen F.
- et al.
Evidence of genotypic diversity among Candida auris isolates by multilocus sequence typing, matrix-assisted laser desorption ionization time-of-flight mass spectrometry and amplified fragment length polymorphism.
Clin Microbiol Infect. 2016; 22 (277.e1-277.e9)https://doi.org/10.1016/j.cmi.2015.10.022
Lockhart et al., 2017
, Kathuria et al., 2015
, - Kathuria Shallu
- Singh Pradeep K.
- Sharma Cheshta
- Prakash Anupam
- Masih Aradhana
- Kumar Anil
- et al.
Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization–time of flight mass spectrometry and DNA sequencing and its antifungal susceptibility profile variability by vitek 2, CLSI broth microdilution, and etest method.
Arendrup et al., 2017
). Regarding second generation triazole susceptibility, fluconazole susceptibility can be used as a surrogate although fluconazole-resistant isolates may occasionally respond to other triazole antifungals (- Arendrup M.C.
- Prakash Anupam
- Meletiadis Joseph
- Sharma Cheshta
- Chowdhary Anuradha
Comparison of EUCAST and CLSI Reference microdilution MICs of eight antifungal compounds for Candida auris and associated tentative epidemiological cutoff values.
Antimicrob Agents Chemother. 2017; 61 (e00485-17)https://doi.org/10.1128/AAC.00485-17
CDC, 2017
). In comparison to CLSI microbroth dilution, similar MIC50 and MIC90 results can likely be obtained by the EUCAST method (Arendrup et al., 2017
), although caution should be used when interpreting Etest and Vitek antifungal susceptibility testing results (- Arendrup M.C.
- Prakash Anupam
- Meletiadis Joseph
- Sharma Cheshta
- Chowdhary Anuradha
Comparison of EUCAST and CLSI Reference microdilution MICs of eight antifungal compounds for Candida auris and associated tentative epidemiological cutoff values.
Antimicrob Agents Chemother. 2017; 61 (e00485-17)https://doi.org/10.1128/AAC.00485-17
Kathuria et al., 2015
).- Kathuria Shallu
- Singh Pradeep K.
- Sharma Cheshta
- Prakash Anupam
- Masih Aradhana
- Kumar Anil
- et al.
Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization–time of flight mass spectrometry and DNA sequencing and its antifungal susceptibility profile variability by vitek 2, CLSI broth microdilution, and etest method.
Table 2Tentative MIC (mg/L) breakpoints for Candida auris susceptibility (
CDC, 2017
) and published MIC ranges by CLSI microbroth dilution (Prakash et al., 2016
, - Prakash A.
- Sharma C.
- Singh A.
- Kumar Singh P.
- Kumar A.
- Hagen F.
- et al.
Evidence of genotypic diversity among Candida auris isolates by multilocus sequence typing, matrix-assisted laser desorption ionization time-of-flight mass spectrometry and amplified fragment length polymorphism.
Clin Microbiol Infect. 2016; 22 (277.e1-277.e9)https://doi.org/10.1016/j.cmi.2015.10.022
Lockhart et al., 2017
, Kathuria et al., 2015
, - Kathuria Shallu
- Singh Pradeep K.
- Sharma Cheshta
- Prakash Anupam
- Masih Aradhana
- Kumar Anil
- et al.
Multidrug-resistant Candida auris misidentified as Candida haemulonii: characterization by matrix-assisted laser desorption ionization–time of flight mass spectrometry and DNA sequencing and its antifungal susceptibility profile variability by vitek 2, CLSI broth microdilution, and etest method.
Arendrup et al., 2017
).- Arendrup M.C.
- Prakash Anupam
- Meletiadis Joseph
- Sharma Cheshta
- Chowdhary Anuradha
Comparison of EUCAST and CLSI Reference microdilution MICs of eight antifungal compounds for Candida auris and associated tentative epidemiological cutoff values.
Antimicrob Agents Chemother. 2017; 61 (e00485-17)https://doi.org/10.1128/AAC.00485-17
| Antifungal drug | Tentative MIC breakpoint | Published MIC50 range | Published MIC90 range |
|---|---|---|---|
| Fluconazole | ≥32 | 64–128 | 64–256 |
| Voriconazole | N/A | 0.5–2 | 4–8 |
| Amphotericin B | ≥2 | 0.5–1 | 2–4 |
| Anidulafungin | ≥4 | 0.125–0.5 | 0.5–1 |
| Caspofungin | ≥2 | 0.25–0.5 | 1 |
| Micafungin | ≥4 | 0.125–0.25 | 0.25–2 |
a Also applies to other second generation triazole antifungals.
b Consider using fluconazole susceptibility as a surrogate, although fluconazole-resistant isolates may occasionally respond to other triazole antifungals.
Based on these results, echinocandins are the empiric drugs of choice for C.auris infections in adults and children over the age of 2 months. Amphotericin B–while less reliable–should be considered for patients not responding to echinocandin therapy, depending on MIC results. A mouse model testing antifungal therapy on nine strains of C. auris suggested that micafungin may be particularly fungicidal and more active than tentative MIC breakpoints may suggest (
Lepak et al., 2017
), however further clinical studies in humans are needed. It is important to note that resistance may develop on therapy and close clinical follow-up and potentially repeat MIC testing may be indicated for patients who are responding poorly to antifungal therapy.- Lepak Alexander J.
- Zhao Miao
- Berkow Elizabeth L.
- Lockhart Shawn R.
- Andes David R.
Pharmacodynamic optimization for treatment of invasive Candida auris infection.
Antimicrob Agents Chemother. 2017; (AAC.00791-17)https://doi.org/10.1128/AAC.00791-17
Much like colonization with other multidrug-resistant species, CDC does not recommend systemic antifungal therapy for patients who are colonized with C. auris (
CDC, 2017
).Infection control
C. auris can cause widespread and persistent contamination of environmental surfaces within healthcare facilities and has been associated with both intra-hospital and inter-hospital transmission of clonal strains in multiple countries (
Kim et al., 2009
, Chowdhary et al., 2013
, Schelenz et al., 2016
, Calvo et al., 2016
, Morales-López et al., 2017
, European Centre for Disease Prevention and Control, 2016
, Ben-Ami et al., 2017
, Tsay et al., 2017
, Piedrahita et al., 2017
). The largest reported outbreaks to date were in a cardio-thoracic center in the United Kingdom (22 patients infected and an additional 28 patients colonized) (Schelenz et al., 2016
) and a surgical intensive care unit in Spain (33 cases of C. auris fungemia) (European Centre for Disease Prevention and Control, 2016
). From 77 clinical cases in the United States, CDC used groin and axilla swabs to screen an additional 390 close contacts (mainly patients on the same ward of a known clinical case) and identified C. auris colonization in another 45 individuals. Patients within similar geographic regions in this study commonly had overlapping stays in the same acute care hospital or long-term care facility, further supporting healthcare exposure as a key method of transmission (Tsay et al., 2017
).Given the risk of nosocomial transmission of this multidrug-resistant pathogen, infection control measures are vital to slowing the spread of C. auris. CDC recommends that all hospitalized patients with C. auris infection or colonization be treated using both Standard Precautions and Contact Precautions () and housed in a private room with daily and terminal cleaning with a disinfectant agent active against Clostridium difficile spores (
US EPA OCSPP, 2015
, Cadnum et al., 2017
). Receiving healthcare facilities should also be notified prior to transfer of an infected or colonized patient. Infection control precautions should be maintained until a patient is no longer infected or colonized with C. auris although there is uncertainty as to how best to monitor for ongoing colonization (CDC, 2017
). There are no clear data on the efficacy of decolonization measures for patients colonized with C. auris, however this has been attempted with chlorhexidine in healthcare facilities during outbreaks (Schelenz et al., 2016
, Calvo et al., 2016
, European Centre for Disease Prevention and Control, 2016
).Future directions
As C. auris cases continue to be found throughout the world, there is urgent need for improved diagnostics, antifungal therapies, and infection control measures. PCR and real-time PCR assays to rapidly identify C. auris have shown excellent accuracy in development and could be performed in laboratories that do not have the ability to perform MALDI-TOF or molecular sequencing techniques (
Kordalewska et al., 2017
). The development of new antifungal medications with activity against C. auris will be vital to controlling C. auris as therapeutic options are already limited. SCY-078, a novel triterpene glucan synthase inhibitor, is currently in phase III trials for invasive and mucocutaneous candidiasis and has recently shown promising activity in vitro against C. auris (- Kordalewska Milena
- Zhao Yanan
- Lockhart Shawn R.
- Chowdhary Anuradha
- Berrio Indira
- Perlin David S.
Rapid and accurate molecular identification of the emerging multidrug resistant pathogen Candida auris.
J Clin Microbiol. 2017; (JCM.00630-17)https://doi.org/10.1128/JCM.00630-17
Larkin et al., 2017
, - Larkin Emily
- Hager Christopher
- Chandra Jyotsna
- Mukherjee Pranab K.
- Retuerto Mauricio
- Salem Iman
- et al.
The emerging pathogen Candida auris: growth phenotype, virulence factors, activity of antifungals, and effect of SCY-078, a novel glucan synthesis inhibitor, on growth morphology and biofilm formation.
Antimicrob Agents Chemother. 2017; 61 (e02396-16)https://doi.org/10.1128/AAC.02396-16
Berkow et al., 2017
). Finally, aggressive infection control measures are critical to reducing the spread of C. auris. Antimicrobial stewardship, hand hygiene, and contact precautions will continue to be of paramount importance. More information is needed, however, about effective measures to reduce patient colonization and environmental contamination in healthcare facilities which have served as sites of ongoing transmission of this emerging pathogen.- Berkow Elizabeth L.
- Angulo David
- Lockhart Shawn R.
In vitro activity of a novel glucan synthase inhibitor, SCY-078, against clinical isolates of Candida auris.
Antimicrob Agents Chemother. 2017; 61 (e00435-17)https://doi.org/10.1128/AAC.00435-17
Funding sources
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Conflict of interest
The authors report no conflicts of interest.
References
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- Comparison of EUCAST and CLSI Reference microdilution MICs of eight antifungal compounds for Candida auris and associated tentative epidemiological cutoff values.Antimicrob Agents Chemother. 2017; 61 (e00485-17)https://doi.org/10.1128/AAC.00485-17
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Article info
Publication history
Published online: September 06, 2017
Accepted:
August 30,
2017
Received:
August 30,
2017
Corresponding Editor: Eskild Petersen, Aarhus, DenmarkIdentification
Copyright
© 2017 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.
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