Skip to main content Accessibility help
×
Home
Hostname: page-component-5d6d958fb5-gz6rp Total loading time: 0.69 Render date: 2022-11-27T05:22:41.865Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "displayNetworkTab": true, "displayNetworkMapGraph": false, "useSa": true } hasContentIssue true

Clinical, microbiological, and genomic characteristics of clade-III Candida auris colonization and infection in southern California, 2019–2022

Published online by Cambridge University Press:  02 September 2022

Annabelle de St. Maurice
Affiliation:
Department of Clinical Epidemiology and Infection Prevention, Los Angeles, California
Urvashi Parti
Affiliation:
Department of Clinical Epidemiology and Infection Prevention, Los Angeles, California
Victoria E. Anikst
Affiliation:
Department of Pathology and Laboratory Medicine, UCLA David Geffen School of Medicine, Los Angeles, California
Thomas Harper
Affiliation:
Department of Clinical Epidemiology and Infection Prevention, Los Angeles, California
Ruel Mirasol
Affiliation:
Department of Pathology and Laboratory Medicine, UCLA David Geffen School of Medicine, Los Angeles, California
Ayrton J. Dayo
Affiliation:
Department of Pathology and Laboratory Medicine, UCLA David Geffen School of Medicine, Los Angeles, California
Omai B. Garner
Affiliation:
Department of Pathology and Laboratory Medicine, UCLA David Geffen School of Medicine, Los Angeles, California
Kavitha K. Prabaker*
Affiliation:
Department of Clinical Epidemiology and Infection Prevention, Los Angeles, California
Shangxin Yang*
Affiliation:
Department of Pathology and Laboratory Medicine, UCLA David Geffen School of Medicine, Los Angeles, California
*
Author for correspondence: Shangxin Yang, E-mail: shangxinyang@mednet.ucla.edu. Or Kavitha Prabaker, E-mail: KPrabaker@mednet.ucla.edu
Author for correspondence: Shangxin Yang, E-mail: shangxinyang@mednet.ucla.edu. Or Kavitha Prabaker, E-mail: KPrabaker@mednet.ucla.edu
Rights & Permissions[Opens in a new window]

Abstract

Background:

Candida auris is an emerging fungal pathogen causing outbreaks in healthcare facilities. Five distinctive genomic clades exhibit clade-unique characteristics, highlighting the importance of real-time genomic surveillance and incorporating genotypic information to inform infection prevention practices and treatment algorithms.

Methods:

Both active and passive surveillance were used to screen hospitalized patients. C. auris polymerase chain reaction (PCR) assay on inguinal-axillary swabs was performed on high-risk patients upon admission. All clinical yeast isolates were identified to the species level. C. auris isolates were characterized by both phenotypic antifungal susceptibility tests and whole-genome sequencing.

Results:

From late 2019 to early 2022, we identified 45 patients with C. auris. Most had a tracheostomy or were from a facility with a known outbreak. Moreover, 7 patients (15%) were only identified through passive surveillance. Also, 8 (18%) of the patients had a history of severe COVID-19. The overall mortality was 18%. Invasive C. auris infections were identified in 13 patients (29%), 9 (69%) of whom had bloodstream infections. Patients with invasive infection were more likely to have a central line. All C. auris isolates were resistant to fluconazole but susceptible to echinocandins. Genomic analysis showed that 1 dominant clade-III lineage is circulating in Los Angeles, with very limited intrahost and interhost genetic diversity.

Conclusions:

We have demonstrated that a robust C. auris surveillance program can be established using both active and passive surveillance, with multidisciplinary efforts involving the microbiology laboratory and the hospital epidemiology team. In Los Angeles County, C. auris strains are highly related and echinocandins should be used for empiric therapy.

Type
Original Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

Candida auris is a multidrug-resistant emerging fungal pathogen. Reference Jeffery-Smith, Taori and Schelenz1 It may be difficult to identify with standard laboratory methods, which may lead to misdiagnosis and increased transmission. Reference Lockhart, Etienne and Vallabhaneni2 Multiple healthcare-associated outbreaks of C. auris have occurred across the United States. Reference Lockhart, Etienne and Vallabhaneni2,Reference Zhu, O’Brien and Leach3 From July 2021 to December 2021, the CDC identified 3,772 cases of colonized C. auris in the United States. 4 Genomic epidemiology has characterized the global emergence of 5 major clades of C. auris. Reference Chow, Munoz and Gade5 Each clade is differentiated by their geographic origination. Clade I is from South Asia, clade II is from East Asia, clade III is from Africa, clade IV is from South America, and clade V is from Iran. Reference Di Pilato, Codda and Ball6,Reference Chow, de Groot, Badali, Abastabar, Chiller and Meis7 These clades also exhibit unique clinical and microbiological characteristics. For instance, clade I has the highest frequency of antifungal resistance; clades I, III, and IV are frequently associated with outbreaks. Clade II, which has not been associated with outbreaks, is also less pathogenic and less drug resistant. Reference Kwon, Shin and Byun8,Reference Welsh, Sexton, Forsberg, Vallabhaneni and Litvintseva9 Clade-unique characteristics highlight the importance of real-time genomic surveillance and incorporating C. auris genotypic information to inform infection prevention practices and treatment algorithms.

Antiseptic practice in the healthcare setting, agricultural antifungal usage, and high frequency of global travel have all been speculated to contribute to the emergence of these multidrug-resistant yeasts. Reference Sharma and Chakrabarti10,Reference Perlin, Rautemaa-Richardson and Alastruey-Izquierdo11 In the United States, exposure to long-term acute-care hospital (LTACH) and skilled nursing facility (SNF) are risk factors for C. auris colonization and infection. Reference Zhu, O’Brien and Leach3,12 We previously reported a community outbreak of genetically related clade-III C. auris, which started in late 2019 in the Los Angeles area. All isolates were resistant to fluconazole but susceptible to echinocandins, and all cases had exposure history to an LTACH or SNF. Reference Price, Mirasol and Ward13 Based on our findings, we continued to perform active surveillance for high-risk patients for C. auris and perform real-time genomic surveillance to monitor the evolution of the outbreak. Here, we summarize the clinical, microbiological, and genomic characteristics of our C. auris cases from 2019 to 2022.

Methods

Candida auris screening and isolation precautions

Candida auris screening at our institution includes both active and passive surveillance (Fig. 1). Beginning October 2019, all high-risk patients were screened for C. auris colonization using an in-house PCR test on composite swabs of bilateral axillae and groin collected using an ESwab (Becton Dickinson, Franklin Lakes, NJ). Reference Price, Mirasol and Ward13 The DNA was extracted using the EZ1 Tissue Extraction kit on the EZ1 Advanced XL (Qiagen, Germantown, MD) and the polymerase chain reaction (PCR) was performed using the C. auris Primer Pair and Universal Master Mix on the LIAISON MDX (DiaSorin Molecular, Cypress, CA). The limit of detection of the PCR test was determined to be 100 colony-forming units per milliliter. In accordance with the Centers fo Disease Control and Prevention (CDC) and the Los Angeles County Department of Public Health (LACDPH) guidelines, 12,14 high-risk patients included those admitted to a facility with a known C. auris outbreak, those who had an overnight hospitalization in a state or country with known C. auris transmission, those with a history of carbapenem-resistant Enterobacterales (CRE), those with a history of tracheostomy or mechanical ventilation, or whose who had been in contact with someone with C. auris colonization or infection. On September 1, 2021, the LACDPH recommended that acute-care hospitals screen all patients admitted from LTACHs and ventilator-capable SNFs (vSNFs). At our facility, we began screening patients who met criteria in the emergency department on July 14, 2021, and the program expanded to screen patients from all SNFs (including those without ventilator units) on September 2, 2021. Patients with a known history of C. auris were often screened upon admission; however, this was not mandatory because patients may be intermittently colonized.

Fig. 1. Workflow of the UCLA hospital C. auris screening program.

Fig. 2. Timeline and positive C. auris cases identified by either active or passive surveillance.

Patients with suspected or known C. auris (eg, those awaiting C. auris test results) were immediately placed in contact/spore isolation. The environmental services staff was notified if a C. auris confirmed or suspect patient changed rooms or was discharged, and the room was then cleaned using a sporicidal disinfectant. Ultraviolet disinfection was performed, followed by cleaning validation with adenosine triphosphate (ATP). Reference Nante, Ceriale, Messina, Lenzi and Manzi15

Microbiological workup and passive surveillance

PCR-positive inguinal-axillary swabs obtained through active surveillance were inoculated onto the CHROMagar (Hardy Diagnostics, Santa Maria, CA) and were incubated at 35°C, ambient air, for up to 3 weeks. Passive surveillance was also implemented to identify to the species level all yeasts grown from clinical samples using a VITEK matrix-assisted laser desorption/ionization time-of-flight mass spectroscopy (MALDI-TOF MS) system (bioMérieux, Hazelwood, MO). Broth microdilution–based antifungal susceptibility testing was performed using panels prepared in house as previously described. Reference Price, Mirasol and Ward13

Genomic surveillance

Whole-genome sequencing and data analysis were performed as previously described. Reference Price, Mirasol and Ward13 Genes implicated in antifungal resistance (ie, erg11 for azole and fks1 for echinocandin) were analyzed for mutations. The copy number of erg11 gene was estimated using the ratio of the average mapping coverage of the single gene over the whole genome.

Chart review and research ethics

We included all hospitalized C. auris cases at our healthcare system from October 1, 2019, to February 28, 2022. The electronic medical record was utilized to abstract clinical and laboratory information from the patient’s first hospitalization when C. auris was detected. To evaluate the efficacy of our screening, we excluded C. auris cases who did not have a prior history of C. auris and whose cases were not identified by PCR within 48 hours of admission. Immunosuppression included patients with primary or secondary immunodeficiencies. Cases with positive cultures were reviewed by 2 experienced infectious disease physicians (A.d.S.M. and K.P.) to determine whether they had a clinical infection.

This study has been reviewed by the UCLA Human Research Protection Program and was approved with an exemption from the institutional review board.

Statistical analysis

Data were analyzed using STATA software (StataCorp, College Station, TX). The χ Reference Lockhart, Etienne and Vallabhaneni2 test, Fisher exact test, and Wilcoxon rank-sum test were used as appropriate.

Results

Results of C. auris screening

In 2.5 years (October 2019–February 2022), we identified 65 positive results among 1,380 C. auris screening PCR tests performed (4.7% positivity), which led to 45 C. auris cases of 1,129 unique patients screened (4.0% prevalence) (Fig. 2). Moreover, 32 patients were detected by screening PCR within 48 hours of admission. Of these 32 patients, 11 (34%) had a known history of C. auris and the remaining 21 were newly identified as being colonized with C. auris. Also, 9 cases were excluded because they did not have a known history of C. auris and were not detected by PCR within 48 hours of admission. Of these 9 cases, 4 did not meet criteria for screening on admission, 3 had indeterminate PCR results on admission, and 2 met the criteria for screening but screening was missed or delayed on admission.

Our passive surveillance system identified 7 cases through fungal culture that would not have been identified otherwise. Of these, 3 cases were identified by respiratory culture, 2 by blood culture, 1 by permacather tip culture, and 1 by urine culture.

Demographics and clinical characteristics

Most patients with C. auris colonization or infection (60%) were male, and the median age of all patients was 66 years (Table 1). All 45 patients had at least 1 comorbidity; however, only 16% were immunosuppressed. Immunocompromising conditions identified included active malignancy or cirrhosis. Most patients had a history of tracheostomy (82%) or were from a facility with a known C. auris outbreak (89%). Facility A accounted for 32 (71%) of C. auris patients identified. Moreover, 8 (18%) of the patients had a history of severe COVID-19 within the past year, and 6 had respiratory failure due to COVID-19 at the time of C. auris colonization or infection. Mortality during the index C. auris hospitalization was 18%. Other demographic characteristics are listed in Table 1.

Table 1. Demographic Characteristics of C. auris Colonized Versus Infected Patients

Note. IQR, interquartile range; CRE, carbapenem-resistant Enterobacterales; MDRO, multidrug-resistant organism; LTACH, long-term acute-care hospital; SNF, skilled nursing facility.

a In some instances type of diabetes was unspecified in the chart.

Of the 45 patients identified with C. auris, 18 (40%) had positive cultures for C. auris. Among the 18 patients with clinical cultures growing C. auris, 13 patients (72%) were categorized as having a clinical infection (Table 2). Of 13 patients with clinical infections, 11 were treated with an echinocandin alone and 1 patient was treated with a combination of echinocandin and liposomal amphotericin. Also, 1 patient died prior to their blood culture growing C. auris and was therefore untreated.

Table 2. Characteristics of Patients (n=13) with Invasive C. auris

a For 1 patient, the blood culture grew C. auris after the patient died; therefore, the patient did not receive treatment.

b One patient received combination therapy with caspofungin and liposomal amphotericin.

When comparing the patients who had clinical infection to those who were colonized with C. auris, patients who had a clinical infection were significantly more likely to have a central line (Table 1). The mortality rates during the index hospitalization between the colonized and infected patients were not significantly different.

Microbiological characteristics and antifungal susceptibility patterns

C. auris was isolated from only 19 (45%) of 42 PCR-positive inguinal or axillary swabs, indicating a low sensitivity of regular fungal culture for C. auris screening without enrichment medium such as dulcitol broth. Reference Welsh, Bentz and Shams16 Antifungal susceptibility testing was performed on 39 isolates from 28 patients, including 18 patients with infections and 10 patients with colonization alone. All isolates were resistant to fluconazole with MIC ≥ 64 mg/mL but were susceptible to echinocandins. The minimum inhibitory concentrations (MICs) ranged from ≤0.03 to 1 for anidulafungin, from ≤0.03 to 0.5 for caspofungin, and from ≤0.03 to 1 for micafungin (Fig. 3A). For other azoles without Clinical and Laboratory Standards Institute (CLSI) break points, the MICs ranged from 0.12 to 4 for voriconazole, from ≤0.03 to 1 for itraconazole, and from ≤0.03 to 0.5 for posaconazole (Fig. 3B). For amphotericin B, 11 (28%) of 39 isolates were considered resistant (Fig. 3C).

Fig. 3. Summary of antifungal susceptibility results and MIC distribution for echinocandins (3A), azoles (3B) and amphotericin B (3C). Note: We adopted the CDC tentative MIC breakpoints for C. auris: amphotericin B (≥2 µg/mL), fluconazole (≥32 µg/mL), anidulafungin (≥4 µg/mL), caspofungin (≥ 2µg/mL), micafungin (≥4 µg/mL). Voriconazole, itraconazole, and posaconazole were also tested but without interpretative criteria.

Genomic characteristics

Overall, 32 isolates from 28 patients (18 infected and 10 colonized) were sequenced, with at least 1 isolate per patient and 2 isolates in 4 patients. Sufficient sequence reads (1,392,156–6,212,112; median 2,588,576) were acquired for each isolate, resulting in >90% whole-genome coverage (91.15%–97.75%; median, 97.67%) with at least 10× depth in all isolates. All of the UCLA C. auris isolates were in the clade III. Except for UCLA-466 and UCLA-891, all other isolates clustered closely together, with only 2–50 single-nucleotide polymorphisms (SNPs) (Fig. 4A and Supplementary Fig. S1 online), which indicated a single origin. Reference Price, Mirasol and Ward13 They are loosely related to other domestic clade-III C. auris stains, including SRR7909359 isolated in a patient in Indiana in 2017 and SRR12073435 found in Florida in 2019 (Fig. 4B), with 69–99 SNP differences and 47–77 SNP differences, respectively (Supplementary Fig. S1 online). UCLA-466 is genetically distinctive, with 73–97 SNPs compared to all other UCLA isolates, and it branched separately in the SNP tree (Fig. 4A). It is also less related to the Indiana and the Florida C. auris strains, with 135 and 122 SNPs, respectively, suggesting a different entry without a known origin. UCLA-891 (isolated in February 2022) clustered closely with the Florida strain with only 21 SNPs, which is consistent with the history that this patient was transferred from a healthcare facility in Florida in late 2021. Notably, in 4 patients, we sequenced 2 isolates per patient from samples collected at different sources within 10 days, and the results showed very limited intrahost genetic diversity, with only 2–11 SNP difference.

Fig. 4. (A) SNP phylogenetic tree of the UCLA C. auris isolates. (B) K-mer phylogenetic tree of C. auris in the United States by states and clades.

In the erg11 gene, all isolates possess the 2 mutations, p.V125A and p.F126L, which are well known for causing fluconazole resistance in clade-III C. auris (Supplementary Table S1 online). Reference Chow, Munoz and Gade5,Reference Price, Mirasol and Ward13 Except for UCLA-891, which is related to the Florida strain, all other isolates did not have increased gene copy number, which had been reported in a small percentage of the global clade-III C. auris. Reference Chow, Munoz and Gade5 UCLA-891 possessed 2 copies of the erg11 gene, indicating an additional azole resistance mechanism. However, its phenotypic azole resistance profile is not different from other isolates, with an MIC of >64 for fluconazole, an MIC of 1 for voriconazole, an MIC of 0.5 for itraconazole, and an MIC of 0.06 for posaconazole. In the fks1 gene, all isolates have a p.I1572L polymorphism that is not associated with antifungal resistance. One isolate (UCLA-466) carries an additional polymorphism p.I1095L, consistent with its unique phylogeny indicating a separate entry. No mutations were identified at S639, which had been linked to echinocandin resistance. Reference Chow, Munoz and Gade5

Discussion

In this study, we have described a robust surveillance system established by a multidisciplinary team consisting of clinical microbiologists, infectious diseases specialists, environmental services, informational technology specialists, and clinical epidemiologists. In this system, C. auris cases of colonization and infection were effectively identified using a combination of active screening by a highly sensitive PCR test and passive surveillance relying on accurate species-level identification for all yeasts grown from clinical samples. We identified our first C. auris case as early as October 2019. From November 2019 to June 2020, no cases were identified by either active or passive surveillance. However, since July 2020, more cases have been identified, with a peak during the second and third quarters of 2021, with as many as 5 cases identified monthly.

In this study, 29% of patients identified through surveillance had C. auris infection. Comorbidities were present in all patients with C. auris, including patients who were colonized; however, infected patients were more likely to have a central line. Most of the clinical infections identified were bloodstream infections, which is similar to the findings of other studies. Reference Jeffery-Smith, Taori and Schelenz1 Interestingly, although half of infected C. auris patients developed fungemia in our study, mortality did not differ significantly between C. auris infected versus colonized patients, likely due to the small number of cases. The overall mortality rate in our patient population was 18%, which is lower than the 30%–60% mortality rates reported in other studies Reference Tsay, Kallen, Jackson, Chiller and Vallabhaneni17 ; this rate is likely low because we were conducting active surveillance. As our screening criteria expands to include patients admitted from all SNFs and LTACHs, we will likely find more patients colonized with C. auris outside known outbreak facilities, and potentially we will identify new facilities with C. auris outbreaks.

We identified most patients during the COVID-19 pandemic. The interaction between severe acute respiratory coronavirus virus 2 (SARS-CoV-2) and Candida infections has been documented. In one study, patients with Candida and SARS-CoV-2 coinfection often did not have typical candidemia risk factors, but high healthcare utilization during the pandemic likely contributed to their infections; unfortunately, this study did not include patients with C. auris. Reference Seagle, Jackson and Lockhart18 A different study of patients infected with C. auris during the pandemic in India reported that the use of tocilizimab, duration of ICU stay, and high ferritin level were predictors of candidemia. Reference Rajni, Singh and Tarai19 Among our patients, 8 (18%) had histories of severe COVID-19 with prolonged hospitalization. Reuse of PPE due to supply shortages, increased antimicrobial use, and prolonged hospital stay may have contributed to the spread of C. auris within healthcare facilities, precipitating outbreaks during the pandemic. Reference Prestel, Anderson and Forsberg20,Reference Eckardt, Canavan and Guran21 Additionally, some healthcare facilities placed patients in cohorts based on COVID-19 status alone before patients were identified as being colonized with multidrug-resistant organisms. Reference Eckardt, Canavan and Guran21 Timely screening and identification of patients colonized with C. auris can improve isolation measures and help prevent the spread of C. auris within an institution.

Despite following the CDC and LACDPH guidelines for active screening of the patients with high risk, 4 patients (9%) did not meet screening criteria on admission, suggesting increasing community spread which rendered the selected screening scheme less effective. Universal screening may become increasingly important as spread continues; however, universal screening may still miss cases. In our study, 3 patients had indeterminate PCR results and 1 patient had a negative PCR but later developed infection. We later modified our active surveillance process to repeat PCR screening with a new swab rather than repeat PCR on the original swab to increase sensitivity of our active surveillance. Further research should be conducted to determine the most sensitive methods to test for C. auris colonization. For instance, culture using dulcitol enrichment broth has shown high sensitivity for effectively isolating C. auris from patients and their environment. Reference Welsh, Bentz and Shams16 Among our patients, 7 (16%) were only identified through passive surveillance, which highlights the importance of continuing passive surveillance in parallel with active screening.

To our knowledge, this is the first study to characterize many clade-III C. auris cases in the United States. Our genomic analysis showed that only 1 dominant and unique lineage has been circulating in the LA area in the past 2.5 years. Very limited genetic diversity was observed in the general patient population and within hosts. We also showed a recent interstate transmission of C. auris that was introduced from Florida to southern California, which demonstrates the importance of screening patients recently admitted from facilities in high-prevalence states. All the isolates identified so far were resistant to fluconazole but susceptible to echinocandins. The interpretation of the amphotericin B MIC results in C. auris remains challenging due to a lack of method standardization. The consistent drug-susceptibility pattern for azoles and echinocandins, and the limited genetic diversity of the C. auris outbreak strain characterized in this study, can serve as reliable evidence to guide effective empiric treatment in Los Angeles, that is, using echinocandins as the first-line antifungal drug for treating C. auris infections.

This study had several limitations. Data were collected retrospectively; thus, some of the information about patient-level risk factors was incomplete, including travel. A standard definition for C. auris colonization versus infection is lacking. This study was performed at a single institution, and 71% of our patients with C. auris came from a single facility; therefore, our C. auris isolates may not cover all the community strains in Los Angeles. Very limited genes known to be associated with antifungal resistance were analyzed, which highlights an urgent need for more expansive understanding of molecular mechanisms for drug resistance in C. auris. Adherence to our screening guidelines was not consistent; 2 patients met screening criteria but did not have a screening PCR sent on admission. Missed screening opportunities could be partially due to staffing challenges during the COVID-19 pandemic. In addition, we missed 1 screening opportunity due to a patient being directly admitted from a low-risk facility; however, this patient had been admitted to a high-risk facility within the prior 12 months and should have been screened. Admission history is difficult to obtain from chronically ill patients, many of whom may be nonverbal and may not be accompanied by family members.

In summary, we have demonstrated that a robust C. auris surveillance program can be established with multidisciplinary efforts involving both the microbiology laboratory and the hospital epidemiology team. Our study has provided real-time and critical information about the characteristics of the outbreak C. auris strain that can be used to guide effective treatment policies. This type of screening does require significant institutional support because screening is not reimbursed by insurance and may be perceived as low yield given the low percentage of patients who test positive for C. auris. However, given our high-risk population, this type of active surveillance plays an instrumental role in controlling the spread of C. auris in the hospital setting.

Supplementary material

To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2022.204

Acknowledgment

We thank the UCLA Clinical Microbiology Laboratory for their technical assistance.

Financial support

This study was funded by the UCLA Department of Pathology and Laboratory Medicine.

Conflicts of interest

All authors report no conflicts of interest relevant to this article.

References

Jeffery-Smith, A, Taori, SK, Schelenz, S, et al. Candida auris: a review of the literature. Clin Microbiol Rev 2018;31:e0002917.CrossRefGoogle ScholarPubMed
Lockhart, SR, Etienne, KA, Vallabhaneni, S, et al. Simultaneous emergence of multidrug-resistant candida auris on 3 continents confirmed by whole-genome sequencing and epidemiological analyses. Clin Infect Dis 2017;64:134140.CrossRefGoogle ScholarPubMed
Zhu, Y, O’Brien, B, Leach, L, 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:e0150319.CrossRefGoogle ScholarPubMed
Tracking Candida auris. Centers for Disease Control and Prevention website. https://www.cdc.gov/fungal/candida-auris/tracking-c-auris.html. Published 2022. Accessed March 27, 2022, 2022.Google Scholar
Chow, NA, Munoz, JF, Gade, L, et al. Tracing the evolutionary history and global expansion of Candida auris using population genomic analyses. mBio 2020;11:e0336419.CrossRefGoogle ScholarPubMed
Di Pilato, V, Codda, G, Ball, L, et al. Molecular epidemiological investigation of a nosocomial cluster of C. auris: evidence of recent emergence in Italy and ease of transmission during the COVID-19 pandemic. J Fungi (Basel) 2021;7:140.CrossRefGoogle ScholarPubMed
Chow, NA, de Groot, T, Badali, H, Abastabar, M, Chiller, TM, Meis, JF. Potential fifth clade of Candida auris, Iran, 2018. Emerg Infect Dis 2019;25:17801781.CrossRefGoogle ScholarPubMed
Kwon, YJ, Shin, JH, Byun, SA, et al. Candida auris clinical isolates from South Korea: identification, antifungal susceptibility, and genotyping. J Clin Microbiol 2019;57:e0162418.CrossRefGoogle ScholarPubMed
Welsh, RM, Sexton, DJ, Forsberg, K, Vallabhaneni, S, Litvintseva, A. Insights into the unique nature of the East Asian clade of the emerging pathogenic yeast Candida auris . J Clin Microbiol 2019;57:e0000719.CrossRefGoogle ScholarPubMed
Sharma, M, Chakrabarti, A. On the origin of Candida auris: ancestor, environmental stresses, and antiseptics. mBio 2020;11:e02102-20.CrossRefGoogle ScholarPubMed
Perlin, DS, Rautemaa-Richardson, R, Alastruey-Izquierdo, A. The global problem of antifungal resistance: prevalence, mechanisms, and management. Lancet Infect Dis 2017;17:e383e392.CrossRefGoogle ScholarPubMed
Screening for Candida auris colonization. Centers for Disease Control and Prevention website. https://www.cdc.gov/fungal/candida-auris/c-auris-screening.html. Published 2022. Accessed March 28, 2022, 2022.Google Scholar
Price, TK, Mirasol, R, Ward, KW, et al. Genomic characterizations of clade III lineage of Candida auris, California, USA. Emerg Infect Dis 2021;27:12231227.CrossRefGoogle ScholarPubMed
Candida auris. Los Angeles County Publish Health Department wesbite. http://publichealth.lacounty.gov/acd/Diseases/CandidaAuris.htm. Published 2022. Accessed March 28, 2022, 2022.Google Scholar
Nante, N, Ceriale, E, Messina, G, Lenzi, D, Manzi, P. Effectiveness of ATP bioluminescence to assess hospital cleaning: a review. J Prev Med Hyg 2017;58:e177e183.Google ScholarPubMed
Welsh, RM, Bentz, ML, Shams, A, et al. Survival, persistence, and isolation of the emerging multidrug-resistant pathogenic yeast Candida auris on a plastic healthcare surface. J Clin Microbiol 2017;55:29963005.CrossRefGoogle ScholarPubMed
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;66:306311.CrossRefGoogle Scholar
Seagle, EE, Jackson, BR, Lockhart, SR, et al. The landscape of candidemia during the coronavirus disease 2019 (COVID-19) pandemic. Clin Infect Dis 2022;74:802811.CrossRefGoogle ScholarPubMed
Rajni, E, Singh, A, Tarai, B, et al. A high frequency of Candida auris bloodstream infections in coronavirus disease 2019 patients admitted to intensive care units, northwestern India: a case–control study. Open Forum Infect Dis 2021;8:ofab452.CrossRefGoogle Scholar
Prestel, C, Anderson, E, Forsberg, K, et al. Candida auris outbreak in a COVID-19 specialty care unit—Florida, July–August 2020. Morb Mortal Wkly Rep 2021;70:5657.CrossRefGoogle Scholar
Eckardt, P, Canavan, K, Guran, R, et al. Containment of a carbapenem-resistant Acinetobacter baumannii complex outbreak in a COVID-19 intensive care unit. Am J Infect Control 2022;50:477481.CrossRefGoogle Scholar
Figure 0

Fig. 1. Workflow of the UCLA hospital C. auris screening program.

Figure 1

Fig. 2. Timeline and positive C. auris cases identified by either active or passive surveillance.

Figure 2

Table 1. Demographic Characteristics of C. auris Colonized Versus Infected Patients

Figure 3

Table 2. Characteristics of Patients (n=13) with Invasive C. auris

Figure 4

Fig. 3. Summary of antifungal susceptibility results and MIC distribution for echinocandins (3A), azoles (3B) and amphotericin B (3C). Note: We adopted the CDC tentative MIC breakpoints for C. auris: amphotericin B (≥2 µg/mL), fluconazole (≥32 µg/mL), anidulafungin (≥4 µg/mL), caspofungin (≥ 2µg/mL), micafungin (≥4 µg/mL). Voriconazole, itraconazole, and posaconazole were also tested but without interpretative criteria.

Figure 5

Fig. 4. (A) SNP phylogenetic tree of the UCLA C. auris isolates. (B) K-mer phylogenetic tree of C. auris in the United States by states and clades.

Supplementary material: File

de St. Maurice et al. supplementary material

de St. Maurice et al. supplementary material

Download de St. Maurice et al. supplementary material(File)
File 18 KB
You have Access Open access

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Clinical, microbiological, and genomic characteristics of clade-III Candida auris colonization and infection in southern California, 2019–2022
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

Clinical, microbiological, and genomic characteristics of clade-III Candida auris colonization and infection in southern California, 2019–2022
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

Clinical, microbiological, and genomic characteristics of clade-III Candida auris colonization and infection in southern California, 2019–2022
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *