Multiple introductions and subsequent transmission of multidrug-resistant Candida auris in the USA: a molecular epidemiological survey.
Open accessAbstract
Background Transmission of multidrug-resistant Candida auris infection has been reported in the USA. To better understand its emergence and transmission dynamics and to guide clinical and public health responses, we did a molecular epidemiological investigation of C auris cases in the USA.Methods In this molecular epidemiological survey, we used whole-genome sequencing to assess the genetic similarity between isolates collected from patients in ten US states (California, Connecticut, Florida, Illinois, Indiana, Maryland, Massachusetts, New Jersey, New York, and Oklahoma) and those identified in several other countries (Colombia, India, Japan, Pakistan, South Africa, South Korea, and Venezuela). We worked with state health departments, who provided us with isolates for sequencing. These isolates of C auris were collected during the normal course of clinical care (clinical cases) or as part of contact investigations or point prevalence surveys (screening cases). We integrated data from standardised case report forms and contact investigations, including travel history and epidemiological links (ie, patients that had shared a room or ward with a patient with C auris). Genetic diversity of C auris within a patient, a facility, and a state were evaluated by pairwise differences in single-nucleotide polymorphisms (SNPs).Findings From May 11, 2013, to Aug 31, 2017, isolates that corresponded to 133 cases (73 clinical cases and 60 screening cases) were collected. Of 73 clinical cases, 66 (90%) cases involved isolates related to south Asian isolates, five (7%) cases were related to South American isolates, one (1%) case to African isolates, and one (1%) case to east Asian isolates. Most (60 [82%]) clinical cases were identified in New York and New Jersey; these isolates, although related to south Asian isolates, were genetically distinct. Genomic data corroborated five (7%) clinical cases in which patients probably acquired C auris through health-care exposures abroad. Among clinical and screening cases, the genetic diversity of C auris isolates within a person was similar to that within a facility during an outbreak (median SNP difference three SNPs, range 0-12).Interpretation Isolates of C auris in the USA were genetically related to those from four global regions, suggesting that C auris was introduced into the USA several times. The five travel-related cases are examples of how introductions can occur. Genetic diversity among isolates from the same patients, health-care facilities, and states indicates that there is local and ongoing transmission.Funding US Centers for Disease Control and Prevention.
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The clades differ by tens to hundreds of thousands of DNA base pairs, but isolates are highly clonal within each clade.
“The clades differ by tens to hundreds of thousands of DNA base pairs, but isolates are highly clonal within each clade (Chow et al., 2018).”
From Murine model of colonization with fungal pathogen Candida auris to explore skin tropism, host risk factors and therapeutic strategies (2021) · cites this paper as Chow et al., 2018
The Results report small SNP differences among sampled isolates in the south Asian clade, including 1–26 SNPs among 42 New York clinical isolates. That supports close relatedness in this subset, but our copy does not give a tens-to-hundreds-of-thousands-base-pairs difference between clades or establish that isolates are highly clonal within every clade. (LLM, conf=0.84)
Experimental — accuracy not yet measuredOngoing transmission of C. auris has been detected in several areas in the United States, primarily in Illinois, New Jersey, and New York.
“ongoing transmission of C. auris has been detected in several areas in the United States, primarily in Illinois, New Jersey, and New York (66)”
From Population-Based Active Surveillance for Culture-Confirmed Candidemia — Four Sites, United States, 2012–2016 (2019) · cites this paper as [66]
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Allert, S., Schulz, D., Kämmer, P., Großmann, P., Wolf, T., Schäuble, S., Panagiotou, G., Brunke, S., & Hube, B. (2022) · Virulence · doi:10.1080/21505594.2022.2026037 · Cited by 66 · see citing works
Multidrug-resistant Candida auris : an epidemiological review
Chakrabarti, A., & Singh, S. (2020) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2020.1750368 · Cited by 66 · see citing works
Fluconazole-resistant Candida parapsilosis: A new emerging threat in the fungi arena
Escribano, P., & Guinea, J. (2022) · Frontiers in Fungal Biology · doi:10.3389/ffunb.2022.1010782 · Cited by 65 · see citing works
Emergence of the novel sixth Candida auris Clade VI in Bangladesh
Khan, T., Faysal, N. I., Hossain, M. M., Mah‐E‐Muneer, S., Haider, A., Moon, S. B., Sen, D., Ahmed, D., Parnell, L. A., Jubair, M., et al. (2024) · Microbiology Spectrum · doi:10.1128/spectrum.03540-23 · Cited by 62 · see citing works
Self-citationGarcía-Bustos, V., Salavert, M., Gaitán, A. C. R., Cabañero-Navalón, M. D., Sigona-Giangreco, I. A., & Pemán, J. (2020) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2020.02.001 · Cited by 62 · see citing works
Ong, C. W., Chen, S. C. ‐., Clark, J. E., Halliday, C. L., Kidd, S. E., Marriott, D. J. E., Marshall, C. L., Morris, A. J., Morrissey, C. O., Roy, R., et al. (2019) · Internal Medicine Journal · doi:10.1111/imj.14612 · Cited by 60 · see citing works
Dong, P., Zong, C., Dagher, Z., Hui, J., Li, J., Zhan, Y., Zhang, M., Mansour, M. K., & Cheng, J. (2021) · Science Advances · doi:10.1126/sciadv.abd5230 · Cited by 55 · see citing works
What are the 100 most cited fungal genera?
Bhunjun, C. S., Chen, Y. J., Phukhamsakda, C., Boekhout, T., Groenewald, J. Z., McKenzi, E. H. C., Francisco, E. C., Frisvad, J. C., Groenewald, M., Hurdeal, V. G., et al. (2024) · Studies in Mycology · doi:10.3114/sim.2024.108.01 · Cited by 57 · see citing works
Expert recommendations for prevention and management of Candida auris transmission
Aldejohann, A. M., Wiese‐Posselt, M., Gastmeier, P., & Kurzai, O. (2022) · Mycoses · doi:10.1111/myc.13445 · Cited by 57 · see citing works
Abid, F. B., Salah, H., Sundararaju, S., Dalil, L., Abdelwahab, A. H., Salameh, S., Ibrahim, E. B., Almaslmani, M. A., Tang, P., Pérez‐López, A., et al. (2023) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2023.04.025 · Cited by 55 · see citing works
Colistin interacts synergistically with echinocandins against Candida auris
Bidaud, A.-L., Djènontin, E., Botterel, F., Chowdhary, A., & Dannaoui, É. (2020) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2020.105901 · Cited by 53 · see citing works
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Dickwella Widanage, M. C., Singh, K., Li, J., Yarava, J. R., Scott, F. J., Xu, Y., Gow, N. A. R., Mentink-Vigier, F., Wang, P., Lamoth, F., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-61678-1 · Cited by 51 · see citing works
Vatanshenassan, M., Boekhout, T., Mauder, N., Robert, V., Maier, T. H. P., Meis, J. F. G. M., Berman, J. G., Then, E., Kostrzewa, M., & Hagen, F. (2020) · Journal of Fungi · doi:10.3390/jof6030146 · Cited by 51 · see citing works
Arıkan-Akdağlı, S., Ghannoum, M. A., & Meis, J. F. G. M. (2018) · Journal of Fungi · doi:10.3390/jof4040129 · Cited by 49 · see citing works
Candida auris in the UK: Introduction, dissemination, and control
Borman, A. M., & Johnson, E. M. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008563 · Cited by 49 · see citing works
Castelo‐Branco, D. D. S. C. M., Lockhart, S. R., Chen, Y., Santos, D. A., Hagen, F., Hawkins, N. J., Lavergne, R., Meis, J. F. G. M., Pape, P. L., Rocha, M. F. G., et al. (2021) · Mycoses · doi:10.1111/myc.13404 · Cited by 49 · see citing works
Self-citationHata, D. J., Humphries, R. M., & Lockhart, S. R. (2019) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2018-0508-ra · Cited by 51 · see citing works
Self-citationControlling the Diffusion of Multidrug-Resistant Organisms in Intensive Care Units
Kernéis, S., & Lucet, J. (2019) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0039-1696980 · Cited by 49 · see citing works
Tian, S., Bing, J., Chu, Y., Chen, J., Cheng, S., Wang, Q., Zhang, J., Ma, X., Zhou, B., Liu, L., et al. (2021) · Emerging Microbes & Infections · doi:10.1080/22221751.2021.1934557 · Cited by 47 · see citing works
Krämer, A., Lexow, F., Bludau, A., Köster, A. M., Misailovski, M., Seifert, U., Eggers, M., Rutala, W. A., Dancer, S. J., & Scheithauer, S. (2024) · Clinical Microbiology Reviews · doi:10.1128/cmr.00186-23 · Cited by 47 · see citing works
da Silva, K. J. G., Lucini, F., Santos, R., Santos, D. A., Meis, J. F. G. M., Melhem, M. D. S. C., Peres, N. T. A., Bastos, R. W., & Rossato, L. L. (2025) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2025.04.003 · Cited by 45 · see citing works
Zhang, S. X., Carroll, K. C., Lewis, S., Totten, M., Mead, P. A., Samuel, L. P., Steed, L. L., Nolte, F. S., Thornberg, A., Reid, J. L., et al. (2020) · Journal of Clinical Microbiology · doi:10.1128/jcm.02096-19 · Cited by 45 · see citing works
Codda, G., Willison, E., Magnasco, L., Morici, P., Giacobbe, D. R., Mencacci, A., Marini, D., Mikulska, M., Bassetti, M., Marchese, A., et al. (2023) · Eurosurveillance · doi:10.2807/1560-7917.es.2023.28.14.2300161 · Cited by 44 · see citing works
MycoSNP: A Portable Workflow for Performing Whole-Genome Sequencing Analysis of Candida auris
Bagal, U. R., Phan, J., Welsh, R. M., Misas, E., Wagner, D., Gade, L., Litvintseva, A. P., Cuomo, C. A., & Chow, N. A. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2417-3_17 · Cited by 44 · see citing works
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Self-citationSkin Metagenomic Sequence Analysis of Early Candida auris Outbreaks in U.S. Nursing Homes
Huang, X., Welsh, R. M., Deming, C., Proctor, D. M., Thomas, P. J., Program, N. C. S., Gussin, G., Huang, S. S., Kong, H. H., Bentz, M. L., et al. (2021) · mSphere · doi:10.1128/msphere.00287-21 · Cited by 41 · see citing works
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Candida auris outbreak involving liver transplant recipients in a surgical intensive care unit
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Self-citationWhole genome sequence of first Candida auris strain, isolated in Russia
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Outbreaks of Fungal Infections in Hospitals: Epidemiology, Detection, and Management
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Overview about Candida auris: What's up 12 years after its first description?
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- Authors
- Chow, N. A., Gade, L., Tsay, S. V., Forsberg, K., Greenko, J. A., Southwick, K. L., Barrett, P. M., Kerins, J. L., Lockhart, S. R., Chiller, T. M., Litvintseva, A. P., Adams, E., Barton, K., Beer, K. D., Bentz, M. L., Berkow, E. L., Black, S., Bradley, K. K., Brooks, R., Chaturvedi, S., Clegg, W., Cumming, M., DeMaria, A., Dotson, N., Epson, E., Fernandez, R., Fulton, T., Greeley, R., Jackson, B., Kallen, A., Kemble, S., Klevens, M., Kuykendall, R., Le, N. H., Leung, V., Lutterloh, E., Mcateer, J., Pacilli, M., Peterson, J., Quinn, M., Ross, K., Rozwadowski, F., Shannon, D., Skrobarcek, K. A., Vallabhaneni, S., Welsh, R., & Zhu, Y.
- Affiliations
- Centers for Disease Control and Prevention (US)
- New York State Department of Health (US)
- New Jersey Department of Health (US)
- Chicago Department of Public Health (US)
- Corresponding author
- Chow, Nancy A
- ORCID
- Chow, Nancy A
- Gade, Lalitha
- Tsay, Sharon V
- Forsberg, Kaitlin
- Greenko, Jane A
- Southwick, Karen L
- Kerins, Janna L
- Lockhart, Shawn R
- Chiller, Tom M
- Litvintseva, Anastasia P
- Bentz, Meghan L
- Berkow, Elizabeth L
- Black, Stephanie
- Brooks, Richard
- Chaturvedi, Sudha
- Cumming, Melissa
- DeMaria, Alfred
- Epson, Erin
- Jackson, Brendan
- Kallen, Alexander
- Kemble, Sarah
- Leung, Vivian
- Pacilli, Massimo
- Ross, Kathleen
- Rozwadowski, Faye
- Skrobarcek, Kimberly A
- Vallabhaneni, Snigdha
- Welsh, Rory
- Zhu, Yan
- Venue
- The Lancet Infectious Diseases
- Publisher
- Elsevier BV
- Published
- 2018-12
- Volume
- 18
- Issue
- 12
- Pages
- 1377-1384
- ISSN
- 1473-3099 (ISSN-L)
- PMC
- PMC6556114
- OpenAlex
- W2894978041
- Cited by
- 289
- References
- 19
- Citations by year
- 2026: 14 · 2025: 28 · 2024: 43 · 2023: 40 · 2022: 37 · 2021: 47 · 2020: 34 · 2019: 40 · 2018: 6
- FWCI
- 24.02
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Lancet Infectious Diseases (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (CC999999)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- Candida auris, multidrug resistance, fungal transmission, molecular epidemiology, whole genome sequencing, single nucleotide polymorphisms, genetic diversity, travel-associated infection, hospital outbreak, contact investigation, United States, South Asia, New York, New Jersey, outbreak investigation, infection control, travel medicine
- MeSH terms
- Whole Genome Sequencing, Communicable Diseases, Imported, Adult, Aged, Aged, 80 and over, Candida, Candidiasis, Female, Genotype, Humans, Male, Middle Aged, Prospective Studies, Travel, United States, Prevalence, Molecular Epidemiology, Disease Transmission, Infectious, Drug Resistance, Multiple, Fungal, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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