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Nosocomial infection of C. auris in COVID-19 Intensive Care Unit in Türkiye and Phylogenetic Analysis of Isolates

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Abstract

Background

The difficulties in the identification of C. auris and the delays in the implementation of infection control precautions contribute to outbreaks. This study analyzed 10 patients with COVID-19 and C. auris candidemia, their characteristic and clinical features and phylogenetic features, and the antifungal susceptibilities of the isolates.

Method

C. auris were detected in the COVID-19 ICU of a university hospital between January and August 2021. Identification to species level was performed using MALDI-TOF MS. Antifungal susceptibilities were determined by the Sensititre YeastOne YO10 panel. The isolates were whole genome sequenced to assess genetic relatedness and a phylogenetic tree was drawn including various C. auris clades.

Results

The mean growth time in blood cultures was 38.8 h. C. auris candidemia developed on the average 27th day of ICU admission. All were susceptible to anidulafungin and micafungin, while they were resistant to fluconazole and amphotericin B. Only three isolates were found to be resistant to caspofungin. All patients died. With the WGS method, all isolates were found in a close resemblance to each other in terms of total nucleotide similarity (with a minimum of 96% pairwise alignment). Our isolates showed the closest similarity to South Asian clade (Clade I).

Conclusions

This study is the first to evaluate the phylogenetic characteristics of C. auris using WGS and to determine antifungal susceptibilities in Türkiye on COVID-19 patients. The mortality rate was very high in patients who have both COVID-19 and C. auris candidemia.

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References

  1. Centers for Disease Control and Prevention. Infection Prevention and Control for Candida auris. https://www.cdc.gov/fungal/candida-auris/c-auris-infection-control.html. Accessed 2022, July 12.

  2. Kathuria S, Singh PK, Sharma C, Prakash A, Masih A, Kumar A, 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. J Clin Microbiol. 2015;53(6):1823–30. https://doi.org/10.1128/JCM.00367-15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kim TH, Kweon OJ, Kim HR, Lee MK. Identification of uncommon Candida species using commercial identification systems. J Microbiol Biotechnol. 2016;26(12):2206–13. https://doi.org/10.4014/jmb.1609.09012.

    Article  PubMed  Google Scholar 

  4. Di Pilato V, Codda G, Ball L, Giacobbe DR, Willison E, Mikulska M, 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(2). https://doi.org/10.3390/jof7020140

  5. 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(9):1780–1. https://doi.org/10.3201/eid2509.190686.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Rudramurthy SM, Chakrabarti A, Paul RA, Sood P, Kaur H, Capoor MR, et al. Candida auris candidaemia in Indian ICUs: analysis of risk factors. J Antimicrob Chemother. 2017;72(6):1794–801. https://doi.org/10.1093/jac/dkx034.

    Article  CAS  PubMed  Google Scholar 

  7. Hoenigl M, Seidel D, Sprute R, Cunha C, Oliverio M, Goldman GH, et al. COVID-19-associated fungal infections. Nat Microbiol. 2022;7(8):1127–40. https://doi.org/10.1038/s41564-022-01172-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Reslan L, Araj GF, Finianos M, El Asmar R, Hrabak J, Dbaibo G, et al. Molecular characterization of Candida auris isolates at a major tertiary care center in Lebanon. Front Microbiol. 2021;12:770635. https://doi.org/10.3389/fmicb.2021.770635

  9. Centers for Disease Control and Prevention (CDC), Tracking C.auris. https://www.cdc.gov/fungal/candida-auris/tracking-c-auris.html?CDC_AA_refVal=https%3A%2F%2Fwww.cdc.gov%2Ffungal%2Fdiseases%2Fcandidiasis%2Ftracking-c-auris.html. Accessed 21 July 2022.

  10. Jeffery-Smith A, Taori SK, Schelenz S, Jeffery K, Johnson EM, Borman A, et al. Candida auris: a Review of the Literature. Clin Microbiol Rev. 2018;31(1). https://doi.org/10.1128/CMR.00029-17

  11. Phua J, Weng L, Ling L, Egi M, Lim CM, Divatia JV, et al. Intensive care management of coronavirus disease 2019 (COVID-19): challenges and recommendations. Lancet Respir Med. 2020;8(5):506–17. https://doi.org/10.1016/S2213-2600(20)30161-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Komec S, Karabicak N, Ceylan AN, Gulmez A, Ozalp O. Three Candida auris case reports from Istanbul, Turkey. Mikrobiyol Bul. 2021;55(3):452–60. https://doi.org/10.5578/mb.20219814.

    Article  PubMed  Google Scholar 

  13. Bolukbasi Y, Erkose Genc G, Orhun G, Kuskucu MA, Cagatay A, Onel M, et al. First case of COVID-19 positive Candida auris Fungemia in Turkey. Mikrobiyol Bul. 2021;55(4):648–55. https://doi.org/10.5578/mb.20219716.

    Article  PubMed  Google Scholar 

  14. Kurt AF, Kuskucu MA, Balkan II, Baris A, Yazgan Z, Serife Oz A, et al. Candida auris Fungemia and a local spread taken under control with infection control measures: First report from Turkey. Indian J Med Microbiol. 2021;39(2):228–30. https://doi.org/10.1016/j.ijmmb.2021.03.007.

    Article  PubMed  Google Scholar 

  15. Centers for Disease Control and Prevention (CDC). C. auris: Antifungal susceptibility testing and interpretation, 2020. https://www.cdc.gov/fungal/candida-auris/c-auris-antifungal.html. Accessed May 29, 2020.

  16. Gosselin S, Fullmer MS, Feng Y, Gogarten JP. Expanding the utility of sequence comparisons using data from whole genomes. bioRxiv. 2020:2020.01.15.908137. https://doi.org/10.1101/2020.01.15.908137

  17. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49(W1):W293–6. https://doi.org/10.1093/nar/gkab301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Rhodes J, Fisher MC. Global epidemiology of emerging Candida auris. Curr Opin Microbiol. 2019;52:84–9. https://doi.org/10.1016/j.mib.2019.05.008.

    Article  PubMed  Google Scholar 

  19. Mirhendi H, Charsizadeh A, Aboutalebian S, Mohammadpour M, Nikmanesh B, de Groot T, et al. South Asian (Clade I) Candida auris meningitis in a paediatric patient in Iran with a review of the literature. Mycoses. 2022;65(2):134–9. https://doi.org/10.1111/myc.13396.

    Article  CAS  PubMed  Google Scholar 

  20. Chybowska AD, Childers DS, Farrer RA. Nine things genomics can tell us about Candida auris. Front Genet. 2020;11:351. https://doi.org/10.3389/fgene.2020.00351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Chen J, Tian S, Han X, Chu Y, Wang Q, Zhou B, et al. Is the superbug fungus really so scary? A systematic review and meta-analysis of global epidemiology and mortality of Candida auris. BMC Infect Dis. 2020;20(1):827. https://doi.org/10.1186/s12879-020-05543-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lone SA, Ahmad A. Candida auris-the growing menace to global health. Mycoses. 2019;62(8):620–37. https://doi.org/10.1111/myc.12904.

    Article  PubMed  Google Scholar 

  23. Kayaaslan B, Eser F, Kaya Kalem A, Bilgic Z, Asilturk D, Hasanoglu I, et al. Characteristics of candidemia in COVID-19 patients; increased incidence, earlier occurrence and higher mortality rates compared to non-COVID-19 patients. Mycoses. 2021;64(9):1083–91. https://doi.org/10.1111/myc.13332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Riche CVW, Cassol R, Pasqualotto AC. Is the frequency of Candidemia increasing in COVID-19 patients receiving corticosteroids? J Fungi (Basel). 2020;6(4). https://doi.org/10.3390/jof6040286

  25. Zhang Z, Zhu R, Luan Z, Ma X. Risk of invasive candidiasis with prolonged duration of ICU stay: a systematic review and meta-analysis. BMJ Open. 2020;10(7):e036452. https://doi.org/10.1136/bmjopen-2019-036452

  26. Public Health England. Guidance for the labrotory investigation, management and infection prevention and control for cases of Candida auris. . https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/637685/Updated_Candida_auris_Guidance_v2.pdf. Accessed 2017, August 11.

  27. Alsuhaibani M, Kobayashi T, McPherson C, Holley S, Marra AR, Trannel A, et al. Impact of COVID-19 on an infection prevention and control program, Iowa 2020–2021. Am J Infect Control. 2022;50(3):277–82. https://doi.org/10.1016/j.ajic.2021.11.015.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Prestel C, Anderson E, Forsberg K, Lyman M, de Perio MA, Kuhar D, et al. Candida auris Outbreak in a COVID-19 Specialty Care Unit—Florida, July–August 2020. MMWR Morb Mortal Wkly Rep. 2021;70(2):56–7. https://doi.org/10.15585/mmwr.mm7002e3

  29. Villanueva-Lozano H, Trevino-Rangel RJ, Gonzalez GM, Ramirez-Elizondo MT, Lara-Medrano R, Aleman-Bocanegra MC, et al. Outbreak of Candida auris infection in a COVID-19 hospital in Mexico. Clin Microbiol Infect. 2021. https://doi.org/10.1016/j.cmi.2020.12.030.

    Article  PubMed  PubMed Central  Google Scholar 

  30. 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. https://doi.org/10.1093/cid/ciw691.

    Article  CAS  PubMed  Google Scholar 

  31. Sharma C, Kumar N, Pandey R, Meis JF, Chowdhary A. Whole genome sequencing of emerging multidrug resistant Candida auris isolates in India demonstrates low genetic variation. New Microbes New Infect. 2016;13:77–82. https://doi.org/10.1016/j.nmni.2016.07.003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by Gilead Sciences.

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Authors and Affiliations

  1. Department of Infectious Disease and Clinical Microbiology, Marmara University School of Medicine, Istanbul, Turkey

    Buket Erturk Sengel, Elif Tukenmez Tigen, Aytan Seydaliyeva, Volkan Korten & Zekaver Odabasi

  2. Institute of Health Sciences, Department of Biostatistics and Bioinformatics, Acibadem University, Istanbul, Turkey

    Berkay Yekta Ekren & Ugur Sezerman

  3. Department of Medical Microbiology, Marmara University School of Medicine, Istanbul, Turkey

    Elvan Sayin & Nilgun Cerikcioglu

  4. Department of Anesthesiology and Reanimation, Critical Care, Marmara University School of Medicine, Istanbul, Turkey

    Ismail Cinel

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  1. Buket Erturk Sengel
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Correspondence to Buket Erturk Sengel.

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The authors declared no potential conflicts of interest with respect to the authorship and/or publication of this article.

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Marmara University School of Medicine Institutional Ethical Review Board issued approval 09.2021.578. The collected data did not include any patient or employee identifying information.

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Handling Editor: Macit Ilkit.

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Erturk Sengel, B., Ekren, B.Y., Sayin, E. et al. Nosocomial infection of C. auris in COVID-19 Intensive Care Unit in Türkiye and Phylogenetic Analysis of Isolates. Mycopathologia 188, 765–773 (2023). https://doi.org/10.1007/s11046-023-00782-6

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  • DOI: https://doi.org/10.1007/s11046-023-00782-6

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