Increasing prevalence, molecular characterization and antifungal drug susceptibility of serial Candida auris isolates in Kuwait
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Candida auris is an emerging yeast pathogen of global significance. Its multidrug-resistant nature and inadequacies of conventional identification systems pose diagnostic and therapeutic challenges. This study investigated occurrence of C. auris in clinical specimens in Kuwait and its susceptibility to antifungal agents. Clinical yeast strains isolated during 3.5-year period and forming pink-colored colonies on CHROMagar Candida were studied by wet mount examination for microscopic morphology and Vitek 2 yeast identification system. A simple species-specific PCR assay was developed for molecular identification and results were confirmed by PCR-sequencing of rDNA. Antifungal susceptibility testing of one isolate from each patient was determined by Etest. The 280 isolates forming pink-colored colonies on CHROMagar Candida, were identified by Vitek 2 as Candida haemulonii (n = 166), Candida utilis (n = 49), Candida kefyr (n = 45), Candida guilliermondii (n = 9), Candida famata (n = 6) and Candida conglobata (n = 5). Species-specific PCR and PCR-sequencing of rDNA identified 166 C. haemulonii isolates as C. auris (n = 158), C. haemulonii (n = 6) and Candida duobushaemulonii (n = 2). C. auris isolates originated from diverse clinical specimens from 56 patients. Of 56 C. auris isolates tested, all were resistant to fluconazole, 41/56 (73%) and 13/56 (23%) were additionally resistant to voriconazole and amphotericin B, respectively. Eleven (20%) isolates were resistant to fluconazole, voriconazole and amphotericin B. One isolate was resistant to caspofungin and micafungin. Increasing isolation of C. auris in recent years from diverse clinical specimens including bloodstream shows that C. auris is an emerging non-albicans Candida species in Kuwait causing a variety of infections. Inability of conventional identification methods to accurately identify this pathogen and multidrug-resistant nature of many strains calls for a greater understanding of its epidemiology, risk factors for acquiring C. auris infection and management strategies in high-risk patients. This is the first comprehensive study on the emergence of this multidrug-resistant yeast from Kuwait and the Middle East.
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The pitavastatin-fluconazole interactions were not sufficient to restore fluconazole activity in several fluconazole-resistant isolates; two C. albicans and four C. auris isolates maintained their resistance profiles to fluconazole.
“Of note, although pitavastatin was able to demonstrate broad-spectrum synergistic interactions with fluconazole, these interactions were not sufficient to restore the antifungal activity of fluconazole in several fluconazole-resistant isolates. Considering the current resistance breakpoints for azole drugs, two C. albicans and four C. auris isolates maintained their resistance profiles to fluconaz”
From Repurposing approach identifies pitavastatin as a potent azole chemosensitizing agent effective against azole-resistant Candida species (2020) · cites this paper as [32]
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Lockhart, S. R., Etienne, K. A., Vallabhaneni, S., Farooqi, J., Chowdhary, A., Govender, N. P., Colombo, A. L., Calvo, B., Cuomo, C. A., Desjardins, C. A., et al. (2017) · Clinical Infectious Diseases · doi:10.1093/cid/ciw691 · Cited by 1,662 · see citing works
Satoh, K., Makimura, K., Hasumi, Y., Nishiyama, Y., Uchida, K., & Yamaguchi, H. (2009) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2008.00083.x · Cited by 1,381 · see citing works
First hospital outbreak of the globally emerging Candida auris in a European hospital
Schelenz, S., Hagen, F., Rhodes, J. L., Abdolrasouli, A., Chowdhary, A., Hall, A., Ryan, L., Shackleton, J., Trimlett, R., Meis, J. F., et al. (2016) · Antimicrobial Resistance & Infection Control · doi:10.1186/s13756-016-0132-5 · Cited by 768 · see citing works
Chowdhary, A., Sharma, C., & Meis, J. F. (2017) · PLOS Pathogens · doi:10.1371/journal.ppat.1006290 · Cited by 750 · see citing works
Candida auris: a Review of the Literature
Jeffery-Smith, A., Taori, S. K., Schelenz, S., Jeffery, K. J., Johnson, E. M., Borman, A. M., Candida auris Incident Management Team, Manuel, R. J., & Brown, C. S. (2017) · Clinical Microbiology Reviews · doi:10.1128/cmr.00029-17 · Cited by 610 · see citing works
Chowdhary, A., Prakash, A., Sharma, C., Kordalewska, M., Kumar, A., Sarma, S., Tarai, B., Singh, A., Upadhyaya, G., Upadhyay, S., et al. (2018) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkx480 · Cited by 577 · see citing works
Kathuria, S., Singh, P. K., Sharma, C., Prakash, A., Masih, A., Kumar, A., Meis, J. F. G. M., & Chowdhary, A. (2015) · Journal of Clinical Microbiology · doi:10.1128/jcm.00367-15 · Cited by 536 · see citing works
Welsh, R. M., Bentz, M. L., Shams, A., Houston, H., Lyons, A., Rose, L. J., & Litvintseva, A. P. (2017) · Journal of Clinical Microbiology · doi:10.1128/jcm.00921-17 · Cited by 499 · see citing works
Incidence, characteristics and outcome of ICU-acquired candidemia in India
Chakrabarti, A., Sood, P., Rudramurthy, S. M., Chen, S., Kaur, H., Capoor, M., Chhina, D., Rao, R., Eshwara, V. K., Xess, I., et al. (2015) · Intensive Care Medicine · doi:10.1007/s00134-014-3603-2 · Cited by 454 · see citing works
Calvo, B., Melo, A. S. D. A., Mena, A. J. P., Hernandez, M., Francisco, E. C., Hagen, F., Meis, J. F. G. M., & Colombo, A. L. (2016) · Journal of Infection · doi:10.1016/j.jinf.2016.07.008 · Cited by 448 · see citing works
Candida auris: an Emerging Fungal Pathogen
Spivak, E. S., & Hanson, K. E. (2018) · Journal of Clinical Microbiology · doi:10.1128/jcm.01588-17 · Cited by 393 · see citing works
Multidrug-resistant endemic clonal strain of Candida auris in India
Chowdhary, A., Anil Kumar, V., Sharma, C., Prakash, A., Agarwal, K., Babu, R., Dinesh, K. R., Karim, S., Singh, S. K., Hagen, F., et al. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2027-1 · Cited by 373 · see citing works
Candida auris candidaemia in Indian ICUs: analysis of risk factors
Rudramurthy, S. M., Chakrabarti, A., Paul, R. A., Sood, P., Kaur, H., Capoor, M. R., Kindo, A. J., Marak, R. S. K., Arora, A., Sardana, R., et al. (2017) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkx034 · Cited by 357 · see citing works
Vallabhaneni, S., Kallen, A., Tsay, S., Chow, N., Welsh, R., Kerins, J., Kemble, S. K., Pacilli, M., Black, S. R., Landon, E., et al. (2016) · MMWR. Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm6544e1 · Cited by 302 · see citing works
Multidrug-Resistant <i>Candida haemulonii</i> and <i>C. auris</i> , Tel Aviv, Israel
Ben-Ami, R., Berman, J., Novikov, A., Bash, E., Shachor-Meyouhas, Y., Zakin, S., Maor, Y., Tarabia, J., Schechner, V., Adler, A., et al. (2017) · Emerging Infectious Diseases · doi:10.3201/eid2302.161486 · Cited by 297 · see citing works
Arendrup, M. C., Prakash, A., Meletiadis, J., Sharma, C., & Chowdhary, A. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00485-17 · Cited by 270 · see citing works
<i>Candida auris</i>–Associated Candidemia, South Africa
Magobo, R. E., Corcoran, C., Seetharam, S., & Govender, N. P. (2014) · Emerging Infectious Diseases · doi:10.3201/eid2007.131765 · Cited by 259 · see citing works
Vallabhaneni, S., Kallen, A., Tsay, S., Chow, N., Welsh, R., Kerins, J., Kemble, S. K., Pacilli, M., Black, S. R., Landon, E., et al. (2017) · American Journal of Transplantation · doi:10.1111/ajt.14121 · Cited by 247 · see citing works
Invasive Infections with Multidrug-Resistant Yeast Candida auris , Colombia
Morales-López, S. E., Parra‐Giraldo, C. M., Ceballos-Garzón, A., Martínez, H. P., Rodríguez, G. J., Álvarez, C., & Rodríguez, J. Y. (2016) · Emerging infectious diseases · doi:10.3201/eid2301.161497 · Cited by 244 · see citing works
Can Multidrug-Resistant Candidaauris Be Reliably Identified in Clinical Microbiology Laboratories?
Mizusawa, M., Miller, H., Green, R., Lee, R. E., Jr., Durante, M., Perkins, R., Hewitt, C. M., Simner, P. J., Carroll, K. C., Hayden, R. T., et al. (2016) · Journal of Clinical Microbiology · doi:10.1128/jcm.02202-16 · Cited by 218 · see citing works
Effectiveness of Disinfectants Against Candida auris and Other Candida Species
Cadnum, J. L., Shaikh, A., Piedrahita, C. T., Thriveen Sankar, C., Jencson, A. L., Larkin, E. L., Ghannoum, M. A., & Donskey, C. J. (2017) · Infection Control and Hospital Epidemiology · doi:10.1017/ice.2017.162 · Cited by 209 · see citing works
Kordalewska, M., Zhao, Y., Lockhart, S. R., Chowdhary, A., Berrío, I., & Perlin, D. S. (2017) · Journal of Clinical Microbiology · doi:10.1128/jcm.00630-17 · Cited by 195 · see citing works
Candida aurisCandidemia in Kuwait, 2014
Emara, M., Ahmad, S., Khan, Z., Joseph, L., Al-Obaid, I., Purohit, P., & Bafna, R. (2015) · Emerging infectious diseases · doi:10.3201/eid2106.150270 · Cited by 185 · see citing works
Self-citationCastanheira, M., Messer, S. A., Rhomberg, P. R., & Pfaller, M. A. (2016) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2016.02.009 · Cited by 159 · see citing works
Nosocomial fungemia by Candida auris: First four reported cases in continental Europe
Gaitán, A. C. R., Moret, A. M., Hontangas, J. L. L., Molina, J. M. R., López, A., Hernández-Cabezas, A., Maseres, J. B. M., Chouman-Arcas, R., Ruiz, M. D. G., Chiveli, M.-A., et al. (2017) · Revista Iberoamericana de Micología · doi:10.1016/j.riam.2016.11.002 · Cited by 158 · see citing works
Tsay, S. V., Kallen, A. J., Jackson, B. R., Chiller, T. M., & Vallabhaneni, S. (2017) · Clinical Infectious Diseases · doi:10.1093/cid/cix744 · Cited by 155 · see citing works
Abdolrasouli, A., Armstrong‐James, D., Ryan, L., & Schelenz, S. (2017) · Mycoses · doi:10.1111/myc.12699 · Cited by 150 · see citing works
Candida auris : An emerging multidrug-resistant pathogen
Sears, D., & Schwartz, B. S. (2017) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2017.08.017 · Cited by 146 · see citing works
Surface disinfection challenges for Candida auris: an in-vitro study
Kean, R., Sherry, L., Townsend, E. R., McKloud, E., Short, B., Akinbobola, A., Mackay, W. G., Williams, C., Jones, B., & Ramage, G. (2017) · Journal of Hospital Infection · doi:10.1016/j.jhin.2017.11.015 · Cited by 125 · see citing works
Khan, Z. U., Al‐Sweih, N., Ahmad, S., Al-Kazemi, N., Khan, S. I., Joseph, L., & Chandy, R. G. (2007) · Journal of Clinical Microbiology · doi:10.1128/jcm.00222-07 · Cited by 105 · see citing works
Self-citationPharmacodynamic Optimization for Treatment of Invasive Candida auris Infection
Lepak, A. J., Zhao, M., Berkow, E. L., Lockhart, S. R., & Andes, D. R. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00791-17 · Cited by 92 · see citing works
Lockhart, S. R., Jackson, B. R., Vallabhaneni, S., Ostrosky-Zeichner, L., Pappas, P. G., & Chiller, T. (2017) · Journal of Clinical Microbiology · doi:10.1128/jcm.01355-17 · Cited by 61 · see citing works
Kumar, A., Sachu, A., Mohan, K., Vinod, V., Dinesh, K. R., & Karim, S. (2017) · Revista Iberoamericana de Micología · doi:10.1016/j.riam.2016.11.004 · Cited by 60 · see citing works
Khan, Z. U., Ahmad, S., Hagen, F., Fell, J. W., Kowshik, T., Chandy, R. G., & Boekhout, T. (2009) · Antonie van Leeuwenhoek · doi:10.1007/s10482-009-9406-8 · Cited by 59 · see citing works
Self-citationActinomucor elegans var. kuwaitiensis isolated from the wound of a diabetic patient
Khan, Z. U., Ahmad, S., Mokaddas, E. M., et al. (2008) · Antonie van Leeuwenhoek · doi:10.1007/s10482-008-9251-1 · Cited by 58 · see citing works
Self-citationMalassezia pachydermatis fungemia in a preterm neonate resistant to fluconazole and flucytosine
Al‐Sweih, N., Ahmad, S., Joseph, L., et al. (2014) · Medical Mycology Case Reports · doi:10.1016/j.mmcr.2014.04.004 · Cited by 54 · see citing works
Self-citationAsadzadeh, M., Ahmad, S., Hagen, F., Meis, J. F. G. M., Al‐Sweih, N., & Khan, Z. (2015) · PLoS ONE · doi:10.1371/journal.pone.0142880 · Cited by 54 · see citing works
Self-citationEUCAST technical note on Amphotericin B
Lass-Flörl, C., Arendrup, M. C., Rodriguez-Tudela, J.-L., Cuenca-Estrella, M., Donnelly, P., & Hope, W. (2011) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2011.03644.x · Cited by 49 · see citing works
Ahmad, S., Mustafa, A. S., Khan, Z., et al. (2004) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2004.01.002 · Cited by 46 · see citing works
Self-citationKodamaea ohmeri as an emerging pathogen: a case report and review of the literature
Al‐Sweih, N., Khan, Z. U., Ahmad, S., et al. (2011) · Medical Mycology · doi:10.3109/13693786.2011.572300 · Cited by 45 · see citing works
Self-citationEpidemiology ofCandidacolonization in an intensive care unit of a teaching hospital in Kuwait
Ahmad, S., Khan, Z., Mustafa, A. S., & Khan, Z. (2003) · Medical Mycology · doi:10.1080/1369378031000147458 · Cited by 41 · see citing works
Self-citationAntifungal susceptibility of clinical Candida parapsilosis isolates in Kuwait
Asadzadeh, M., Al‐Sweih, N., Ahmad, S., & Khan, Z. U. (2008) · Mycoses · doi:10.1111/j.1439-0507.2008.01492.x · Cited by 30 · see citing works
Self-citationImportation, Mitigation, and Genomic Epidemiology of Candida auris at a Large Teaching Hospital
Lesho, E. P., Bronstein, M. Z., McGann, P., Stam, J. A., Kwak, Y. I., Maybank, R. A., McNamara, J., Callahan, M., Campbell, J., Hinkle, M. K., et al. (2017) · Infection Control and Hospital Epidemiology · doi:10.1017/ice.2017.231 · Cited by 29 · see citing works
Candida auris : An emerging multidrug-resistant pathogen of global significance
Khan, Z., & Ahmad, S. (2017) · Current Medicine Research and Practice · doi:10.1016/j.cmrp.2017.11.004 · Cited by 23 · see citing works
Self-citationAl‐Sweih, N., Ahmad, S., Joseph, L., Khan, S. I., Vayalil, S., Chandy, R. G., & Khan, Z. (2015) · Journal of Clinical Microbiology · doi:10.1128/jcm.03351-14 · Cited by 16 · see citing works
Self-citationAl‐Sweih, N., Ahmad, S., Khan, S., et al. (2017) · Journal de Mycologie Médicale · doi:10.1016/j.mycmed.2017.01.010 · Cited by 14 · see citing works
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- [42]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 1 9 doi: 10.1093/jac/dkx480 29325167 · DOI · Paper page
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- Authors
- Khan, Z., Ahmad, S., Al-Sweih, N., Joseph, L., Alfouzan, W., & Asadzadeh, M.
- Affiliations
- Kuwait University (KW)
- Corresponding author
- Khan, Ziauddin
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2018-04-09
- Volume
- 13
- Issue
- 4
- Pages
- e0195743
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5891028
- OpenAlex
- W2796525063
- Cited by
- 109
- References
- 46
- Citations by year
- 2026: 9 · 2025: 5 · 2024: 11 · 2023: 10 · 2022: 11 · 2021: 13 · 2020: 19 · 2019: 22 · 2018: 9
- FWCI
- 11.89
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Kuwait University Research Sector (MI01/15)
- 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, Candida haemulonii, Candida duobushaemulonii, non-albicans Candida, antifungal resistance, fluconazole resistance, voriconazole resistance, amphotericin B resistance, caspofungin resistance, micafungin resistance, molecular identification, species-specific PCR, rRNA gene sequencing, clinical isolates, bloodstream infection, emerging fungal pathogens, Kuwait
- MeSH terms
- Aged, 80 and over, Antifungal Agents, Candida, Candidiasis, Female, Humans, Kuwait, Microbial Sensitivity Tests, Prevalence
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