Emerg Infect DisEmerging Infect. DisEIDEmerging Infectious Diseases1080-60401080-6059Centers for Disease Control and Prevention24963796407387613-176510.3201/eid2007.131765Letters to the EditorLetterCandida auris–Associated Candidemia, South AfricaCandida auris, South AfricaMagoboRindidzani E.CorcoranCraigSeetharamSharonaGovenderNelesh P.National Institute for Communicable Diseases, Johannesburg, South Africa (R.E. Magobo, N.P. Govender); National Health Laboratory Service, Johannesburg, South Africa (S. Seetharam); University of the Witwatersrand, Johannesburg (S. Seetharam, N.P. Govender); Ampath National Reference Laboratory, Pretoria, South Africa (C. Corcoran)Address for correspondence: Nelesh P. Govender, National Institute for Communicable Diseases–Centre for Opportunistic, Tropical and Hospital Infections, Private Bag X4, Sandringham, 2132, South Africa; email: neleshg@nicd.ac.za7201420712501252Keywords: Candida aurisSouth Africacandidemia, fungal

To the Editor: We noted the report by Chowdhary et al. (1) and report Candida auris as a causative agent of candidemia in South Africa, with an estimated prevalence of 0.3% (N.P. Govender et al., unpub. data). First isolated in 2009, C. auris is an emerging species associated with clinical disease (26). We analyzed 4 isolates submitted to the National Institute for Communicable Diseases (Johannesburg, South Africa) from 4 patients with candidemia who had been admitted to different public- and private-sector hospitals from October 2012 through October 2013.

Identification of the isolates was undertaken by using ChromAgar Candida medium (Mast Diagnostics, Merseyside, UK), Vitek-2 YST (bioMérieux, Marcy ľEtoile, France), API 20C AUX (bioMérieux), and sequencing of internal transcribed spacer (ITS) and D1/D2 domains of the ribosomal RNA gene (7), followed by microbroth dilution susceptibility testing (8). All isolates were misidentified as C. haemulonii and Rhodotorula glutinis by Vitek-2 YST and API 20C AUX assays, respectively (Table).

Identification and antifungal susceptibility results of 4 <italic>Candida auris</italic> isolates from 4 male patients with candidemia, South Africa, October 2012–October 2013*
Isolate IDPatient age, yHospital unitVitek-2 YST†API 20C AUX†DNA sequence analysis‡MIC
AMBFLXVRCPOSITC5FCCASMFGAFG
20885High-careC. haemuloniiRhodotorula glutinisC. auris1>2560.50.030.120.120.250.060.25
20960Medical ICUC. haemuloniiR. glutinisC. auris0.5>25610.060.120.120.120.060.12
22473BurnC. haemuloniiR. glutinisC. auris1>25620.060.250.120.250.120.25
29327Trauma ICUC. haemuloniiR. glutinisC. auris1640.250.0150.060.060.030.060.06

*AMB, amphotericin B; FLX, fluconazole; VRC, voriconazole; POS, posaconazole; ITC, itraconazole; 5FC, flucytosine; CAS, caspofungin; MFG, micafungin; AFG, anidulafungin.
†bioMérieux, Marcy ľEtoile, France.
‡Sequence data for the 4 isolates have been deposited in GenBank, accession nos. KJ1236762–KJ126765 and KJ126758–KJ126761 for the internal transcribed spacer and D1/D2 regions, respectively.

Similar to the findings of Chowdhary et al., all isolates assimilated N-acetyl-glucosamine (1). With the use of the CBS-KNAW database, pairwise sequence alignment of ITS region showed 99% sequence homology to Kuwait isolates, and alignment of D1/D2 domain showed 98% homology to the Kuwait/India isolates (9). In a neighbor-joining phylogenetic tree based on ITS sequences, South Africa isolates formed a cluster with India and Kuwait isolates (Technical Appendix Figure).

Fluconazole MICs were high for all isolates (Table). Isolates 209 and 224 showed reduced voriconazole susceptibility with MICs of 1 μg/mL and 2 μg/mL, respectively, which is above the epidemiologic cutoff value for 11 Candida species (10). Isolates were susceptible to amphotericin B and echinocandins at low MICs Clinical data were available for 1 patient (Technical Appendix Table). Two C. haemulonii isolates were identified during laboratory-based sentinel surveillance for candidemia in South Africa; the ITS region of one isolate was sequenced and the isolate identified as C. auris (N.P. Govender, pers. comm.). In this study, C. auris was misidentified by routinely used tests and was accurately identified by sequencing, in keeping with previous findings (1,3,4,6).

Technical Appendix

Phylogenetic relatedness of internal transcribed spacer region of the ribosomal RNA gene of Candida auris with closely related Candida species and clinical characteristics of a patient with candidemia caused by C. auris, South Africa.

Suggested citation for this article: Magobo RE, Corcoran C, Seetharam S, Govender NP. Candida auris–associated candidemia, South Africa [letter]. Emerg Infect Dis [Internet]. 2014 Jul [date cited]. http://dx.doi.org/10.3201/eid2007.131765

Acknowledgments

We thank Serisha Naicker for technical assistance.

The work was supported by the National Institute for Communicable Diseases. N.P.G. has received honoraria from MSD (Pty) Ltd South Africa (Merck) and Pfizer for speaking engagements and has received a research grant from Pfizer South Africa.

ReferencesChowdhary A, Sharma C, Duggal S, Agarwal K, Prakash A, Kumar Singh P, New clonal strain of Candida auris, Delhi, India. Emerg Infect Dis. 2013;19:16703 . 10.3201/eid1910.13039324048006Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K, Yamaguchi H. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol Immunol. 2009;53:414 10.1111/j.1348-0421.2008.00083.x19161556Kim MN, Shin JH, Sung H, Lee K, Kim EC, Roy N, Candida haemulonii and closely related species at 5 university hospitals in Korea: identification, antifungal susceptibility, and clinical features. Clin Infect Dis. 2009;48:e5761 10.1086/59710819193113Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, First three reported cases of nosocomial fungemia caused by Candida auris. J Clin Microbiol. 2011;49:313942 10.1128/JCM.00319-1121715586Oh BJ, Shin JH, Kim MN, Sung H, Lee K, Joo MY, Biofilm formation and genotyping of Candida haemulonii, Candida pseudohaemulonii, and a proposed new species (Candida auris) isolates from Korea. Med Mycol. 2011;49:98102 10.3109/13693786.2010.49356320560864Chowdhary A, Kumar VA, Sharma C, Prakash A, Agarwal K, Babu R, Multidrug resistant endemic clonal strain of Candida auris in India. Eur J Clin Microbiol Infect Dis. 2013 Epub ahead of print.White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press; 1990 p. 315–22.Clinical and Laboratory Standards Institute. Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard. 3rd ed. Wayne (PA): The Institute; 2008CBS-KNAW Fungal Biodiversity Centre. Pairwise sequence alignment tool [cited 2013 Nov 1]. http://www.cbs.knaw.nl/Collections/BioloMICSSequences.aspx?file=allPfaller MA, Diekema DJ. Progress in antifungal susceptibility testing of Candida spp. by use of Clinical and Laboratory Standards Institute broth microdilution methods, 2010 to 2012. J Clin Microbiol. 2012;50:284656 10.1128/JCM.00937-1222740712