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Invasive infections with multidrug-resistant yeast Candida auris, Colombia.

Candida auris is an emerging multidrug-resistant fungus that causes a wide range of infections that are sometimes associated with high mortality rates (1-4). C. auris was first isolated in Japan and described as a new species in 2009 (5). In 2011, it was described as a cause of fungemia in South Korea (4) and was later isolated from patients in India (2), South Africa (6), Kuwait (3), and Venezuela (1).

We report 17 clinical isolates of C. auris recovered from 17 patients hospitalized in 6 institutions in the northern region of Colombia from February through July 2016. We reviewed patient medical records; analyzed microbiological, demographic, and clinical variables; and evaluated the mortality rate 30 days after yeast isolation. The initial pathogen identification was made with the method available at each institution: VITEK 2 system (bioMerieux, Marcy l'Etoile, France); Phoenix (Becton Dickinson, Franklin Lakes, New Jersey, USA); MicroScan AutoSCAN 4 and MicroScan Walkaway (Beckman Coulter, Brea, California, USA); and API Candida (bioMerieux) (Table). Given the unusual prevalence of C. haemulonii and discordance in the micromorphologic characteristics of some isolates, we cultured strains in CHROMagar Candida medium (CHROMagar Candida, Paris, France) and identified them by using matrix-assisted laser desorption/ionization time-of-fight (MALDI-TOF) mass spectrometry (Bruker Daltonik, Bremen, Germany). All the isolates showed pink colonies on CHROMagar Candida medium and were identified as C. auris by MALDI-TOF mass spectrometry (scores >2.0).

We tested yeast isolates for in vitro susceptibility by VITEK cards (caspofungin, micafungin, fluconazole, voriconazole, and amphotericin B). Additionally, we performed the agar diffusion method using Etest strips (bioMerieux, France) to amphotericin B according to the manufacturer's instructions. C. parapsilosis ATCC 22019 was used as the control. The range, mode, MIC50, and MIC90 were calculated.

Of the 17 patients, 9 were men (52.9%); age range was 0-77 years (median 36 years). Fifteen (88.2%) were hospitalized in intensive care units and 2 in medical wards; no patients were transferred between hospitals.

Blood samples from 13 (76.4%) patients showed fungemia; for the remaining 4, C. auris was isolated from peritoneal fluid, cerebrospinal fluid, bone, or urine (Table). Most patients had a central venous catheter (n = 16, 94.1%), a urinary catheter (n = 15, 88.2%), and mechanical ventilation (n = 10, 58.8%). Additionally, some had risk factors described previously for candidemia: erythrocyte transfusion (n = 12, 70.5%), parenteral nutrition (n = 8, 47%), abdominal surgery (n = 7, 41.1%), hemodialysis (n = 5, 29.4%), diabetes (n = 3, 17.6%), pancreatitis (n = 2, 11.7%), cancer (n = 2, 11.7%), and HIV infection (n = 1, 5.8%).

The average number of days from hospitalization to isolation of C. auris was 27.5 days (SD [+ or -] 19.9 days). Before the isolation of C. auris, 15 (88.2%) and 12 (70.6%) patients received broad-spectrum antimicrobial therapy and antifungal therapy, respectively. Of the latter, 8 received fluconazole, 2 caspofungin, 1 fluconazole and caspofungin, and 1 fluconazole, caspofungin, and anidulafungin (given at a different time periods) (Table). The time from isolation of C. auris to the initial application of effective antifungal therapy averaged 3.7 days. The 30-day mortality rate in all patients and in those who had fungemia was 35.2% and 38.4%, respectively.

C. auris is phylogenetically related to C. haemulonii, for which it is often mistaken with the methods currently used for identification (2-6). Our isolates were originally misidentified as C. haemulonii, C. famata, C. albicans, or C. tropicalis, depending on the method used in the hospital. The identification of isolates by MALDI-TOF mass spectrometry has also been described in the literature as an adequate and fast method for identifying C. auris (7).

Because the Clinical and Laboratory Standards Institute does not currently provide breakpoints for C. auris, no categorical interpretation of results is available; thus, only the MICs obtained for antifungal drugs tested in our study were indicated (Table). Although misleading, elevated MICs of amphotericin B by VITEK card have been previously described (7); this study also found discrepancies with Etest strips, which could lead to the selection of inappropriate therapy if only 1 method is used.

The presence of C. auris in these patients has clinical and epidemiologic implications, considering the associated mortality rate confirmed in this report and the absence of sufficient technology in clinical laboratories both to confirm their identification and to carry out testing for antifungal susceptibility. The lack of suitable diagnostics complicates patient treatment and changes on the empiric treatment of invasive Candida spp. infections are needed.

Our data contributes to the knowledge of the epidemiology of this species at a regional level. Although we had already reported Candida spp. in Colombia (8), no information regarding these species on the Caribbean coast is available. Given the association of Candida spp. with outbreaks in hospitals, according to the Centers for Disease Control and Prevention, it is necessary to further strengthen measures for fungal infection control to prevent possible spread.


We thank Laura Marcela Ramirez and Juan Sebastian Monroy for their technical support and Heidy Pinzon, Kelin Esquea, Liliana Gomez, Alba Mosquera, Yiceth Acosta, Yenixa Fuentes, Leandro Narvaez, Luis Rodrigo Ramirez, and Sindy Jimenez for providing the isolates.

Ms. Morales-Lopez is a bacteriologist and doctoral candidate in the Microbiology program at the Universidad de Buenos Aires, Argentina. She works as an associate teacher of medical microbiology at Universidad Popular del Cesar in Valledupar, Colombia. Her areas of interest are medical microbiology and antimicrobial drug resistance.


(1.) Calvo B, Melo ASA, Perozo-Mena A, Hernandez M, Francisco EC, Hagen F, et al. First report of Candida auris in America: clinical and microbiological aspects of 18 episodes of candidemia. J Infect. 2016; 73:369-74.

(2.) Chowdhary A, Sharma C, Duggal S, Agarwal K, Prakash A, Singh PK, et al. New clonal strain of Candida auris, Delhi, India. Emerg Infect Dis. 2013; 19:1670-3. eid1910.130393

(3.) Emara M, Ahmad S, Khan Z, Joseph L, Al-Obaid I, Purohit P, et al. Candida auris candidemia in Kuwait, 2014. Emerg Infect Dis. 2015; 21:1091-2.

(4.) Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, et al. First three reported cases of nosocomial fungemia caused by Candida auris. J Clin Microbiol. 2011; 49:3139-42.

(5.) Satoh 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; 53:41-4.

(6.) Magobo RE, Corcoran C, Seetharam S, Govender NP Candida auris-associated candidemia, South Africa. Emerg Infect Dis. 2014; 20:1250-1.

(7.) 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; 53:1823-30.

(8.) Parra C, LePape P, Ceballos A, Cortes G, Alvarez-Moreno C, Valderrama S, et al. Performance of MALDI-TOF MS for the identification of emerging yeast of hospital patients, species distribution, in a third level hospital Bogota-Colombia.

In: Abstracts of the 26th European Congress of Clinical Microbiology and Infectious Diseases; Amsterdam; 2016 Apr 9-12. Abstract 5556. Basel: European Congress of Clinical Microbiology and Infectious Diseases; 2016.

Address for correspondence: Jose Y. Rodriguez, Centro de Investigaciones, Microbiologicas del Cesar (CIMCE), Calle 16c no 19d-14 Barrio Dangond, Valledupar, Colombia; email:

Soraya E. Morales-Lopez, Claudia M. Parra-Giraldo, Andres Ceballos-Garzon, Heidys P. Martinez, Gerson J. Rodriguez, Carlos A. Alvarez-Moreno, Jose Y. Rodriguez

Author affiliations: Universidad Popular del Cesar, Valledupar, Colombia (S.E. Morales-Lopez, H.P. Martinez); Pontificia Universidad Javeriana, Bogota, Colombia (C.M. Parra-Giraldo, A. Ceballos-Garzon); Centro de Investigaciones Microbiologicas del Cesar (CIMCE), Valledupar, Colombia (G.J. Rodriguez, J.Y. Rodriguez); Clinica Laura Daniela, Valledupar (G.J. Rodriguez, J.Y Rodriguez); Universidad Nacional de Colombia, Bogota (C.A. Alvarez-Moreno); Clinica Universitaria Colombia, Colsanitas, Colombia (C.A. Alvarez-Moreno)

DOI: 10.3201/eid2301.161497
Table. Identification and antifungal susceptibilities of Candida
auris clinical isolates of six hospitals, northern region of
Colombia, 2016 *

Isolate   Hospital    Specimen    Biochemical identification   Pre-
ID          no.        origin              (system)            AFT

001          1         Blood        C. haemulonii (VITEK)      None
002          1          CSF        C. tropicalis (MicroScan    CAS
003          1         Blood       C. famata (API Candida)     FLC
004          5         Blood       C. haemulonii (Phoenix)     FLC
005          2         Blood        C. haemulonii (VITEK)      FLC
006          4         Blood        C. haemulonii (VITEK)      None
007          3       Peritoneal     C. albicans (MicroScan     FLC
                       fluid              autoSCAN)
008          2         Blood        C. haemulonii (VITEK)      FLC
009          1         Blood       C. tropicalis (MicroScan    FLC,
                                  Walkaway)/ C. famata (API    CAS
010          5          Bone        C. haemulonii (VITEK)      FLC,
011          6         Urine       C. haemulonii (Phoenix)     None
012          3         Blood        C. albicans (MicroScan     FLC
013          3         Blood        C. haemulonii (VITEK)      None
014          3         Blood        C. haemulonii (VITEK)      FLC
015          2         Blood        C. haemulonii (VITEK)      None
016          2         Blood        C. haemulonii (VITEK)      FLC
017          4         Blood        C. haemulonii (VITEK)      CAS
MIC (mg/L) range


Isolate           VITEK cards                        Etest/AMB
           FLC      MCF      CAS      VRC     AMB    24 h    48 h

001        16      0.12     <0.25    0.25      8     0.75     1
002        16      0.12     <0.25    <0.12     8     0.75     1

003        16      <0.06    <0.25    <0.12     8      1       1
004        16      0.12     <0.25    0.25     >16     1      1.5
005        >64     0.25      0.5       2      >16     1      1.5
006        >64     0.12     <0.25     0.5      8      1       1
007        16      0.12     <0.25    0.25      8      1      1.5

008        16      0.12     <0.25    0.25      8     0.38    0.75
009        32      0.12     <0.25    0.25      8      2       3

010        16      0.12     <0.25    0.25      8     0.75     1

011        32      0.12     <0.25    0.25      8     1.5     1.5
012        32      0.12     <0.25      1       8      1       2

013        32      0.12     <0.25      1       8     0.75     2
014        >64     0.12     <0.25      2       8     1.5     1.5
015        32      0.12     <0.25    0.25      8     0.75     2
016        >64     0.12     <0.25      2      >16     1       2
017        >64     0.12     <0.25      2      >16     2       4
MIC        16 to    <0.06    <0.25    <0.12   8 to    0.38    0.75
           >64    to 0.25   to 0.5   to 2     >16    to 2    to 4
MIC50      32      0.12     <0.25    0.25      8      1      1.5
MIC90      >64     0.12     <0.25      2      >16     2       2

* AFG, anidulafungin; AMB, amphotericin B; CAS, caspofungin; CSF,
cerebrospinal fluid; FLC, fluconazole; ID, identification; MCF,
micafungin; MIC50, minimal inhibitory concentration for 50% of yeast;
MIC90, minimal inhibitory concentration for 90% of yeast; Pre-AFT,
use of antifungal therapy before the isolation of C. auris; VRC,
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Article Details
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Author:Morales-Lopez, Soraya E.; Parra-Giraldo, Claudia M.; Ceballos-Garzon, Andres; Martinez, Heidys P.; R
Publication:Emerging Infectious Diseases
Geographic Code:3COLO
Date:Jan 1, 2017
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