International Journal of Antimicrobial Agents 59 (2022) 106558

Contents lists available at ScienceDirect

International Journal of Antimicrobial Agents

journal homepage: www.elsevier.com/locate/ijantimicag

Short Communication

Head-to-head comparison of CLSI, EUCAST, Etest and VITEK®2 results

for Candida auris susceptibility testing
Andrés Ceballos-Garzon a,b, Guillermo Garcia-Effron c, Susana Cordoba d, Jose Y. Rodriguez e,
Carlos Alvarez-Moreno f, Patrice Le Pape a, Claudia Marcela Parra-Giraldo b,∗,
Soraya Morales-López g,∗
a
Université de Nantes, Cibles et Médicaments des Infections et du Cancer, IICiMed, EA 1155, F-44000, Nantes, France
b
Unidad de Proteómica y Micosis Humanas, Grupo de Enfermedades Infecciosas, Departamento de Microbiología, Facultad de Ciencias, Pontificia
Universidad Javeriana, Bogotá D.C. 110231, Colombia
c
Laboratorio de Micología y Diagnóstico Molecular, Cátedra de Parasitología y Micología, Facultad de Bioquímica y Ciencias Biológicas, Universidad
Nacional del Litoral, Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Santa Fe, Argentina
d
Departamento Micología, Instituto Nacional de Enfermedades Infecciosas ‘Dr C. G. Malbrán’, Buenos Aires, Argentina
e
Centro de Investigaciones Microbiológicas del Cesar, CIMCE, Valledupar, Colombia
f
Facultad de Medicina, Universidad Nacional de Colombia, Clinica Universitaria Colombia, Clinica Colsanitas, Bogotá, Colombia
g
Grupo CINBIOS, Programa de Microbiología, Universidad Popular del Cesar, Valledupar, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: The susceptibility of 31 Candida auris clinical isolates was evaluated by four methods, namely the mi-
Received 16 November 2021 crodilution reference method according to Clinical and Laboratory Standards Institute (CLSI) and European
Accepted 20 February 2022
Committee on Antimicrobial Susceptibility Testing (EUCAST) guidelines as well as Etest and VITEK®2. Es-
sential agreement between the two reference methods was 90%. Etest showed a better overall agreement
Editor: Professor Emmanuel Roilides with the reference methods (94% and 81% for CLSI and EUCAST, respectively) than VITEK®2 (70% and
72%, respectively). Discrepancies were found for fluconazole (FLC) and amphotericin B. Considering cat-
Keywords:
Candida auris egorical agreement (CDC tentative breakpoints), the majority of isolates were considered FLC-resistant
Susceptibility testing (93.6% and 80.6% by CLSI and EUCAST, respectively). Furthermore, all isolates were considered susceptible
CLSI to echinocandins by all methods. Susceptibility results should be interpreted with care if the VITEK®2
EUCAST system is used to guide therapeutic decisions for C. auris infections.
Etest © 2022 Elsevier Ltd and International Society of Antimicrobial Chemotherapy. All rights reserved.

1. Introduction
Candida auris is considered a public-health threat of consider-
able interest owing to its rapid spread [1] and association with
COVID-19 (coronavirus disease 2019) patients [2]. Candidaemia
caused by C. auris is associated with high mortality rates (30–66%)
[3], due, at least in part, to difficulties in achieving a correct iden-
tification and to the variable patterns of antifungal susceptibility
that this species presents. To date, there are no phenotypic meth-
ods able to correctly identify all C. auris strains. One phenotypic
method is the VITEK®2 system (version 8.01) (bioMérieux) that
was alleged to identify C. auris, but it was demonstrated that its
capability is partial as it can only partially identify South American
and South Asian isolates [4]. Another example is the CHROMagarTM
Candida Plus chromogenic medium that is able to identify C. auris
∗
Corresponding authors.
E-mail addresses: Claudia.parra@javeriana.edu.co (C.M.
sorayaeugeniam@hotmail.com (S. Morales-López).
but is not able to differentiate closely related species (i.e. Candida
vulturna and Candida pseudohaemulonii can cause false-positive re-
sults) [5]. Thus, DNA sequencing and matrix-assisted laser desorp-
tion/ionisation time-of-flight (MALDI-TOF) are still required for re-
liable identification.
Another important issue regarding C. auris is its antifungal sus-
ceptibility profile. The vast majority of strains show high minimum
inhibitory concentrations (MICs) to fluconazole (FLC) and in some
cases also to amphotericin B (AMB) or echinocandins, resulting in
multidrug resistance [6]. Currently there are no specific suscep-
tibility cut-off values for C. auris established by the Clinical and
Laboratory Standards Institute (CLSI) or the European Committee
on Antimicrobial Susceptibility Testing (EUCAST). Therefore, the US
Centers for Disease Control and Prevention (CDC) established ten-
tative resistance breakpoints as follows: FLC, ≥32 μg/mL; AMB,
≥2 μg/mL; anidulafungin (ANF), ≥4 μg/mL; caspofungin (CSF),
≥2 μg/mL; and micafungin (MCF), ≥4 μg/mL [7]. In the clinical
setting, treatment decisions are guided by antifungal susceptibil-
Parra-Giraldo),
ity results obtained using commercial methodologies, since refer-

https://doi.org/10.1016/j.ijantimicag.2022.106558
0924-8579/© 2022 Elsevier Ltd and International Society of Antimicrobial Chemotherapy. All rights reserved.
A. Ceballos-Garzon, G. Garcia-Effron, S. Cordoba et al. International Journal of Antimicrobial Agents 59 (2022) 106558

Table 1
Antifungal activities of the eight tested drugs against Candida auris (n = 31) performed by CLSI, EUCAST, Etest and VITEK®2 methods

Drug Method No. (cumulative %) of C. auris strains with MIC (μg/mL) of:

0.015 0.03 0.06 0.12 0.25 0.5 1 2 4 8 >8

AMB CLSI 3 (9.7) 28 (100)

EUCAST 5 (16.1) 19 (77.4) 7 (100)
Etest 6 (19.4) 22 (90.3) 3 (100)
VITEK®2 3 (9.7) 0 (9.7) 2 (16.1) 6 (35.5) 13 (77.4) 7 (100)
ANF CLSI 6 (19.4) 5 (35.5) 16 (87.1) 2 (93.5) 2 (100)
EUCAST 1 (3.2) 13 (45.2) 10 (77.4) 4 (90.3) 1 (93.5) 1 (96.8) 0 (96.8) 1 (100)
CSF CLSI 5 (16.1) 6 (35.5) 7 (58.1) 6 (77.4) 3 (87.1) 4 (100)
EUCAST 3 (9.7) 8 (35.5) 9 (64.5) 7 (87.1) 2 (93.5) 1 (96.8) 1 (100)
Etest 1 (3.2) 4 (16.1) 17 (70.0) 9 (100)
VITEK®2 30 (96.8) 1 (100)
MCF CLSI 9 (29.0) 9 (58.1) 8 (83.9) 4 (96.8) 0 (96.8) 1 (100)
EUCAST 1 (3.2) 4 (16.1) 14 (61.3) 11 (96.8) 0 (96.8) 0 (96.8) 0 (96.8) 1 (100)
Etest 4 (12.9) 0 (12.9) 26 (96.8) 1 (100)
VITEK®2 4 (12.9) 0 (12.9) 26 (96.8) 1 (100)
ITC CLSI 1 (3.2) 2 (9.7) 9 (38.7) 6 (58.1) 12 (96.8) 0 (96.8) 1 (100)
EUCAST 2 (6.5) 2 (12.9) 6 (32.3) 6 (51.6) 15 (100)
PSC CLSI 1 (3.2) 0 (3.2) 3 (12.9) 9 (41.9) 17 (96.8) 1 (100)
EUCAST 2 (6.5) 6 (25.8) 7 (48.4) 6 (67.7) 5 (83.9) 5 (100)
VRC CLSI 2 (6.5) 0 (6.5) 0 (6.5) 18 (64.5) 10 (96.8) 1 (100)
EUCAST 2 (6.5) 3 (16.1) 5 (32.3) 11 (67.7) 8 (93.5) 0 (93.5) 2 (100)
Etest 1 (3.2) 0 (3.2) 9 (32.3) 8 (58.1) 6 (77.4) 7 (100)
VITEK®2 3 (9.7) 0 (9.7) 11 (45.2) 4 (58.1) 7 (80.6) 6 (100)
0.12 0.25 0.5 1 2 4 8 16 32 64 >64
FLC CLSI 2 (6.5) 0 (6.5) 29 (100)
EUCAST 3 (9.7) 3 (19.4) 1 (22.6) 10 (54.8) 14 (100)
Etest 2 (6.5) 0 (6.5) 1 (9.7) 28 (100)
VITEK®2 1 (3.2) 0 (3.2) 3 (12.9) 8 (38.7) 10 (71.0) 0 (71.0) 9 (100)

CLSI, Clinical and Laboratory Standards Institute; EUCAST, European Committee on Antimicrobial Susceptibility Testing; MIC, minimum inhibitory concentration; AMB, am-
photericin B; ANF, anidulafungin; CSF, caspofungin; MCF, micafungin; ITC, itraconazole; PSC, posaconazole; VRC, voriconazole; FLC, fluconazole.
a
MIC50 and MIC90 values (MICs at which ≥50% and ≥90% of the strains are inhibited, respectively) are depicted in bold and underlined, respectively.

ence methods are time-consuming and require several quality con-
trol steps and infrastructure that make them unsuitable for daily
routine [8]. Therefore, it is of great importance to compare anti-
fungal susceptibility results obtained using commercial and refer-
ence techniques. Consequently, the aim of the present study was
to evaluate the correlation of the antifungal susceptibility testing
(AST) results for C. auris obtained by the two commercial Etest and
VITEK®2 systems and the microdilution reference method follow-
ing CLSI and EUCAST guidelines.
2. Materials and methods
2.1. Isolates and identification
A total of 31 clinical isolates of C. auris were collected from in-
dividual patients in five tertiary care hospitals in Colombia from
2015–2018. Isolates were recovered from different samples includ-
ing urine (n = 5), blood (n = 24), cerebrospinal fluid (n = 1) and
abdominal fluid (n = 1). Moreover, 17 isolates (55%) were obtained
from men and 14 isolates (45%) were from women (Supplementary
Table S1). The isolate collection included strains isolated in differ-
ent Colombian cities, including the first isolates of C. auris reported
from an outbreak in the north and centre of the country [9,10]. Iso-
lates were identified using proteomic- and molecular-based meth-
ods i.e. MALDI-TOF mass spectrometry using the C. auris database
(in-house and Bruker Daltonics) [11] and by a single-tube PCR
method based on the amplification of internal transcribed spacer
(ITS) regions [12].
2.2. Antifungal susceptibility testing
Reference AST was carried out following the CLSI document
M27Ed4 [13] and EUCAST E.Def 7.3.2 [14]. Antifungal drugs in-
cluded AMB, FLC, itraconazole (ITC), posaconazole (PSC), voricona-
zole (VRC), ANF, CSF and MCF. Etest® (bioMérieux, Marcy-l’Étoile,
France) and VITEK®2 (bioMérieux) protocols were performed fol-
lowing the manufacturer’s instructions. Candida krusei ATCC 6258
and Candida parapsilosis ATCC 22019 were used as quality control
strains. MIC, MIC50 and MIC90 values were established, and essen-
tial agreement (EA) was considered as discrepancies in MIC re-
sults of no more than ±2 serial two-fold dilutions [15]. Categori-
cal agreement was determined following the CDC’s tentative cut-
off values determined using CLSI [7]. When interpretative break-
points existed, discrepancies were considered as very major error
(VME) when reference methods categorised a strain as resistant
and the commercial method as susceptible (false susceptibility),
and major error (ME) when reference methods classified the iso-
late as susceptible and the commercial method as resistant (false
resistance). Results were analysed by one-way analysis of variance
(ANOVA) with Tukey’s correction for multiple comparisons on log2
MICs (significance, P < 0.05) using GraphPad Prism software v.8.0.1
(GraphPad Software Inc., La Jolla, CA, USA).
3. Results and discussion
Susceptibility results obtained by the reference methods
showed a good correlation within two dilutions (90% EA for CLSI
vs. EUCAST) (Table 1). For ITC and PSC, MIC90 values were the same
by both reference methods. In contrast, for MCF, VRC and ANF,
MIC90 values were 1-fold lower by EUCAST; and for AMB and FLC,
MIC90 values were 1-fold higher by EUCAST. Notably, the MIC90
value for CSF was 2-fold lower by EUCAST. The ANF MIC range was
wider when tested by EUCAST than by CLSI. On the other hand,
MIC50 values were equal for AMB, MCF, ITC and FLC, while they
were 1-fold lower for ANF, CSF and VRC. Regarding commercial
methods, EA for MICs was high by Etest (94% and 81% vs. CLSI and

2
A. Ceballos-Garzon, G. Garcia-Effron, S. Cordoba et al. International Journal of Antimicrobial Agents 59 (2022) 106558

Fig. 1. In vitro antifungal susceptibilities of 31 clinical Candida auris isolates, with categorical classification following US Centers for Disease Control and Prevention (CDC)
cut-off values. The grey and blue colours indicate susceptibility (S) and resistance (R) grades, respectively. A P-value of <0.05 was used to indicate statistical significance as
follows. ∗ P ≤ 0.05; ∗ ∗ P ≤ 0.01; ∗ ∗ ∗ P ≤ 0.001; ∗ ∗ ∗ ∗ P ≤ 0.0 0 01. CLSI, Clinical and Laboratory Standards Institute; EUCAST, European Committee on Antimicrobial Susceptibility
Testing; AMB, amphotericin B; CSF, caspofungin; ANF, anidulafungin; MCF, micafungin; FLC, fluconazole.

EUCAST, respectively) but low by VITEK®2 (70% and 72%, respec-
tively).
The range of AMB MICs was as narrow for Etest as for reference
methods (0.5–1 μg/mL for CLSI and 0.5–2 μg/mL for EUCAST and
Etest). Moreover, these three methods showed equal MIC50 val-
ues (1 μg/mL) and very similar MIC90 values (1 μg/mL for CLSI
and Etest and 2 μg/mL for EUCAST). In contrast, AMB MICs ob-
tained by VITEK®2 ranged from 0.5 μg/mL to >8 μg/mL, and the
MIC50 and MIC90 values were ≥8-fold higher than those obtained
by other methods. Despite the described similarities in the MICs
obtained by CLSI, EUCAST and Etest, some discrepancies in inter-
pretation of the AMB results were observed. Indeed, while no resis-
tance was reported for AMB by CLSI (CDC tentative cut-off), seven
(22.6%) and three (9.7%) isolates were considered AMB-resistant by
EUCAST and Etest, respectively, exhibiting a high number of ME.
Categorical differences were much more pronounced for VITEK®2
since all of the C. auris isolates but three were considered AMB-
resistant (90.3% and 83.9% ME using CLSI and EUCAST as reference
method, respectively) (Fig. 1).
Based on the CDC tentative breakpoints, the majority of iso-
lates were considered FLC-resistant (93.6% and 80.6% by CLSI and
EUCAST, respectively). Although there were no significant differ-
ences between the two reference methodologies (P = 0.9965), MIC
ranges were wider by EUCAST than by CLSI method (8 to >64
μg/mL and 16–64 μg/mL, respectively) and four VME in EUCAST
were detected. By contrast, similar CLSI data were obtained by
Etest (FLC MIC50 and MIC90 >64 μg/mL, ranging from 16 μg/mL to
>64 μg/mL) with 29 resistant strains. On the other hand, VITEK®2
showed a wider FLC MIC range (2 to >64 μg/mL) and a 2-fold
lower MIC50 value. Within this range, 12 VME (38.7%) were de-
tected (FLC-susceptible by VITEK®2 and FLC-resistant by the refer-
ence methods).
Since no CDC tentative breakpoints for other triazoles were pro-
posed, Candida glabrata epidemiological cutoff values published by
the CLSI were applied [16]. In these conditions, our C. auris isolates
exhibited high rates of resistance to VRC but susceptibility to PSC
and ITC, and a very high CLSI/Etest correlation for VRC. Finally, all
of the tested isolates were considered susceptible to echinocandins
by all methods.
In general, MIC data for C. auris reported worldwide have been
based on CLSI and only a few, limited to AMB, have been based
on EUCAST [17]. However, MICs obtained by the CLSI and EUCAST
methods have shown good correlation results for Candida species,
including C. auris [17,18]. Our results also demonstrated a high EA
between the two reference methodologies, as described by Aren-
drup et al [17].
However, the latter proposed epidemiological cut-off (ECOFF)
values and derivatives of these (dECOFF) for categorical interpre-
tation using CLSI and EUCAST. Nevertheless, these need to be fur-
ther evaluated in multicentre studies with MIC data from differ-

3
A. Ceballos-Garzon, G. Garcia-Effron, S. Cordoba et al.
Fig. 2. Categorical classification following Clinical and Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST) epi-
demiological cut-off values proposed by Arendrup et al [17].. The grey and blue bars indicate susceptibility (S) and resistance (R) grades, respectively. AMB, amphotericin B;
ANF, anidulafungin; MCF, micafungin; ITC, itraconazole; VRC, voriconazole; FLC, fluconazole.
ent countries, as only Indian isolates were included. For instance,
Ruiz-Gaitán et al. compared AST in 73 Spanish isolates of C. auris
using EUCAST, Sensititre® YeastOne® (SYO) and Liofilchem® MIC
Test Strip methods (EA > 90% between EUCAST and SYO); they
used the ECOFFs proposed by Arendrup et al. to determine cate-
gorical agreement with the Spanish isolates and with data from
other studies, including our own [19].
Here, applying those ECOFFs, we found some discrepancies in
categorical classification compared with the results obtained us-
ing the CDC cut-off values, mainly for AMB, which resulted in all
but five strains being classified as resistant by EUCAST, contrary to
what was observed when using the ECOFFs (CLSI) and CDC cut-off
values. Overall, isolates were found to be susceptible to echinocan-
dins, which is consistent with the categorisation obtained when
the CDC cut-off values were applied. Regarding ITC and VRC, all
but one were categorised as sensitive, evidencing a good correla-
tion (Fig. 2).
On the other hand, Etest MICs were comparable with the results
obtained by CLSI and EUCAST, with most of our C. auris strains
being FLC-resistant but susceptible to echinocandins as previously
described [9,10].
These strains also showed high MICs to VRC, mirroring C.
glabrata susceptibility patterns [20]. VITEK®2 showed a good cor-
relation for echinocandins, but analysis of AMB and FLC MIC results
showed >83% ME and 38.7% VME, respectively.
We are aware that a weakness of our study was not having C.
auris strains from all four phylogenetic clades (only South Amer-
ican strains, commonly clade IV), however the strains were ob-
tained from different cities in Colombia and displayed different
susceptibility profiles. Therefore, the results obtained are relevant
and highlight the failure of a conventional susceptibility testing
4
International Journal of Antimicrobial Agents 59 (2022) 106558
method commonly used in the hospital setting compared with the
reference method.
In conclusion, this study demonstrates the possibility of
misidentifying C. auris antifungal resistance in routine microbiol-
ogy laboratories, highlighting that the susceptibility of C. auris to
FLC and AMB should be interpreted with care if VITEK®2 is used
to guide therapeutic decisions.
Acknowledgment
The authors wish to thank Campus France (Eiffel scholarship).
Funding
This work was financed by the Research Vice Presidency of the
Pontificia Universidad Javeriana [grant ID 20291] and MINCIENCIAS
807–2018 [Code 120380763646] in Bogotá, Colombia to CMPG;
the Ministerio de Ciencia y Tecnología Argentina [grant PICT-2016-
1985] to GGE; the Instituto Nacional de Enfermedades Infecciosas
Malbrán to SC; and the Universidad Popular del Cesar to SML.
Competing interests
PLP has received grants from Astellas, Basilea, MSD and Pfizer
and speaker’s fees from Gilead, Basilea, Pfizer and MSD. All other
authors declare no competing interests.
Ethical approval
Not required.
A. Ceballos-Garzon, G. Garcia-Effron, S. Cordoba et al.
Supplementary materials
Supplementary material associated with this article can be
found, in the online version, at doi:10.1016/j.ijantimicag.2022.
106558.
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