| |

Received: 7 December 2016    Revised: 22 February 2017    Accepted: 23 February 2017

DOI: 10.1111/myc.12617

REVIEW ARTICLE

Otomastoiditis caused by Candida auris: Case report and

literature review

Hyoung Il Choi | Jin An | Jae Joon Hwang | Soo-youn Moon  | Jun Seong Son

Department of Internal Medicine, Kyung Hee

University Hospital at Gangdong, Seoul, Korea
Correspondence
Jun Seong Son, MD, PhD, Division of
Infectious Diseases, Kyung Hee University
Hospital at Gangdong, Seoul, Korea.
Email: isonjs@naver.com
Summary
Fungal otomastoiditis is a rare disease, but can be fatal for immunocompromised pa-
tients. Recently, there have been increasing cases of otologic infection caused by
Candida auris. Candida auris can be easily misdiagnosed for other species and treat-
ment is difficult due to multidrug resistance. Clinician should be aware of this rare
pathogen, and it should be treated with appropriate antifungal agent with surgical
debridement.

KEYWORDS
Candida auris, fungal otomastoiditis, multidrug resistance

1 |  INTRODUCTION
Fungal otomastoiditis is a rare infectious disease. The diagnosis of
fungal otomastoiditis requires an experienced clinical suspicion. In
patients who have prolonged otorrhoea, otalgia and progressive
audio-­vestibular symptoms despite adequate antibacterial therapy,
the possibility of fungal infection should be considered.1 Aspergillus fu-
migatus is considered the most common causative organism of fungal
otomastoiditis.2 So far, the otologic infections caused by Candida auris
are not common and reported in 15 patients from Korea and 1 patient
from Japan in 2009.3,4 In this report, we describe C. auris otomastoid-
itis and its role as a newly emerging causative organism.
2 |  THE STUDY
On 5 August 2013, a 54-­year-­old man with a history of pontine
haemorrhage 3 months prior visited the emergency department for
fever. When he arrived at the emergency department, he was stu-
porous, and physical examination revealed bloody discharge in his
left ear. The patient had a blood pressure of 111/85 mm Hg, and
a temperature of 36.8°C. Routine laboratory tests revealed a white
blood cell count of 54 600 /μL, and a C-­reactive protein level of
4.16 mg/dL. The temporal computed tomography (CT) scan showed
bilateral acute otomastoiditis (Figure 1A). The attending physician
prescribed the empirical meropenem and vancomycin for possible
sepsis. Culture of the ear discharge and blood failed to reveal any
causative organism.
On the eighth day of hospitalisation, discharge in left ear was still
present. Ear discharge cultures were repeated, and Candida haemulonii
was identified by VITEK® 2 (bioMérieux, France). This fungus was con-
firmed to be C. auris by molecular identification. A portion of the large
subunit (LSU) rRNA gene was amplified and sequenced. The deter-
mined sequences were compared with the Gen-­Bank public database
using the BLASTn program (http://blast.ncbi.nlm.nih.gov/Blast.cgi).
The antifungal susceptibility test was done for fluconazole, amphoter-
icin B, itraconazole, voriconazole and caspofungin using microdilution
methods according to CLSI guidelines.5 The isolate was susceptible to
fluconazole with MIC of 4 μg/ml. The MIC for amphotericin B, itracon-
azole, voriconazole and caspofungin were 0.12 μg/mL, <0.03 μg/mL,
<0.03 μg/mL and 0.06 μg/mL respectively (Table 1).
On the 41st day of hospitalisation, follow-­up CT scan showed no
improvement in the bilateral otomastoiditis (Figure 1B). Therefore,
ventilation tube was inserted and surgical debridement was per-
formed for infection control. Culture of the surgical specimen revealed
the Candida species again and pathological testing revealed chronic
active inflammation with granulation tissue. The attending physician
prescribed an antifungal agent (fluconazole 300 mg IV once a day), and
empirical antibiotics were discontinued.
On 19 December, the 76th day of hospitalisation, the patient was
discharged with symptomatic improvement. The antifungal treatment
was continued orally (fluconazole 300 mg po once a day) for 143 days.

Mycoses. 2017;1–5. © 2017 Blackwell Verlag GmbH |  1

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2       CHOI et al.

(A) (B) (C)

F I G U R E   1   CT findings of the otomastoiditis.(A) The patient’s temporal bone computed tomography. Fluid in both mastoid air cells. (arrow)
Bilateral acute otomastoiditis. (B) The patient’s second follow-­up temporal bone computed tomography. Remained fluid in both mastoid air
cells (arrows). Bilateral otomastoiditis. (C) After treated to long-­term antifungal agent, the patient’s third follow-­up temporal bone computed
tomography. Well aeration of temporal bone and tympanic cavities without any finding related with inflammation. (arrows)

On 12 February 2014, the patient remained stable after discon-
tinuation of antifungal treatment. Follow-­up CT showed the tympanic
cavities without any inflammatory findings (Figure 1C).
3 |  DISCUSSION
Fungal otomastoiditis is rare and most cases have been reported in
immunocompromised patients. Risk factors for invasive fungal disease
include cytotoxic drugs, irradiation, prolonged neutropenia, graft-­vs-­
host disease, T-­cell immunodeficiency, broad-­spectrum antibiotics,
systemic corticosteroids, prolonged hospitalisation, and status and
type of underlying malignancy.6 It can occur as a primary infection
or in conjunction with a bacterial infection, usually as a result of pro-
longed antibiotic treatment. Khanna et al.7 reported that a pure fun-
gal infection was observed in only 9.0% of chronic suppurative otitis
media cases.
The most common fungal pathogens of otomastoiditis are
Aspergillus species (A. flavus and A. fumigatus). Other fungal patho-
gens are Candida, Mucor, Blastomyces, Scedosporium apiospermum and
Lecythophora hoffmannii.1 Most cases of Aspergillus species otomas-
toiditis were diagnosed in immunocompromised patients and treated
with long-­term systemic antifungal therapy and surgical debridement.8
Typically, when Candida is isolated in ear discharge, it is frequently
presumed to be colonisation or contamination. However, in our case,
C. auris was isolated in ear discharge repeatedly and also in the closed
deep tissue specimen. Furthermore, after initiating antifungal treat-
ment, clinical improvement was observed in the patient.
Candida auris is a rare, non-­albicans Candida species, and it does
not frequently cause human infection. However, it has been increas-
ingly reported. Most cases are mainly related to otologic infection and
systemic fungal infection. The first case of C. auris infection was re-
ported in Japan in 2009, and it was isolated from a patient with ex-
ternal otitis. Subsequently, isolation of C. auris from ear specimens of
15 patients with chronic otitis media was reported in South Korea in
2009. Since then, several cases of fungaemia caused by C. auris have
been also reported (Table 1).
Candida auris is notable for its resistance to azole antifungal agents
and its potential for clonal transmission.9 Isolation of C. auris is very
difficult because it cannot be well differentiated by current culture
methods, and it should be based on molecular methods such as PCR
sequencing analysis.10 Candida auris is commonly misidentified as
C. haemulonii by routine identification systems by VITEK® (bioMérieux,
France). Candida haemulonii is also known to be resistant to amphoteri-
cin B and azoles.11 In our case, culture of the surgical specimen initially
revealed the presence of C. haemulonii. However, it was confirmed to
be C. auris using molecular identification testing.
Although C. haemulonii and C. auris differ in susceptibility to ampho-
tericin B, both organisms were known to be resistant to azole antifun-
gal agents.12 Chowdhary et al.11 reported the susceptibility of C. auris
for various antifungal agents by in vitro antifungal susceptibility testing.
In that study, all isolates (15 C. auris) were resistant to fluconazole, and
11 isolates were resistant to voriconazole. Also, 47% of C. auris isolates
were resistant to flucytosine, and 40% had high minimum inhibitory
concentration (MIC) (≥1 μg/mL) of caspofungin. However, amphoteri-
cin B and anidulafungin showed good activity against C. auris.
The treatment of fungal otomastoiditis is not easy. It is necessary
to combine surgical debridement with the appropriate use of systemic
antifungal agents.2 Although C. auris in our case was susceptible to flu-
conazole, choosing fluconazole for empirical treatment of fungal oto-
mastoiditis would be worrisome because of resistance. Considering
the various resistances of C. auris, the treatment regimen should be
based on antifungal susceptibility results.
In conclusion, C. auris is an emerging opportunistic pathogen in
otologic infections. If a Candida species such as C. auris or C. haemu-
lonii is isolated in a patient with otologic infection, the clinician should
choose the appropriate antifungal agent according to susceptibility re-
sults and combine this therapy with surgical debridement.
T A B L E   1   Thirty-­five cases of Candida auris infections in the literatures

MIC (μg/mL)
CHOI et al.

Antifungal Final
Year of report Author Patient no. Age/Sex Isolation site regimen outcome AMB FLU ITR VRC CAS MFG AFG
3
2009 Kim et al. 1 NA Ear discharge NA NA 1 128 2 1 0.125 0.03 NA
2 NA Ear discharge NA NA 1.5 128 2 0.5 0.25 0.06 NA
3 NA Ear discharge NA NA 0.75 8 0.5 0.125 0.125 0.03 NA
4 NA Ear discharge NA NA 1.5 128 2 2 0.25 0.03 NA
5 NA Ear discharge NA NA 0.5 128 2 1 0.25 0.03 NA
6 NA Ear discharge NA NA 0.38 64 1 0.5 0.125 0.03 NA
7 NA Ear discharge NA NA 0.38 64 2 1 0.25 0.03 NA
8 NA Ear discharge NA NA 0.75 32 1 0.25 0.25 0.03 NA
9 NA Ear discharge NA NA 1.5 4 0.125 0.03 0.125 0.03 NA
10 NA Ear discharge NA NA 1 4 0.25 0.03 0.125 0.03 NA
11 NA Ear discharge NA NA 1 2 0.25 0.03 0.125 0.03 NA
12 NA Ear discharge NA NA 1.5 4 0.125 0.03 0.125 0.03 NA
13 NA Ear discharge NA NA 0.75 4 0.125 0.06 0.25 0.03 NA
14 NA Ear discharge NA NA 1.5 64 4 2 0.25 0.03 NA
2009 Satoh et al.4 15 70 y/F Ear discharge NA NA NA 2 0.063 0.031 NA NA NA
9
2011 Lee et al. 16 1 y/F Blood AMB/FLU Recovery 0.5 128 2 1 0.06 0.03 NA
17 74 y/M Blood, CVC FLU/AMB Expire 0.5 128 2 1 0.06 0.03 NA
18 1 y/M Blood FLU/AMB Expire 1 2 0.125 0.03 0.06 0.03 NA
2013 Chowdhary et al.13 19 3 d/F Blood CAS Expire 0.25-­1 16-­64 0.125-­0.25 0.125-­1 0.125-­ 0.06-­ 0.125-­
20 10 d/F Blood AMB Recovery 0.25 0.125 0.5

21 28 d/F Blood AMB Recovery

22 45 d/F Blood AMB Recovery
23 10 y/M Blood None Expire
24 45 y/M Blood None Expire
25 47 y/F Blood AMB Expire
26 59 y/M Blood AMB Expire
27 60 y/F Blood CAS Recovery
28 65 y/F Blood AMB Recovery
29 67 y/M Blood FLU Recovery
30 74 y/M Blood CAS Expire
14
2014 Emara et al. 31 27 y/F Blood AMB Expire 0.064 >256 NA 0.38 0.064 NA NA
|

(Continues)
      3
T A B L E   1   (Continued)
|
4      

MIC (μg/mL)
Antifungal Final
Year of report Author Patient no. Age/Sex Isolation site regimen outcome AMB FLU ITR VRC CAS MFG AFG
15
2014 Magobo et al. 32 85 y/M Blood NA NA 1 >256 0.12 0.5 0.25 0.06 0.25
33 60 y/M Blood NA NA 0.5 >256 0.12 1 0.12 0.06 0.12
34 73 y/M Blood NA NA 1 >256 0.25 2 0.25 0.12 0.25
35 27 y/M Blood NA NA 0.25 64 0.06 0.25 0.03 0.06 0.06
2016 Calvo et al.16 36 30 d/F Blood AMB/VRC Expire 1-­2 >64 NA 4 NA NA 0.06-­
37 21 y/M Blood FLU/VRC/ Recovery 0125
CAS
38 13 d/F Blood VRC/AMB/ Expire
CAS
39 72 y/F Blood FLU Recovery
40 17 d/M Blood FLU Expire
41 40 y/M Blood VRC/CAS Recovery
42 23 d/F Blood CAS Recovery
43 18 d/M Blood FLU/VRC/ Expire
CAS
44 2 d/M Blood CAS Recovery
45 12 d/M Blood VRC/CAS Recovery
46 11 d/M Blood AMB/CAS Recovery
47 29 y/M Blood FLU Recovery
48 18 d/F Blood VRC Recovery
49 48 y/M Blood FLU/AFG Expire
50 14 y/F Blood VRC/AFG/ Recovery
CAS
51 10 d/F Blood FLU Recovery
52 2 m/F Blood VRC/CAS Recovery
53 1 m/M Blood VRC/CAS Recovery
2016 Schelenz et al.17 54-­103 Age: 53 y Colonisation (28, NA NA 0.5-­2 >256 NA NA NA NA NA
(n=50) (19-­78) 56%)
Sex: F (17, Blood (9, 18%)
24%), M (33, Wound (3, 6%)
66%) Urine (1, 2%)
Vascular tip (7,
14%)
Unknown (2, 4%)
(Continues)
CHOI et al.
CHOI et al. |
      5

REFERENCES

0.124-­
AFG
1. Varghese R, Nair RM, Kavalakkat FJ. Fungal otomastoiditis: a case se-

NA
16
ries in immunocompetent adults. Indian J Otolaryngol Head Neck Surg.
2014;66:110‐113.

0.06-­4
MFG
2. Viswanatha B, Naseeruddin K. Fungal infections of the ear in im-

NA
munocompromised host: a review. Mediterr J Hematol Infect Dis.
2011;3:e2011003.
0.03-­ 3. Kim MN, Shin JH, Sung H et al. Candida haemulonii and closely related

AFG, anidulafungin; AMB, amphotericin B; CAS, caspofungin; CVC, central venous catheter; FLU, fluconazole; ITC, itraconazole; MFG, micafungin; NA, not available; VRC, voriconazole.
0.06
CAS

16 species at 5 university hospitals in Korea: identification, antifungal

susceptibility, and clinical features. Clin Infect Dis. 2009;48:e57‐e61.
4. Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K, Yamaguchi
0.03-­16

<0.03
H. Candida auris sp. nov., a novel ascomycetous yeast isolated from
VRC

the external ear canal of an inpatient in a Japanese hospital. Microbiol

Immunol. 2009;53:41‐44.
5. Clinical and Laboratory Standards Institue. Reference Method for Broth
0.125-­2

<0.03 Dilution Antifungal Susceptibility Testing of Yeasts: 4th Informational

Supplement: M23-S4. Wayne, PA: Clinical and Laboratory Standards
ITR

Some data are presented as median age (range) or number of patients and percentage. Antifungal susceptibilities were shown as range in some articles. Institue; 2012.
6. Slack CL, Watson DW, Abzug MJ, Shaw C, Chan KH. Fungal mas-
4-­256

toiditis in immunocompromised children. Arch Otolaryngol Head Neck

FLU

Surg. 1999;125:73‐75.
MIC (μg/mL)

7. Khanna V, Chander J, Nagarkar NM, Dass A. Clinicomicrobiologic

evaluation of active tubotympanic type chronic suppurative otitis
0.38-­4
AMB

0.12

media. J Otolaryngol. 2000;29:148‐153.

8. Psevdos GJ, Fefer J, Patel V, Srivastava S, Sharp V. Aspergillus fumi-
gatus otomastoiditis and skull base osteomyelitis in a patient with
Expire (24,
(17, 41%)
Recovery

Recovery
outcome

advanced acquired immunodeficiency syndrome. Infect Dis Clin Pract.

59%)

2011;19:218‐220.
Final

9. Lee WG, Shin JH, Uh Y et al. First three reported cases of nosocomial
fungemia caused by Candida auris. J Clin Microbiol. 2011;49:3139‐3142.
CAS (8, 20%)
FLU (9, 22%)

10. Cendejas-Bueno E, Kolecka A, Alastruey-Izquierdo A et al.

VRC (2, 5%)
Antifungal

None (15,

AMB (15,

Reclassification of the Candida haemulonii complex as Candida haemu-

regimen

37%)

37%)

lonii (C. haemulonii group I), C. duobushaemulonii sp. nov. (C. haemulonii

FLU

group II), and C. haemulonii var. vulnera var. nov.: three multiresistant
human pathogenic yeasts. J Clin Microbiol. 2012;50:3641‐3651.
11. Chowdhary A, Anil Kumar V, Sharma C et al. Multidrug-­resistant en-
Respiratory tract
Blood (25, 61%)

Other (7, 17%)

demic clonal strain of Candida auris in India. Eur J Microbiol Infect Dis.
Urine (7, 17%)

Ear discharge
Isolation site

2014;33:919‐926.
12. Khillan V, Rathore N, Kathuria S, Chowdhary A. A rare case of break-
(2, 5%)

through fungal pericarditis due to fluconazole-­resistant Candida

auris in a patient with chronic liver disease. JMM Case Rep. 2014.
Doi:10.1099/jmmcr.0.T00018
37%), M (26,

13. Chowdhary A, Sharma C, Duggal S, et al. New clonal strain of Candida

Sex: F (15,
Age: 54 y

auris, Delhi, India. Emerg Infect Dis. 2013;19:1670‐1673.

Age/Sex

(24-­69)

58 y/M
63%)

14. Emara M, Ahmad S, Khan Z, et al. Candida auris candidemia in Kuwait,

2014. Emerg Infect Dis. 2015;21:1091‐1092.
15. Magobo RE, Corcoran C, Seetharam S, Govender NP. Candida auris ­
associated candidemia, South Africa. Emerg Infect Dis. 2014;20:1250‐1251.
Patient no.

16. Calvo B, Melo AS, Perozo-Mena A, et al. First report of Candida auris
104-­144
(n=41)

in America: Clinical and microbiological aspects of 18 episodes of can-

didemia. J Infect. 2016;73:369‐374.
145

17. Schelenz S, Hagen F, Rhodes JL, et al. First hospital outbreak of the
globally emerging Candida auris in a European hospital. Antimicrob
18

Resist Infect Control. 2016;5:35.

Lockharat et al.

Choi et al. (this

18. Lockhart SR, Etienne KA, Vallabhaneni S, et al. Simultaneous

Emergence of Multidrug-­Resistant Candida auris on 3 Continents
Confirmed by Whole-­Genome Sequencing and Epidemiological
Author
T A B L E   1   (Continued)

case)

Analyses. Clin Infect Dis. 2017;64:134‐140.

How to cite this article: Choi HI, An J, Hwang JJ, Moon S-y,
Year of report

Son JS. Otomastoiditis caused by Candida auris: Case report

and literature review. Mycoses. 2017;00:1–5. https://doi.
2016

2016

org/10.1111/myc.12617