Mycopathologia
DOI 10.1007/s11046-015-9864-7
Otomycosis in Iran: A Review
Maral Gharaghani • Zahra Seifi
Ali Zarei Mahmoudabadi
•
Received: 20 November 2014 / Accepted: 16 January 2015
Ó Springer Science+Business Media Dordrecht 2015
Abstract Fungal infection of the external auditory
canal (otitis externa and otomycosis) is a chronic,
acute, or subacute superficial mycotic infection that
rarely involves middle ear. Otomycosis (swimmer’s
ear) is usually unilateral infection and affects more
females than males. The infection is usually symptomatic and main symptoms are pruritus, otalgia, aural
fullness, hearing impairment, otorrhea, and tinnitus.
Fungal species such as yeasts, molds, dermatophytes,
and Malassezia species are agents for otitis externa.
Among molds, Aspergillus niger was described as the
most common agent in the literature. Candida albicans was more prevalent than other yeast species.
Otomycosis has a worldwide distribution, but the
prevalence of infection is related to the geographical
location, areas with tropical and subtropical climate
showing higher prevalence rates. Otomycosis is a
secondary infection and is more prevalent among
swimmers. As a result, a higher incidence is reported
in summer season, when more people interested in
swimming. Incidence of otomycosis in our review
M. Gharaghani A. Zarei Mahmoudabadi
Department of Medical Mycology, School of Medicine,
Ahvaz Jundishapur University of Medical Sciences,
Ahvaz, Iran
Z. Seifi A. Zarei Mahmoudabadi (&)
Health Research Institute, Infectious and Tropical
Diseases Research Centre, Ahvaz Jundishapur University
of Medical Sciences, Ahvaz, Iran
e-mail: [email protected]
ranged from 5.7 to 81 %, with a mean value of 51.3 %.
Our results showed that 78.59 % of otomycosis agents
were Aspergillus, 16.76 % were Candida species, and
the rest (4.65 %) were other saprophytic fungi. Among
Iranian patients, incidence of infection was highest in
summer, followed by autumn, winter, and spring. In
Iran, otomycosis was most prevalent at the age of
20–40 years and the lowest prevalence was associated
with being\10 years old. The sex ratio of otomycosis
in our study was (M/F) 1:1.53.
Keywords
Iran
Otomycosis Aspergillus niger Yeasts Introduction
External ear infections (otitis externa) are one of the
most common diseases that ear specialists deal with.
Otitis externa (swimmer’s ear) is a common condition affecting the auricle, auditory canal, eardrum,
and middle ear with itches that become painful,
edematous, and red [1]. Swimmer’s ear is prevalent
among swimmers due to exposure to water for a long
time [2]. The ears are constantly exposed to biotic
elements of biosphere and may thus be infected by
various microorganisms such as bacteria, viruses, and
fungi. The cause of otitis externa may be either
infection due to microorganisms or non-infectious
(eczema and psoriasis) or both. Otomycosis or fungal
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Mycopathologia
otitis externa is a superficial mycotic infection
sometimes involving middle ear [3], which comprises more than 10 % of all otitis externa infections
[4]. Bacterial infections of ears are usually acute,
whereas fungal infections may be either acute or
subacute and due to inflammation and pruritus [5].
Severe infections are usually due to bacteria and
possibly result in secretion of pus. Although otomycosis cannot be taken seriously in most of the cases,
immune compromise resulting from otomycosis is
life-threatening to the patients.
Otomycosis has the highest incidence in hot and
humid seasons (summer) and the lowest in cold season
(winter). Several fungal agents cause otomycosis,
including yeasts (Candida), molds (Aspergillus and
Mucor), dermatophytes and Malassezia species [4, 6,
7]. In patients with otomycosis, dermatophytes are the
most common causes of tinea capitis and tinea barbae.
In rare cases, dematiaceous fungi such as Epicoccum,
Exophiala and Nattrassia mangiferae (Pycnidial synanamorph: Hendersonula toruloidea) cause otomycosis [8–10]. Literature search reveals that not much
work has been done on Iranian patients with otomycosis. In addition, a true distribution pattern for
otomycosis is not available. As a result, in this review,
we collected all available published papers about
otomycosis (epidemiology, diagnosis, treatment, and
in vitro assessment tests) in Iran from different
international resources (ISI, PubMed, Google Scholar,
Scopus, and Google) and local databases (Magiran,
ISC, and Journal sites). All data were extracted
carefully and analyzed using Microsoft Excel. In
addition, distribution maps of otomycosis and some of
its etiologic agents were drawn.
and the rest infected the left ear [13]. In another
study conducted at southwest Iran, 19.23 % of
studied patients had bilateral otomycosis [14].
Prasad et al. [15] reported that only 5 % of patients
with otomycosis presented bilateral infection. In
addition, they concluded that the infection in
females is more prevalent in the right ear.
The most prominent disease symptoms are itching, inflammation of external ear canal, otalgia,
otorrhea, pruritus, feeling of fullness, tinnitus, and
hearing impairment [5, 9, 16]. Fungus balls (densely
impacted wax comprising fungal mycelia and epithelial cells) are produced in the tympanic membrane due to developing diseases [2, 10]. Fungal
masses can partially block the external canal and
lead to hearing loss or even deafness in some
patients [7, 12]. At physical examination using
otoscope, white, gray, black, or creamy (wet newspaper) caseous debris masses can be found in the
external auditory meatus (Fig. 1). Fluffy white
discharges were present when C. albicans and
Aspergillus fumigatus are etiologic agents, whereas
A. niger produces black colonies (pepper-like).
Otomycosis due to dermatophytes in adults is
usually associated with tinea barbae, whereas in
children, it is associated with tinea capitis [10]
(Fig. 2). Otomycosis with Malassezia species has
been rarely reported in the literature [17].
Clinical Features
Otomycosis may occur as an acute, subacute, or
chronic noninvasive infection (chronic colonization)
with inflammation and exudate. The infection rarely
involves tympanic membrane and the middle ear
and is unilateral in approximately 90 % of the
immunocompetent patients, without any preponderance of the right or left side [11]. On the other hand,
the infection is occasionally considered bilateral
among immunocompromised patients [12]. In an
epidemiological study in Kashan, Iran, 25 % of the
infection was bilateral, 40.4 % infected the right ear
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Fig. 1 Otoscopic image of ear canal with otomycosis [18]
Mycopathologia
showed that all studied cases of otomycosis occurred
after treatment with topical ofloxacin antibiotics
drops. Several researchers reported that worldwide
the prevalence of otomycosis is highest in summer due
to dry dusty winds in this season [23, 26, 27].
Etiologic Agents
Fig. 2 Otomycosis due to dermatophytes
Risk Factors for Otomycosis
Otomycosis is a secondary infection due to several
predisposing factors such as swimming, warm conditions, foreign bodies into ear canal, traumatic inoculation, loss of cerumen, alternation in immunity,
working in dry dusty environment, poor hygiene,
using hearing aids, diabetes mellitus, external ear
seborrheic dermatitis, genetic factors, history of
tympanic membrane perforation, ear surgery, open
mastoid cavity, cleaning external ear canal with
matchsticks, and instilling coconut oil and earwax in
the external ear canal [1–3, 5, 15, 19–21]. One of the
most important factors for otomycosis is long-term
exposure to moisture: the prevalence of infection was
reported to be five times higher in swimmers than in
non-swimmers [6]. Zarei Mahmoudabadi et al. [19]
reported the infection with different species of saprophytic fungi such as A. niger, A. flavus, Rhizopus,
Penicillium, and Candida albicans in hearing aid mold
wearers. In addition, Sturgulewski et al. [22] reported
that hearing aids can act as a potential source of
microbial contamination and cause fungal colonization among long-term hearing aid wearers. Some
researchers have believed that wearing traditional
head coverings might increase the humidity of the ear
canal and provide favorable conditions for fungal
growth [23, 24].
Long-term topical treatment with broad-spectrum
antibiotics (fluoroquinolones) and steroids [3, 4] is the
important predisposing factor. Jackman et al. [25]
Approximately 61 species of different fungi (molds,
yeasts, dermatophyte, and Malassezia) have been
identified as the cause of otomycosis [9]. In the
literature, several saprophytic fungi and A. niger were
described as the most common agents for otomycosis
[3]. In addition, A. awamori and A. tubingensis are
other black Aspergillus involved in otomycosis [28].
Other agents include A. flavus, A. fumigatus, Scedosporium apiospermum (sexual state: Petriellidium boydii), Scopulariopsis, Penicillium, Chrysosporium,
Rhizopus, Absidia, and Cryptococcus species [7, 10,
13, 15, 29]. Pigmented fungi, Alternaria, and Cladosporium species were also reported as causative agents.
Although nearly all of the saprophytic fungi are
presented in the atmosphere as airborne fungi, their
concentration differs according to location, altitude,
time of day, season, and climatic conditions [30]. In
addition, endogenous organisms such as C. albicans,
C. guilliermondii, C. parapsilosis, Malassezia, and
Rhodotorula species contributed to the infection in
some cases [9, 31]. Most researchers from around the
world showed that A. niger served as the most common
otomycosis agent [3, 15, 23, 32–35]. On the other hand,
C. albicans was identified as the first isolated agent in
some reports [36]. Moreover, Viswanatha et al. [12]
reported C. albicans as the commonest agent (52 %)
among immunocompromised patients.
Dermatophytes rarely cause otomycosis (dermatophytosis of the external ear); however, some reports
show that Microsporum canis complex, Trichophyton
rubrum complex, T. mentagrophytes complex, and
Epidermophyton floccosum were isolated from otomycosis [6, 10, 33, 37]. In some reports, mixed
infections due to two different fungal species and/or
mixed fungal–bacterial infections were also reported
[7, 18]. Our results show that 78.59 % of otomycosis
agents were Aspergillus, 16.76 % were Candida
species, and the rest (4.65 %) were other saprophytic
fungi. The details about all reported agents in our
study are categorized in Table 1.
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Mycopathologia
Table 1 Frequency of otomycosis agents reported by Iranian
researchers [1, 2, 4, 5, 8, 10, 11, 14, 18, 20, 26, 31, 37–47]
Otomycosis agent
No.
%
Aspergillus niger
781
51.15
Aspergillus flavus
260
17.03
Candida albicans
174
11.39
Aspergillus fumigatus
112
7.33
Candida sp.
65
4.26
Penicillium
21
1.38
Aspergillus sp.
19
1.24
Aspergillus terreus
15
0.98
Unknown moulds
11
0.72
Candida parapsilosis
11
0.72
Cladosporium
6
0.39
Aspergillus nidulans
8
0.52
Mucor
6
0.39
Alternaria
4
0.26
Rhizopus
Nigrospora
5
5
0.33
0.33
Aspergillus glaucus
4
0.26
Candida glabrata
3
0.20
Malassezia
3
0.20
Candida tropicalis
2
0.13
Geotrichum
2
0.13
Fusarium
2
0.13
Curvularia
2
0.13
Aspergillus persicolor
1
0.07
Candida krusei
1
0.07
Scopulariopsis
1
0.07
Epicoccum
1
0.07
Nattrassia mangiferae
1
0.07
Microsporum canis complex
1
Total
1,527
0.07
100
Aspergillus species were reported as the most
common etiologic agent of otomycosis in the literature
[7, 15, 23, 32]. Worldwide, A. niger is considered the
predominant causal organism (65.1 %), followed by
A. flavus (21.7) and A. fumigatus (9.3) (Fig. 3).
However, in reports by Barati et al. [5] and Balouchi
et al. [41], A. flavus was detected as the most common
agent of otomycosis at the center of Iran (Isfahan
province). In the present study, Candida species
caused otomycosis in 16.76 % of cases, C. albicans
with 67.97 % being the most prevalent agent followed
by C. parapsilosis (4.3 %), C. glabrata (1.17 %), C.
tropicalis (0.78 %), C. krusei (0.39 %), and Candida
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sp. (25.39 %). Our results show that dematiaceous
fungi accounted for only 1.24 %, Cladosporium (six
cases) being the most common agent followed by
Nigrospora (five cases) and Alternaria (four cases).
Elahi and Zaini reported the first case of otomycosis
due to N. mangiferae (H. toruloidea) in a 24-year-old
male from Tehran, Iran [8]. Iranian reports have
shown that dermatophyte species are rarely isolated
from patients with otomycosis.
Geographical Distribution Pattern
Otomycosis has a worldwide distribution with a
prevalence of 4 per 1,000 population [2], as low as
9 % (in otitis externa) and as high as 30.4 % (in
patients with symptoms of otitis or inflammatory
conditions) [3]. Several studies show that the highest
prevalence of otomycosis occurs in the hot, humid,
and dusty areas of the tropics and subtropics [15, 25].
Although several reports show that the highest prevalence of otomycosis was observed in summer [23,
48], Garcı́a-Agudo [34] observed a homogeneous
occurrence of otomycosis in all seasons in Spain.
Geographical distribution of otomycosis in the provinces of Iran is shown in Fig. 4. Incidence of
otomycosis in our review ranged from 5.7 (reported
by Yeganeh Mogadam from Isfahan) to 81 %
(reported by Kazemi from Eastern Azarbaidjan), with
a mean value of 51.3 %. This incidence is similar to
Prasad et al.’s report from India [15]. However,
several reports from Turkey (70.1 %), Egypt
(74.2 %), India (78 %), and Ivory Coast (80 %) have
shown that the incidence of otomycosis is much higher
than that reported in our study [32, 33, 49, 50].
However, lower prevalence of otomycosis has also
been reported by Deshmukh et al. [51] and Gutiérrez
et al. [52].
Our review showed that the incidence of otomycosis in summer was highest, followed by autumn,
winter, and spring [2, 4, 41]. However, Barati et al.
[5] reported that the incidence of otomycosis was
highest at the autumn, followed by summer, winter,
and spring. The distribution of primary and secondary otomycosis agents is shown in Figs. 5 and 6,
respectively. As shown, A. niger was distributed in
nearly all otomycosis-prevalent areas reported,
whereas the distribution of secondary otomycosis
agents varied.
Mycopathologia
Fig. 3 Frequency of
Aspergillus species
Fig. 4 Distribution of
otomycosis in Iran
Age and Sex Distribution
Otomycosis is a fungal infection in adulthood
although the other age groups such as children may
also be affected. Some of the researchers have shown
that the incidence of otomycosis was highest in the age
group of 21–30 years and lowest in the age groups of
\10 years and over 60 years [15]. Various surveys
showed that the prevalence of otomycosis varies
among different population. Some authors reported
that it is more frequent in females, while some others
claimed that it is more common in males. For example,
in the study of Anwar and Gohar [16] in Pakistan
during 2010–2012, the prevalence was 59 % in male
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Mycopathologia
Fig. 5 Distribution of the
primary otomycosis agents
in different provinces of Iran
and 41 % in female. In addition, 60, 63, and 54.9 %
positive cases of otomycosis were males in studies in
Tehran (Iran), India, and Spain conducted by Afshari
et al. [44], Prasad et al. [15], and Garcı́a-Agudo et al.
[34], respectively. According to Jia et al.’s report [7]
from Shanghai, the male-to-female ratio was 2:1. On
the other hand, according to Barati et al. [5], the
distribution of otomycosis was nearly similar (50.3 %
for females and 49.7 % for males) between both sexes
in Isfahan. However, based on the worldwide sex
distribution, otomycosis is more frequent in females.
Nemati et al. [42] suggested that traditional head scarf
and ‘Hijab’ commonly worn by Iranian women is an
important factor for otomycosis among Iranian
women. In contrast, this head scarf could protect ears
from fungal spores entering to ear canal. In addition,
Barati et al. [5] reported that wearing head scarf was
not a possible predisposing factor for otomycosis.
Our investigation showed that sex ratio among
Iranian patients with otomycosis was (M/F) 1:1.53.
However, two reports from Iran, Zarei Mahmoudabadi
et al. [20] and Afshari et al. [44], showed that the
frequency of otomycosis was more prevalent among
123
males than among females. In most of the reports from
different countries, the highest incidence of otomycosis was in the age group of 21–30 years [15, 24, 32].
However, Ozcan et al.’s report [23] showed that the
infection most commonly (73.6 %) affects patients
aged between 31 and 60 years. In addition, the highest
number of positive cases of otomycosis was in the age
group of 51–60 years [53]. On the other hand, Aneja
et al. [49] showed that the age group of 31–40 years
was most susceptible to otomycosis in the northeastern
part of Haryana (India). Our report showed that
otomycosis among Iranian patients is most prevalent
at the age range of 20–40 years and the lowest ratio is
associated with \10 years old.
Clinical and Mycological Diagnosis
The diagnosis of otomycosis is based on a set of
evidences, patient’s clinical history, physical examination with an otoscope, and mycological examinations. Although clinical symptoms are not specific,
mass of fungal elements that grow on the floor of the
Mycopathologia
Fig. 6 Distribution of the
secondary otomycosis
agents in different provinces
of Iran
ear canal can be easily observed by means of otoscopic
examination. As a result, definitive diagnosis must be
based on direct and culture examinations. Suitable
samples were taken using two sterile cotton swabs, one
for direct examination and the other for culture. In
addition, ear scraping, exfoliation (scales), and the
masses of debris of epithelial and the cerumen are also
collected for examinations. Tympanic membrane and
skin biopsy samples may be used for histopathology
examinations.
Direct smears were mounted by KOH (10–20 %) or
a lactophenol cotton blue solution. In addition, smears
by stained methylene blue, Giemsa, or Gram stains
provide more details for detection. In addition, KOH
plus Blankophor P or calcofluor white is a more suitable
mounting solution for preparing slides. Several fungal
forms become detectable in direct smears, depending
on the type of organisms. For example, septate hyphae,
yellow, brown-black conidia, and fruiting heads are
fungal forms detected in the direct examination when
Aspergillus species is the causative agent for otomycosis (Fig. 7) [6, 20, 46]. In some cases, a microscopic
image is highly suggestive of the causative agent (A.
niger). Hyaline, wide, non-septate, ribbon-like hyphae
(10–15 l) are indicated otomycosis with zygomycetes fungi (Fig. 7). On the other hand, otomycosis due to
Candida species is characterized by the presence of
clusters of blastoconidia and pseudohyphae. Septate
hyaline hyphae with reproductive structure indicate
hyalohyphomycetes (Penicillium, Acremonium, and
Scopulariopsis species), whereas septate dark hyphae
are usually observed when dematiaceous fungi (Alternaria and Cladosporium species) are causative agents
of otomycosis. Immunofluorescence staining techniques are more accurate, sensitive, and rapid identification methods for diagnosis.
Cyclohexamide-free media, such as the Sabouraud’s dextrose agar, potato dextrose agar, and the
Czapek agar, are suitable media for the cultivation.
Incubation must be performed at room temperature for
3–5 days. Otomycosis could not be confirmed by
growing a few colonies of saprophytic fungi on culture
media; repeated cultures need to be performed.
Morphological characteristics of colonies and microscopic features are the most easily distinguishable
characteristics for saprophytic fungi.
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Mycopathologia
Fig. 7 Spiny brown conidia of A. niger (a), Fruiting bodies of Aspergillus (b), Aseptate hyphae of Rhizopus (c), Dichotomous septate
hyphae (d)
In vitro Study
Zarei Mahmoudabadi et al. [54] treated Lamisil
against otomycosis agents and found that all tested
organisms are highly sensitive to terbinafine in vitro.
The class of azoles, including clotrimazole, fluconazole, ketoconazole, and miconazole, is most effective
against otomycosis agents (0.0,625–32 lg/mL) without any ototoxicity [42]. In a study conducted by
Szigeti et al. [28], all otomycosis isolates of Aspergillus species were highly sensitive to terbinafine, and
moderate susceptibilities to amphotericin B, fluconazole, and ketoconazole were reported.
Prognoses and Therapy
Although otomycosis is an acute or chronic infection
and recurrence was observed in some cases, it has
benign prognosis. The infection is rarely life-threatening, and usually, topical antifungal is enough for
treatment. Several topical antifungals, such as clotrimazole, miconazole, bifonazole, nystatin, and
123
terbinafine, are potentially active against otomycosis
[3, 55, 56]. Topical fluconazole ear drops and
mechanical debridement of visible fungal elements
in the external auditory canal were all relatively
effective, with 83.33 % resolution rate on initial
application. Kiakojuri et al. [43] showed that the
relapse of otomycosis occurred when treatment with
suction clearance and 2 % topical miconazole was
performed. Topical clotrimazole lotion or cream 1 %
is the most popular antifungal used for the treatment of
otomycosis in different studies [16, 38]. In addition,
Jackman et al. [25] concluded that clotrimazole is an
effective antifungal drug against most otomycosis
agents. Vinegar and acetic acid [35], and alcohol and
acetic acid [47] were also used to the treatment of
otomycosis due to species of Aspergillus and Candida.
Both researchers suggested that these traditional
materials have effective significant antifungal activity.
Recently, 7.5 % povidone iodine was reported to be an
effective antifungal in the treatment of otomycosis by
Philip et al. [57]. During a clinical trial in Ahvaz, Iran,
a new ear drop formulation of Lamisil was successfully used for the treatment of otomycosis [58].
Mycopathologia
Conclusion
Otomycosis in Iran, like in other countries, has a high
prevalence because of high temperature, humidity, and
dust. Our results showed that the commonest otomycosis agent was Aspergillus (78.59 %), followed by
Candida species (16.76 %) and other saprophytic fungi
(4.65 %). Incidence of otomycosis in our review
ranged from 5.7 to 81 %, with a mean value of
51.3 %. Among Iranian patients, incidence of infection
was highest in summer, followed by autumn, winter,
and spring. In Iran, otomycosis was most prevalent at
the age of 20–40 years and the lowest prevalence was
associated with being \10 years old. The sex ratio of
otomycosis in our study was (M/F) 1:1.53.
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