Otomycosis in Iran: a Review

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 ranged from 5.7 to 81 %, with a mean value of 51.3 %. canal (otitis externa and otomycosis) is a chronic, Our results showed that 78.59 % of otomycosis agents acute, or subacute superficial mycotic infection that were Aspergillus, 16.76 % were Candida species, and rarely involves middle ear. Otomycosis (swimmer’s the rest (4.65 %) were other saprophytic fungi. Among ear) is usually unilateral infection and affects more Iranian patients, incidence of infection was highest in females than males. The infection is usually symp- summer, followed by autumn, winter, and spring. In tomatic and main symptoms are pruritus, otalgia, aural Iran, otomycosis was most prevalent at the age of fullness, hearing impairment, otorrhea, and tinnitus. 20–40 years and the lowest prevalence was associated Fungal species such as yeasts, molds, dermatophytes, with being\10 years old. The sex ratio of otomycosis and Malassezia species are agents for otitis externa. in our study was (M/F) 1:1.53. Among molds, Aspergillus niger was described as the most common agent in the literature. Candida albi- Keywords Otomycosis Á Aspergillus niger Á Yeasts Á cans was more prevalent than other yeast species. Iran 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 Introduction secondary infection and is more prevalent among swimmers. As a result, a higher incidence is reported External ear infections (otitis externa) are one of the in summer season, when more people interested in most common diseases that ear specialists deal with. swimming. Incidence of otomycosis in our review Otitis externa (swimmer’s ear) is a common condi- tion affecting the auricle, auditory canal, eardrum, and middle ear with itches that become painful, M. Gharaghani Á A. Zarei Mahmoudabadi edematous, and red [1]. Swimmer’s ear is prevalent Department of Medical Mycology, School of Medicine, among swimmers due to exposure to water for a long Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran time [2]. The ears are constantly exposed to biotic elements of biosphere and may thus be infected by Z. Seifi Á A. Zarei Mahmoudabadi (&) various microorganisms such as bacteria, viruses, and Health Research Institute, Infectious and Tropical fungi. The cause of otitis externa may be either Diseases Research Centre, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran infection due to microorganisms or non-infectious e-mail: [email protected] (eczema and psoriasis) or both. Otomycosis or fungal 123 Mycopathologia otitis externa is a superficial mycotic infection and the rest infected the left ear [13]. In another sometimes involving middle ear [3], which com- study conducted at southwest Iran, 19.23 % of prises more than 10 % of all otitis externa infections studied patients had bilateral otomycosis [14]. [4]. Bacterial infections of ears are usually acute, Prasad et al. [15] reported that only 5 % of patients whereas fungal infections may be either acute or with otomycosis presented bilateral infection. In subacute and due to inflammation and pruritus [5]. addition, they concluded that the infection in Severe infections are usually due to bacteria and females is more prevalent in the right ear. possibly result in secretion of pus. Although otomy- The most prominent disease symptoms are itch- cosis cannot be taken seriously in most of the cases, ing, inflammation of external ear canal, otalgia, immune compromise resulting from otomycosis is otorrhea, pruritus, feeling of fullness, tinnitus, and life-threatening to the patients. hearing impairment [5, 9, 16]. Fungus balls (densely Otomycosis has the highest incidence in hot and impacted wax comprising fungal mycelia and epi- humid seasons (summer) and the lowest in cold season thelial cells) are produced in the tympanic mem- (winter). Several fungal agents cause otomycosis, brane due to developing diseases [2, 10]. Fungal including yeasts (Candida), molds (Aspergillus and masses can partially block the external canal and Mucor), dermatophytes and Malassezia species [4, 6, lead to hearing loss or even deafness in some 7]. In patients with otomycosis, dermatophytes are the patients [7, 12]. At physical examination using most common causes of tinea capitis and tinea barbae. otoscope, white, gray, black, or creamy (wet news- In rare cases, dematiaceous fungi such as Epicoccum, paper) caseous debris masses can be found in the Exophiala and Nattrassia mangiferae (Pycnidial syn- external auditory meatus (Fig. 1). Fluffy white anamorph: Hendersonula toruloidea) cause otomy- discharges were present when C. albicans and cosis [8–10]. Literature search reveals that not much Aspergillus fumigatus are etiologic agents, whereas work has been done on Iranian patients with otomy- A. niger produces black colonies (pepper-like). cosis. In addition, a true distribution pattern for Otomycosis due to dermatophytes in adults is otomycosis is not available. As a result, in this review, usually associated with tinea barbae, whereas in we collected all available published papers about children, it is associated with tinea capitis [10] otomycosis (epidemiology, diagnosis, treatment, and (Fig. 2). Otomycosis with Malassezia species has in vitro assessment tests) in Iran from different been rarely reported in the literature [17]. 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.

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 preponder- ance 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 Fig. 1 Otoscopic image of ear canal with otomycosis [18] 123 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

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]. Fig. 2 Otomycosis due to dermatophytes Other agents include A. flavus, A. fumigatus, Scedos- porium apiospermum (sexual state: Petriellidium boy- Risk Factors for Otomycosis dii), Scopulariopsis, Penicillium, Chrysosporium, Rhizopus, Absidia, and Cryptococcus species [7, 10, Otomycosis is a secondary infection due to several 13, 15, 29]. Pigmented fungi, Alternaria, and Clado- predisposing factors such as swimming, warm condi- sporium species were also reported as causative agents. tions, foreign bodies into ear canal, traumatic inocu- Although nearly all of the saprophytic fungi are lation, loss of cerumen, alternation in immunity, presented in the atmosphere as airborne fungi, their working in dry dusty environment, poor hygiene, concentration differs according to location, altitude, using hearing aids, diabetes mellitus, external ear time of day, season, and climatic conditions [30]. In seborrheic dermatitis, genetic factors, history of addition, endogenous organisms such as C. albicans, tympanic membrane perforation, ear surgery, open C. guilliermondii, C. parapsilosis, Malassezia, and mastoid cavity, cleaning external ear canal with Rhodotorula species contributed to the infection in matchsticks, and instilling coconut oil and earwax in some cases [9, 31]. Most researchers from around the the external ear canal [1–3, 5, 15, 19–21]. One of the world showed that A. niger served as the most common most important factors for otomycosis is long-term otomycosis agent [3, 15, 23, 32–35]. On the other hand, exposure to moisture: the prevalence of infection was C. albicans was identified as the first isolated agent in reported to be five times higher in swimmers than in some reports [36]. Moreover, Viswanatha et al. [12] non-swimmers [6]. Zarei Mahmoudabadi et al. [19] reported C. albicans as the commonest agent (52 %) reported the infection with different species of sapro- among immunocompromised patients. phytic fungi such as A. niger, A. flavus, Rhizopus, Dermatophytes rarely cause otomycosis (dermato- Penicillium, and Candida albicans in hearing aid mold phytosis of the external ear); however, some reports wearers. In addition, Sturgulewski et al. [22] reported show that Microsporum canis complex, Trichophyton that hearing aids can act as a potential source of rubrum complex, T. mentagrophytes complex, and microbial contamination and cause fungal coloniza- Epidermophyton floccosum were isolated from oto- tion among long-term hearing aid wearers. Some mycosis [6, 10, 33, 37]. In some reports, mixed researchers have believed that wearing traditional infections due to two different fungal species and/or head coverings might increase the humidity of the ear mixed fungal–bacterial infections were also reported canal and provide favorable conditions for fungal [7, 18]. Our results show that 78.59 % of otomycosis growth [23, 24]. agents were Aspergillus, 16.76 % were Candida Long-term topical treatment with broad-spectrum species, and the rest (4.65 %) were other saprophytic antibiotics (fluoroquinolones) and steroids [3, 4] is the fungi. The details about all reported agents in our important predisposing factor. Jackman et al. [25] study are categorized in Table 1. 123 Mycopathologia

Table 1 Frequency of otomycosis agents reported by Iranian sp. (25.39 %). Our results show that dematiaceous researchers [1, 2, 4, 5, 8, 10, 11, 14, 18, 20, 26, 31, 37–47] fungi accounted for only 1.24 %, Cladosporium (six Otomycosis agent No. % cases) being the most common agent followed by Nigrospora (five cases) and Alternaria (four cases). Aspergillus niger 781 51.15 Elahi and Zaini reported the first case of otomycosis Aspergillus flavus 260 17.03 due to N. mangiferae (H. toruloidea) in a 24-year-old Candida albicans 174 11.39 male from Tehran, Iran [8]. Iranian reports have Aspergillus fumigatus 112 7.33 shown that dermatophyte species are rarely isolated Candida sp. 65 4.26 from patients with otomycosis. Penicillium 21 1.38 Aspergillus sp. 19 1.24 Aspergillus terreus 15 0.98 Geographical Distribution Pattern Unknown moulds 11 0.72 Candida parapsilosis 11 0.72 Otomycosis has a worldwide distribution with a Cladosporium 6 0.39 prevalence of 4 per 1,000 population [2], as low as Aspergillus nidulans 8 0.52 9 % (in otitis externa) and as high as 30.4 % (in Mucor 6 0.39 patients with symptoms of otitis or inflammatory Alternaria 4 0.26 conditions) [3]. Several studies show that the highest Rhizopus 5 0.33 prevalence of otomycosis occurs in the hot, humid, Nigrospora 5 0.33 and dusty areas of the tropics and subtropics [15, 25]. Aspergillus glaucus 4 0.26 Although several reports show that the highest prev- Candida glabrata 3 0.20 alence of otomycosis was observed in summer [23, Malassezia 3 0.20 48], Garcıá-Agudo [34] observed a homogeneous Candida tropicalis 2 0.13 occurrence of otomycosis in all seasons in Spain. Geotrichum 2 0.13 Geographical distribution of otomycosis in the prov- Fusarium 2 0.13 inces of Iran is shown in Fig. 4. Incidence of Curvularia 2 0.13 otomycosis in our review ranged from 5.7 (reported Aspergillus persicolor 1 0.07 by Yeganeh Mogadam from Isfahan) to 81 % Candida krusei 1 0.07 (reported by Kazemi from Eastern Azarbaidjan), with Scopulariopsis 1 0.07 a mean value of 51.3 %. This incidence is similar to Epicoccum 1 0.07 Prasad et al.’s report from India [15]. However, Nattrassia mangiferae 1 0.07 several reports from Turkey (70.1 %), Egypt Microsporum canis complex 1 0.07 (74.2 %), India (78 %), and Ivory Coast (80 %) have Total 1,527 100 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 Aspergillus species were reported as the most been reported by Deshmukh et al. [51] and Gutie´rrez common etiologic agent of otomycosis in the literature et al. [52]. [7, 15, 23, 32]. Worldwide, A. niger is considered the Our review showed that the incidence of otomy- predominant causal organism (65.1 %), followed by cosis in summer was highest, followed by autumn, A. flavus (21.7) and A. fumigatus (9.3) (Fig. 3). winter, and spring [2, 4, 41]. However, Barati et al. However, in reports by Barati et al. [5] and Balouchi [5] reported that the incidence of otomycosis was et al. [41], A. flavus was detected as the most common highest at the autumn, followed by summer, winter, agent of otomycosis at the center of Iran (Isfahan and spring. The distribution of primary and second- province). In the present study, Candida species ary otomycosis agents is shown in Figs. 5 and 6, caused otomycosis in 16.76 % of cases, C. albicans respectively. As shown, A. niger was distributed in with 67.97 % being the most prevalent agent followed nearly all otomycosis-prevalent areas reported, by C. parapsilosis (4.3 %), C. glabrata (1.17 %), C. whereas the distribution of secondary otomycosis tropicalis (0.78 %), C. krusei (0.39 %), and Candida agents varied. 123 Mycopathologia

Fig. 3 Frequency of Aspergillus species

Fig. 4 Distribution of otomycosis in Iran

Age and Sex Distribution \10 years and over 60 years [15]. Various surveys showed that the prevalence of otomycosis varies Otomycosis is a fungal infection in adulthood among different population. Some authors reported although the other age groups such as children may that it is more frequent in females, while some others also be affected. Some of the researchers have shown claimed that it is more common in males. For example, that the incidence of otomycosis was highest in the age in the study of Anwar and Gohar [16] in Pakistan group of 21–30 years and lowest in the age groups of during 2010–2012, the prevalence was 59 % in male 123 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 % males than among females. In most of the reports from positive cases of otomycosis were males in studies in different countries, the highest incidence of otomyco- Tehran (Iran), India, and Spain conducted by Afshari sis was in the age group of 21–30 years [15, 24, 32]. et al. [44], Prasad et al. [15], and Garcıá-Agudo et al. However, Ozcan et al.’s report [23] showed that the [34], respectively. According to Jia et al.’s report [7] infection most commonly (73.6 %) affects patients from Shanghai, the male-to-female ratio was 2:1. On aged between 31 and 60 years. In addition, the highest the other hand, according to Barati et al. [5], the number of positive cases of otomycosis was in the age distribution of otomycosis was nearly similar (50.3 % group of 51–60 years [53]. On the other hand, Aneja for females and 49.7 % for males) between both sexes et al. [49] showed that the age group of 31–40 years in Isfahan. However, based on the worldwide sex was most susceptible to otomycosis in the northeastern distribution, otomycosis is more frequent in females. part of Haryana (India). Our report showed that Nemati et al. [42] suggested that traditional head scarf otomycosis among Iranian patients is most prevalent and ‘Hijab’ commonly worn by Iranian women is an at the age range of 20–40 years and the lowest ratio is important factor for otomycosis among Iranian associated with\10 years old. 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 Clinical and Mycological Diagnosis not a possible predisposing factor for otomycosis. Our investigation showed that sex ratio among The diagnosis of otomycosis is based on a set of Iranian patients with otomycosis was (M/F) 1:1.53. evidences, patient’s clinical history, physical exami- However, two reports from Iran, Zarei Mahmoudabadi nation with an otoscope, and mycological examina- et al. [20] and Afshari et al. [44], showed that the tions. Although clinical symptoms are not specific, frequency of otomycosis was more prevalent among mass of fungal elements that grow on the floor of the 123 Mycopathologia

Fig. 6 Distribution of the secondary otomycosis agents in different provinces of Iran

ear canal can be easily observed by means of otoscopic niger). Hyaline, wide, non-septate, ribbon-like hyphae examination. As a result, definitive diagnosis must be (10–15 l) are indicated otomycosis with zygomyce- based on direct and culture examinations. Suitable tes fungi (Fig. 7). On the other hand, otomycosis due to samples were taken using two sterile cotton swabs, one Candida species is characterized by the presence of for direct examination and the other for culture. In clusters of blastoconidia and pseudohyphae. Septate addition, ear scraping, exfoliation (scales), and the hyaline hyphae with reproductive structure indicate masses of debris of epithelial and the cerumen are also hyalohyphomycetes (Penicillium, Acremonium,and collected for examinations. Tympanic membrane and Scopulariopsis species), whereas septate dark hyphae skin biopsy samples may be used for histopathology are usually observed when dematiaceous fungi (Alter- examinations. naria and Cladosporium species) are causative agents Direct smears were mounted by KOH (10–20 %) or of otomycosis. Immunofluorescence staining tech- a lactophenol cotton blue solution. In addition, smears niques are more accurate, sensitive, and rapid identi- by stained methylene blue, Giemsa, or Gram stains fication methods for diagnosis. provide more details for detection. In addition, KOH Cyclohexamide-free media, such as the Sabou- plus Blankophor P or calcofluor white is a more suitable raud’s dextrose agar, potato dextrose agar, and the mounting solution for preparing slides. Several fungal Czapek agar, are suitable media for the cultivation. forms become detectable in direct smears, depending Incubation must be performed at room temperature for on the type of organisms. For example, septate hyphae, 3–5 days. Otomycosis could not be confirmed by yellow, brown-black conidia, and fruiting heads are growing a few colonies of saprophytic fungi on culture fungal forms detected in the direct examination when media; repeated cultures need to be performed. Aspergillus species is the causative agent for otomyco- Morphological characteristics of colonies and micro- sis (Fig. 7)[6, 20, 46]. In some cases, a microscopic scopic features are the most easily distinguishable image is highly suggestive of the causative agent (A. characteristics for saprophytic fungi. 123 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 terbinafine, are potentially active against otomycosis [3, 55, 56]. Topical fluconazole ear drops and Zarei Mahmoudabadi et al. [54] treated Lamisil mechanical debridement of visible fungal elements against otomycosis agents and found that all tested in the external auditory canal were all relatively organisms are highly sensitive to terbinafine in vitro. effective, with 83.33 % resolution rate on initial The class of azoles, including clotrimazole, fluconaz- application. Kiakojuri et al. [43] showed that the ole, ketoconazole, and miconazole, is most effective relapse of otomycosis occurred when treatment with against otomycosis agents (0.0,625–32 lg/mL) with- suction clearance and 2 % topical miconazole was out any ototoxicity [42]. In a study conducted by performed. Topical clotrimazole lotion or cream 1 % Szigeti et al. [28], all otomycosis isolates of Aspergil- is the most popular antifungal used for the treatment of lus species were highly sensitive to terbinafine, and otomycosis in different studies [16, 38]. In addition, moderate susceptibilities to amphotericin B, fluconaz- Jackman et al. [25] concluded that clotrimazole is an ole, and ketoconazole were reported. 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 Prognoses and Therapy otomycosis due to species of Aspergillus and Candida. Both researchers suggested that these traditional Although otomycosis is an acute or chronic infection materials have effective significant antifungal activity. and recurrence was observed in some cases, it has Recently, 7.5 % povidone iodine was reported to be an benign prognosis. The infection is rarely life-threat- effective antifungal in the treatment of otomycosis by ening, and usually, topical antifungal is enough for Philip et al. [57]. During a clinical trial in Ahvaz, Iran, treatment. Several topical antifungals, such as clo- a new ear drop formulation of Lamisil was success- trimazole, miconazole, bifonazole, nystatin, and fully used for the treatment of otomycosis [58].

123 Mycopathologia

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