Mycopathologia (2011) 172:307–310 DOI 10.1007/s11046-011-9427-5
Otomycosis due to Filamentous Fungi Lidia Garcı´a-Agudo • Pilar Aznar-Marı´n • Fa´tima Gala´n-Sa´nchez • Pedro Garcı´a-Martos • Pilar Marı´n-Casanova • Manuel Rodrı´guez-Iglesias
Received: 19 December 2010 / Accepted: 4 April 2011 / Published online: 17 April 2011 Ó Springer Science+Business Media B.V. 2011
Abstract Otomycosis is common throughout the world but barely studied in Spain. Our objective was to determine the microbiological and epidemiological characteristics of this pathology in Cadiz (Spain) between 2005 and 2010. Samples from patients with suspicion of otomycosis underwent a direct microscopic examination and culture on different media for fungi and bacteria. Mycological cultures were incubated at 30°C for at least seven days. Identification of fungi was based on colonial morphology and microscopic examination of fungal structure. From a total of 2,633 samples, microbial growth was present in 1,375 (52.2%) and fungal isolation in 390 (28.4%). We identified 228 yeasts and 184 filamentous fungi (13.4% of positive cultures and 47.2% of otomycosis), associated with yeasts in 22 cases (5.6%). The most frequent species were Aspergillus flavus (42.4%), A. niger (35.9%), A. fumigatus (12.5%), A. candidus (7.1%), A. terreus (1.6%), and Paecilomyces variotii (0.5%). Infection was predominant in men (54.9%) and patients beyond 55 years old (46.8%). The most common clinical symptoms were itching (98.9%), otalgia (59.3%), and hypoacusis (56.0%). Fall season reported the lowest number of L. Garcı´a-Agudo P. Aznar-Marı´n F. Gala´n-Sa´nchez P. Garcı´a-Martos P. Marı´n-Casanova M. Rodrı´guez-Iglesias (&) Clinical Microbiology Laboratory, Puerta del Mar University Hospital, Avda. Ana de Viya, 21, 11009 Ca´diz, Spain e-mail:
[email protected]
cases (20.1%). Incidence of otomycosis and fungi producing otomycosis vary within the distinct geographical areas. In Cadiz, this infection is endemic due to warm temperatures, high humidity, sea bathing, and wind, which contributes to disseminate the conidia. Despite Aspergillus niger has been reported as the main causative agent, A. flavus is predominant in Cadiz. Although infection is usually detected in warm months, we observed a homogeneous occurrence of otomycosis in almost all the seasons. Keywords Otomycosis Fungi Yeasts Aspergillus Candida
Introduction Otomycosis is a superficial infection involving the external auditory canal caused by yeasts and filamentous fungi. It is worldwide spread, above all in tropical and subtropical regions. It has been estimated to cause 15–20% of external otitis. Predisposing factors of otomycosis mainly include: heat, humidity, a poor personal hygiene, bathing or diving in freshwater or seawater, and previous antibiotic therapy for a bacterial otitis. The frequency and the proportion of the agents involved vary in the different geographical areas. Candida and Aspergillus are the species usually predominant [1–12]. Fungi grow rapidly on the corneous stratum of the skin and give rise to inflammation accompanied by unspecific
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symptoms: itching, hypoacusis, otalgia, and scaling of the epithelium. This pathology is more frequent in warm months. Incidence of otomycosis has increased in recent years due to the use of broad-spectrum antibiotics to treat bacterial otitis, as well as other factors related to immunity alterations. In this study, we carried out a retrospective, epidemiological, and microbiological research concerning otomycosis cases diagnosed in the sanitary area of Cadiz (Spain) in the last 5 years (2005–2009).
Materials and Methods A total of 2,633 patients with suspicion of otomycosis underwent a microbiologic study of the external auditory canal exudate, which was obtained under microscopic vision using a cotton wool swab. Samples were transported, by sterile means, to the Microbiology Laboratory for the bacterial and mycological study. They were stored between 2 and 8°C before processing. The microbiological study included a direct microscopic examination with KOH at 10% and/or cotton blue lactophenol and culture on Sabouraud glucose agar with chloramphenicol and media for bacteria: blood agar, chocolate agar, CLED agar, and/ or MacConkey agar. Mycological cultures were incubated at 30°C for a minimum of 7 days. Identification of yeasts was carried out according to their colonial morphology, formation of germinative tubules, capacity for growth in presence of cycloheximide, and assimilation of carbon compounds through the ID 32C yeast identification system (bioMe´rieux, France). Identification of filamentous fungi was carried out according to the colonial morphology (time of growth, texture, color, presence of fungal elements) and microscopic observation of fungal structures (hyphas, conidiophores, phialides, types of conidiogenesis, and conidia). Information collected from patients with otomycosis included underlying factors and demographic and clinical data.
Results Microbial growth was present in 1,375 samples (52.2%) and fungal isolation in 390, which constitutes a 28.4% of all the positive samples. Direct
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Mycopathologia (2011) 172:307–310
microscopic examination was positive to 184 filamentous fungi in only 162 samples with positive culture (88.0%). A total of 412 isolates were found: 228 yeasts, and 184 filamentous fungi. Filamentous fungi were detected in 13.4% of the positive cultures and in 47.2% of the patients with otomycosis, in 22 cases associated with yeasts (5.6%). All the mixed infections were caused by two species: 12 Aspergillus flavus ? Candida parapsilosis, 4 Aspergillus flavus ? Candida albicans, 4 Aspergillus niger ? Candida parapsilosis, 1 Aspergillus niger ? Candida albicans, and 1 Aspergillus candidus ? Candida parapsilosis. Table 1 shows the distribution of the species. Aspergillus flavus (42.4%) and Aspergillus niger (35.9%) were the most frequent filamentous fungi. The characteristics of patients with otomycosis due to filamentous fungi are collected on Table 2. The infection was more frequent in men (54.9%) and in patients beyond 55 years (age range, 3–81 years). The most usual clinical signs and symptoms were: itching, otalgia, and hypoacusis. The difference among seasons is not significant and the range is between the lowest incidence of cases in fall (20.1%) and summer incidence (27.2%).
Discussion The incidence of otomycosis varies in the different geographical areas and is mainly determined by Table 1 Etiology of 390 otomycosis cases Species Yeasts
Number
Percentage
228
52.8
145
63.6
Candida albicans Candida glabrata
78 3
34.2 1.3
Candida tropicalis
2
0.9
Candida parapsilosis
Filamentous fungi
184
47.2
Aspergillus flavus
78
42.4
Aspergillus niger
66
35.9
Aspergillus fumigatus
23
12.5
Aspegillus candidus
13
7.1
Aspergillus terreus
3
1.6
Paecilomyces variotii
1
Total * Mixed culture in 22 cases
412*
0.5 100
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Table 2 Characteristics of 184 patients with otomycosis due to filamentous fungi Characteristics
Number
Percentage
Sex Men Women
101
54.9
83
45.1
2
1.1
Age in years B5 6–15
3
1.6
16–25
21
11.4
26–35
19
10.3
36–45
24
13.0
46–55
29
15.8
56–65
41
22.3
C65
45
24.5
Pruritus
35
19.0
Pruritus ? otalgia
22
12.0
Pruritus ? otalgia ? otorrhea Pruritus ? otalgia ? hypoacusis
13 48
7.1 26.1
Pruritus ? otalgia ? hypoacusis ? otorrhea
26
14.1
Pruritus ? otorrhea ? hypoacusis
12
6.5
Pruritus ? hypoacusis
15
8.1
Pruritus ? otorrhea
11
6.0
2
1.1
Spring
49
26.6
Summer
50
27.2
Autumn
37
20.1
Winter
48
26.1
Signs and symptoms
Otalgia ? otorrhea ? hypoacusis Seasonal period
environmental conditions. This pathology can reach high percentages in some tropical and subtropical countries and may constitute up to 25% of the infectious otitis [2, 3, 8, 9, 13]. Although this infection usually occurs in the warmest months, we have noticed a uniform distribution throughout all the seasons in Ca´diz, as a result of the mild weather that prevails during almost all the year [5]. All the ages can be affected, although we have detected a high number of cases in patients beyond 55 years old [1, 6, 8, 9, 13]. Distribution by gender is not significant. As to our series, there was a slight prevalence of men, in contrast to other series [6, 8, 9]. In Cadiz, predisposing factors of
otomycosis are especially concerned with an increase in the pH of the external auditory canal and an alteration of the quality and quantity of the earwax, as cause of frequent seawater bathing, along with a warm temperature, a high index of relative humidity and the ever-present wind [8, 9, 12]. In our zone, the infection is endemic and its incidence is high. The most usual clinical signs and symptoms were itching, otalgia, and hypoacusis, which are, despite some slight differences, the usual symptoms and signs described in published series [2, 3, 6, 8, 14]. Fungi causing otomycosis vary geographically. In general, they are yeasts and non-dermatophytes filamentous fungi, part of the common flora found in the external auditory canal, principally of the genera Candida and Aspergillus [2, 5, 7, 11, 12, 16–19]. Occasionally, other genera have also been described: Absidia, Exophiala, Fusarium, Gymnoascus, Mucor, Natrassia, Paecilomyces, Penicillium, Polypaecilum, Pseudoallescheria, Scopulariopsis, and Tritirachium [5, 6, 13, 20–27]. In some publications, Aspergillus is the most frequent genus involved in otomycosis [5, 8–10, 15, 28], while in others the predominant one is Candida [6]. As for our series, Candida was the most frequent genus and C. parapsilosis the prevailing species. Besides C. albicans, other species tend to be occasional [2, 13, 16, 21, 29, 30]. The prevalence of C. parapsilosis in our geographical area may be due to environmental factors or a high preference of this species to colonize the external auditory canal [5, 6, 11]. As for molds, Aspergillus niger is the prevailing one [2, 3, 6, 9, 11, 13 16, 18, 20, 30], probably due to its high preference for the external auditory canal and its ability to produce a great amount of conidia, although other Aspergillus species have also been described frequently, such as A. flavus, A. fumigatus, and A terreus, which are air-borne [6, 8, 13, 15, 16, 20, 21, 31]. Some authors report a higher proportion of otomycosis caused by A. flavus [5, 10] or by A. fumigatus [12, 17]. A. flavus is the prevalent species in Ca´diz. Some isolated cases due to other Aspergillus species (A. candidus, A. chevalieri, A. clavatus, A. glaucus, A. hollandicus, A. japonicus, A. luchuensis, A. niveus, and A. ustus) have been referred, most of them in non-European countries [8, 23, 32–34].
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