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Jundishapur J Microbiol. 2015 September; 8(9): e21776. DOI: 10.5812/jjm.21776 Research Article Published online 2015 September 8.

Etiologic Agents of Otomycosis in the North-Western Area of Iran

1 2,* 3 Abdolhassan Kazemi, Maryam Majidinia, Abbasali Jaafari, Seyyed Amin Ayatollahi 4 5 6 Mousavi, Ali Zarei Mahmoudabadi, and Hossein Alikhah

1Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, IR Iran 2Student Research Committee, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, IR Iran 3Basic Science Department, International Branch, Shahid Sadoughi University of Medical Sciences, Yazd, IR Iran 4Department of Medical Mycology and Parasitology, Faculty of Medicine, Kerman University of Medical Sciences, Kerman, IR Iran 5Health Research Institute, Infectious and Tropical Diseases Research Centre, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, IR Iran 6Publication Office, Tabriz University of Medical Sciences, Tabriz, IR Iran *Corresponding author : Maryam Majidinia, Student Research Committee, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, IR Iran. Tel: +98 9360488846, Fax: +98 4113364666, E-mail: [email protected] Received: ; Revised: ; Accepted: September 17, 2014 March 25, 2015 May 27, 2015

Background: Otomycosis is a superficial fungal often involves the pinna and external auditory canal. It is a pathologic condition, Candida with and , the most common fungal species. It is common worldwide but more prevalent in tropical and subtropical countries Objectives: The aim of this study was to determine the etiologic agents and local epidemiologic pattern of otomycosis in northwest Iran. Patients and Methods: A series of 140 patients with clinically symptomatic otomycosis were studied in 21 cities, towns, and villages throughout northwest Iran between 2009 and 2011. Clinical samples were collected by swabs and then assessed by mycological investigation. Results: Otomycosis was diagnosed in 129 cases (92%, 76 male, 53 female) with the highest prevalence of cases occurring in males between 21 - 40 years of age. From an etiological point of view, 116 patients (90%, 21 - 40 years old) were infected by saprophytic and 9 patients Eurotium (7%) were infected by . Three cases (2%) involved , and in one case (1%) the subject was infected with (the Aspergillus fumigatus Aspergillus niger A. flavus A. fumigatus perfect stage of ). was the most common mold that was isolated, followed by , , Penicillium Fusarium Rhizopus Candida C. albicans C. tropicalis, spp., spp., and spp. A total of 2 belonging to genus , and were isolated. Conclusions: Our study showed a high prevalence of otomycosis in the northwestern area of Iran. As such, proper diagnosis and treatment by aseptic techniques for this disease is urgently needed. Keywords: Aspergillus niger Otomycosis; Fungi; Yeasts;

1. Background sis Alternaria Candida Otomycosis, or fungal infection, is a superficial , , , and , as well various fungal infection of the ear that may include the pinna, dermatophytes (13-18). external auditory canal, and tympanic membrane (1). Based on various studies, the current opinion is that This fungal infection has been reported in both human fungi may cause otomycosis when the ear is in poor and animals (2, 3). The is not the actual cause health. As such, otomycosis is more common amongst but merely a secondary contaminant in cases of people of lower socioeconomic levels or who live under external, therefore otomycosis can be seen in mixed poor hygienic conditions (19-21). The main risk factors bacterial and fungal (3). The causative agents for otomycosis include moisture; minor ; of otomycosis involve various types of fungi, such as the use of broad spectrum antibiotics, steroids, chemo- hyaline saprophytic mold, dematiaceous saprophytic therapeutic agents, or topical ear drops; physical injury; mold, yeasts, and, rarely, pathogenic like der- living in warm and humid climates; and frequent bath- matophytes (4-8). It is notable that the most common ing or swimming (19, 22, 23). In addition, immunocom- As- causative agents of otomycosis are from the genus promised hosts are more vulnerable to otomycosis. pergillus Aspergillus niger, , particularly which has been Patients with diabetes, lymphoma, HIV, endocrine ab- established by many studies (9-12), but some authors normalities, changes in hormonal balance, or a history have collected more than 50 causative fungi species of transplantation, as well as patients receiving chemo- in their studies. These agents include species from the therapy or radiotherapy, are at a greater risk of contract- Penicillium, Fusarium Mucoraceae Scopulariop- genera , , ing otomycosis than healthy individuals. Tortuosity, di-

Copyright © 2015, Ahvaz Jundishapur University of Medical Sciences. This is an open-access article distributed under the terms of the Creative Commons Attribu- tion-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncom- mercial usages, provided the original work is properly cited. Kazemi A et al. ameter, and length of the auditory canal are unrelated room temperature (25°C) and observed for 3 weeks. Cul- to the risk of developing infection (24, 25). In otomyco- tures were examined every day to determine the prob- sis, fungi may cause either true initial invasion or sec- able growth of fungi colonies and their identification. ondary invasion after tissue abnormality resulting from The identification process of the isolated fungi was a primary bacterial infection (26, 27). carried out through traditional methods, including Furthermore, there are various antifungal agents that macromorphological and micromorphological stud- may be used to treat otomycosis. Mercurochrome (1% - ies. Lactophenol cotton blue preparations were made 2% solution), clotrimazole, miconazole, amphotericin B from the cultures and then examined microscopi- ointment, meta cresol acetate (Cresatin), thymol (1%) in cally. The slide culture technique was also used when meta cresol acetate, and phenylmercuric acetate (0.02%) a study of the morphological details of various fungi in sterile water or as borate ointment (0.005% and 0.04%) was necessary for exact identification. The isolated can be used to treat patients after cleaning the ear using yeast species were identified using classic laboratory Burow’s solution, urea-acetic acid solution, or aluminum methods including morphology germ tube produc- acetate solution (5%) (7, 9, 28). Antifungal agents should tion, the production of different spores on corn meal be chosen after fungus identification by direct micros- agar (Oxoid Ltd., UK) with Tween 80, and the API 20C copy examinations and culture, because various types of AUX identification system based upon the assimilation causative fungi are sensitive or resistant to specific types of carbohydrates (bioMerieux, Marcy L’Etoile, France). of antifungal agents. All mycological investigation was carried out in the medical mycology department of the Tabriz university 2. Objectives of medical sciences. These criteria were used to identify The present study was carried out to ascertain the etio- the and to begin treatment with an logic agents and epidemiologic patterns of otomycosis in appropriate antifungal agent. The patients were called northwestern Iran. in for a regular follow-up after four weeks for clinical and mycological reinvestigation, including direct mi- 3. Patients and Methods croscopy examinations and repeated cultures. The study involved 140 patients who presented with 4. Results symptoms of otomycosis from 21 cities, towns, and vil- lages in northwest Iran between 2009 and 2011. Patients Out of 140 cases submitted for investigation, 129 re- reported to the ear, nose and throat (ENT) department sults were otomycosis-positive (92%, 76 male, 53 female). of Tabriz university of medical sciences and were inves- From an etiological point of view, 116 patients (90%, 21 - tigated, prospectively. First of all, clinical details such as 40 years old) were infected by saprophytic mold, and chief complaint, name, age, gender, suspected risk fac- 9 patients (7%) were infected by yeast. Three cases (2%) tors, hygiene status, occupation, history of infection, involved dermatophytes, and in one case (1%), the sub- Eurotium address, and other relevant information were recorded. ject was infected with (the perfect stage of A. fumigatus Informed written consent was obtained from all sub- ). In our results, correlations between the jects. After establishing a clinical diagnosis, specimen pathology of otomycosis with etiology, gender, and and clinical materials from the external auditory canal age were emphasized. The patients belonged to all were collected from all patients by means of sterile cot- age groups, but the highest prevalence of otomycosis ton swabs. Materials were divided into two samples for (73 cases) was found in patients between 21 - 40 years mycological processing. One sample of external audi- of age (57% of positive cases). Among all 129 positive tory debris was clarified with a 10% potassium hydrox- cases, 79 subjects (59%) were male and 53 patients (41%) ide solution on a glass slide. The slide was then heated were female, and nearly all were agricultural workers gently over a low flame and examined directly using a from a low socioeconomic status who exhibited it was microscope. The morphology, amount of fungi (yeast the result of a subjective assessment by the clinician. and mold), and other relevant characteristics (spores, No patients presented with fungal infection elsewhere arthroconidia, septate and non-septate hyphae, etc.) in the body. However, the patients in whom dermato- were identified. phytes were isolated also presented with . C. albi- The second sample of the material was inoculated into Additionally, two of the patients infected with cans two sets of three different media tubes. One tube con- also presented with candidal in tained Sabouraud Dextrose agar (BioMerieux, Marcy-1, their fingernails Etoile, France) with 0.5 mg/mL cyclohexamide (Ap- Before seeking medical attention, the majority of pliChem GmbH, Germany) and 0.05 mg/mL chloram- patients attempted to self-treat their symptoms with phenicol (AppliChem GmbH, Germany). A second set different types of eardrops, including various oils, gar- contained Sabouraud’s Dextrose agar and 0.05 mg/mL lic juice, antibiotics, antiseptics, and steroids, among chloramphenicol. The third tube contained only Sab- other unknown types of materials based on traditional ouraud’s Dextrose Agar. The media were incubated at public medicine, herbal medicine, and domestic ad-

2 Jundishapur J Microbiol. 2015;8(9):e21776 Kazemi A et al. vice. The most common complaint among patients was 5. Discussion an in the external auditory canal and tympanic During recent years, there has been a dramatic increase membrane (100%), followed by aural fullness in 68 sub- in the incidence of mycotic infections and in the diver- jects (53%), ear discharge in 17 cases (13%), and ear ache sity of pathogenic fungi. Otomycosis, a fungal infection in 14 patients (11%). Infection of the left ear was seen in of the ear, is found throughout the world (3). However, it 51 cases (39.5%), while the right ear was involved in 54 is more prevalent in tropical and subtropical countries cases (42%). Bilateral infection was diagnosed in 36 pa- because a high degree of humidity, hot weather, and the tients (18.5%). The most commonly isolated source of A. niger A. flavus A. fumigates presence of dust in the environment favor the dissemi- infection was , followed by , , Penicillium nation and growth of molds. Pruritus, otalgia, hearing various species, various yeasts (specifically, Candida Fusarium loss, and ear fullness are the most common features of a number of species), various species, Eurotium A. glaucus this infection (29). Otomycosis studies in patients with (the perfect state of ), and finally, a Rhizopus suspected have been conducted in many differ- species of (zygomycetes). Isolated yeasts in- C. albicans C. tropicalis ent countries, including the USA (30), Spain (18), Bahrain cluded (7 cases) and (2 cases). mentag- (31), Brazil (32), Turkey (33), Russia (20), Nigeria (20, 34), Isolated dermatophytes included rophytes T. verrucosum Microsporum Nepal (35), Gabon (32), and Iraq (36). The results of these (1 case), (1 case), and canis studies suggest that otomycosis has a global prevalence; (1 case) (Table 1). in addition, findings from these studies demonstrate Foreign bodies, including dead insects and pieces of Aspergillus A. ni- that the saprophytic fungus , especially cotton cloth, were seen in the external auditory canals ger A. fumigatus, C. albicans, of 9 patients (7%). Also, wax was present in the external , and are the main agents of auditory canal in 8 cases (6%). Of all 129 patients, three this infection. In our study, the prevalence of otomycosis were diabetic, but none had a history of systemic cor- was 92%, which is higher than the results found in some ticosteroids, immunosuppressant drugs, endocrine other studies, including work by Kumar (37), who found abnormalities, or external auditory canal anatomical otomycosis in 75.9% of patients; Pardhan et al. (35), who abnormalities. The patients were called in for a regular found otomycosis in 79.4% of patients, Kaur et al. (38), follow-up after four weeks for clinical and mycological who found the disease in 74.7% of patients; Chin and Je- reinvestigation, including direct microscopy examina- gathesan (39), who found it in 74.6% of patients; Aneja tions and repeated cultures. All patients were symptom- et al. (19) who found otomycosis in 78% of patients, and free at that point, and no fungal elements were found by Ozcan et al. (33), who reported that 65% of their patients otoscopy, direct microscopy, or repeated culture. were positive for otomycosis. A higher incidence of otomycosis has been observed in males, most of whom are active in the agriculture in- Table 1. Etiologic Agents of Otomycosis a dustry, are of low socioeconomic status, and who exhibit Fungal Species Incidence poor personal hygiene. This finding does not agree with results from a study by Aneja et al. (19) in which the preva- Aspergillus niger lence of otomycosis in females was higher than in males. 73 (62.9) In addition, our study also reported that 57% of all posi- A. flavus 24 (20.7) tive cases were found in patients between 21 - 40 years of age, which is similar to findings by Ologe and Nwabuisi A. fumigates 11 (9.5) (34). A high prevalence in this age group may be associat- ed with occupational activity, as a significant number of Penicillium 4 (3.4) individuals in this age range hold jobs involving agricul- Fusarium ture, horticulture, harvesting, farm work, and seasonal 2 (1.7) construction work that often takes place in small cities Rhizopus and dusty environments. 1 (0.8) The etiologic agents responsible for otomycosis may be Unknown 1 (0.8) classified into three groups: saprophytic molds, yeasts, and dermatophytes. Furthermore, saprophytic molds 7 (5.4) may be grouped into ascomycetes and zygomycetes (1, 4, 26). As Table 1 demonstrates, saprophytic molds were the C. tropicalis 2 (1.7) most common etiologic agents, responsible for 116 (90%) Dermatophytes cases of otitis external, followed by the yeasts belonging 3 (2.3) Candida to species (9 cases, 7%). The third group, derma- Eurotium tophytes, was observed in 3 cases (2%). Thus, in this study, 1 (0.8) the rate of saprophytic mold infection was approximate- a Values are presented as No. (%). ly 13 times greater than that of other types of fungi. Other authors have also postulated that saprophytic molds are

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