ORIGINAL ARTICLE VISWANATHA, SUMATHA, VIJAYASHREE Otomycosis in immunocompetent and immunocompromised patients: Comparative study and literature review Borlingegowda Viswanatha, MS, DLO; Dadarao Sumatha, MBBS; Maliyappanahalli Siddappa Vijayashree, MBBS, MS Abstract A comparative clinical study was carried out that included 50 cases of otomycosis in immunocompetent patients and 50 cases of otomycosis in immunocompromised patients. Clinical presentation, predisposing factors, mycologic profile, and treatment outcomes were compared. Aspergillus spp were the most commonly isolated fungi in the immunocompetent group, and Candida albicans in the immunocompromised group. Bilateral involvement was more common in the immunocompromised group. All the patients were treated with topical clotrimazole ear drops. Four patients in the immunocompromised group did not respond to treatment with clotrimazole but were treated successfully with fluconazole ear drops. Three patients had a small tympanic membrane perforation due to otomycosis. Introduction Otomycosis is a superficial, subacute, or chronic infection of the outer ear canal, usually unilateral, that is characterized by inflammation, pruritis, and scaling.1 It occurs because the protective lipid/acid balance of the ear is lost.2 Fungi cause 10% of all cases of otitis externa.2 In recent years, opportunistic fungal infections have gained greater importance in human medicine, perhaps because of the huge number of immunocompromised patients. However, such fungi may also produce infection in immunocompetent hosts.1 In immunocompromised patients, treatment of otomycosis should be vigorous to From the Department of ENT, Victoria Hospital and Bangalore Medical College and Research Institute, Bangalore, India. Corresponding author: Dr. Borlingegowda Viswanatha, MS, DLO, #716, 10th Cross, 5th Main, M.C. Layout, Vijayangar, Bangalore - 560 040, Karnataka, India. Email: drbviswanatha@yahoo.co.in 114  www.entjournal.com prevent complications such as hearing loss and invasive temporal bone infection.3 We conducted a comparative clinical study involving 50 immunocompetent and 50 immunocompromised patients with otomycosis. Clinical presentation, predisposing factors, mycologic profile, and treatment outcomes were compared. A review of the literature revealed no reported case series of otomycosis in immunocompromised patients. Patients and methods This prospective study was carried out in 100 patients with otomycosis—50 who were immunocompetent and 50 who were immunocompromised. In the immunocompromised group, 36 patients were diabetic, 9 patients had AIDS, and 5 patients were undergoing radiation therapy. The patients’ clinical profiles regarding age, sex, laterality, and clinical presentation were documented. Only cases of otomycosis in patients with positive cultures were included in this study. Patients with otomycosis associated with otitis media and those already using antifungal ear drops were excluded. The outer part of patients’ external auditory canals was cleaned using sterile swabs, taking material from the deeper portion of the ear canal that was sent for fungus culture. After microscopic suction clearance, antifungal ear drops were given for 3 weeks. All patients were followed for a minimum of 6 weeks. Swabs were also taken from the external auditory canals of 10 immunocompetent and 10 immunocompromised individuals without otomycosis. No fungi were isolated on fungal culture of these swabs. Treatment of patients with otomycosis includes microscopic suction clearance of the fungal mass, disENT-Ear, Nose & Throat Journal  March 2012 Acclaimed Image Quality, Advanced Features... THE NEW LARYNGEAL STROBE KayPENTAX is proud to introduce the Laryngeal Strobe, Model 9400, the latest-generation light source for stroboscopy and general endoscopy. 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Our patients’ initial treatment regimen consisted of clotrimazole ear drops for 3 weeks. Those whose otomycosis did not respond to clotrimazole were switched to fluconazole ear drops. Patients were also advised to keep their ears dry for 3 weeks. Results Table 1. Age and sex distribution of patients participating in the present study Immunocompetent group (n = 50) Immunocompromised group (n = 50) 0 (0%) 0 (0%) 11-20 6 (12%) 0 (0%) 21-30 24 (48%) 2 (4%) 31-40 10 (20%) 18 (36%) 41-50 3 (6%) 26 (52%) Age (yr) 0-10 Demographics. In the immunocom51-60 4 (8%) 2 (4%) petent group, patients’ ages ranged 61-70 3 (6%) 1 (2%) from 18 to 65 years, and the peak 0 (0%) 1 (2%) incidence (48%) was seen in the third 71-80 decade of life. In the immunocompromised group, ages ranged from Sex 38 (76%) 32 (64%) 26 to 74 years, and peak incidence Male (52%) was seen in the fifth decade Female 12 (24%) 18 (36%) of life (table 1). In both groups, a higher incidence was seen in male patients; there were seen more in the immunocompromised than in the more female patients in the immunocompromised group immunocompetent group (table 3). (36%) than the immunocompetent group (24%) (table 1). Clinical examination revealed canal skin erythema and Laterality. Right ear involvement was more common fungal debris in all cases. Three immunocompromised in both the groups: in 26 (52%) of the immunocompe- patients had a small central perforation of the tympanic tent patients and in 18 (36%) of the immunocompro- membrane behind the handle of the malleus. They had mised patients. The left ear was involved in 16 (32%) not previously experienced ear pain or otitis media. and 12 (24%), respectively, of these groups. Bilateral Fungus isolated. In immunocompetent patients Asperinvolvement was seen more in 20 (40%) of the immu- gillus niger was isolated in 28 (56%) of cases, Aspergillus nocompromised patients compared with 8 (16%) of the fumigatus in 9 (18%), Candida albicans in 8 (16%), and immunocompetent patients. Penicillium chrysogenum (previously known as PenicilPredisposing factors. Ear cleaning with sticks and lium notatum) in 5 (10%) (figure). In immunocomproswabs, the use of topical antibiotic or steroid ear drops, and the use of Table 2. Predisposing factors for the development of otomycosis in nonsterile oil in the ear were seen study patients in more immunocompetent paImmunocompetent Immunocompromised tients than immunocompromised group group patients (table 2). No predisposing (n = 50) (n = 50) factors were seen in 8 (16%) of the Predisposing factors 31 (62%) 23 (46%) immunocompetent and 12 (24%) of Ear cleaning with sticks & swabs the immunocompromised patients. Symptoms and complications. Use of nonsterile oil in ear 15 (30%) 11 (22%) Itching and ear discharge were seen 9 (18%) more in the immunocompetent Use of topical antibiotic or 16 (32%) steroid ear drops than in the immunocompromised patients, while ear pain was pres- Swimming habits 4 (8%) 1 (2%) ent in more immunocompromised patients. A blocked sensation, de- None 8 (16%) 12 (24%) creased hearing, and tinnitus were 116  www.entjournal.com ENT-Ear, Nose & Throat Journal  March 2012 VISWANATHA, SUMATHA, VIJAYASHREE Table 3. Symptoms seen in study patients Discussion Otomycosis is described as a fungal infection of the external ear canal. Immunocompetent Immunocompromised This infection is worldwide in disgroup group (n = 50) (n = 50) tribution, but it is more common in tropical and subtropical regions.4 Symptoms Otomycosis is sporadic and caused Itching 46 (92%) 40 (80%) by a wide variety of fungi, most of Ear discharge 38 (76%) 32 (64%) which are saprobes occurring in Ear pain 20 (40%) 24 (48%) diverse types of environmental mateBlocked sensation 16 (32%) 22 (44%) rial.1 In his review of the literature, Decreased hearing 9 (18%) 14 (28%) Wolf stated that no less than 53 Tinnitus 5 (10%) 12 (24%) different species of fungi had been reported to cause the disease.5 Otomised patients, A niger was isolated in 17 (34%) cases, mycosis affects 10% of the population in their lifetime.2 A fumigatus in 5 (10%), C albicans in 26 (52%), and P Fungi are abundant in soil or sand that contains dechrysogenum in 2 (4%) (table 4). composing vegetable matter. This material is desiccated Treatment outcomes. All the patients in our immu- rapidly in tropical sun and blown in the wind as small nocompetent group responded well to treatment, and dust particles. The airborne fungal spores are carried by there were no recurrences. In our immunocompromised water vapors, a fact that correlates the higher rates of group, 4 patients did not respond to treatment with infection with the monsoon, during which the relative clotrimazole ear drops, but they were successfully treated humidity rises to 80%.6 with fluconazole ear drops. A fungal mass does not protrude from the external ear canal, even in most chronic cases. A B This is because the fungus does not find its nutritional requirements outside the external ear canal. In the present study, the Aspergillus growth rate was found to be higher at the temperature of 37°C, a fact that is clinically supported by the predilection of fungi to grow in the inner one-third of the external ear canal.7 An immunocompromised host is more susceptible to otomycosis. D C Patients with diabetes, lymphoma, or AIDS and patients undergoing or receiving chemotherapy or radiation therapy are at increased risk for potential complications from otomycosis.8 Literature review. Incidence by age and sex. In our study, the highest incidence of otomycosis in the immunocompetent patients was seen in the age group of 21 to 30 years (48%), which agreed with the Figure. Photomicrographs (original magnification ×40) show Aspergillus niger (A), 8 Aspergillus fumigatus (B), Candida albicans with budding cells (C), and Penicillium findings of Chander et al, Paulose 9 10 et al, Mohanty et al, and Ho et chrysogenum (D) fungi. 118  www.entjournal.com ENT-Ear, Nose & Throat Journal  March 2012 Visit Allegra.com/hcp for samples and coupons! Are you recommending allergy symptom relief that’s fast* & non-sedating? ONLY ALLEGRA ® ...gives you both! *Starts working at hour one. Applies to first dose only. † Among OTC branded antihistamines. Stops symptoms, not patients ts 4075A 2012 Chattem, Inc. © † VISWANATHA, SUMATHA, VIJAYASHREE al.11 The higher incidence in these Table 4. Fungus isolated in samples obtained from study patients patients may be due to the fact that these people are more exposed to Immunocompetent Immunocompromised group group the mycelia (due to occupational (n = 50) (n = 50) exposure, traveling, etc.), whereas older and younger age groups are Fungus not as exposed to these pathogens. Aspergillus niger 28 (56%) 17 (34%) The highest incidence in our immuAspergillus fumigatus 9 (18%) 5 (10%) nocompromised patients was found Candida albicans 8 (16%) 26 (52%) in the age group of 41 to 50 years 5 (10%) 2 (4%) (52%). This may be due to the fact Penicillium chrysogenum that immunocompromised states • high temperature that closely approximates body are less common in younger age groups. In both our immunocompetent and immunocompro- temperature; and • general diseases, such as diabetes mellitus. mised patients, the incidence of otomycosis was higher in male patients, which agreed with the findings of Paulose Mohanty et al,10 Rama Kumar et al,15 and Than et al16 et al,9 Ho et al,11 Yassin et al,12 and Hueso Gutiérrez et al.13 Laterality. Paulose et al,9 Yassin et al,12 and Yehia et found trauma to be the most common predisposing fac14 al found that otomycosis is predominantly a unilateral tor, as it was in both groups in the present study. Joy et disease and that the right ear is affected more often than al17 conducted an experimental study for the production the left, which also was true in both groups of our pa- of otomycosis in human volunteers. The results were tients. Bilateral involvement was more common in our more positive when trauma was inflicted, and ear wax immunocompromised than in our immunocompetent was absent in most of the cases. Wax probably has an patients (2.5:1). This may be due to bilateral ear canal inhibitory effect on fungal growth.9 Symptoms. The most common symptoms in our pasusceptibility to fungal infection in immunocomprotients were itching, ear pain, ear discharge, a blocked mised patients. All our patients with bilateral otomycosis had similar sensation, decreased hearing, and tinnitus. These were findings in both the ears, and the same fungus was iso- also the symptoms observed by Paulose et al, Mohanty lated on culture from each ear. Chander et al also found et al, and Ho et al.9-11 It should be noted that the correct that the same fungus was responsible in both ears in diagnosis of otomycosis requires a high index of suspicion, given that the most common presenting symptoms, bilateral otomycosis.8 Predisposing factors. Ear cleaning and the use of otalgia and otorrhea, are nonspecific.3 In our study, itching and ear discharge were seen topical ear drops or oils were seen more often in our immunocompetent than in our immunocompromised more in immunocompetent patients than in immunopatients. The use of topical antibiotics and nonsterile oil compromised patients. Pain was present in 24 (48%) changes the physiochemical environment of the ear and immunocompromised patients and in 20 (40%) immunocompetent patients. A blocked sensation, decreased thus favors fungal growth and colonization. Ear cleaning habits may contribute to pathogenesis hearing, and tinnitus were also seen in more immunobecause traumatized external ear canal skin can present compromised than immunocompetent patients. The a favorable condition for fungal growth.12 Mechanical duration of symptoms varied from 5 to 21 days. There was no significant difference in duration of symptoms trauma also aids in the colonization of fungus. Yassin et al stated that airborne fungi are responsible between immunocompetent and immunocompromised for otomycosis.12 They considered many factors in the patients. Fungi isolated. In the studies conducted by Chander external ear canal to contribute to a favorable condition et al, Paulose et al, Mohanty et al, and Yassin et al, Asfor the establishment of many fungi, including12: pergillus spp were the most common fungi isolated, and C albicans was the next most common.8-10,12 • trauma; In our group of immunocompetent patients, A niger • relatively high humidity in the external ear canal; • epithelial debris in various stages of chemical was isolated in 28 (56%) cases, A fumigatus in 9 (18%) cases, C albicans in 8 (16%) cases, and P chrysogenum breakdown; 120  www.entjournal.com ENT-Ear, Nose & Throat Journal  March 2012 OTOMYCOSIS IN IMMUNOCOMPETENT AND IMMUNOCOMPROMISED PATIENTS: COMPARATIVE STUDY AND LITERATURE REVIEW in 5 (10%) cases. In our immunocompromised patients, A niger was isolated in 17 (34%) cases, A fumigatus in 5 (10%) cases, C albicans in 26 (52%) cases, and P chrysogenum in 2 (4%) cases. In tropical countries, Aspergillus spp are considered the predominant organisms implicated in the etiology of otomycosis.1 In separate clinical studies, Rama Kumar15 and Jaiswal18 found C albicans to be responsible for the majority of cases, and it was isolated in 47 and 46%, respectively, of their cases. Treatment. Bassiouny et al studied the effects of antifungal agents and found that clotrimazole and econazole were effective antifungal agents in the treatment of otomycosis.19 According to Stern et al and Jackman et al, clotrimazole is an effective antifungal agent against most yeasts and fungi, and nystatin has the widest spectrum of activity among the antifungals.20,21 In a study by Yadav et al, fluconazole was found to be an effective antifungal agent in the treatment of otomycosis.22 Complications. Tympanic membrane perforation may occur as a complication of otomycosis that starts in an ear with an intact ear drum.3 In the study by Rama Kumar, the incidence of tympanic membrane perforation in otomycosis was found to be 11%.15 He also stated that perforations were more common with otomycosis caused by C albicans. Most of the perforations were behind the handle of the malleus. The mechanism of perforation has been attributed to mycotic thrombosis of the tympanic membrane blood vessels, resulting in avascular necrosis of the tympanic membrane.3,23 Three patients in our immunocompromised group experienced tympanic membrane perforation. The perforations were small and situated in the posterior quadrant of the tympanic membrane. They healed spontaneously with medical treatment. Rarely, fungi can cause invasive otitis externa, especially in immunocompromised patients. Aggressive systemic antifungal therapy is required in these patients, and a high rate of mortality is associated with this condition.2 In conclusion, C albicans and Aspergillus spp were the most commonly isolated fungi seen in immunocompromised and immunocompetent patients, respectively. Bilateral involvement was seen more in the immunocompromised group. Clotrimazole is an effective treatment for otomycosis, and fluconazole is a good alternative for patients in whom clotrimazole is not effective. Rarely, tympanic membrane perforations can occur as a complication of otomycosis in immunocompromised patients. Volume 91, Number 3 References 1. Jadhav VJ, Pal M, Mishra GS. Etiological significance of Candida albicans in otitis externa. Mycopathologia 2003;156(4):313-15. 2. Carney AS. Otitis externa and otomycosis. In: Gleeson MJ, Jones NS, Clarke R, et al (eds). Scott-Brown’s Otolaryngology, Head and Neck Surgery, Vol. 3. 7th ed. London: Hodder Arnold Publishers; 2008:3351-7. 3. Rutt AL, Sataloff RT. Aspergillus otomycosis in an immunocompromised patient. Ear Nose Throat J 2008;87(11):622-3. 4. Aktas E, Yigit N. Determination of antifungal susceptibility of Aspergillus spp. responsible for otomycosis by E-test method. J Mycol Med 2009;19(2):122-5. 5. Wolf FT. Relation of various fungi to otomycosis. Arch Otolaryngology 1947;46(3):361-4. 6. Geaney GP. Tropical otomycosis. J Laryngol Otol 1967;81(9):987-97. 7. Mugliston T, O’Donoghue G. Otomycosis—a continuing problem. J Laryngol Otol 1985;99(4):327-33. 8. Chander J, Maini S, Subrahmanyan S, Handa A. Otomycosis—a clinico-mycological study and efficacy of mercurochrome in its treatment. Mycopathologia 1996;135(1):9-12. 9. Paulose KO, Al Khalifa S, Shenoy P, Sharma RK. Mycotic infection of the ear (otomycosis): A prospective study. J Laryngol Otol 1989;103 (1):30-5. 10. Mohanty JC, Mohanty SK, Sahoo RC, et al. Clinico-microbial profile of otomycosis in Berhampur. Indian Journal of Otology 1999;5(2): 81-3. 11. Ho T, Vrabec JT, Yoo D, Coker NJ. Otomycosis: Clinical features and treatment implications. Otolayngol Head Neck Surg 2006;135 (5):787-91. 12. Yassin A, Maher A, Moawad MK. Otomycosis: A survey in the eastern province of Saudi Arabia. J Laryngol Otol 1978;92(10):869-76. 13. Hueso Gutiérrez P, Jiménez Álvarez S, Sañudo E, et al. Presumption diagnosis: Otomycosis. A 451 patients study [in Spanish]. Acta Otorrinolaringol Esp 2005;56(5):181-6. 14. Yehia MM, Al-Habib HM, Shehab NM. Otomycosis: A common problem in north Iraq. J Laryngol Otol 1990;104(5):387-9. 15. Rama Kumar K. Silent perforation of tympanic membrane and otomycosis. Indian Journal of Otolaryngology and Head & Neck Surgery 1984;36(4):161-2. 16. Than KM, Naing KS, Min M. Otomycosis in Burma, and its treatment. Am J Trop Med Hyg 1980:29(4):620-3. 17. Joy MJ, Agarwal MK, Samant HC. Mycological and bacteriological studies in otomycosis. Indian Journal of Otolaryngology and Head & Neck Surgery 1980;32:72-5. 18. Jaiswal SK. Fungal infection of ear and its sensitivity pattern. Indian Journal of Otolaryngology and Head & Neck Surgery 1990;42(1): 19-22. 19. Bassiouny A, Kamel T, Moawad MK, Hindawy DS. Broad spectrum antifungal agents in otomycosis. J Laryngol Otol 1986;100(8):867-73. 20. Stern JC, Shah MK, Lucente FE. In vitro effectiveness of 13 agents in otomycosis and review of the literature. Laryngoscope 1988;98 (11):1173-7. 21. Jackman A, Ward R, Apri M, Bent J. Topical antibiotic induced otomycosis. Int J Pediatr Otorhinolaryngol 2005;69(6):857-60. 22. Yadav SP, Gulia JS, Jagat S, et al. Role of ototopical fluconazole and clotrimazole in management of otomycosis. Indian Journal of Otology 2007:13;12-15. 23. Stern JC, Lucente FE. Otomycosis. Ear Nose Throat J 1988:67(11):8045, 809-10. www.entjournal.com  121