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CASE REPORT A case of otomycosis caused by Lichtheimia corymbifera (syn. Absidia corymbifera, Mycocladus corymbifer) in a healthy immunocompetent individual

Dhara H Vyas, Parul D Shah Department of Microbiology, Smt. N. H. L. Municipal Medical College, Ellisbridge, Ahmedabad, India

A case of otomycosis caused by Lichtheimia corymbifera from an immunocompetent patient with no known Abstract predisposing factor is reported. A 55-year-old, otherwise healthy male was presented to us with history of left-sided earache and yellowish-white ear discharge since 10 days. Ear discharge and bits of necrotic tissue were collected from ear through otoscope and processed. Direct wet mount by potassium hydroxide (10% KOH) was performed which showed broad, aseptate and branched hyphae suggestive of zygomycosis. On culture after 48 hours, cottony, wooly and fluffy growth was observed. Culture was subjected to Lactophenol Cotton Blue (LCB) mount which confirmed the presence ofL. corymbifera. The patient responded well to suction clearance and debridement followed by drug therapy with amphotericin B.

Keywords: Lichtheimia corymbifera, Otomycosis, Zygomycosis

Introduction congeneric with any of the thermotolerant species. Therefore, this group had to be renamed with the oldest available genus Otomycosis is a subacute or acute superficial mycotic infection name, Lichtheimia,[5] typified by Lichtheimia corymbifera. of the outer ear canal that is caused by opportunistic fungi. According to Hoffmanet al , [5] the genus Lichtheimia contained The infection is usually unilateral and characterized by four species: Lichtheimia corymbifera (syn. Absidia corymbifera, inflammation, pruritus, scaling and severe discomfort such as Mycocladus corymbifer), Lichtheimia ramosa (syn. Absidia suppuration and pain.[1] Otomycosis is caused by some species ramosa, Mycocladus ramosus), Lichtheimia blakesleeana of saprophytic fungi, which are found in nature and / or form (syn. Absidia blakesleeana, Mycocladus blakesleeanus) and a part of the commensal flora of healthy external auditory Lichtheimia hyalospora (syn. Absidia hyalospora, Mycocladus canal. Common ones are Aspergillus niger, Aspergillus flavus, hyalosporus). Of these, only L. corymbifera and L. ramosa Aspergillus fumigatus and Candida spp. especially Candida have been reported from human infections. Others include Mucor, Apophysomyces and Saksenaea species.[3] These fungi albicans. Others are Pseudallescheria boydii, Scopulariopsis are ubiquitous saprophytes found in soil, manure plants and spp., Penicillium, Rhizopus, Absidia, etc.[2] decayed foods and can be pathogenic in immunocompromised patients.[6] Mucormycosis is an opportunistic fungal infection that seldom occurs in individuals with a competent immune system. It is Absidia spp. are filamentous fungi that are cosmopolitan and caused by fungi of order Mucorales and class Zygomycetes and like other members of the class Zygomycetes, they are common most commonly by organisms belonging to genus Rhizopus.[3] The Zygomycetes genus Lichtheimia was first named Mycocladus, Access this article online [4] typified byMycocladus verticillatus. However, the type strain Quick Response Code: of that species turned out to represent a mixed culture of Absidia Website: sensu stricto, and possibly, a Lentamyces species; thus, it was not www.indianjotol.org

Address for correspondence: Dr. Parul D Shah, DOI: Department of Microbiology, Smt. N. H. L. Municipal Medical College, 10.4103/0971-7749.85806 Ahmedabad – 380 006, India. E-mail: [email protected]

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Vyas and Shah: Case of otomycosis by Lichtheimia corymbifera

environment contaminants. A. corymbifera is a relatively rare On aerobic bacterial culture, moderate growth of Staphylococcus case of human zygomycosis.[7] Although infection with A. epidermidis was found. As S. epidermidis is one of the normal corymbifera usually occurs in immunosuppressed individuals, floras of the external auditory canal, isolation of S. epidermidis Absidia infections in immunocompetent hosts have also been was considered as nonpathogenic.[11] described.[8-10] Discussion Case Report Otomycosis is one of the common entities affecting A 55-year-old male presented to our ENT OPD with history of the external auditory meatus and the ear canal. The left-sided earache and ear discharge since 10 days. There was no presenting symptoms include: scaling, pain, pruritus and history of nasal discharge/bleeding or throat pain. There was erythema. Wax formation is also common.[11] According to no fever, vomiting or any other associated symptoms. Patient a clinicomycological study by Ravinder Kaur et al, earache was not suffering from diabetes or any other chronic illness. and ear discharge are the major complaints in 65.2% and [12] History of chronic infection of ear, use of oil, eardrops, steroids, 50.5% patients, respectively. Symptoms correlated well swimming and other immunocompromised conditions were with our patient. A study done by Hueso Gutierrez et al ruled out. Patient had an agricultural background. showed that of the positive samples that came from the ENT clinic (84.3% of the positive samples) 60.56% had not had [13] On general examination, he was found to be normal. On ear previous otological pathology. Otomycosis can occur in examination, yellowish-white sticky thick discharge along both temperate and tropical environment. The prevalence [1] with bits of necrotic tissue was found in the left ear. Right ear of disease is greatest in hot, humid and dusty areas. examination was normal. Radiological examination did not Otomycosis has a worldwide distribution and it is estimated reveal any bony involvement. Routine laboratory parameters that approximately 10-20% of total external otitis cases are were normal. due to otomycosis. Otomycosis is more frequent in adults and is less common among children.[2] Tissue material was sent for mycological examination. Tissue Zygomycetes is one of the causative agents of otomycosis. was minced and subjected to wet mount preparation by Lichtheimia is one among different genera of Zygomycetes. potassium hydroxide (10% KOH) examination. Zygomycosis The most commonly isolated species is L. corymbifera. It is was confirmed by the presence of broad, aseptate fungal of interest to note that the patient was a dairy farmer and elements with ribbon-like appearances at places in direct we speculate that he became colonized with A. corymbifera microscopy. following occasional exposure to the fungus. Associations between Absidia infection and farms have been previously Multiple ear discharge specimens were collected with sterile described. A study in Finland reported high airborne fungal swab sticks and were rolled over the surface of two different spore concentration including that of A. corymbifera, which Sabouraud’s dextrose agar (SDA) media with antibiotics to rule is also found in feeding and bedding material in daily farm out any possibility of contamination. Cultures were incubated barns.[14] There have been two case reports of fungal infection at 25°-C and 37°-C aerobically. Cottony, wooly and fluffy with A. corymbifera associated with farming.[8-10] Still, over 30 growth was observed after 48 hours which rapidly filled the cases of disease with this organism have been recorded in the entire Petri dish with abundant aerial mycelium [Figure1]. literature, although Furbinger gets the credit for describing Initially the colony was white which later turned to olive-gray the first case of zygomycosis due to A. corymbifera as a cause dotted appearance at places with no pigment on the reverse. of pulmonary zygomycosis in 1876.[15,16] In lactophenol cotton blue (LCB) mount, broad, hyaline, thin-walled aseptate hyphal elements were seen. There was a A. corymbifera grows readily upon routine mycology media ribbon-like appearance with irregular diameter and branching that grow more rapidly at 37°-C than at 25°-C. It is capable of at approximately 90°. Long hyaline sporangiophores bearing growth at temperatures up to 48°-C-52°-C which distinguishes prominent funnel-shaped apophyses were observed [Figure 2]. it from other Absidia spp.[17] A. corymbifera produces wooly, Hyaline sporangia were pyriform in shape [Figure 3] and had cottony colonies which can fill a Petri dish in 24 hours. Absidia prominent conical columellae with a pointed projection at the is characterized by differentiation of hyphae into arched apex. Sporangiospores were hyaline, unicellular, round to oval stolons bearing more or less verticillate sporangiophores at and greenish in color [Figure 4]. Collarette [Figure 4] and the raised part of the stolon (internode) and rhizoids formed nipple-like projection (Hershey’s kiss) were observed among at the point of contact with substrate (at the node). This the sporangia after their rupture [Figure 5]. feature distinguishes Absidia from Rhizopus spp., where the sporangia arise from the nodes opposite the rhizoids. The The growth macroscopically and microscopically was sporangia are relatively small, globose, and pyriform or pear consistent with Lichtheimia spp. shaped and are supported by a characteristic funnel-shaped

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Vyas and Shah: Case of otomycosis by Lichtheimia corymbifera

Figure 1: Cottony, wooly growth with olive-gray sporangia at places Figure 2: Long hyaline sporangiophores with aggregates of oval on SDA plate sporangiospores in LCB mount (40 ×)

Figure 3: Pyriform sporangium in LCB mount (40 ×) Figure 4: Long, oval, greenish sporangiospores with collarette in LCB mount (40 ×)

The only species of genus Absidia found in animals and man are A. ramosa and A. corymbifera. Although closely related, the two are distinguishable by the regularly ovoid spores of A. ramosa and the irregularly ovoid to globose spores of A. corymbifera. In our case reported here, on morphological basis, we diagnosed it to be Absidia corymbifera.[19]

In conclusion, aggressive and early treatment of mucormycosis is paramount; ideally with a combination of surgical removal of devitalized tissue and intravenous administration of amphotericin B.[20] In a review of patients with pulmonary zygomycosis, it was found that mortality was significantly lower in patients treated surgically rather than medically (11% vs 68%, P = 0.0004).[21] This case illustrates the importance Figure 5: Columellae with nipple-like projection (resembling Hershey’s of clinical suspicion, isolation of fungus followed by prompt kiss) in LCB mount (40 ×) antifungal treatment with surgical debridement.

apophysis. This distinguishes Absidia from the genera Mucor References and Rhizomucor which have large and globose sporangia without an apophysis.[18] 1. Zarei Mahmoudabadi A. Mycological studies in 15 cases of

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Vyas and Shah: Case of otomycosis by Lichtheimia corymbifera

otomycosis. Pakistan J Med Sci 2006;22:486-8. LA. Presumed diagnosis: Otomycosis. A study of 451 patients. 2. Zarei Mahmoudabadi A, Abdoulhosien Masoomi A, Mohammadi Acta Otorrinolaringol Esp 2005;56:181-6. H. Clinical and Mycological studies of otomycosis. Pakistan J of 14. Hanhela R, Louhealainen K, Pasanen AL. Prevalence of microfungi Med Sci 2010;26:187-90. in Finnish cow barns and some aspects of the occurrence of 3. Thomas AJ, Shah S, Mathew MS, Chacko N. Apophysomyces Wallemia Sebi and Fusaria. Scand J Work Environ Health elegans- Renal Mucormycosis in a healthy host: A case report 1995;21:223-8. from South India. Indian J Med Microbiol 2008;26:269-71. 15. Espinel- Ingroff A, Oakley LA, Kerkering TM. Opportunistic 4. Hoffmann K, Discher S, Voigt K. Revision of the genus Absidia zygomycotic infections: A literature review. Mycopathologia (Mucorales, Zygomycetes) based on physiological, phylogenetic, 1987;97:33-41. and morphological characters; thermotolerant Absidia spp. 16. Scholer HJ, Muller E, Schipper MA. Mucorales. In: Howard DH form a coherent group, Mycocladiaceae fam. Nov. Mycol Res (editor). Textbook of Fungi pathogenic for humans and animals. 2007;111:1169-83. A. Biology. New York, N.Y: Marcel Dekker; 1983. p. 9-59. 5. Hoffmann K, Walther G, Voigt K. Mycocladus vs. Lichtheimia, 17. Flores M, Welch D. Culture media. In: Isenberg HD, Editor. Clinical a correction (Lichtheimiaceae fam. Nov., Mucorales, Microbiology Procedures Handbook. Washington DC: ASM Press; Mucoromycotina). Mycol Res 2009;113:277-8. 1992. p. 6.72. 6. Sugar AM. Mucormycosis. Clin Infect Dis 1992;14:S126-9. 18. Ellis D, Davis S, Alexiou H, Handke R, Bartley R. Absidia 7. Kindo AJ, Shams NR, Srinivasan V, Kalyani J, Mallika M. Multiple corymbifera. In: Ellis D (editor). Textbook of Descriptions of Discharging Sinuses-An unusual presentation caused by Absidia Medical Fungi, 2nd ed. Australia: Published by authors; 2007. p. 1. corymbifera. Indian J Med Microbiol 2007;25:291-3. 19. Morrison VA, McGlave PB. Mucormycosis in the BMT population. 8. Gordon G, Indeck IM, Bross K, Dapoor KA, Brotman S. Injury Bone Marrow Transplant 1993;11:383-8. from silage wagon accident complicated by mucormycosis. J 20. Pagano L, Ricci P, Tonso A, Nosari A, Cudillo L, Montillo M, et al. Trauma 1988;28:866-7. Mucormycosis in patients with haematological malignancies: 9. Lake FR, McAleer R, Tribe AE. Pulmonary mucormycosis without A retrospective clinical study of 37 cases. GIMEMA Infection underlying systemic disease. Med J Aust 1988;149:323-45. Program. Br J Haematol 1997;99:331-6. 10. Marshall DH, Brownstein S, Jackson WB, Mintsioulis G, Gilbert 21. Tedder M, Spratt JA, Anstadt MP. Pulmonary Mucormycosis: SM, Al- Zeerah BF. Post- traumatic corneal mucormycosis caused Results of medical and surgical therapy. Ann Thorac Surg by Absidia corymbifera. Ophthalmology 1997;104:1107-11. 1994;57:1044-50. 11. Murray PA. Manual of Clinical Microbiology. 6th ed. Washington DC.USA: American Society for Microbiology; 1995. 12. Kaur R, Mittal N, Kakkar M, Aggarwal AK, Mathur MD. How to cite this article: Vyas DH, Shah PD. A case of otomycosis Otomycosis: A clinicomycologic study. Ear Nose Throat J caused by Lichtheimia corymbifera (syn. Absidia corymbifera, 2000;79:606-9. Mycocladus corymbifer) in a healthy immunocompetent individual. Indian J Otol 2011;17:33-6. 13. Hueso Gutierrez P, Jimenez Alvarez S, Gil-Carcedo Sanudo E, Gil-Carcedo Garcia LM, Ramos Sanchez C, Vallejo Valdezate Source of Support: Nil. Conflict of Interest: None declared.

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