Corneal ulcer due to a rare pleosporalean member of the genus Bipolaris following cow tail injury to the eye: A case report and review of literature

Abstract

Aspergillus and Fusarium are the most common fungi causing mycotic keratitis. Injury to the eye with vegetable matter, cow tail injury, long-term use of topical steroids are some of the risk factors for mycotic keratitis. There are few case reports of keratitis caused by Bipolaris. The human pathogenic species in the genus are Bipolaris spicifera, Bipolaris hawaiiensis, Bipolaris papendorfii, and Bipolaris australiensis. Most commonly reported keratitis is caused by B. hawaiiensis, followed by B. spicifera. Literature review showed only one case report of keratitis due to B. australiensis reported from Australia. We present a first case report of keratitis due to B. australiensis (currently Curvularia australienis) from India.

The genus Bipolaris are ubiquitous, saprophytic ascomycetous fungi of the order pleosporales. Most of the species of this large genus are pathogenic to graminicolous plants and found in dead plant material and soil. The human pathogenic species in the genus are Bipolaris spicifera, Bipolaris hawaiiensis, Bipolaris papendorfii, and Bipolaris australiensis are pathogenic to humans. B. australiensis has been known to be involved in humans causing peritonitis, subcutaneous phaeohyphomycoses fungal sinusitis, and disseminated infection. We report a case of keratitis caused by B. australiensis (currently Curvularia australienis) following cow tail injury to the eye.

Case Report

A 59-year-old man presented to our hospital, with redness, pain, and defective vision in the left eye (LE) of 15-day duration. He gave a history of injury to the LE with a cow's tail while milking the cow. Further, he consulted a local ophthalmologist and was prescribed topical moxifloxacin thrice a day, natamycin thrice a day, and ointment moxifloxacin thrice a day. There was no history of diabetes mellitus or using steroid eye drops. As there was no relief, he subsequently visited our hospital.

On examination, his best-corrected visual acuity was 6/12 improving with pinhole to 6/6 in the right eye (RE) and 6/36 in the LE. RE examination was normal. Slit-lamp evaluation of the LE revealed ciliary congestion with the corneal infiltrate measuring 3.5 mm × 3 mm [Fig. 1]. There was no hypopyon.

Figure 1.

Slit-lamp examination revealing the corneal infiltrate measuring 3.5 mm × 3 mm

Scrapings were taken from the corneal lesion under topical anesthesia for Gram's staining and 10% potassium hydroxide (KOH) mount. Additional scrapings were taken to inoculate 5% sheep blood agar (SBA) and Sabouraud dextrose agar (SDA) plates (Hi-Media Laboratories Pvt. Ltd, Mumbai, India).

The patient was started on topical natamycin Q 1 hourly, fluconazole Q 1 hourly, ciprofloxacin Q 1 hourly, and atropine eye drops three times a day.

The KOH mount of the corneal scrapings showed phaeoid, septate, branching, filamentous mold suggestive of keratomycoses due to phaeoid fungi. The SBA and SDA plates were incubated at 37°C and 25°C, respectively. The blood agar plates after 24 h incubation had no bacterial growth. Fungal growth was observed following 4 days of incubation of the SDA plates. KOH microscopy with phaeoid fungal elements and SDA media with growth consistent with phaeoid fungi confirmed the fungal etiology for the case. Subsequently the fungi were identified as B. australiensis based on macroscopic and microscopic characters. The colonies on SDA after 7 days of incubation at 25°C showed spreading, gray to brownish black, velvety texture colonies [Fig. 2]. The reverse of the fungal colonies showed brown pigmentation. The slide culture mount in lactophenol cotton blue mount showed solitary, smooth-walled conidiophore with characteristic geniculate and verruculose nodes. The conidia in clusters were smooth-walled, ellipsoidal, rounded ends, pale brown, straight, and 4–5 distoseptation [Fig. 3]. The morphological identification of the isolate was carried out based on conidial structure, presence of an inconspicuous to slightly protuberant hilum, formation of germ tubes from polar cells, and ontogeny of conidial septum.[1] The identity was further confirmed by matrix-assisted laser desorption ionization-time of flight mass spectrometry analysis and internal transcribed spacer 2 sequencing region rDNA gene compared with GenBank DNA sequences database.

Figure 2.

Obverse macroscopic colony morphology of Bipolaris australiensis on Sabouraud dextrose agar after 7 days of incubation at 25°C showed spreading, gray to brownish black, velvety texture colonies

Figure 3.

Slide culture mount in lactophenol cotton blue mount showing (a) solitary, smooth-walled conidiophore (b) geniculate and verruculose nodes in conidiophores (c) smooth-walled, ellipsoidal, rounded ends, pale brown, straight, 4–5 distoseptate conidia in clusters (400)

He responded well to the topical therapy. On follow-up, the ulcer was seen regressing and the vision improved to 6/9. Ulcer healed completely by 4 weeks.

Discussion

Bipolaris species are a dematiaceous fungus, part of the hyphomycetes group of fungi. The common species inciting human disease include B. australiensis, B. hawaiiensis, and B. spicifera. Colonies are woolly, gray to black. Conidial germination is from both poles and/or end cells and hence the genus “Bipolaris.”

Bipolaris is a genus of dematiaceous fungi known to cause disease in both immunocompetent and immunocompromised humans. B. spicifera and B. hawaiiensis are the most commonly recovered pathogenic species from human disease. B. australiensis is a relatively rare clinical isolate form from cutaneous and subcutaneous lesions. B. hawaiensis is an aggressive species and is isolated from cases of invasive sinusitis, brain lesions, sputum samples, and lung tissue. B. australiensis has been known to be involved in humans causing peritonitis, subcutaneous phaeohyphomycoses, fungal sinusitis, and disseminated infection.[2] Ophthalmologic manifestations include keratitis, optic neuropathy from contiguous sinusitis, and endogenous endophthalmitis. Most common cause of mycotic keratitis is trauma in agricultural workers. Our patient sustained injury with cow tail. The three most common species – B. spicifera, B. hawaiiensis, and B. australiensis have all been reported as causative agents of mycotic keratitis.[3,4,5] Most common isolate from the corneal lesion was B. hawaiiensis.[3,4,6,7] and B. spicifera in two cases.[5,8] Literature search showed only one report of keratitis due to B. australiensis.[9] There was one case of keratitis due to B. oryzae.[10]

Therapeutic options for Bipolaris infections are limited because many dematiaceous fungi are resistant to amphotericin B. Itraconazole shows consistent and potent activity against these organisms. Bipolaris is sensitive to topical natamycin. Our patient responded well to topical therapy with natamycin and ketoconazole. As the patient was responding well to combination of natamycin and ketoconazole, we did not change to itraconazole. Delay in the diagnosis led to endophthalmitis following Bipolaris keratitis in a case reported by Bashir et al.[6] One patient underwent penetrating keratoplasty as there was no response to medical therapy.[7] Of the eight reports of Bipolaris keratitis [Table 1], five reports were from India. However, none of them were caused by B. australiensis. Our patient is the first case report of B. australiensis keratitis from India. In 2012, genus Bipolaris, which comprises over 45 species had undergone taxonomic revisions based on molecular phylogenetic studies wherein the pathogen B. australiensis has now been shifted to the genus Curvularia.[1]

Table 1.

Global review of keratomycoses cases due to members of the genus Bipolaris with the site of involvement, ocular presentation, mode of penetrating injury, management, and outcome

In summary, although it is rare, B. australiensis can be implicated in ophthalmic infection. It should be considered as a potential pathogen, especially in high-risk group patients, such as farmers, who come in contact with cattle and are susceptible to cow tail injury of the eye. Early diagnosis and prompt therapy resulted in a favorable outcome in our patient.

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Conflicts of interest

There are no conflicts of interest.