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Year : 2011  |  Volume : 54  |  Issue : 3  |  Page : 565-568
Characteristics of microsporidial keratoconjunctivitis in an eastern indian cohort: A case series

1 Corneal and Ocular surface disease clinic, Priyamvada Birla Aravind Eye Hospital, Kolkata, India
2 Department of Ophthalmology, Sanjiban Hospital, Howrah, India
3 Department of Microbiology, Vidyasagar University, Midnapore, West Bengal, India

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Date of Web Publication20-Sep-2011


Background: Microsporidia are intracellular parasites responsible for human infections. Recently, there has been an increase in the incidence of microsporidial keratoconjunctivitis (MKC) affecting normal individuals worldwide. Aim: To determine the characteristics of MKC in an Indian cohort. Materials and Methods: This is a retrospective, noncomparative, observational case series, involving patients with MKC between June and September 2009. Of the 24 patients identified, microbiological confirmation in direct smear was obtained in 22 cases and selected. Standard microbiological workup was performed in all the cases. We studied the demographics, predisposing conditions, antecedent treatment received before presentation, clinical characteristics, treatment offered, and resolution time with sequel. The management consisted of simple debridement and application of chloramphenicol ointment (1%) two times a day. Results: Mean age of onset was 18.7 years (95% CI, 15.7-21.7; range, 11-36s years). All patients gave history of prior outdoor activity and exposure to rain water/mud. Antecedent treatment comprised of Acyclovir eye ointment (45.4%) and antibiotic eye drop (27.3%) most commonly. Microsporidia were identified in Gram stain (81.8%), 10% potassium hydroxide mount (72.7%), modified Ziehl-Neelsen staining (36.4%), and Giemsa (18.2%). Majority presented as unilateral superficial keratoconjunctivitis with punctate epithelial keratitis. Mean resolution time was 9 days (95%CI, 7.9-10.2). Conclusions: MKC can occur in normal patients with exposure to rain and mud, related to outdoor activity often misdiagnosed as viral ocular infections. Strong clinical suspicion with proper microbiological evaluation helps to diagnose this commonly misdiagnosed condition.

Keywords: Keratoconjunctivitis, Microsporidia sp, ophthalmic pathology, rain

How to cite this article:
Sengupta J, Saha S, Khetan A, Pal D, Gangopadhyay N, Banerjee D. Characteristics of microsporidial keratoconjunctivitis in an eastern indian cohort: A case series. Indian J Pathol Microbiol 2011;54:565-8

How to cite this URL:
Sengupta J, Saha S, Khetan A, Pal D, Gangopadhyay N, Banerjee D. Characteristics of microsporidial keratoconjunctivitis in an eastern indian cohort: A case series. Indian J Pathol Microbiol [serial online] 2011 [cited 2021 Dec 4];54:565-8. Available from: https://www.ijpmonline.org/text.asp?2011/54/3/565/85094

   Introduction Top

Microsporidia are intracellular parasites with more than a thousand species, of which 12 have been reported to be responsible for human infections. [1] Since the first description of infectious keratitis owing to Microsporidia sp in 1990, several isolated cases or case series have been reported. [2],[3],[4],[5]

Primarily known as an infection occurring only in an immunocompromised state, multiple reports have subsequently shown an association with immunocompetent hosts also, like in contact lens usage, topical steroid therapy, and post-LASIK cases to name a few. [6],[7],[8] Also, there has been a traditional distinction in the pattern of involvement between the two immune states--superficial (genus Encephalitozoon) in immunocompromised and deeper lesions (genus Nosema and Microsporidium) in immunocompetent individuals. [5],[7] The treatment offered varies in different series and includes topical fumagillin, dibromopropamadine isethionate, fluoroquinolones, as well as systemic albendazole and itraconazole. [3],[7],[9],[10],[11]

It is important to note that although our understanding of the disease is as yet incomplete, there has been an increase in the incidence of microsporidial keratoconjunctivitis (MKC), as evident from recently published reports from India and Singapore. [3],[12]

The purpose of this study is to appreciate the changing epidemiological patterns in a cluster of cases of MKC from an Indian cohort, providing newer insights into the disease process and its management.

   Materials and Methods Top

This is a retrospective, noncomparative observational case series. Records of patients diagnosed as MKC in the cornea services between January and December 2009 were recovered with the help of database recovery system. Only cases with clinical diagnosis of the condition supplemented with microscopic confirmation of the parasite presenting between June and September were selected for analysis after obtaining permission from the institutional review board. Cases were selected across a particular period, which is the rainy season in this part of the country. A detailed history including information about high-risk behavioral pattern was obtained, followed by a systemic evaluation by an internist. Ophthalmological evaluation included symptoms at presentation, visual acuity, and slit lamp biomicroscopic examination of the anterior segment of the eye. We studied the demographics, predisposing conditions, antecedent treatment received before presentation, clinical characteristics, treatment offered, and resolution time with sequel.

All the patients underwent mechanical debridement with a sterile no. 15 blade on a Bard-Parker handle (Sharp Edge Industries, Ahmadabad, India) under topical anesthesia with 1% proparacaine hydrochloride. Samples were collected for microscopic evaluation. The first sample was used for 10% potassium hydroxide (KOH) wet mount preparation and subsequent samples were evaluated using Grams stain, modified 1% Acid fast stain (Kinyoun's modification of Ziehl-Neelsen stain), and Giemsa stain, maintaining the same order in all the cases. Treatment following mechanical debridement consisted of application of chloramphenicol eye ointment (1%) two times a day till complete healing of the epithelial defect was obtained and carboxymethylcellulose eye drop (0.5%) used four times/day up to a maximum period of 1 month after complete resolution.

   Results Top

A total of 36 cases of MKC were identified in the 12-month period between January and December 2009. Of these, 24 cases presented during the study period of June to September. Among these cases, microscopic detection of organism was obtained in 22 cases (23 eyes) and included in the study. The mean age of involvement was 18.7 years (Range: 11-36 years). Males (20 cases, 90.9%) were more commonly affected than females (2 cases, 9.1%). Predisposing activity in all these cases involved simultaneous exposure to rain and mud during outdoor activities. Such exposure commonly included playing cricket (4 cases, 18.2%), soccer (12 cases, 54.5%), golf (3 cases, 13.6%), rugby (1 case, 4.54%) and was unidentified in two (9.1%) cases. The mean period from predisposing activity to symptomatic onset was 18.4 days (Range: 5-30 days). The period from symptomatic onset to diagnosis of MKC ranged between 9 to 16 days with a mean of 11.5 days. Treatment received before diagnosis of the condition consisted of Acyclovir eye ointment (10 cases, 45.4%), antibiotic eye drop (6 cases, 27.3%), lubrication (5 cases, 22.5%), and topical steroid (2 cases) either singly or in combination. All cases were unilateral, except one where the other eye was involved 7 days after the first eye, presenting as a superficial keratoconjunctivitis with a papillary/follicular reaction. The lesions were classically epithelial, multifocal, diffuse, coarse, punctate , and raised, staining positive with fluorescein without any stromal involvement [Figure 1]a-c. The anterior chamber also did not reveal any cellular reaction. In one eye where topical steroids were being used before presentation, a coalescence of individual lesions was observed giving rise to a geographic pattern [Figure 1]d. Direct microscopy of corneal scraping demonstrated the organism in Gram stain (81.8%; 95% CI, 60.8-93.3), 10% KOH wet mount (72.7%; 95% CI, 51.6-87.1), 1% Acid fast (36.4%; 95% CI, 19.6-57.1), and Giemsa stain (18.2%; 95% CI, 6.7-39.1) [Figure 2]a-d. Complete resolution was obtained in all the cases within a mean period of 9 days (95% CI, 7.9-10.2 days). No episode of recurrence or residual sequel was noted in these cases. Cases where topical steroids were used resolved after 14 and 16 days, respectively.
Figure 1: Diff erent clinical pictures of Microsporidial keratoconjunctivitis, (a)Classical lesions suggestive of microsporidial keratoconjunctivitis (x10), (b) Discrete coarse lesions with clear underlying stroma and intervening cornea (x10), (c) Individual lesions were fluorescein stain positive (x10), (d) Pretreated with steroids showing coalescence of lesions (x10)

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Figure 2: Microscopic picture after different staining procedure, (a) KOH wet mount showing particles suggestive of microsporidial cysts. (Unstained, x100), (b) Confirmatory 1% Acid Fast stain of corneal scraping sample. (modifi ed ZN stain, x100), (c) Microsporidial cyst from corneal scraping sample (Giemsa stain, x100), (d) Intraepithelial particles in Gram's stain suggestive of microsporidia from corneal scraping sample. (Gram's, x100)

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   Discussion Top

Microsporidiosis has been recognized in both vertebrate and invertebrate hosts. In human beings, Microsporidia are considered opportunistic and rare pathogens. Although Joseph et al. [3] observed a prevalence of 0.4% in microbiologically proven cases of infective keratitis from India, a later report from Singapore shows that the current incidence of MKC is on the rise. [12] This series of 22 patients clustered over a short span of time from a single hospital highlights the endemicity in the general population. Serological studies revealing the presence of high levels of specific antibodies directed against Encephalitozoon spp. in 4.7% of blood donors support such observation. [13]

Whether the rise in numbers is related to enhanced awareness among cornea specialists leading to more identification of the cases or a real increase remains to be answered, particularly in view of the fact that these patients were most commonly diagnosed as atypical viral keratoconjunctivitis in this series and also elsewhere. [3],[12]

Another important aspect of this set of patients is the seasonal peaking in the occurrence of cases (61.1%) with some form of exposure to rain and mud related to outdoor activity. This risk factor, which is now being reported frequently, deserves further attention. [12],[14] The routes of transmission of Microsporidia and sources of infection in human beings have long been an unanswered question with speculations. Water has been considered an important route of spread, particularly in view of life cycle of certain species of Microsporidia. Case reports of intestinal microsporidiosis have implicated fecal-oral route of transmission through swimming pool, water distribution system, and male homosexuality. [15] This is further substantiated with studies showing contamination of surface water with microsporidial DNA; however, the potential risk of transmission from water could not be definitely concluded. [16] Similarly, soil/mud exposure has been reported in 50% cases by Loh et al. In view of such risk factors, the probable role of "contaminated water" vis a vis the low hygienic living condition as a potential source of infection has to be kept in consideration in developing countries like India with improper facilities of sanitation and deserves further investigation.

The other essential factor in this study that draws attention is the low average age of the afflicted patients, which is explained by their involvement in outdoor activities. The cases in this series were considered immunocompetent based on their no-risk behavioral pattern as well as due to the seasonal conglomeration. Serological testing for HIV was not performed in any of these cases. However, such association was explained to all including the need for investigation into their immune status in nonresponsive situations or with recurrence of infection later on.

An overwhelming majority of 21 cases presented with unilateral superficial keratoconjunctivitis with punctate epithelial keratitis. Only one patient developed bilateral disease in our series. This is in contrast to the classical description of ocular involvement in immunocompetent individuals in whom a deeper lesion is more common. On the other hand, HIV-infected individuals present frequently as bilateral superficial keratoconjunctivitis. Recent reports however show a considerable overlap. For example, M. vitaformae causes both epithelial and stromal disease in immunocompetent hosts. [17] The major drawback in most studies including our series is dependence on direct microscopy to identify the cysts and lack of species identification. Such data for obvious reasons will be immensely useful to better elucidate the disease characteristics.

The interaction between the local host immunity and organism characteristics in determining laterality and presentation in normal individuals is a matter of interest and requires further studies. There is no consensus regarding appropriate management of these cases in available literature which includes specific antimicrosporidial therapy with fumagillin to fourth-generation fluoroquinolones and others, systemic ketoconazole and albendazole. Our cases responded to simple debridement and local application of chloramphenicol ointment resulting in complete resolution.

The role of topical steroids is controversial, particularly because of the induction of local immunosuppression and possibility of penetration of the organisms into the deeper stroma. [2] On the other hand, successful use of steroids was reported in one series in patients with stromal edema and keratic precipitates. [12] In this series, only two patients were pretreated with topical steroids, which were discontinued at the time of presentation to our services. None of the cases showed any deep penetration. In one of these cases, there was a confluence of individual lesions giving rise to a geographic pattern. However, as they constitute a small sample in our series, the role of steroids in this subset cannot be commented upon, except for a probable prolongation in the disease process. We contemplate that the intact local defense mechanism in immunocompetent individuals plays an important role in limiting these infections into the superficial cornea. These cases probably serve as an accidental host where the Microsporidia are unable to complete its life cycle, independent of any antimicrobial chemotherapy.

   Conclusions Top

MKC can occur in normal patients with exposure to rain and mud, related to outdoor activity. There seems to be a seasonal trend in occurrence of the disease, peaking around the rainy season, though cases are found across the year. Contaminated water and low hygienic living conditions in developing countries like India seem to predispose individuals to such infections, which probably remain endemic in the general population and require further studies. These cases are often misdiagnosed as viral ocular infections. Strong clinical suspicion with proper microbiological evaluation helps to diagnose this commonly missed condition. In cases with microsporidial superficial keratoconjunctivitis, simple debridement seems to be adequate in controlling the infection, with local defense mechanisms playing a more important role compared with antimicrobial therapy. In view of the recent increase in number of cases with a similar pattern across the globe, individual species identification is becoming more important to better our understanding about the disease process.

   References Top

1.Franzen C, Müller A. Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clin Microbiol Rev 1999;12:243-85.  Back to cited text no. 1
2.Friedberg DN, Stenson SM, Orenstein JM. Microsporidial keratoconjunctivitis in acquired immunodeficiency syndrome. Arch Ophthalmol 1990;108:504-8.  Back to cited text no. 2
3.Joseph J, Sridhar MS, Murthy S, Sharma S. Clinical and microbiological profile of microsporidial keratoconjunctivitis in southern India. Ophthalmology 2006;113:531-7.  Back to cited text no. 3
4.Fogla R, Padmanabhan P, Therese KL, Biswas J, Madhavan HN. Chronic microsporidial stromal keratitis in an immunocompetent, non-contact lens wearer. Indian J Ophthalmol 2005;2:123-5.  Back to cited text no. 4
5.Chan CM, Theng JT, Li L, Tan DT. Microsporidial keratoconjunctivitis in healthy individuals: A case series. Ophthalmology 2003;110:1420-5.  Back to cited text no. 5
6.Theng J, Chan C, Ling ML, Tan D. Microsporidial keratoconjunctivitis in a healthy contact lens wearer without human immunodeficiency virus infection. Ophthalmology 2001;108:976-8.  Back to cited text no. 6
7.Rosberger DF, Serdarevic ON, Erlandson RA, Bryan RT, Schwartz DA, Visvesvara GS, et al. Successful treatment of microsporidial keratoconjunctivitis with topical fumagillin in a patient with AIDS. Cornea 1993;12:261-5.  Back to cited text no. 7
8.Moon SJ, Mann PM, Matoba AY. Microsporidial keratoconjunctivitis in a healthy patient with a history of LASIK surgery. Cornea 2003;22:271-2.  Back to cited text no. 8
9.McCluskey PJ, Goonan PV, Marriott DJ, Field AS. Microsporidial keratoconjunctivitis in AIDS. Eye 1993;7:80-3.  Back to cited text no. 9
10.Didier ES, Rogers LB, Brush AD, Wong S, Traina-Dorge V, Bertucci D, et al. Diagnosis of disseminated microsporidian Encephalitozoon hellem infection by PCR-Southern analysis and successful treatment with albendazole and fumagillin. J Clin Microbiol 1996;34:947-52.  Back to cited text no. 10
11.Sridhar MS, Sharma S. Microsporidial keratoconjunctivitis in a HIV-seronegative patient treated with debridement and oral itraconazole. Am J Ophthalmol 2003;136:745-6.  Back to cited text no. 11
12.Loh RS, Chan CM, Ti SE, Lim L, Chan KS, Tan DT, et al. Emerging prevalence of microsporidial keratitis in Singapore: Epidemiology, clinical features, and management. Ophthalmology 2009;116:2348-53.  Back to cited text no. 12
13.Van Gool T, Vetter JC, Weinmayr B, Van Dam A, Derouin F, Dankert J, et al. High seroprevalence of Encephalitozoon species in immunocompetent subjects. J Infect Dis 1997;175:102.  Back to cited text no. 13
14.Reddy AK, Balne PK, Garg P, Krishnaiah S. Is Microsporidial Keratitis A Seasonal Infection in India. Clin Microbiol Infect 2009 Oct 14.  Back to cited text no. 14
15.Hutin YJ, Sombardier MN, Liguory O, Sarfati C, Derouin F, Modaï J, et al. Risk factors for intestinal microsporidiosis in patients with human immunodeficiency virus infection: A case-control study. J Infect Dis 1998;178:904-7.  Back to cited text no. 15
16.Fournier S, Liguory O, Santillana-Hayat M, Guillot E, Sarfati C, Dumoutier N, et al. Detection of microsporidia in surface water: A one-year follow-up study. FEMS Immunol Med Microbiol 2000;29:95-100.  Back to cited text no. 16
17.Chan KS, Koh TH. Extraction of microsporidial DNA from modified trichrome-stained clinical slides and subsequent species identification using PCR sequencing. Parasitology 2008;135:701-3.  Back to cited text no. 17

Correspondence Address:
Jayangshu Sengupta
Corneal and Ocular Surface Disease Clinic, Priyamvada Birla Aravind Eye Hospital, 10, Loudon Street, Kolkata - 700 017, West Bengal
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0377-4929.85094

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