BEWARE OF FOREIGN BODY SENSATION” THIS LIVE WORM CAN SWIM THROUGH YOUR EYE! A CASE SERIES ON INCREASING PREVALANCE OF OCULAR DIROFILARIASIS IN TROPICAL INDIA: A DISEASE OF TRAVEL TO FOREIGN LANDS

INTRODUCTION

Dirofilariasis is a parasitic infection transmitted in humans by Culex and Aedes mosquito, with Primary host as dogs and cats, Man as dead end. Common ocular infection sites in humans are eyelids, subconjunctival, sub-tenons or intraocular. D. Tenius and D. Repens mainly involve eye.

MATERIALS AND METHODS:

Four patients who presented to us who were not improving with topical and oral steroids treated from elsewhere for conjunctivitis. Detailed history was taken for all patients. All were assessed for Visual Acuity with Snellens Chart, Slit lamp evaluation and Fundus evaluation with 90D lens. A snap shot study was done. Slit lamp videos records of the mobile worm and its site were noted after anterior segment evaluation under slit lamp.

Patients were planned for excision of the worm under local anesthesia under operating microscope after routine blood investigations and general examination. Excisional biopsy and histopathological report was studied and reported. In all cases the entire tissue was processed using routine technique and sections were examined using haematoxylin and eosin stain. Consent was taken from all patients. All patients were followed up within a week to confirm resolution of all symptoms and requested to come back to us in case of similar symptoms.

RESULTS

Slit-lamp examination revealed conjunctival chemosis with a coiled live worm in the subconjunctival space (case 1, 3 & 4), at the temporal limbus, sub tenons space (case 2)

All patients had their visual acuity. Both eye - Visual Acuity 6/6 and Fundus normal.

Worm was removed under the operating microscope, topical anesthesia (lignocaine) given. Conjunctival peritomy (2mm) was done and whole of live-coiled worm was removed without snapping. It measured between10-12 cm in length in all cases. Histopathology revealed female Dirofilaria species.

Kim U, Gupta M, Vidhya N et al reported different sites of ocular Dirofilariasis as per following : Reported ocular sites are anterior chamber, periorbital region, subcutaneous orbital mass, subconjuctival, orbital rim, as lidtumour & eyelids. Dirofilariasis due to Dirofilaria repens is also seen involving buccal mucosa in a patient who presented with a facial swelling in literature (12).

DISCUSSION

The mature D. repens live in the tissues and organs of vertebrates, while their immature stages prefer the blood and lymph vessels. D. repens is a subdermal parasite in dogs. Pamplione S, Canestri TG et all mentioned that the parasite, called D. conjunctivae and normally found in humans, is a form of D. repens. (1,2).

Dirofilaria species may be divided into two groups:

• Subgenus Dirofilaria represented by Dirofilaria immitis, which is characterized by a relatively smooth cuticle and normally found in the right heart and pulmonary vessels of dogs, the natural hosts. Pulmonary lesions are the most common findings in humans infected with D.immitis (1,2).

• Subgenus Nochtiella, which parasitize the subcutaneous tissue. Species of this group have longitudinal ridges on the cuticle. Representative species are Dirofilaria (Nochtiella) repens found in dogs and cats, and Dirofilaria (Nochtiella) tenius found in raccoons (1,2)

Human Dirofilariasis is a rare helminthic infection. This may be due to the fact that the diagnosis of Dirofilaria infection in human beings remains difficult, as symptoms exhibited by the patient are diverse. Symptoms vary in severity.

In most cases the infections are asymptomatic or mild and uncomplicated, especially until the worm dies. Only after their death insitu painful inflammatory reactions occur around the worms causing subcutaneous nodular lesions, necessitating excision. During the migration of the worm through subcutaneous tissue, inflammatory reactions may develop like mild fugitive swelling or subcutaneous nodule which can be painful and tender. (3).

Orihel TC, Eberhard MC et al said the most common symptoms in ocular dirofilariasis are localized pruritus, pain, swelling, oedema, hyperemia of the conjunctiva, sensation of movement under the skin of the conjunctiva. (4).

Pamplione S, Canestri TG et al found allergic reaction with fever, urticaria and facial oedema may occur (2). In majority of instances, parasites are found in excised nodule and tissue biopsy specimens. Less frequently they are removed from the tissues intact. Bruijing et al also mentions about the predominance of female worms are found more frequently than male. (3,4).

Simon F, Morchon R et all studied the most important risk factors regarding human infections are mosquito density, warm climate with extended mosquito breeding season, outdoors human activities and the abundance of microfilaraemic dogs (5).

Diagnosis is usually established with the surgical removal of the adult worm (4,13). Ruiz–Moreno JM, Bornay–Linores FJ et all studied the serological tests for management of this condition. Microfilaria have never been reported in humans (6). Eosinophilia occurs in less than 15 % cases with D. immitis and rarely with D.repens (6). In this case also, blood smears were negative for microfilaria and there was no eosinophilia. All dirofilaria have fine transverse striations on the cuticle and abundant somatic musculature. D.repens is a nematode with a long thin filiform appearance All except D.immitis and few others have prominent external longitudinal ridges. Longitudinal ridges of D.repens are broader and less distinct.

The number of reproductive tubes and their contents (eggs, microfilariae or sperm) help to determine the sex of the parasite and the reproductive state of female worm. They have rounded anterior end with buccal cavity. In contrast to the rounded short tail of female worm the male worms have a coiled tail.

Surgical removal of the worm not only establishes the diagnosis in most cases but also presents a definitive cure. Simple extraction of the worm or complete surgical excision of the Dirofilaria lesion is the treatment of choice for human Dirofilariasis. (4,5,7,12).

Gendelman et al described use of a cryoprobe can be used for immobilizing the worm in case of excessive motility (7). There is no need for chemotherapy as microfilaraemia is extremely rare (8). In a small number of cases, Ivermectin and/or Diethylcarbamazine has been tried with good results (9).

The symbiosis of filarial nematodes and intracellular Wolbachia bacteria has recently been exploited as a target for antibiotic therapy of filariasis. Antibiotic treatment of filarial nematodes results in sterility and inhibits larval development and adult worm viability. In the first trial on human onchocerciasis, depletion of bacteria following treatment with Doxycycline resulted in a complete and long-term block of embryogenesis (10). Precise identification of Dirofilaria species may be achieved with DNA analysis, based on polymerase chain reaction but the large number of specific probes required limits, the usefulness of this method (11).

Increasing prevalence of this infection is seen more in tropical parts of India especially South India, The first two cases of human ocular dirofilarial infection in India were reported by Joseph et al & George and Kurian in same part of India (Kerala) in 1976 and 1978 respectively (13,14). In 1989, Badhe and Sane reported the first case of subcutaneous infection with Dirofilaria showed a child manifesting portal cavernoma with pulmonary dirofilariasis from India (15). Nadgiret al in 2001 and Gautam et al in 2002 reported subconjunctival dirofilariasis due to Dirofilaria repens in several reports from various parts of India (16). Sekhar et al reported several other incidences of ocular dirofilariasis from India in 2000 and similar report by Ittyerah in 2003 mentioned about Dirofilaria repens and Dirofilaria tenuis cause sub conjunctival dirofilariasis (17).

In 2005, Padmaja et al reported subcutaneous dirofilariasis due to D repens in a 35-year-old male (18).

Sabu et al identified twelve worms from different human patients as Dirofilaria repens based on morphology from southern part of India (19). In order to predict the natural history of dirofilarial infection in this region, 160 blood smears of dogs. In 2013, Kim et all reported three cases of ocular dirofilaria repens, sites being preseptal and orbital region. Patients were treated with parenteral and oral steroids and not improving. Excisional biopsy and subsequent removal of the worm resolved the symptoms (12).

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Figure Legend 1:

Case 2: Subconjunctival Dirofilaria at temporal limbus (B) - live motile worm was noticed at the temporal limbus under slit lamp

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Figure Legend 2:

Case 1: 10 cm long worm

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Figure Legend 3:

Transverse section through a mature female Dirofilaria repens removed from the temporal limbus of a 65-year-old female (Case1). Characteristic features are the arrangement of the longitudinal muscles and the multilayered cuticle, which is expanded in the region of the large lateral chords.

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In 2014, Gupta V et all reported bilateral intraocular dirofilariasis in Delhi, North India (21). Because of the variety of locations of the worm and the symptoms produced, cases of dirofilariasis in humans and animals may attract the attention of veterinarians, ophthalmologists, dermatologists, radiologists and general practitioners. Based on the present observations, it may be concluded that dirofilariasis in humans due to D. repens infection is a fast emerging zoonosis in India (12,20).

CONCLUSION

Dirofilariasis is associated with travel to ‘Foreign’ lands. Literature shows predominance in South India especially Kerala, Karnataka, Tamil Nadu. Kerala is studded with a network of backwaters serving breeding ground of mosquitoes for transmission. World literature reviews diversity in Italy, Sri Lanka, Russia, Romania and Mediterranean regions. Surgical removal of the worms is the treatment of choice.