Ocular thelaziasis: A case report from Assam, India.

We report here a case of human ocular thelaziasis that was discovered accidentally during cataract surgery. A 58-year-old farmer attended an eye camp for diminished vision of the left eye, which was diagnosed later on as cataract. He was referred to a tertiary care hospital in Assam. During the cataract surgery, two small, motile, chalky white, translucent worms were removed from the left fornix. They were identified as female Thelazia callipaeda. Rare occurrence of this disease and its association with both extra and intraocular manifestations leading to ocular morbidity is the rationale for presenting this case.

INTRODUCTION

Thelaziasis is an arthropod-borne ocular disease, caused by Thelazia callipaeda, a nemathelminthes, transmitted by Drosophila flies to mammals including humans.[1] T. callipaeda, a tissue nematode, is primarily a parasite of the dog, rabbit, cat, foxes, and occasionally human. The adult worm inhabits the orbit, conjunctival sac, or lacrimal glands. It is primarily reported from oriental countries of South Asia like India, Myanmar, China, Thailand, Japan, Korea, and Russia, and hence the parasite is also known as “Oriental Eye Worm.”[12] Clinical manifestation includes conjunctivitis, ocular pruritis, lacrimation, congestion and discharge, corneal edema, and corneal ulceration in severe infection. The role of vector (fly) involved in the transmission of thelaziasis has been a matter of discussion; however, studies on vectors confirmed that Phortica okadai and Phortica variegata is the vector of T. callipaeda in China and Southern Europe. In India, the role of vector in the transmission of thelaziasis has not been studied so far. The increase in the number of human cases in India merits for the study of transmission dynamics of thelaziasis.[3]

Two species of Thelazia, namely T. callipaeda and Thelazia californiensis (reported from California) are known to cause human thelaziasis. An infected person or animal harbors the first-stage larvae (developed from the egg) in the lacrimal secretions. Arthropod vectors feeding on such infected lacrimal secretions ingest these larvae, which undergo three molts inside the midgut of the vector in 2–3 weeks’ time and develop into infective third-stage larvae which are infective to humans. Third-stage larvae are transmitted accidentally to another susceptible host by the vector when it feeds on such lacrimal secretions. The third-stage larvae develops into adult worm within 35 days in the eye of the infected person.[1] Humans are considered accidental hosts.[4] We report here a case of ocular thelaziasis in an adult male patient from a rural area of Assam.

CASE REPORT

A 58-year-old male, Hindu farmer, from a rural area of Morigaon district of Assam, attended an eye camp in March 2017. He presented with gradual progressive diminution of vision of the left eye for the last 3 years with watering from the left eye for the last 2 years. The patient did not give any history of pain, itching, redness of eye, or seeing any floating object in the field of vision during this period. In the camp, he was diagnosed to have cataract of the left eye and was referred to a tertiary care hospital in Assam for cataract surgery. He had cataract surgery of the right eye 3 years back. The patient could not recollect any history of trauma.

On examination, he was diagnosed with senile hypermature cataract of the left eye with pseudophakia of the right eye. There was no conjunctival congestion, and the cornea and pupils were normal. Vision was recorded as perception of light positive in the left eye. Fundus examination revealed no details due to dense cataract in the left eye. The patient was advised for cataract operation of the left eye. Routine blood examination and blood sugar were normal. In March 2017, cataract operation was carried out on the left eye. During the operation, two white, motile, translucent, thread-like worms were observed crawling in the lower fornix of the conjunctiva. They were removed with sterile forceps, put in 10% formalin, and sent to the Microbiology Department, Gauhati Medical College, for identification. However, operation proceeded following the application of antiseptics, and the patient was discharged with a vision of 6/6. After that, the patient did not come for follow-up.

Morphologically, the worms were thin, thread like, and white to creamy in color. Both the worms were female, and they were 9–10 mm and 8–9 mm in length. On microscopic examination, a distinct buccal capsule was observed at the anterior part of the worm; the anterior end was found to bear a pair of prominent cephalic extensions protruding forward and a rectangular buccal cavity with no tooth-like structures [Figure 1a]. A muscular esophagus was observed, and the intestine could be traced up to the posterior end which was blunt and not curved with spicules. The anal opening was distinct [Figure 1b]. The vulva was anterior to the esophago-intestinal junction [Figure 1c]. This differentiates T. callipaeda from T. californiensis as the latter's vulval opening is posterior to the esophago-intestinal junction. Numerous coiled larvae were seen in the uterus. Mature eggs were also seen in the posterior half [Figure 1d], and larvae were seen in the anterior half of the worm [Figure 1e]. Transverse cuticular striations were seen on the whole body of the worm [Figure 1f]. On the basis of these morphological characteristics, the worms were identified as female T. callipaeda. As the worm was preserved in 10% formalin, the extraction of DNA and molecular analysis could not be done for the confirmation of identification of species.

Figure 1

(a) Anterior portion of female Thelazia callipaeda showing cephalic end and rectangular buccal part; (b) Blunt posterior end showing the intestine and the anal opening (arrow); (c) Anterior portion of the worm with the vulval opening located anterior to esophago–intestinal junction; (d) Numerous eggs in the posterior half; (e) Larvae in the anterior half of the worm; (f) Transverse cuticular striations (×400) (a: Anal opening, b: Buccal cavity, v: Vulval opening, l: Larvae, Eg: Egg, sc: Striated cuticle)

The symptoms of the patient resolved immediately after the removal of the worms and irrigation of the eye with povidone-iodine.

DISCUSSION

Human thelaziasis has been reported worldwide. Probably, the first case of T. callipaeda infection was reported from Salem district, Tamil Nadu, India, in 1948.[5] Subsequently, there are a few cases of thelazia infestation among humans reported from India including four reports from Assam[1356789101112] [Table 1]. There are earlier reports of this parasite in dogs from Assam which bears significance from the public health point of view since it has been reported in human from Assam[367] and the neighboring state of Manipur.[11]

Table 1

Indian data on human thelaziasis

The present case belonged to a rural family whose livelihood is farming and cattle rearing. The factors that commonly predispose for human thelaziasis are unhygienic living conditions and the surrounding environment. Cattle rearing, contact with stray dogs, mountainous terrains, and rainy season make the humans vulnerable to ocular thelaziasis. Conjunctival and corneal injuries and traumatic conjunctivitis facilitate the introduction of the larvae into the subconjunctival space and vitreous cavity.[1] In the present case, cattle rearing was the predisposing factor. In addition, the northeastern region of India has mountainous and foothill terrains with heavy and long monsoon with favorable temperature throughout the year, providing an ideal home for a variety of insects that play an important role in transmitting many vector-borne diseases of medical and veterinary importance.

Several other studies have reported incidental discovery of the worm only during intracapsular cataract surgery without any other ocular manifestations.[711] Interestingly, in the present case, the worm was discovered during intracapsular cataract surgery.

It is difficult to differentiate between T. callipaeda and T. californiensis when morphological characteristics are not clearly evident. T. callipaeda is different morphologically from T. californiensis based on the numbers of pre- and post-cloacal papillae in the male and the position of the vulva in the female.[1314] In adult female of T. callipaeda, the vulva is located in the anterior region of the body. The vagina opens anterior to the esophagus–intestinal junction. In adult males, the caudal end is ventrally curved have 15 pairs of papillae on the ventral surface of the caudal end, 10 of which are pre-cloacal and 5 post-cloacal.[15] In female T. californiensis, the vulva is located behind the esophageal–intestinal junction. The males have 6–7 pairs of precloacal papillae.[16] In the present case, the vulval opening was located anterior to the esophagus–intestinal junction based on which the worm was identified as female T. callipaeda.

For the confirmation of species, DNA barcoding approach has been useful. Some researchers have applied molecular diagnostic methods such as polymerase chain reaction amplification of the mitochondrial cytochrome c oxidase subunit 1gene (cox1, 689 bp) and the first internal transcribed spacer of ribosomal DNA, ITS1.[1718] However, in comparison with a single gene, the complete mitochondrial (mt) genome can provide more markers for molecular identification and provide the potential to discover population variants or cryptic species.[19] These available mtDNA databases help to compare the diversity of mt genomes among closely-related Thelazia taxa. Another genetic marker, the nicotinamide dehydrogenase complex 6 gene has also been shown to have high sequence variability among all isolates, which is worth considering for future population genetic studies of T. callipaeda.[20]

Although the treatment of ocular thelaziasis is topical organophosphates, 1% moxidectin, and 10% imidacloprid in animals; mechanical removal of the parasite is the only curative treatment for human ocular thelaziasis. In the present case also, symptoms resolved immediately after the removal of the worms and irrigation with povidone-iodine.

CONCLUSION

Prevention of thelaziasis is possible by taking protective measures such as using bed nets at night, maintaining personal hygiene, keeping the surroundings clean, and creating public awareness about the disease.[1] In India, the public health and prevention strategies play important role, as a high infestation rate is found among dogs and cattle. Previous reports of ocular infection in human as well as in animals justify the prevalence of this parasite and its zoonotic potential in Assam, necessitating detailed epidemiological surveillance.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.