Canine thelaziosis is a nematode infection affecting the eyes and associated tissues. In dogs two species of so-called ‘eyeworms’ have been described: Thelazia callipaeda (also named ‘oriental eyeworm’) and Thelazia californiensis. The disease is characterized by conjunctivitis and keratoconjunctivitis or even corneal ulcers. The vectors for the eyeworms are flies.

Pathogen

Belonging into the family Thelaziidae, order Spirurida, suborder Spirurina, two out of 16 species of Thelazia have been detected in dogs and humans (Skrjabin et al., 1967): Thelazia callipaeda and Thelazia californiensis. The former has also been detected in cats, rabbits, foxes and wolves (Kozlov, 1961; Otranto et al., 2007; Skrjabin et al., 1967). Apart from dogs and humans, the latter spirurid has been described in sheep, deer, coyotes and bears (Anderson, 2000).

The nematodes possess a size of approximately 7.5 to 19 mm. The intermediate hosts of T. callipaeda are fruitflies of the genus Phortica.

The parasites are living in the orbital cavity and associated tissues. Adult females are viviparous and release first stage larvae (L1) into the lachrymal secretions of the host. Secretophagous non-biting flies feed on these secretions and become infected with the L1. In the arthropod vector, the larvae undergo their development from L1 to L3, the third stage infective larva, while remaining encapsulated in different parts of the vector’s body. This is depending upon the different species of Thelazia. Finally they migrate through the arthropods’ coeloma to the labella. The infective L3 emerge from the labella of the infected flies as soon as those feed on the lachrymal secretions of receptive animals. In the definite host the L3 develops into the adult stage in the ocular cavity within 3-6 weeks.

Distribution

For long time T. callipaeda has been considered to be mainly distributed in the Russian Federation and the Far East (China, Japan, India, Indonesia, Thailand, Korea, Myanmar, etc.) (Bhaibulaya et al., 1970; Hong et al., 1995; Kosin et al., 1989). However,  this nematode infection has also been detected in Europe (e.g., Italy (e.g., Otranto et al., 2003a; Rossi and Bertaglia, 1989), France (Dorchies et al., 2007), Switzerland (Schnyder et al, 2007, Malacrida et al., 2008).

T. californiensis has been reported only in the western USA (Dozie et al., 1996; Skrjabin et al., 1967).

Pathogenesis and Transmission

Concerning the vector of T. callipaeda it has been hypothesized, based on study results, that only Phortica variegata males may act as an intermediate host under natural conditions (Otranto et al., 2006). It was further speculated that the specificity in the development of T. callipaeda in male P. variegata might have biased the zooophilic behavior of the fly (Otranto et al., 2006). For details on developmental cycle see Pathogen(s).

A seasonal activity in the reproduction of T. callipaeda, coinciding with the presence/absence of the vector could be observed, with activity of the intermediate host from early spring to early autumn (Otranto et al., 2004).

Clinical symptoms are mainly caused by L3 and/or L4 immature stages and appear to be similar to those of allergic conjunctivitis (Otranto, 2008). Symptoms of thelaziosis are mainly due to the lateral serration of the T. callipaeda cuticle which is responsible for mechanical damage of the conjunctival and corneal epithelium (Otranto et al., 2003b). Clinical manifestations (here for human thelaziosis) are related to the number of nematodes present in the eye, their location, the host-immune response and the occurrence of secondary infection with bacteria (Shen et al., 2006). Tangled worms are mostly localized in the conjunctival sac and the medial or lateral canthus, but have also been detected in the anterior chamber (here in humans) (Shen et al., 2006).

Diagnosis

Diagnosis of canine (and human) thelaziosis is usually based on the finding of the adult nematode on the conjunctiva at the clinical and ophthalmological examinations. The larvae or adult nematodes appear as a thin, creamy-white thread in the conjunctival sac. The nematodes can be collected by flushing saline from the medial canthus, with the eye secretions then submitted to a microscopical parasitic examination in order to detect the typical newborn L1. Generally diagnosis can be difficult if small numbers of adults are present.

Clinical signs

Both, adult and larval stages of eyeworms are responsible for eye diseases with symptoms ranging from mild (e.g., lacrimation, ocular discharge, epiphora) to severe (e.g., conjunctivitis, keratitis, corneal opacity or ulcers).

Treatment

As treatment adult and larvae may be removed mechanically by rinsing the conjunctival sac with sterilized saline and fluids or by picking them out with a fine forceps or cotton swap. In the latter case local anesthesia is recommended for detection and recovery (Shen et al., 2006). The symptoms generally resolve quickly after successful treatment.

Apart from mechanical removal, a local therapy with moxidectin (1-2 drops of an aqueous 1 % solution, approximately 0.006 mg) eliminated the worm burden in 48 dogs (30 of those showing clinical signs) within 2 min (Lia et al., 2004). The topical instillation of organophosphates has also proven to be highly effective against T. callipaeda (Rossi and Peruccio, 1989). A single spot-on application of moxidectin (2.5 %) plus imidacloprid (10 %) was effective for the control of thelaziosis in 21 dogs within 5 (90 %) to 9 days (95 %) (Biancardi and Otranto, 2005). Thus problems linked to mechanical removal of worms or restraining of dogs for topical treatment can be overcome. Injectable sustained-release formulation of moxidectin provided one season protection against T. callipaeda infection in dogs (Rossi et al., 2007).

The systemic or local chemotherapy is preferable in comparison to a mechanical removal. And the sustained-release formulation is more likely expected to reduce the prevalence of dog thelaziosis and thus also the potential zoonotic risk in endemic areas (Otranto, 2008).

Further information

• Otranto, D.: Thelazia callipaeda eyeworm: a “neglected” CVBD of human concern. Proceedings of the 3rd Int. CVBD Symposium, 2008, 94-102 (Download)

References

• Anderson, R.C.: Nematode Parasites of Vertebrates. Their Development and Transmission. 2^nd edn., 2000, CAB International, Wallingford, Oxon, UK
• Bhaibulaya, M., Prasertsilpa, S., Vajrasthira, S.: Thelazia callipaeda Railliet and Henry, 1910, in man and dog in Thailand. Am. J. Trop. Med. Hyg., 19, 1970, 476-479
• Bianciardi, P., Otranto, D.: Treatment of dog thelaziosis caused by Thelazia callipaeda (Spirurida, Thelaziidae) using a topical formulation of imidacloprid 10% and moxidectin 2.5%.Vet. Parasitol., 129, 2005, 89-93
• Dorchies, P., Chaudieu, G., Siméon, L.A., Cazalot, G., Cantacessi, C., Otranto, D.: First reports of autochthonous eyeworm infection by Thelazia callipaeda (Spirurida, Thelaziidae) in dogs and cat from France. Vet. Parasitol., 149, 2007, 294-297
• Dozie, A.M., Lucius,R.W., Aldeen, W., et al.: Thelazia californiensis conjunctival infestation. Opht. Lit., 49, 1996, 225
• Hong, S.T., Park, Y.K., Lee, S.K., et al.: Two human cases of Thelazia callipaeda infection in Korea. Korean J. Parasitol., 33, 1995, 139-144
• Kosin, E., Kosman, M.L., Depary, A.A.: First case of human thelaziasis in Indonesia.,Southeast Asian J. Trop. Med. Public Health, 20, 1989, 233-236
• Kozlov, D.P.: The life cycle of nematode, Thelazia callipaeda parasitic in the eye of the man and carnivores. Doklady Akademii Nauk SSSR, 142, 1961, 732-733 (in Russian)
• Lia, R.P., Traversa, D., Agostini, A., Otranto, D.: Field efficacy of moxidectin 1 per cent against Thelazia callipaeda in naturally infected dogs. Vet. Rec. 154, 2004, 143-145 (comment in: Vet. Rec.154, 2004, 248)
• Malacrida,F., Hegglin, D., Bacciarini, L., Otranto, D., Nägeli, F., Nägeli, C.,Bernasconi, C., Scheu, U., Balli, A., Marengo, M., Togni, L., Deplazes, P., Schnyder, M.:Emergence of canine ocular thelaziosis caused by Thelazia callipaeda in southern Switzerland. Vet. Parasitol. 157, 2008, 321-327
• Otranto, D.: Thelazia callipaeda eyeworm: a”neglected” CVBD of human concern. Proceedings of the 3rd Int. CVBD Symposium, 2008, 94-102
• Otranto, D., Ferroglio, E., Lia, R.P., Traversa, D., Rossi, L.: Current status and epidemiological observation of Thelazia callipaeda, 2003a, 315-325
• Otranto, D., Lia, R.P., Traversa, D., Giannetto, S.: Thelazia callipaedaParassitologia, 45, 2003b, 125-133
• Otranto, D., Lia, R.P., Buono, V., Traversa, D., Giangaspero, A.: Biology of Thelazia callipaeda
• Otranto, D., Cantacessi, C., Testini, G., Lia, R.P.: Phortica variegataintermediate host of Thelazia callipaeda under natural conditions: evidence for pathogen transmission by a male arthropod vector. Int. J. Parasitol., 36, 2006, 1167-1173
• Otranto, D., Cantacessi, C., Mallia, E., Lia, R.P.: First report of Thelazia callipaeda
• Rossi, L., Bertaglia, P.P.: Presence of Thelazia callipaeda
• Rossi, L., Peruccio, C.:Thelaziosi oculare nel Cane: aspetti clinici e terapeutici. Veterinaria, 2, 1989, 47-50 (in Italian)
• Rossi, L., Rigano, C., Tomio, E., Frassetto, D., Ferroglio, E.: Use of sustained-release moxidectin to prevent eyeworm (Thelazia callipaeda
• Schnyder, M., Malacrida, F., Bacciarini, L., Otranto,D., Deplazes,P.: Autochthonus transmission of Thelazia callipaeda21st Int. Conf. of the WAAVP, Ghent, Belgium, 2007, 055, p. 157
• Shen, J., Gasser, R.B., Chu, D., Wang, Z., Yuan, X., Cantacessi, C., Otranto, D.: Human thelaziosis – a neglected parasitic disease of the eye. J. Parasitol., 92, 2006, 872-875
• Skrjabin, K.I., Sobolev, A.A., Ivashkin, V.M.: Principles of Nematology. Vol. IX. Spirurata of Animals and Man and the Disease caused by them (Part 4): Thelazioidea. Izdatel’sto Akademii Nauk SSSR, published by Israel Program for Scientific Translations