Tracking the Vector of Onchocerca lupi in a Rural Area of Greece

Domenico Otranto

, Filipe Dantas-Torres, Elias Papadopoulos, Dušan Petrić, Aleksandra Ignjatović Ćupina, and Odile Bain

Author affiliations: Università degli Studi di Bari, Valenzano, Italy (D. Otranto, F. Dantas-Torres); Aggeu Magalhães Research Centre Oswaldo Cruz Foundation, Recife, Brazil (F. Dantas-Torres); Faculty of Veterinary Medicine, Thessaloniki, Greece (E. Papadopoulos); University of Novi Sad Faculty of Agriculture, Novi Sad, Serbia (D. Petrić, A. Ignjatović Ćupina); and Muséum National d’Histoire Naturelle, UMR 7205 CNRS, Paris, France (O. Bain)

Suggested citation for this article
During a hot Mediterranean summer, an expedition brought parasitologists from Brazil, France, Greece, Italy, and Serbia to a wooded area near Xanthi, Thrace, northeastern Greece, near the Turkish border, on the track of the vector of the little-known nematode Onchocerca lupi. The scientific purposes of the expedition blended then with stories of humans, animals, and parasites in this rural area.

The Beginnings: What’s that Worm in the Turkish Blue Eye?

In the early months of 2010, Nermin Sakru, a microbiologist from the Medical School of Trakya University, Erdine, Turkey, contacted one of the authors (D.O.) seeking advice on how to identify a nematode extracted from the eye of an 18-year-old girl who had never traveled out of her native Trakya. Nematodes that might have caused such an infestation were many (1), including Thelazia callipaeda. This helminth, which infests carnivores and humans, has been studied for more than a decade at the University of Bari in southern Italy (2–5); this research was what led the Turkish colleague to establish original contact. The patient complained of pain and redness in the left eye and reported being bitten by a fly on the left eyelid in the evening (around 5:00 PM), ≈30 days before onset of symptoms. Pain caused by a biting insect was suggestive of infestation other than by T. callipaeda, which is transmitted by Phortica variegata (Diptera, Drosophilidae), an insect that gently feeds on the ocular secretions of its hosts during the pleasantly warm Mediterranean summers (6).
Some days later, the nematode was morphologically and molecularly identified as a little spirurid, Onchocerca lupi, known to infest dog eyes, inducing an acute or chronic ocular disease characterized by conjunctivitis, photophobia, lacrimation, discharge, and exophthalmia. At that time, this helminth infestation had never been reported in dogs in Turkey, and information on the biologic features of the nematode was still meager, despite its wide distribution in Greece, Germany, Hungary, Portugal, and Switzerland and the increasing number of reported cases (7). O. lupi nematode infestation in humans (8) and its biologic and pathogenic affinity with Onchocerca volvulus, the agent of river blindness, heightened the interest of D.O. and F.D.T. in the life cycle of this nematode. The idea of investigating the biologic features of O. lupi soon began to move across the convoluted pathways of their brains like larvae of Oestrus ovis (the nasal bot fly) migrating toward the central nervous system, the main decisional center of all animals!

Organizing the Scientific Expedition: Paris and Antwerp

In the early autumn of 2010, D.O. and F.D.T. had the opportunity to work at O.B.’s laboratories at the Natural History Museum in Paris to morphologically describe dermal microfilariae of a filarioid of the genus Cercopithifilaria, isolated some months earlier from a dog in Sicily (9,10). Those days were short in sunlight, as fall reached Paris much earlier than southern Italy, making the laboratory not the coziest place for late shifts. The helminthology laboratory of the museum is a historically rich place where such eminent scientists as Alain G. Chabaud had described numerous nematodes of medical and veterinary concern for more than 30 years (11,12). Working in that small laboratory with simple, dated, yet handy, equipment led to inspiring discussions about prospective studies. By dealing with the zoonotic infestation by O. lupi nematodes, they realized how important this parasite species could be, even as a model for better understanding of O. volvulus pathogenesis. A major gap in the knowledge of this parasite species was with regard to its vector.
D.O., F.D.T., and O.B. supposed that, as in several other Onchocerca species, the potential vector of O. lupi could be a black fly (Diptera, Simuliidae) (13) or even a biting midge (Diptera, Ceratopogonidae) (14), so they decided to carry out a field study in an area where this parasite species is endemic. The choice for the best places to look for animal cases was not easily made as this infestation had never been reported in Italy, Brazil, or France. However, O.B. recalled that canine onchocercosis caused by O. lupi infestation was reported in the Chalkidiki peninsula, province of Thessaloniki, Greece (15), where E.P. has been active for 2 decades in veterinary parasitology.
Months later, during the annual meeting of the European Network for Arthropod Vector Surveillance for Human Public Health (Antwerp, April 2011), 2 Serbian entomologists (D.P. and A.I.C.) with expertise on black fly taxonomy and biology were hearing about this new parasite and the enthusiastic plans of an Italian researcher (D.O.) keen on studying its vector. The hypothesis of this scientific expedition blended then with stories of researchers and parasitologists in the years of the Yugoslav Wars (1991–1995) (16). Scientists around the table agreed that, sometimes, research activities do soothe physical and mental pains, helping to get wars out of people’s minds. Once back in Novi Sad (Serbia), D.P. and A.I.C. decided they would take part in the expedition with O.B., F.D.T., D.O., and E.P.