Tracking the Vector of Onchocerca Lupi in a Rural Area of Greece
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ANOTHER DIMENSION 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 uring a hot Mediterranean summer, an expedition lupi, known to infest dog eyes, inducing an acute or chronic Dbrought parasitologists from Brazil, France, Greece, ocular disease characterized by conjunctivitis, photopho- Italy, and Serbia to a wooded area near Xanthi, Thrace, bia, lacrimation, discharge, and exophthalmia. At that time, northeastern Greece, near the Turkish border, on the track this helminth infestation had never been reported in dogs of the vector of the little-known nematode Onchocerca in Turkey, and information on the biologic features of the lupi. The scientifi c purposes of the expedition blended then nematode was still meager, despite its wide distribution in with stories of humans, animals, and parasites in this rural Greece, Germany, Hungary, Portugal, and Switzerland and area. the increasing number of reported cases (7). O. lupi nema- tode infestation in humans (8) and its biologic and patho- The Beginnings: What’s that Worm genic affi nity with Onchocerca volvulus, the agent of river in the Turkish Blue Eye? blindness, heightened the interest of D.O. and F.D.T. in the In the early months of 2010, Nermin Sakru, a microbi- life cycle of this nematode. The idea of investigating the ologist from the Medical School of Trakya University, Er- biologic features of O. lupi soon began to move across the dine, Turkey, contacted one of the authors (D.O.) seeking convoluted pathways of their brains like larvae of Oestrus advice on how to identify a nematode extracted from the ovis (the nasal bot fl y) migrating toward the central nervous eye of an 18-year-old girl who had never traveled out of her system, the main decisional center of all animals! native Trakya. Nematodes that might have caused such an infestation were many (1), including Thelazia callipaeda. Organizing the Scientifi c Expedition: This helminth, which infests carnivores and humans, has Paris and Antwerp been studied for more than a decade at the University of In the early autumn of 2010, D.O. and F.D.T. had the Bari in southern Italy (2–5); this research was what led the opportunity to work at O.B.’s laboratories at the Natural Turkish colleague to establish original contact. The patient History Museum in Paris to morphologically describe complained of pain and redness in the left eye and report- dermal microfi lariae of a fi larioid of the genus Cercopith- ed being bitten by a fl y on the left eyelid in the evening ifi laria, isolated some months earlier from a dog in Sicily (around 5:00 PM), ≈30 days before onset of symptoms. (9,10). Those days were short in sunlight, as fall reached Pain caused by a biting insect was suggestive of infesta- Paris much earlier than southern Italy, making the labora- tion other than by T. callipaeda, which is transmitted by tory not the coziest place for late shifts. The helminthology Phortica variegata (Diptera, Drosophilidae), an insect that laboratory of the museum is a historically rich place where gently feeds on the ocular secretions of its hosts during the such eminent scientists as Alain G. Chabaud had described pleasantly warm Mediterranean summers (6). numerous nematodes of medical and veterinary concern for Some days later, the nematode was morphologically more than 30 years, (11,12). Working in that small labora- and molecularly identifi ed as a little spirurid, Onchocerca tory with simple, dated, yet handy, equipment led to inspir- ing discussions about prospective studies. By dealing with Author affi liations: Università degli Studi di Bari, Valenzano, Italy the zoonotic infestation by O. lupi nematodes, they real- (D. Otranto, F. Dantas-Torres); Aggeu Magalhães Research Centre ized how important this parasite species could be, even as Oswaldo Cruz Foundation, Recife, Brazil (F. Dantas-Torres); Fac- a model for better understanding of O. volvulus pathogen- ulty of Veterinary Medicine, Thessaloniki, Greece (E. Papadopou- esis. A major gap in the knowledge of this parasite species los); University of Novi Sad Faculty of Agriculture, Novi Sad, Serbia was with regard to its vector. (D. Petrić, A. Ignjatović Ćupina); and Muséum National d’Histoire D.O., F.D.T., and O.B. supposed that, as in several Naturelle, UMR 7205 CNRS, Paris, France (O. Bain) other Onchocerca species, the potential vector of O. lupi DOI: http://dx.doi.org/10.3201/eid1807.AD1807 could be a black fl y (Diptera, Simuliidae) (13) or even a 1196 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 7, July 2012 ANOTHER DIMENSION biting midge (Diptera, Ceratopogonidae) (14), so they de- fi xed at 9 days—a terribly short time for such an ambitious cided to carry out a fi eld study in an area where this parasite task. species is endemic. The choice for the best places to look The fi rst step toward retrieval of the developmental in- for animal cases was not easily made as this infestation had fective larvae in a putative vector collected in the fi eld was never been reported in Italy, Brazil, or France. However, to identify an area of O. lupi infestation. The fi rst meeting O.B. recalled that canine onchocercosis caused by O. lupi took place in a clean, pretty hotel in the vicinity of Thes- infestation was reported in the Chalkidiki peninsula, prov- saloniki airport. While some of us (D.O., F.D.T., O.B.) ar- ince of Thessaloniki, Greece (15), where E.P. has been ac- rived by plane, others (D.P., A.I.C.) arrived from Serbia tive for 2 decades in veterinary parasitology. after a many hours of driving. Almost nobody knew each Months later, during the annual meeting of the Europe- other, and the fi rst dinner, in spite of the tiredness, was the an Network for Arthropod Vector Surveillance for Human real kick-off meeting for the discussion and planning of the Public Health (Antwerp, April 2011), 2 Serbian entomolo- fi eld activities. At the end of the fi rst day, all team members gists (D.P. and A.I.C.) with expertise on black fl y taxonomy were focused on their own duties and commitments in the and biology were hearing about this new parasite and the expedition. enthusiastic plans of an Italian researcher (D.O.) keen on Early in the morning of the second day, after we had studying its vector. The hypothesis of this scientifi c expedi- a chat over a coffee with A. Komnenou for better defi ning tion blended then with stories of researchers and parasitolo- the localities where O. lupi infestations had been reported, gists in the years of the Yugoslav Wars (1991–1995) (16). the expedition moved to a wooded area near Xanthi. In an- Scientists around the table agreed that, sometimes, research cient times, Thrace was considered the fourth continent, af- activities do soothe physical and mental pains, helping to ter Europe, Asia, and Africa, because of its great difference get wars out of people’s minds. Once back in Novi Sad from the rest of Greece. Geographically, it belongs to the (Serbia), D.P. and A.I.C. decided they would take part in Balkans, with 5 major river systems and few safe anchor- the expedition with O.B., F.D.T., D.O., and E.P. ages. In this area, until late in the 20th century, population centers were formed in the foothills of the valleys, far from In Thessaloniki on the Way to Xanthi the mosquito- and pirate-infested marshy coastal lowlands. In June 2011, participants of the expedition team from Our hotel was located just outside Xanthi, on the way the National History Museum in Paris (O.B.), the School of to Mount Koula near the small river Kosinthos. Most roads Veterinary Medicine of Bari (D.O. and F.D.T.), the School were constantly crossed by turtles (Testudo graeca) that of Veterinary Medicine of Thessaloniki (E.P. and Socrates carried ticks (Hyalomma aegyptium). This place was cho- Ptochos), and the Faculty of Agriculture, University of sen for the small stream in a large, stony valley and for Novi Sad in Serbia (D.P. and A.I.C.) received the fi rst mes- the overall environmental characteristics of the surround- sage in preparation for the expedition: ings―bushes and oaks representing the optimal biotope for black fl ies (putative vectors of O. lupi). “The main aim of our expedition is to study the We were the only guests at the hotel, and the owner al- occurrence of O. lupi infested dogs and to identify lowed us to use a large dining room as our makeshift labo- the vector of this nematode. It will be a fi eldwork ratory (Figure 1). We set up 3 optical microscopes and a whose protocol might require some adjustments stereomicroscope on 4 tables, together with slides, entomo- according to the preliminary results. Skin and logic forceps, and ethanol necessary for checking, at night, blood samples will be collected from dogs samples collected during daytime. living in areas around rivers to diagnose O. lupi Kalimera, Xanthi: The Frontier Land infestation. In the meantime, adult black fl ies shall The expedition team members soon learned that Xan- be collected by dry ice baited traps and drop nets thi was the hometown of Democritus (c. 460 BCE–370 directly on dogs. During the study, samples will BCE), the ancient Greek philosopher who formulated be processed and examined at night in accordance the atomic theory for the cosmos. With a population of with the fi eld activities.” ≈55,500, this region is a frontier land.