Abstract
Thelazia callipaeda, originally known as an “Oriental eyeworm,” is a small nematode parasitizing the conjunctival sacs of domestic and wild animals and humans. Previous studies conducted in Serbia have reported the eyeworm infections in dogs, cats, and foxes, as well as in a human patient. As the data regarding thelaziosis from wildlife is still scarce, the aim of this study was to investigate the presence of T. callipaeda in gray wolf (Canis lupus) from Serbia. All collected nematodes were morphologically identified as T. callipaeda males (n = 64) or females (n = 225). Molecular characterization, conducted by PCR amplification followed by sequence analysis of partial cytochrome c oxidase subunit 1 gene (cox1), revealed only haplotype 1 of T. callipaeda. The overall prevalence of thelaziosis was 38.1% (8/21). In all positive animals, both eyes were affected, with a total parasitic load ranging from four to 132 worms per animal. Our results indicate the important epidemiological role of wolves as wildlife reservoirs of T. callipaeda, expanding geographic range of infection, as well as intra- and interspecies contact rates, although the role of other wild carnivore species (i.e., foxes and jackals) should be investigated in future studies.
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References
Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. CABI Publishing, Wallingford, p 672
Čabanová V, Miterpáková M, Oravec M, Hurníková Z, Jerg S, Nemčíková G, Červenská MB (2018) Nematode Thelazia callipaeda is spreading across Europe. The first survey of red foxes from Slovakia. Acta Parasitol 63(1):160–166. https://doi.org/10.1515/ap-2018-0018
Casiraghi M, Anderson TJC, Bandi C, Bazzocchi C, Genchi C (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122(1):93–103. https://doi.org/10.1017/S0031182000007149
Colella V, Kirkova Z, Fok É, Mihalca AD, Tasić-Otašević S, Hodžić A, Dantas-Torres F, Otranto D (2016) Increase in eyeworm infections in eastern Europe. Emerg Infect Dis 22(8):1513–1515. https://doi.org/10.3201/eid2208.160792
Dorchies P, Chaudieu G, Siméon LA, Cazalot G, Cantacessi C, Otranto D (2007) First reports of autochthonous eyeworm infection by Thelazia callipaeda (Spirurida, Thelaziidae) in dogs and cat from France. Vet Parasitol 149(3-4):294–297. https://doi.org/10.1016/j.vetpar.2007.08.005
Gajić B, Bogunović D, Stevanović J, Kulišić Z, Simeunović P, Stanimirović Z (2014) Canine and feline thelaziosis caused by Thelazia callipaeda in Serbia. Acta Vet-Beograd 64(4):447–455. https://doi.org/10.2478/acve-2014-0042
Hodžić A, Latrofa MS, Annoscia G, Alić A, Beck R, Lia RP, Dantas-Torres F, Otranto D (2014) The spread of zoonotic Thelazia callipaeda in the Balkan area. Parasit Vectors 7(1):352. https://doi.org/10.1186/1756-3305-7-352
Karamanlidis AA, Gabriel Hernando M, Georgiadis L, Kusak J (2016) Activity, movement, home range and habitat use of an adult gray wolf in a Mediterranean landscape of northern Greece. Mammalia. https://doi.org/10.1515/mammalia-2015-0091
Máca J, Otranto D (2014) Drosophilidae feeding on animalsand the inherent mystery of their parasitism. Parasite Vector 7:516. https://doi.org/10.1186/s13071-014-0516-4
Magnis J, Naucke TJ, Mathis A, Deplazes P, Schnyder M (2010) Local transmission of the eye worm Thelazia callipaeda in southern Germany. Parasitol Res 106:715–717. https://doi.org/10.1007/s00436-009-1678-4
Malacrida F, Hegglin D, Bacciarini L, Otranto D, Nägeli F, Nägeli C, Bernasconi C, Scheu U, Balli A, Marenco M, Togni L, Deplazes P, Schnyder M (2008) Emergence of canine ocular thelaziosis caused by Thelazia callipaeda in southern Switzerland. Vet Parasitol 157:321–327. https://doi.org/10.1016/j.vetpar.2008.07.029
Mihalca AD, Ionică AM, D’Amico G, Daskalaki AA, Deak G, Matei IA, Șimonca V, Iordache D, Modrý D, Gherman CM (2016) Thelazia callipaeda in wild carnivores from Romania: new host and geographical records. Parasite Vector 9(1):350. https://doi.org/10.1186/s13071-016-1628-9
Miró G, Montoya A, Hernández L, Dado D, Vázquez MV, Benito M, Villagrasa M, Brianti E, Otranto D (2011) Thelazia callipaeda: infection in dogs: a new parasite for Spain. Parasite Vector 4:148. https://doi.org/10.1186/1756-3305-4-148
Moura AE, Tsingarska E, Dąbrowski MJ, Czarnomska SD, Jędrzejewska B, Pilot M (2014) Unregulated hunting and genetic recovery from a severe population decline: the cautionary case of Bulgarian wolves. Conserv Genet 15:405–417. https://doi.org/10.1007/s10592-013-0547-y
Otranto D, Deplazes P (2019) Zoonotic nematodes of wild carnivores. Int J Parasitol Parasites Wildl 9:370–383. https://doi.org/10.1016/j.ijppaw.2018.12.011
Otranto D, Lia RP, Traversa D, Giannetto S (2003) Thelazia callipaeda (Spirurida, Thelaziidae) of carnivores and humans: morphological study by light and scanning electron microscopy. Parassitologia 45:125–133
Otranto D, Lia RP, Buono V, Traversa D, Giangaspero A (2004) Biology of Thelazia callipaeda (Spirurida, Thelaziidae) eyeworms in naturally infected definitive hosts. Parasitology 129(5):627–633
Otranto D, Testini G, De Luca F, Hu M, Shamsi S, Gasser RB (2005) Analysis of genetic variability within Thelazia callipaeda (Nematoda: Thelazioidea) from Europe and Asia by sequencing and mutation scanning of mitochondrial cytochrome c oxidase subunit 1 gene. Mol Cell Probes 19:306–313. https://doi.org/10.1016/j.mcp.2005.05.001
Otranto D, Cantacessi C, Testini G, Lia RP (2006) Phortica variegata as an intermediate host of Thelazia callipaeda under natural conditions: evidence for pathogen transmission by a male arthropod vector. Int J Parasitol 36(10-11):1167–1173. https://doi.org/10.1016/j.ijpara.2006.06.006
Otranto D, Cantacessi C, Mallia E, Lia RP (2007) First report of Thelazia callipaeda (Spirurida, Thelaziidae) in wolves in Italy. J Wildl Dis 43(3):508–511. https://doi.org/10.7589/0090-3558-43.3.508
Otranto D, Dantas-Torres F, Mallia E, DiGeronimo PM, Brianti E, Testini G, Traversa D, Lia RP (2009) Thelazia callipaeda (Spirurida, Thelaziidae) in wild animals: report of new host species and ecological implications. Vet Parasitol 166(3–4):262–267. https://doi.org/10.1016/j.vetpar.2009.08.027
Otranto D, Cantacessi C, Dantas-Torres F, Brianti E, Pfeffer M, Genchi C, Guberti V, Capelli G, Deplazes P (2015) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: Helminths and arthropods. Vet Parasitol 213(1–2):24–37. https://doi.org/10.1016/j.vetpar.2015.04.020
Papadopoulos E, Komnenou A, Thomas A, Ioannidou E, Colella V, Otranto D (2018) Spreading of Thelazia callipaeda in Greece. Transbound Emerg Dis 65(1):248–252. https://doi.org/10.1111/tbed.12626
Pavlović I, Jakić-Dimić D, Kureljušić B, Ćirović D, Jezdimirović N, Drobnjak M (2017) First occurrence of Thelazia callipaeda in foxes (Vulpes vulpes L.) in Serbia. Balk J Wildlife Res 4(1):1–5. https://doi.org/10.15679/bjwr.v4i1.31
Ražen N, Brugnoli A, Castagna C, Groff C, Kaczensky P, Kljun F, Knauer F, Kos I, Krofel M, Luštrik R, Majić A, Rauer G, Righetti D, Potočnik H (2016) Long-distance dispersal connects Dinaric-Balkan and Alpine grey wolf (Canis lupus) populations. Eur J Wildl Res 62(1):137–142. https://doi.org/10.1007/s10344-015-0971-z
Rossi L, Bertaglia P (1989) Presence of Thelazia callipaeda Railliet and Henry, 1910, in Piedmont, Italy. Parassitologia 31:167–172
Skrjabin KI, Sobolev AA, Ivashkin VM (1967) Spirurata of animals and man and the disease caused by them. Part 4: Thelazioidea. In: Skrjabin KI (ed) Essential of nematodology, vol XVI. Academy of Sciences of the USSR, Moscow, p 624 in Russian
Tasić-Otašević S, Gabrielli S, Trenkić-Božinović M, Petrović A, Gajić B, Colella V, Momčilović S, Cancrini G, Otranto D (2016) Eyeworm infections in dogs and in a human patient in Serbia: a one health approach is needed. Comp Immunol Microbiol Infect Dis 45:20–22. https://doi.org/10.1016/j.cimid.2016.01.003
Vieira L, Rodrigues TF, Costa Á, Diz-Lopes D, Machado J, Coutinho T, Tuna J, Latrofa MS, Cardoso L, Otranto D (2012) First report of canine ocular thelaziosis by Thelazia callipaeda in Portugal. Parasit Vectors 5:124. https://doi.org/10.1186/1756-3305-5-124
Acknowledgments
We are most grateful to Srđan Vučković and Marija Spasić who kindly helped in sample collection.
Funding
This work was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (grant nos. 173006 and 173025).
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Bojan, G., Vanja, BS., Aleksandra, P. et al. First report of eyeworm infection by Thelazia callipaeda in gray wolf (Canis lupus) from Serbia. Parasitol Res 118, 3549–3553 (2019). https://doi.org/10.1007/s00436-019-06519-z
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DOI: https://doi.org/10.1007/s00436-019-06519-z