Abstract
Thelazia callipaeda (Spirurida, Thelaziidae) is a vector-borne zoonotic eyeworm able to infect a broad spectrum of carnivores. Here, we describe the first case of bilateral infection by T. callipaeda in the eyes of an adult female Iberian wolf (Canis lupus signatus) in central Spain. Nematodes collected were morphologically identified (n = 42), and two specimens were molecularly characterized. At the sequence analysis of the partial mitochondrial cytochrome c oxidase subunit 1 gene, T. callipaeda haplotype 1 (the only haplotype circulating in Europe) was detected. The role of the Iberian wolf as a natural reservoir for T. callipaeda in the life cycle of this emerging zoonosis and the implications in conservation are discussed.
References
Anderson RC (2000) Nematode parasites of vertebrates. Their development and transmission, 2nd edn. CABI Publishing, Guilford, p 750
Blanco-Gutiérrez JC, Alonso García EM, Sánchez Aragonés J, de Lucas Veguillas J, Clemente J, Cerezo G (2012) Uso de los centros de reunión y movimientos de una reproductora radiomarcada en Guadalajara. III Congreso Ibérico del Lobo. 23-25 Noviembre 2012. Lugo, Spain
Calero-Bernal R, Otranto D, Pérez-Martín JE, Serrano FJ, Reina D (2013) First report of Thelazia callipaeda in wildlife from Spain. J Wildl Dis 49:458–460. https://doi.org/10.7589/2012-10-268
Calero-Bernal R, Sánchez-Murillo JM, Alarcón-Elbal PM, Sánchez-Moro J, Latrofa MS, Dantas-Torres F, Otranto D (2014) Resolution of canine ocular thelaziosis in avermectin-sensitive Border Collies from Spain. Vet Parasitol 200:203–206. https://doi.org/10.1016/j.vetpar.2013.12.014
Castelló JR (2018) Canids of the world. Wolves, wild dogs, foxes, jackals, coyotes, and their relatives. Princeton University Press, Princeton, p 98
do Vale B, Lopes AP, da Conceição Fontes M, Silvestre M, Cardoso L, Coelho AC (2019) Thelaziosis due to Thelazia callipaeda in Europe in the 21st century-a review. Vet Parasitol 275:108957. https://doi.org/10.1016/j.vetpar.2019.108957
Gajić B, Bugarski-Stanojević V, Penezić A, Kuručki M, Bogdanović N, Ćirović D (2019) First report of eyeworm infection by Thelazia callipaeda in gray wolf (Canis lupus) from Serbia. Parasitol Res 118:3549–3553. https://doi.org/10.1007/s00436-019-06519-z
Gama A, Pires I, Canado M, Coutinho T, Lopes AP, Latrofa MS, Cardoso L, Dantas-Torres F, Otranto D (2016) First report of Thelazia callipaeda infection in wild European rabbits (Oryctolagus cuniculus) in Portugal. Parasit Vectors 9:236. https://doi.org/10.1186/s13071-016-1526-1
Ionică AM, Deak G, D'Amico G, Stan GF, Chișamera GB, Constantinescu IC, Adam C, Lefkaditis M, Gherman CM, Mihalca AD (2019) Thelazia callipaeda in mustelids from Romania with the European badger, Meles meles, as a new host for this parasite. Parasit Vectors 12:370. https://doi.org/10.1186/s13071-019-3631-4
Marino V, Gálvez R, Montoya A, Mascuñán C, Hernández M, Barrera JP, Domínguez I, Zenker C, Checa R, Sarquis J, Miró G (2020) Spain as a dispersion model for Thelazia callipaeda eyeworm in dogs in Europe. Prev Vet Med 175:104883. https://doi.org/10.1016/j.prevetmed.2020.104883
Mihalca A, 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. Parasit Vectors 9:350. 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. Parasit Vectors 4:148. https://doi.org/10.1186/1756-3305-4-148
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, Ferroglio E, Lia RP, Traversa D, Rossi L (2003) Current status and epidemiological observations of Thelazia callipaeda (Spirurida, Thelaziidae) in dogs, cats and foxes in Italy: a “coincidence” or a parasitic disease of the old continent? Vet Parasitol 116:315–325. https://doi.org/10.1016/j.vetpar.2003.07.022
Otranto D, Lia RP, Traversa D, Giannetto S (2004) Thelazia callipaeda (Spirurida, Thelaziidae) of carnivores and humans: morphological study by light and scanning electron microscopy. Parassitologia 45:125–133
Otranto D, Lia RP, Cantacessi C, Testini G, Troccoli A, Shen JL, Wang ZX (2005a) Nematode biology and larval development of Thelazia callipaeda (Spirurida, Thelaziidae) in the drosophilid intermediate host in Europe and China. Parasitology 131:847–855. https://doi.org/10.1017/S0031182005008395
Otranto D, Lia RP, Testini G, Milillo P, Shen JL, Wang ZX (2005b) Musca domestica is not a vector of Thelazia callipaeda in experimental or natural conditions. Med Vet Entomol 19:1–5. https://doi.org/10.1111/j.0269-283X.2005.00554.x
Otranto D, Testini G, Deluca F, Hu M, Shamsi S, Gasser RB (2005c) 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. Mol Cell Probes 19:306–313. https://doi.org/10.1016/j.mcp.2005.05.001
Otranto D, Cantacessi C, Mallia E, Lia RP (2007) First report of Thelazia callipaeda (Spirurida, Thelaziidae) in wolves in Italy. J Wildl Dis 43:508–511. 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 166:262–267. https://doi.org/10.1016/j.vetpar.2009.08.027
Papadopoulos E, Komnenou A, Thomas A, Ioannidou E, Colella V, Otranto D (2017) Spreading of Thelazia callipaeda in Greece. Transbound Emerg 65:248–252. https://doi.org/10.1111/tbed.12626
Rossi L, Bertaglia PP (1989) Presence of Thelazia callipaeda Railliet & Henry, 1910, in Piedmont, Italy. Parassitologia 31:167–172
Seixas F, Travassos P, Coutinho T, Lopes AP, Latrofa MS, dos Anjos PM, Cardoso L, Otranto D (2018) The eyeworm Thelazia callipaeda in Portugal: current status of infection in pets and wild mammals and case report in a beech marten (Martes foina). Vet Parasitol 252:163–166. https://doi.org/10.1016/j.vetpar.2018.02.007
Skrjabin KI, Sobolev AA, Ivashkin VM (1967) Principles of nematology. Vol. IX. Spirurata of animals and man and the disease caused by them. Part. 4: Thelazioidea. Izdatel’sto Akademii Nauk SSSR, Israel Program for Scientific Translations, Washington, USA, pp. 8–58
Acknowledgments
This work is included within the Rural Development Plan of Castilla-La Mancha (media 4.4: Plan de Desarrollo Rural), supported by the FEDER fund. We thank the Dirección General de Medio Ambiente y Desarrollo Sostenible (especially Antonio Aranda and Marino López de Carrión). We are indebted to all the wardens (Agentes de Medio Ambiente) of Castilla-La Mancha for their tireless field work, especially to all the wildlife rangers in charge of surveillance and tracking of Iberian wolves in the Northwest Guadalajara. Special thanks go to the livestock producers from the Sierra Norte in Guadalajara province.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Una Ryan
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nájera, F., de Lucas-Veguillas, J., Vela, Á. et al. First report of Thelazia callipaeda in a free-ranging Iberian wolf (Canis lupus signatus) from Spain. Parasitol Res 119, 2347–2350 (2020). https://doi.org/10.1007/s00436-020-06735-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-06735-y