Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter October 15, 2017

First report of pneumonia caused by Angiostrongylus vasorum in a golden jackal

Pavle Gavrilović, Darko Marinković, Igor Todorović and Aleksandra Gavrilović
From the journal Acta Parasitologica

Abstract

Angiostrongylosis caused by metastrongyloid nematode Angiostrongylus vasorum is an emerging parasitic disease in Europe and the red fox (Vulpes vulpes) is considered as a main reservoir species for this parasite. Little is known about the role of other wild canids in the epidemiology of angiostrongylosis. The present paper provides the first description of pathomorphological lesions caused by A. vasorum in a golden jackal (Canis aureus). The paper describes a case of co-infection with A. vasorum and Dirofilaria immitis in a one-year-old female golden jackal, legally hunted near the City of Kovin, South Banat, Serbia. The postmortem examination revealed severe pneumonia, proliferative endarteritis, the presence of two adult males of D. immitis in the right atrium, and the presence of 15 adult forms of A. vasorum (11 females and 4 males) in the pulmonary arteries. Native microscopy of an impression smear of the lung tissue found numerous larvae compatible with the A. vasorum first larval stage. This paper provides the first evidence that angiostrongylosis exists in the golden jackal in Serbia and confirms that the golden jackal should be considered as a very suitable definitive host for A. vasorum. The results suggest the possibility that the golden jackal may act as reservoir species and as an important transmitter of A. vasorum larvae.

References

Arnold J., Humer A., Heltai M., Murariu D., Spassov N., Hackländer K. 2012. Current status and distribution of golden jackals Canis aureus in Europe. Mammal Review, 42, 1–11. 10.1111/j.1365-2907.2011.00185.xSearch in Google Scholar

Benda T., Csivincsik Á., Nemes C., Turbók J., Zsolnai A., Simonyai E., et al. 2017. Lethal Angiostrongylus vasorum infection in a Hungarian dog. Acta Parasitologica, 62, 221–224. 10.1515/ap-2017-0027Search in Google Scholar PubMed

Bourque A.C., Conboy G., Miller L.M., Whitney H. 2008. Pathological findings in dogs naturally infected with Angiostrongylus vasorum in Newfoundland and Labrador, Canada. Journal of Veterinary Diagnostic Investigation, 20, 11–20. 10.1177/104063870802000103Search in Google Scholar PubMed

Ćirović D., Penezić A., Milenković M., Paunović M. 2008. Present distribution and factors of range spread of golden jackal (Canis aureus L., 1758) in Serbia. In: Proceedings of the International Conference on large carnivores, Žagubica, Serbia, 93–102Search in Google Scholar

Elsheikha H.M., Holmes S.A., Wright I., Morgan E.R., Lacher D.W. 2014. Recent advances in the epidemiology, clinical and diagnostic features, and control of canine cardiopulmonary angiostrongylosis. Veterinary Research, 45, 92. 10.1186/s13567-014-0092-9Search in Google Scholar PubMed PubMed Central

Furtado A.P., Melo F.T., Giese E.G., dos Santos J.N. 2010. Morphological redescription of Dirofilaria immitis. Journal of Parasitology, 96, 499–504. 10.1645/GE-2178Search in Google Scholar

Gavrilović P., Blitva-Robertson G., Özvegy J., Kiskároly F., Becskei Z. 2015. Case report of dirofilariasis in grey wolf in Serbia. Acta Parasitologica, 60, 175–178. 10.1515/ap-2015-0025Search in Google Scholar PubMed

Gavrilović P., Vasković N., Živulj A., Jovanović M. 2014. Examination of D. immitis presence in foxes in Serbia (in Serbian with English summary). Veterinarski Glasnik, 68, 387–393. 10.2298/VETGL1406387GSearch in Google Scholar

Guilhon J. 1963. Recherches sur le cycle évolutif du strongle des vaisseaux du chien. Bulletin de l’Académie Vétérinaire, 36, 431–442. (In French)10.4267/2042/67410Search in Google Scholar

Guilhon J., Cens B. 1973. Angiostrongylus vasorum (Baillet. 1866): etude biologique et morphologique. Annales de Parasitologie Humaine et Comparée, 48, 567–59610.1051/parasite/1973484567Search in Google Scholar

Helm J.R., Morgan E.R., Jackson M.W., Wotton P., Bell R. 2010. Canine angiostrongylosis: an emerging disease in Europe. Journal of Veterinary Emergency and Critical Care, 20, 98–109. 10.1111/j.1476-4431.2009.00494.xSearch in Google Scholar PubMed

Jefferies R., Shaw S.E., Willesen J., Viney M.E., Morgan E.R. 2010. Elucidating the spread of the emerging canid nematode Angiostrongylus vasorum between Palaearctic and Nearctic ecozones. Infection, Genetics and Evolution, 10, 561–568. 10.1016/j.meegid.2010.01.013Search in Google Scholar PubMed

Kawabata A., Nakagaki K., Yoshida M., Shirota K. 2008. Histopathological comparison of pulmonary artery lesions between raccoon dogs (Nyctereutes procyonoides) and domestic dogs experimentally infected with Dirofilaria immitis. Journal of Veterinary Medical Science, 70, 301–30310.1292/jvms.70.301Search in Google Scholar PubMed

Koch J., Willesen J.L. 2009. Canine pulmonary angiostrongylosis: an update. The Veterinary Journal, 179, 348–359. 10.1016/j.tvjl.2007.11.014Search in Google Scholar PubMed

McGarry J.W., Morgan E.R. 2009. Identification of first-stage larvae of metastrongyles from dogs. Veterinary Record, 165, 258–26110.1136/vr.165.9.258Search in Google Scholar PubMed

Milenković M. 1983. Jackal, Canis aureus Linnaeus, 1758 (Mammalia, Canidae) in eastern Serbia. In: Proceedings on the Fauna of Serbia, Belgrade, Serbia, 257–262Search in Google Scholar

Milenković M. 1987. Distribution of the jackal Canis aureus Linnaeus 1758 (Mammalia, Canidae) in Yugoslavia. In: Proceedings on the Fauna of SR Serbia IV, Belgrade, Serbia, 233–246Search in Google Scholar

Milenković M., Paunović M. 2003. Phenomenon of golden jackal (Canis aureus Linnaeus, 1758), expansion in Serbia. In: Proceedings of the Carpathian Workshop on Large Carnivore Conservation, Brasov, Romania, 35Search in Google Scholar

Morgan E., Shaw S. 2010. Angiostrongylus vasorum infection in dogs: continuing spread and developments in diagnosis and treatment. Journal of Small Animal Practice 51, 616–621. 10.1111/j.1748-5827.2010.01000.xSearch in Google Scholar PubMed

Morgan E.R., Tomlinson A., Hunter S., Nichols T., Roberts E., Fox M.T., Taylor M.A. 2008. Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Veterinary Parasitology, 154, 48–57. 10.1016/j.vetpar.2008.02.030Search in Google Scholar PubMed

Morgan E.R., Jefferies R., Krajewski M., Ward P., Shaw S.E. 2009. Canine pulmonary angiostrongylosis: the influence of climate on parasite distribution. Parasitology International, 58, 406410. 10.1016/j.parint.2009.08.003Search in Google Scholar PubMed

Morgan E.R., Shaw S.E., Brennan S.F., De Waal T.D., Jones B.R., Mulcahy G. 2005. Angiostrongylus vasorum: a real heart-breaker. Trends in Parasitology, 21, 49–51. 10.1016/j.pt.2004.11.006Search in Google Scholar PubMed

Penezić A. 2016. Diet of the Golden Jackal (Canis aureus L. 1758) in Serbia. PhD Thesis, University of Belgrade, Belgrade, Serbia.Search in Google Scholar

Penezić A., Selaković A., Pavlović I., Ćirkovic D. 2014. First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from Serbia. Parasitology Research, 9, 3281–3285. 10.1007/s00436-014-3991-9Search in Google Scholar PubMed

Polizopoulou Z.S., Koutinas A.F., Saridomichelakis M.N., Patsikas M.N., Leontidis L.S., Roubies N.A., Desiris A.K. 2000. Clinical and laboratory observations in 91 dogs infected with Dirofilaria immitis in northern Greece. Veterinary Record, 146, 466–46910.1136/vr.146.16.466Search in Google Scholar PubMed

Savić I.R., Paunović M., Milenković M., Stamenković S. 1995. Diversity of mammal (Mammalia) fauna of Yugoslavia, with an overview of species of international significance. In: (Eds V. Stevanović and V. Vasić) Biodiversity of Yugoslavia, with an overview of species of international importance. Faculty of Biology and Ekolibri, Belgrade, 517–554Search in Google Scholar

Serres E. 1854. Entozoaires trouvés dans l’oreille droite, le ventricule correspondant et l’artěre pulmonaire d’un chien. Journal des Vétérinaires du Midi, 7, 70. (In French)Search in Google Scholar

Simin S., Kosić L.S., Kuruca L., Pavlović I., Savović M., Lalošević V. 2014. Moving the boundaries to the South-East: first record of autochthonous Angiostrongylus vasorum infection in a dog in Vojvodina province, northern Serbia. Parasites & Vectors 7, 396–402. 10.1186/1756-3305-7-396Search in Google Scholar

Sreter T., Szell Z., Marucci G., Pozio E., Varga I. 2003. Extraintestinal nematode infections of red foxes (Vulpes vulpes) in Hungary. Veterinary Parasitology, 115, 329–33410.1016/S0304-4017(03)00217-6Search in Google Scholar PubMed

Šálek M., Červinka J., Banea O.C., Krofel M., Ćirović D., Selanec I., et al. 2014. Population densities and habitat use of the golden jackal (Canis aureus) in farmlands across the Balkan Peninsula. European Journal of Wildlife Research, 60, 193–20010.1007/s10344-013-0765-0Search in Google Scholar

Takács A., Szabó L., Juhász L., Takács A.A., Lanszki J., Takács P.T., Heltai M. 2014. Data on the parasitological status of golden jackal (Canis aureus L., 1758) in Hungary. Acta Veterinaria Hungarica 62, 33–41. 10.1556/AVet.2013.058Search in Google Scholar PubMed

Traversa D., Di Cesare A., Conboy G. 2010. Canine and feline cardiopulmonary parasitic nematodes in Europe: emerging and underestimated. Parasites & Vectors, 3, 62. 10.1186/1756-3305-3-62Search in Google Scholar PubMed PubMed Central

Traversa D., Di Cesare A., Meloni S., di Regalbono A.F., Milillo P., Pampurini F., Venco L. 2013. Canine angiostrongylosis in Italy: occurrence of Angiostrongylus vasorum in dogs with compatible clinical pictures. Parasitology Research, 112, 2473–80. 10.1007/s00436-013-3412-5Search in Google Scholar PubMed PubMed Central

Received: 2017-7-3
Revised: 2017-7-31
Accepted: 2017-8-16
Published Online: 2017-10-15
Published in Print: 2017-12-20

© 2017 W. Stefański Institute of Parasitology, PAS