First identification of Echinococcus multilocularis in golden jackals in Croatia
-
Magda Sindičić
,
Iva Štimac
Abstract
Alveolar echinococcosis, caused by the tapeworm Echinococcus multilocularis, is one of the world’s most dangerous zoonosis and an emerging disease with growing incidence in humans. The disease has been reported in new areas and host species in the last two decades, and the primary hosts of the parasite – red fox, golden jackal and grey wolf – are expanding their distribution in Europe. Here we report the morphological and molecular identification of Echinococcus multilocularis tapeworms in one of 29 carcasses of adult golden jackals in Croatia, where the only previous report of the parasite was in red foxes in 2016. These results suggest that alveolar echinococcosis should be treated as an emerging disease in Croatia.
Acknowledgements
This work was funded by the Croatian Science Foundation, project ‘Molecular epidemiology of selected parasitic diseases of wildlife’, code 3421.
References
Beck R., Mihaljević Ž., Brezak R., Bosnić S., Lohman Janković I., Deplazes P. 2018. First detection of Echinococcus multilocularis in Croatia. Parasitology Research, 117, 617–621. 10.1007/s00436-017-5732-3Search in Google Scholar PubMed
Boubaker G., Marinova I., Gori F., Hizem A., Müller N., Casulli A. et al. 2016. A dual PCR-based sequencing approach for the identification and discrimination of Echinococcus and Taenia taxa. Molecular and Cellular Probes, 30, 211–21710.1016/j.mcp.2016.05.004Search in Google Scholar PubMed
Conraths F.J., Deplazes P. 2015. Echinococcus multilocularis: Epidemiology, surveillance and state-of-the-art diagnostics from a veterinary public health perspective. Veterinary Parasitology, 213, 149–16110.1016/j.vetpar.2015.07.027Search in Google Scholar PubMed
Carmena D., Cardona G.A. 2014. Echinococcosis in wild carnivorous species: Epidemiology, genotypic diversity, and implications for veterinary public health. Veterinary Parasitology, 202, 69–94. 10.1016/j.vetpar.2014.03.009Search in Google Scholar PubMed
Ćirović D., Pavlović I., Kulišić Z., Ivetić V., Penezić A., Ćosić N. 2012. Echinococcus multilocularis in the European beaver (Castor fiber L.) from Serbia: first report. Veterinary Record, 171, 100. 10.1136/vr.l00879Search in Google Scholar
Deplazes P., Hegglin D., Gloor S., Romig T. 2004. Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology, 20, 210.1016/j.pt.2003.11.011Search in Google Scholar PubMed
Fabbri E., Caniglia R., Galov A., Arbanasić H., Lapini L., Bošković I. et al. 2014. Genetic structure and expansion of golden jackals (Canis aureus) in the north-western distributionrange (Croatia and eastern Italian Alps). Conservation Genetics, 15, 187–199. /10.1007/s10592-013-0530-7Search in Google Scholar
Guerra D., Hegglin D., Bacciarini L., Schnyder M., Deplazes P. 2014. Stability of the southern European border of Echinococcus multilocularis in the Alps: evidence that Microtus arvalis is a limiting factor. Parasitology, 0, 1–10. 10.1017/S0031182014000730Search in Google Scholar PubMed
Hall T. 2004. BioEdit. Ibis Therapeutics, Carlsbad, CA, 92008, USA. (http://www.mbio.ncsu.edu/BioEdit/bioedit.html)Search in Google Scholar
Jones A., Pybus M.J. 2010. Taeniasis and echinococcosis. In: (Eds W.M. Samuel, M.J. Pybus and A.A. Kocan) Parasitic Diseases of Wild Mammals, Manson Publishing Ltd., London, pp.150–19210.1002/9780470377000.ch7Search in Google Scholar
Kaczensky P., Chapron G., von Arx M., Huber D., Andrén H., Linnell J.D.C. 2013. Status, Management and Distribution of Large Canivores – Bear, Lynx, Wolf & Wolverine – in Europe. European CommissionSearch in Google Scholar
Konig A., Romig T. 2010. Fox tapeworm Echinococcus multilocularis, an underestimated threat: a model for estimating risk of contact. Wildlife Biology, 16, 258–26610.2981/09-059Search in Google Scholar
Lalošević D., Lalošević V., Simin V., Miljević M., Čabrilo B., Bjelić Čabrilo O. 2016. Spreading of multilocular echinococcosis in southern Europe: the first record in foxes and jackals in Serbia, Vojvodina Province. European Journal of Wildlife Research. 10.1007/s10344-016-1050-9Search in Google Scholar
Mörner T., Obendorf D.L., Artois M., Woodford M.H. 2002. Surveillance and monitoring of wildlife diseases. Revue Scientifique Et Technique, 21, 67–7610.20506/rst.21.1.1321Search in Google Scholar
Nakao M., Yokoyama N., Sako Y., Fukunaga M., Ito A. 2002. The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion, 1, 497–50910.1016/S1567-7249(02)00040-5Search in Google Scholar
Oksanen A., Mar Siles-Lucas, Karamon J., Possenti A., Conraths F.J., Romig T. et al. 2016. The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: a systematic review and meta-analysis. Parasites & Vectors, 9, 51910.1186/s13071-016-1746-4Search in Google Scholar PubMed PubMed Central
Schweiger A., Ammann R.W., Candinas D., Clavien P.A., Eckert J., Gottstein B. et al. 2007. Human alveolar echinococcosis after fox population increase, Switzerland. Emerging Infectious Diseases, 13, 878–88210.3201/eid1306.061074Search in Google Scholar PubMed PubMed Central
Széll Z., Marucci G., Pozio E., Sréter T. 2013. Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Veterinary Parasitology, 197, 393–396.10.1016/j.vetpar.2013.04.032Search in Google Scholar PubMed
Torgerson P.R., Keller K., Magnotta M., Ragland N. 2010. The global burden of alveolar echinococcosis. PLoS Neglected Tropical Diseases, 4, 72210.1371/journal.pntd.0000722Search in Google Scholar PubMed PubMed Central
Trouwborst A., Krofel M., Linnell J.D.C. 2015. Legal implications of range expansions in a terrestrial carnivore: the case of the golden jackal (Canis aureus) in Europe. Biodiversity and Conservation, 24, 2593–2610. 10.1007/s10531-015-0948-ySearch in Google Scholar
© 2018 W. Stefański Institute of Parasitology, PAS
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