Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-23T10:23:29.669Z Has data issue: false hasContentIssue false

First detection of Echinococcus multilocularis in rodent intermediate hosts in Turkey

Published online by Cambridge University Press:  11 August 2017

HAMZA AVCIOGLU*
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
ESIN GUVEN
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
IBRAHIM BALKAYA
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
RIDVAN KIRMAN
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
MOHAMMED MEBAREK BIA
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
HATICE GULBEYEN
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
ALI KURT
Affiliation:
Department of Pathology, Erzurum Regional Education and Research Hospital, Erzurum 25240, Turkey
SALI YAYA
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey
SADIK DEMIRTAS
Affiliation:
Department of Biology, Faculty of Arts and Science, Ondokuz Mayıs University, 55139 Samsun, Turkey
*
*Corresponding author: Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum 25240, Turkey. E-mail: hamzaavcioglu@yahoo.com

Summary

Echinococcus multilocularis is the causative agent of alveolar echinococcosis (AE), a potentially fatal zoonotic disease. Large parts of Turkey are considered as endemic for E. multilocularis. The aim of this study was to determine the occurrence of metacestode of E. multilocularis in wild rodents in Erzurum, an endemic region for human AE in Turkey. During the sampling period, a total of 498 rodents were trapped in twenty counties of Erzurum Province. Suspected lesions were observed on the livers of 48 rodents, and then partial fragment of mitochondrial 12S rRNA gene was PCR-amplified. Five liver samples exhibited E. multilocularis infection. The prevalence of E. multilocularis for Microtus spp. was 1·3%. All of the infected rodents had fertile metacestodes. Infected rodents were morphologically and molecularly analysed and were confirmed to be Microtus irani by the mitochondrial cytochrome b gene sequence analysis. This is the first report of the presence of E. multilocularis in rodent intermediate hosts in Turkey. Our findings of infected M. irani with protoscoleces show that this rodent can act as suitable intermediate host for E. multilocularis’ life cycle in Turkey. However, there was a complete lack of data on the infection of carnivores from the country. An extensive survey is recommended to determine the prevalence of E. multilocularis in definitive hosts in this endemic region.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Avcioglu, H., Guven, E., Balkaya, I., Kirman, R., Bia, M. M. and Gulbeyen, H. (2016). First molecular characterization of Echinococcus multilocularis in Turkey. Vector Borne and Zoonotic Diseases 16, 627629.Google Scholar
Barabasi, S. S., Marosfi, L., Barabasi, Z. S. and Cozma, V. (2011). Natural alveolar echinococcosis with Echinococcus multilocularis in wild rodents. Scientia Parasitologica 12, 1121.Google Scholar
Burlet, P., Deplazes, P. and Hegglin, D. (2011). Age, season and spatio-temporal factors affecting the prevalence of Echinococcus multilocularis and Taenia taeniaeformis in Arvicola terrestris . Parasite and Vectors 4, 6.CrossRefGoogle ScholarPubMed
Corbet, G. B. (1978). The Mammals of the Palaearctic Region: a Taxonomic Review. British Museum (Natural History), British Museum (Natural History) and Cornell University Press, London, UK.Google Scholar
Davidson, R. K., Romig, T., Jenkins, E., Tryland, M. and Robertson, L. J. (2012). The impact of globalisation on the distribution of Echinococcus multilocularis . Trends in Parasitology 28, 239247.Google Scholar
Deplazes, P., Dinkel, A. and Mathis, A. (2003). Molecular tools for studies on the transmission biology of Echinococcus multilocularis . Parasitology 127, 5361.Google Scholar
Deplazes, P., Hegglin, D., Gloor, S. and Romig, T. (2004). Wilderness in the city: the urbanization of Echinococcus multilocularis . Trends in Parasitology 20, 7784.Google Scholar
Deplazes, P., Rinaldi, L., Alvarez Rojas, C. A., Torgerson, P. R., Harandi, M. F., Romig, T., Antolova, D., Schurer, J. M., Lahmar, S., Cringoli, G., Magambo, J., Thompson, R. C. and Jenkins, E. J. (2017). Global distribution of alveolar and cystic echinococcosis. Advances in Parasitology 95, 315493.CrossRefGoogle ScholarPubMed
Dyachenko, V., Beck, E., Pantchev, N. and Bauer, C. (2008). Cost-effective method of DNA extraction from taeniid eggs. Parasitology Research 102, 811813.CrossRefGoogle ScholarPubMed
Eckert, J. (1998). Alveolar echinococcosis (Echinococcus multilocularis) and other forms of echinococcosis (Echinococcus oligarthrus and Echinococcus vogeli). In Zoonoses (ed. Palmer, S. R., Lord Soulsby, and Simpson, D. I. H.), pp. 689716. Oxford University Press, Oxford, UK.Google Scholar
Eckert, J. and Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107135.Google Scholar
Eckert, J., Schantz, P. M., Gasser, R. B., Torgerson, P. R., Bessonov, A. S., Movsessian, S. O., Thakur, A., Grimm, F. and Nikogossian, M. A. (2001). Geographic distribution and prevalence. In Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern (ed. Eckert, J., Gemmell, M. A., Meslin, F.- X. and Pawlowski, Z. S.), pp. 101143. WHO/OIE, Paris, France.Google Scholar
Giraudoux, P., Raoul, F., Afonso, E., Ziadinov, I., Yang, Y., Li, L., Li, T., Quéré, J. P., Feng, X., Wang, Q., Wen, H., Ito, A. and Craig, P. S. (2013). Transmission ecosystems of Echinococcus multilocularis in China and Central Asia. Parasitology 140, 16551666.Google Scholar
Gottstein, B., Saucy, F., Deplazes, P., Reichen, J., Demierre, G., Busato, A., Zuercher, C. and Pugin, P. (2001). Is high prevalence of Echinococcus multilocularis in wild and domestic animals associated with disease incidence in humans? Emerging Infectious Diseases 7, 408412.Google Scholar
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 42, 9598.Google Scholar
Hnatiuk, J. M. (1966). First occurrence of Echinococcus multilocularis Leuckart, 1863 in Microtus pennsylvanicus in Saskatchewan. Canadian Journal of Zoology 44, 493493.CrossRefGoogle Scholar
Hofer, S., Gloor, S., Müller, U., Mathis, A., Hegglin, D. and Deplazes, P. (2000). High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120, 135142.CrossRefGoogle ScholarPubMed
Holmes, J. C., Mahrt, J. L. and Samuel, W. M. (1971). The occurrence of Echinococcus multilocularis Leuckart, 1863 in Alberta. Canadian Journal of Zoology 49, 575576.Google Scholar
Ito, A., Romig, T. and Takahashi, K. (2003). Perspective on control options for Echinococcus multilocularis with particular reference to Japan. Parasitology 127, 159172.CrossRefGoogle ScholarPubMed
Jaarola, M. and Searle, J. B. (2002). Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Molecular Ecology 11, 26132621.Google Scholar
Kritsky, D. C., Leiby, P. D. and Miller, G. E. (1977). The natural occurrence of Echinococcus multilocularis in the bushy-tailed woodrat, Neotoma cinerea rupicola, in Wyoming. The American Journal of Tropical Medicine and Hygiene 26, 10461047.Google Scholar
Leiby, P. D., Carney, W. P. and Woods, C. E. (1970). Studies on sylvatic echinococcosis. 3. Host occurrence and geographic distribution of Echinococcus multilocularis in the north central United States. Journal of Parasitology 56, 11411150.CrossRefGoogle ScholarPubMed
Liccioli, S., Duignan, P. J., Lejeune, M., Deunk, J., Majid, S. and Massolo, A. (2013). A new intermediate host for Echinococcus multilocularis: the southern red-backed vole (Myodes gapperi) in urban landscape in Calgary, Canada. Parasitology International 62, 355357.CrossRefGoogle ScholarPubMed
Merdivenci, A. (1963). Türkiye'de tilki (Vulpes vulpes) lerde ilk helmintolojik araştırma ve ilk Echinococcus multilocularis (Leuckart, 1884) Vogel, 1935, olayı. Veteriner Hekimler Derneği Dergisi 3, 290.Google Scholar
Meyer, A., Kocher, T. D., Basasibwaski, P. and Wilson, A. C. (1990). Monophyletic origin of Lake Victoria cichlid fishes suggested by mithochondrial DNA sequences. Nature 347, 550553.Google Scholar
Miller, A. L., Olsson, G. E., Walburg, M. R., Sollenberg, S., Skarin, M., Ley, C., Wahlstrom, H. and Hoglund, J. (2016). First identification of Echinococcus multilocularis in rodent intermediate hosts in Sweden. International Journal for Parasitology: Parasites and Wildlife 5, 5663.Google Scholar
Nowak, R. M. (1999). Walker's Mammals of the World, Vol. 2, 6th Edn. Johns Hopkins University Press, Baltimore, USA.Google Scholar
Oksanen, A., Siles-Lucas, M., Karamon, J., Possenti, A., Conraths, F. J., Romig, T., Wysocki, P., Mannoci, A., Mipatrini, D., La Torre, G., Boufana, B. and Casulli, A. (2016). The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: a systematic review and meta-analysis. Parasite and Vectors 9, 519.Google Scholar
Presnell, J. K. and Schreibman, M. P. (1997). Humason's Animal Tissue Techniques, 5th Edn. The Johns Hopkins University Press. Ltd., London, UK.Google Scholar
Reperant, L. A., Hegglin, D., Tanner, I., Fischer, C. and Deplazes, P. (2009). Rodents as shared indicators for zoonotic parasites of carnivores in urban environments. Parasitology 136, 329337.Google Scholar
Romig, T., Deplazes, P., Jenkins, D., Giraudoux, P., Massolo, A., Craig, P. S., Wassermann, M., Takahashi, K. and de la Rue, M. (2017). Ecology and life cycle patterns of Echinococcus species. Advances in Parasitology 95, 213314.Google Scholar
Stieger, C., Hegglin, D., Schwarzenbach, G., Mathis, A. and Deplazes, P. (2002). Spatial and temporal aspects of urban transmission of Echinococcus multilocularis . Parasitology 124, 631640.Google Scholar
Torgerson, P. R. and Deplazes, P. (2009). Echinococcosis: diagnosis and diagnostic interpretation in population studies. Trends in Parasitology 25, 164170.Google Scholar
Torgerson, P. R., Keller, K., Magnotta, M. and Ragland, N. (2010). The global burden of alveolar echinococcosis. PLoS Neglected Tropical Diseases 4, e722.CrossRefGoogle ScholarPubMed
Vuitton, D., Zhou, H., Bresson-Hadni, S., Wang, Q., Piarroux, M., Raoul, F. and Giraudoux, P. (2003). Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127, 87107.Google Scholar
Zagorodnyuk, I. V. (1990). Karyotype variation and systematics of the grey voles (Rodentia, Arvicolini). 1. Species composition and chromosome numbers. Vestnik Zoologii 2, 2637.Google Scholar