Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-11T09:36:51.412Z Has data issue: false hasContentIssue false
  • English
  • Français

The situation of echinococcosis in stray dogs in Turkey: the first finding of Echinococcus multilocularis and Echinococcus ortleppi

Published online by Cambridge University Press:  18 May 2021

Hamza Avcioglu Open the ORCID record for Hamza Avcioglu [Opens in a new window] ,
Esin Guven Open the ORCID record for Esin Guven [Opens in a new window] ,
Ibrahim Balkaya ,
Ridvan Kirman ,
Muzaffer Akyuz Open the ORCID record for Muzaffer Akyuz [Opens in a new window] ,
Mohammed Mebarek Bia ,
Hatice Gulbeyen  and
Sali Yaya
Hamza Avcioglu*
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey
Esin Guven
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey
Ibrahim Balkaya
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey
Ridvan Kirman
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey
Muzaffer Akyuz
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey
Mohammed Mebarek Bia
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey Department of Parasitology, Parasitology Research Center and Parasite Resource Bank, Chungbuk National University, School of Medicine, Cheongju28644, Korea
Hatice Gulbeyen
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey
Sali Yaya
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Atatürk University, Erzurum25240, Turkey
*
Author for correspondence: Hamza Avcioglu, E-mail: havcioglu@atauni.edu.tr
Get access Rights & Permissions [Opens in a new window]

Abstract

Echinococcosis, caused by larval stage of the genus Echinococcus, is one of the most important zoonotic diseases worldwide. The purpose of this study was to determine the presence and prevalence of Echinococcus species in stray dogs of Erzurum, a highly endemic region for cystic echinococcosis (CE) and alveolar echinococcosis (AE) in Turkey. The study samples consisted of 446 stray dog faecal specimens collected from an animal shelter in Erzurum, Turkey, between October 2015 and February 2016. The faecal samples were collected from individual dogs for the isolation of taeniid eggs using the sequential sieving and flotation method (SSFM). Molecular analyses and sequencing revealed the prevalence of Echinococcus spp. as 14.13% (63/446) in faecal samples. The stray dogs harboured five different Echinococcus spp.: E. granulosus s.s. (G1/G3) (n = 41), E. equinus (G4) (n = 3), E. ortleppi (G5) (n = 1), E. canadensis (G6/G7) (n = 3) and E. multilocularis (n = 16). E. granulosus s.s. was the most abundant species. Surprisingly, the occurrence of E. multilocularis in dogs was revealed for the first time in Turkey. E. ortleppi was also reported for the first time in Turkey. These findings highlight a significant public health risk for human AE and CE, presenting useful baseline data on Echinococcus spp. infection in dogs for designing control strategies.

Keywords

E. multilocularisE. ortleppiEchinococcosisstray dogsTurkey
Type
Research Article
Information
Parasitology , Volume 148 , Issue 9 , August 2021 , pp. 1092 - 1098
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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

Addy, F, Wassermann, M, Banda, F, Mbaya, H, Aschenborn, J, Aschenborn, O, Koskei, P, Umhang, G, De La Rue, M, Elmahdi, E, Mackenstedt, U, Kern, P and Romig, T (2017) Genetic polymorphism and population structure of Echinococcus ortleppi. Parasitology 144, 450–458.CrossRefGoogle ScholarPubMed
Ahmed, ME, Eltom, KH, Musa, NO, Ali, IA, Elamin, FM, Grobusch, MP and Aradaib, IM (2013) First report on circulation of Echinococcus ortleppi in the one humped camel (Camelus dromedaries) Sudan. BMC Veterinary Research 9, 127.CrossRefGoogle ScholarPubMed
Altintas, N (2008) Parasitic zoonotic diseases in Turkey. Veterinaria Italiana 44, 633–646.Google ScholarPubMed
Alvarez Rojas, CA, Romig, T and Lightowlers, MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. International Journal for Parasitology 44, 9–18.CrossRefGoogle ScholarPubMed
Amer, S, Helal, IB, Kamau, E, Feng, Y and Xiao, L (2015) Molecular characterization of Echinococcus granulosus sensu lato from farm animals in Egypt. PLoS One 10, e0118509.CrossRefGoogle ScholarPubMed
Antolová, D, Reiterová, K, Miterpaková, M, Dinkel, A and Dubinský, P (2009) The first finding of Echinococcus multilocularis in dogs in Slovakia: an emerging risk for spreading of infection. Zoonoses and Public Health 56, 53–58.CrossRefGoogle ScholarPubMed
Arslan, MO and Umur, S (1997) Erzurum mezbahalarında kesilen koyun ve sığırlarda hidatidozun yayılışı ve ekonomik önemi. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 3, 167–171.Google Scholar
Avcioglu, H, Guven, E, Balkaya, I, Kirman, R, Bia, MM and Gulbeyen, H (2016) First molecular characterization of Echinococcus multilocularis in Turkey. Vector-Borne and Zoonotic Diseases 16, 627–629.CrossRefGoogle ScholarPubMed
Avcioglu, H, Guven, E, Balkaya, I, Kirman, R, Bia, MM, Gulbeyen, H, Kurt, A, Yaya, S and Demirtas, S (2017a) First detection of Echinococcus multilocularis in rodent intermediate hosts in Turkey. Parasitology 144, 1821–1827.CrossRefGoogle Scholar
Avcioglu, H, Guven, E, Balkaya, I, Bia, MM, Kirman, R, Gulbeyen, H, Yaya, S and Akyuz, M (2017b) Slaughterhouse survey of cystic echinococcosis in Erzurum province, Turkey. XXVII World Congress of Echinococcosis, 4th–7th October, Algiers, Algeria.Google Scholar
Avcioglu, H, Guven, E, Balkaya, I and Kirman, R (2018) Echinococcus multilocularis in a Eurasian lynx (Lynx lynx) in Turkey. Parasitology 145, 1147–1150.CrossRefGoogle Scholar
Avcioglu, H, Guven, E, Balkaya, I, Kirman, R, Akyuz, M, Bia, MM, Gulbeyen, H and Yaya, S (2021) Echinococcus multilocularis in Red Foxes in Turkey: increasing risk in urban. Acta Tropica 216, 105826.CrossRefGoogle ScholarPubMed
Beiromvand, M, Akhlaghi, L, Fattahi Massom, SH, Mobedi, I, Meamar, AR, Oormazdi, H, Motevalian, A and Razmjou, E (2011) Detection of Echinococcus multilocularis in carnivores in Razavi Khorasan province, Iran using mitochondrial DNA. PLOS Neglected Tropical Diseases 5, e1379.CrossRefGoogle ScholarPubMed
Boufana, B, Stidworthy, MF, Bell, S, Chantrey, J, Masters, N, Unwin, S, Wood, R, Lawrence, RP, Potter, A, McGarry, J, Redrobe, S, Killick, R, Foster, AP, Mitchell, S, Greenwood, AG, Sako, Y, Nakao, M, Ito, A, Wyatt, K, Lord, B and Craig, PS (2012) Echinococcus and Taenia spp. from captive mammals in the United Kingdom. Veterinary Parasitology 190, 95–103.CrossRefGoogle ScholarPubMed
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.CrossRefGoogle ScholarPubMed
Bruzinskaite, R, Sarkunas, M, Torgerson, PR, Mathis, A and Deplazes, P (2009) Echinococcosis in pigs and intestinal infection with Echinococcus spp. in dogs in southwestern Lithuania. Veterinary Parasitology 160, 237–241.CrossRefGoogle ScholarPubMed
Craig, P, Mastin, A, van Kesteren, F and Boufana, B (2015) Echinococcus granulosus: epidemiology and state of the art of diagnostics in animals. Veterinary Parasitology 213, 132–148.CrossRefGoogle ScholarPubMed
Cucher, MA, Macchiaroli, N, Baldi, G, Camicia, F, Prada, L, Maldonado, L, Avila, HG, Fox, A, Gutiérrez, A, Negro, P, López, R, Jensen, O, Rosenzvit, M and Kamenetzky, L (2016) Cystic echinococcosis in South America: systematic review of species and genotypes of Echinococcus granulosus sensu lato in humans and natural domestic hosts. Tropical Medicine & International Health 21, 166–175.CrossRefGoogle ScholarPubMed
de la Rue, ML, Takano, K, Brochado, JF, Costa, CV, Soares, AG, Yamano, K, Yagi, K, Katoh, Y and Takahashi, K (2011) Infection of humans and animals with Echinococcus granulosus (G1 and G3 strains) and E. ortleppi in Southern Brazil. Veterinary Parasitology 177, 97–103.CrossRefGoogle Scholar
Deplazes, P and Eckert, J (1996) Diagnosis of the Echinococcus multilocularis infection in final hosts. Applied Parasitology 37, 245–252.Google ScholarPubMed
Deplazes, P, Hegglin, D, Gloor, S and Romig, T (2004) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 77–84.CrossRefGoogle ScholarPubMed
Deplazes, P, Rinaldi, L, Rojas, CA, Torgerson, P, Harandi, M, Romig, T, Antolova, D, Schurer, JM, Lahmar, S, Cringoli, G, Magambo, J, Thompson, RCA and Jenkins, EJ (2017) Global distribution of alveolar and cystic echinococcosis. Advances in Parasitology 95, 315–493.CrossRefGoogle ScholarPubMed
Dinkel, A, Njoroge, EM, Zimmermann, A, Walz, M, Zeyhle, E, Elmahdi, IE, Mackenstedt, U and Romig, T (2004) A PCR system for detection of species and genotypes of the Echinococcus granulosus–complex, with reference to the epidemiological situation in Eastern Africa. International Journal for Parasitology 34, 645–653.CrossRefGoogle ScholarPubMed
Dyachenko, V, Pantchev, N, Gawlowska, S, Vrhovec, MG and Bauer, C (2008) Echinococcus multilocularis infections in domestic dogs and cats from Germany and other European countries. Veterinary Parasitology 157, 244–253.CrossRefGoogle ScholarPubMed
Ebrahimipour, M, Sadjjadi, SM, Darani, HY and Najjari, M (2017) Molecular studies on cystic echinococcosis of camel (Camelus dromedarius) and report of Echinococcus ortleppi in Iran. Iranian Journal of Parasitology 12, 323–331.Google ScholarPubMed
Eckert, J, Gemmell, M, Meslin, F and Pawlowski, Z (2001) WHO–OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Paris: World Organisation for Animal Health.Google Scholar
Erdogan, E, Ozkan, B, Mutlu, F, Karaca, S and Sahin, I (2017) Molecular characterization of Echinococcus granulosus isolates obtained from different hosts. Mikrobiyoloji Bülteni 51, 79–86.CrossRefGoogle ScholarPubMed
Eryildiz, CA and Sakru, NB (2012) Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace region, Turkey. Balkan Medical Journal 29, 261–267.Google ScholarPubMed
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, 408–412.CrossRefGoogle ScholarPubMed
Gurler, AT, Gori, F, Bolukbas, CS, Umur, S, Açıcı, M and Deplazes, P (2018) Investigation of Echinococcus multilocularis in environmental definitive host feces in the Asian and the European parts of Turkey. Frontiers in Veterinary Science 5, 48.CrossRefGoogle ScholarPubMed
Gurler, AT, Bolukbas, CS, Acıcı, M and Umur, S (2019) Overview of Echinococcus multilocularis in Turkey and in the world. Turkish Society for Parasitology 43, 18–35.CrossRefGoogle Scholar
Hojgård, S, Sundstrom, K, Christensson, D, Hallgren, G, Hjertqvist, M, Wallensten, A, Vagsholm, I and Wahlstrom, H (2012) Willingness to pay for compulsory deworming of pets entering Sweden to prevent introduction of Echinoccoccus multilocularis. Preventive Veterinary Medicine 106, 9–23.CrossRefGoogle ScholarPubMed
Huttner, M, Siefert, L, Mackenstedt, U and Romig, T (2009) A survey of Echinococcus species in wild carnivores and livestock in East Africa. International Journal for Parasitology 39, 1269–1276.CrossRefGoogle ScholarPubMed
Kamenetzky, L, Gutierrez, AM, Canova, SG, Haag, KL, Guarnera, EA, Parra, A, García, GE and Rosenzvit, MC (2002) Several strains of Echinococcus granulosus infect livestock and humans in Argentina. Infection, Genetics and Evolution 2, 129–136.CrossRefGoogle ScholarPubMed
Kamiya, M, Lagapa, JTG, Nonaka, N, Ganzorig, S, Oku, Y and Kamiya, H (2006) Current control strategies targeting sources of echinococcosis in Japan. Revue Scientifique Et Technique-Office International des Epizooties 25, 1055–1065.CrossRefGoogle ScholarPubMed
Kapel, CMO, Torgerson, PR, Thompson, RCA and Deplazes, P (2006) Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats. International Journal for Parasitology 36, 79–86.CrossRefGoogle ScholarPubMed
Karamon, J, Sroka, J, Dąbrowska, J, Bilska-Zając, E, Zdybel, J, Kochanowski, M, Różycki, M and Cencek, T (2019) First report of Echinococcus multilocularis in cats in Poland: a monitoring study in cats and dogs from a rural area and animal shelter in a highly endemic region. Parasite and Vectors 12, 313.CrossRefGoogle Scholar
Kesik, HK, Kilinc, SG, Simsek, S and Gul, A (2019) Occurrence of liver hydatid cysts in a donkey and molecular characterization of Echinococcus equinus. Journal of Parasitology 105, 442–445.CrossRefGoogle Scholar
Knapp, J, Bart, JM, Giraudoux, P, Glowatzki, ML, Breyer, I, Raoul, F, Deplazes, P, Duscher, G, Martinek, K, Dubinsky, P, Guislain, MH, Cliquet, F, Romig, T, Malczewski, A, Gottstein, B and Piarroux, R (2009) Genetic diversity of the cestode Echinococcus multilocularis in red foxes at a continental scale in Europe. PLoS Neglected Tropical Diseases 3, 452.CrossRefGoogle Scholar
Kurt, A, Avcioglu, H, Guven, E, Balkaya, I, Oral, A, Kirman, R, Bia, MM and Akyuz, M (2020) Molecular characterization of Echinococcus multilocularis and Echinococcus granulosus from cysts and formalin-fixed paraffin-embedded tissue samples of human isolates in Northeastern Turkey. Vector-Borne and Zoonotic Diseases 20, 593–602.CrossRefGoogle ScholarPubMed
Kuru, BB, Aypak, S and Aysul, N (2013) Prevalence of Echinococcus granulosus determined with polymerase chain reaction in dogs in Aydın district. Turkish Society for Parasitology 37, 78–83.Google ScholarPubMed
Latif, AA, Tanveer, A, Maqbool, A, Siddiqi, N, Kyaw-Tanner, M and Traub, RJ (2010) Morphological and molecular characterisation of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Veterinary Parasitology 170, 44–49.CrossRefGoogle ScholarPubMed
Macin, S, Orsten, S, Samadzade, R, Colak, B, Cebeci, H and Fındık, D (2021) Human and animal cystic echinococcosis in Konya, Turkey: molecular identification and the first report of E. equinus from human host in Turkey. Parasitology Research 19, 1–6.Google Scholar
Mathis, A, Deplazes, P and Eckert, J (1996) An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. Journal of Helminthology 70, 219–222.CrossRefGoogle ScholarPubMed
Mbaya, H, Magambo, J, Njenga, S, Zeyhle, E, Mbae, C, Mulinge, E, Wassermann, M, Kern, P and Romig, T (2014) Echinococcus spp. in Central Kenya: a different story. Parasitology Research 113, 3789–3794.CrossRefGoogle ScholarPubMed
Mehmood, S, Simsek, S, Celik, F, Kesik, H, Kilinc, S and Ahmed, H (2020) Molecular survey on cattle and sheep hydatidosis and first detection of Echinococcus canadensis (G6/G7) in sheep in Turkey. Parasitology 147, 1055–1062.CrossRefGoogle ScholarPubMed
Morishima, Y, Sugiyama, H, Arakawa, K and Kawanaka, M (2006) Echinococcus multilocularis in dogs, Japan. Emerging Infectious Diseases Journal 12, 1292–1294.CrossRefGoogle Scholar
Moro, P and Schantz, PM (2009) Echinococcosis: a review. International Journal of Infectious Diseases 13, 125–133.CrossRefGoogle ScholarPubMed
Mulinge, E, Magambo, J, Odongo, D, Njenga, S, Zeyhle, E, Mbae, C, Kagendo, D, Addy, F, Ebi, D, Wassermann, M, Kern, P and Romig, T (2018) Molecular characterization of Echinococcus species in dogs from four regions of Kenya. Veterinary Parasitology 255, 49–57.CrossRefGoogle ScholarPubMed
Oge, H, Oge, S, Gonenc, B, Sarimehmetoglu, O and Ozbakis, G (2017) Coprodiagnosis of Echinococcus granulosus infection in dogs from Ankara, Turkey. Veterinary Parasitology 242, 44–46.CrossRefGoogle ScholarPubMed
Oguz, B, Ozdal, N, Kilinc, OO and Deger, MS (2018) Preliminary studies on the prevalence and genotyping of Echinococcus granulosus infection in stray dogs in Van Province, Turkey. Journal of Veterinary Research 62, 497–502.CrossRefGoogle ScholarPubMed
Oksanen, A, Siles-Lucas, M, Karamon, J, Possenti, A, Conraths, FJ, Romig, T, Wysocki, P, Mannocci, 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.CrossRefGoogle ScholarPubMed
Oter, K, Bilgin, Z, Tınar, R and Tuzer, E (2011) Tapeworm infections in stray dogs and cats in İstanbul, Turkey. Kafkas Universitesi Veteriner Fakultesi Dergisi 17, 595–599.Google Scholar
Pednekar, RP, Gatne, ML, Thompson, RC and Traub, RJ (2009) Molecular and morphological characterization of Echinococcus from food producing animals in India. Veterinary Parasitology 165, 58–65.CrossRefGoogle Scholar
Romig, T, Dinkel, A and Mackenstedt, U (2006) The present situation of echinococcosis in Europe. Parasitology International 55, 187–191.CrossRefGoogle ScholarPubMed
Romig, T, Ebi, D and Wassermann, M (2015) Taxonomy and molecular epidemiology of Echinococcus granulosus sensu lato. Veterinary Parasitology 213, 76–84.CrossRefGoogle ScholarPubMed
Romig, T, Deplazes, P, Jenkins, D, Giraudoux, P, Massolo, A, Craig, PS, Wassermann, M, Takahashi, K and de la Rue, M (2017) Ecology and life cycle patterns of Echinococcus species. Advances in Parasitology 95, 213–314.CrossRefGoogle ScholarPubMed
Shi, Y, Wan, X, Wang, Z, Li, J, Jiang, Z and Yang, Y (2019) First description of Echinococcus ortleppi infection in China. Parasite and Vectors 12, 398.CrossRefGoogle ScholarPubMed
Simsek, S and Cevik, A (2014) First detection and molecular characterization of Echinococcus equinus in a mule in Turkey. Acta Parasitologica 59, 773–777.CrossRefGoogle Scholar
Simsek, S, Balkaya, I and Koroglu, E (2010) Epidemiological survey and molecular characterization of Echinococcus granulosus in cattle in an endemic area of eastern Turkey. Veterinary Parasitology 172, 347–349.CrossRefGoogle Scholar
Simsek, S, Kaplan, M and Ozercan, IH (2011) A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitology Research 109, 411–416.CrossRefGoogle ScholarPubMed
Simsek, S, Roinioti, E and Eroksuz, H (2015) First report of Echinococcus equinus in a donkey in Turkey. Korean Journal of Parasitology 53, 731–735.CrossRefGoogle Scholar
Snabel, V, Altintas, N, D'Amelio, S, Nakao, M, Romig, T, Yolasigmaz, A, Gunes, K, Turk, M, Busi, M, Hüttner, M, Sevcová, D, Ito, A, Altintas, N and Dubinský, P (2009) Cystic echinococcosis in Turkey: genetic variability and first record of the pig strain (G7) in the country. Parasitology Research 105, 145–154.CrossRefGoogle ScholarPubMed
Soriano, SV, Pierangeli, NB, Pianciola, L, Mazzeo, M, Lazzarini, LE, Saiz, MS, Kossman, AV, Bergagna, HF, Chartier, K and Basualdo, JA (2010) Molecular characterization of Echinococcus isolates indicates goats as reservoir for Echinococcus canadensis G6 genotype in Neuquen, Patagonia Argentina. Parasitology International 59, 626–628.CrossRefGoogle ScholarPubMed
Thompson, RC (2017) Biology and systematics of Echinococcus. Advances in Parasitology 95, 65–109.CrossRefGoogle ScholarPubMed
Thompson, RA and McManus, DP (2002) Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452–457.CrossRefGoogle ScholarPubMed
Tigre, W, Deresa, B, Haile, A, Gabriel, S, Victor, B, Pelt, JV, Devleesschauwer, B, Vercruysse, J and Dorny, P (2016) Molecular characterization of Echinococcus granulosus s.l. cysts from cattle, camels, goats and pigs in Ethiopia. Veterinary Parasitology 215, 17–21.CrossRefGoogle ScholarPubMed
Torgerson, PR, Rosenheim, K, Tanner, I, Ziadinov, I, Grimm, F, Brunner, M, Shaiken, S, Shaikenov, B, Rysmukhambetova, A and Deplazes, P (2009) Echinococcosis, toxocarosis and toxoplasmosis screening in a rural community in eastern Kazakhstan. Tropical Medicine & International Health 14, 341–348.CrossRefGoogle Scholar
Torgerson, PR, Keller, K, Magnotta, M and Ragland, N (2010) The global burden of alveolar echinococcosis. PLOS Neglected Tropical Diseases 4, 722.CrossRefGoogle ScholarPubMed
Trachsel, D, Deplazes, P and Mathis, A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911–920.CrossRefGoogle ScholarPubMed
Umhang, G, Comte, S, Raton, V, Hormaz, V, Boucher, JM, Favier, S, Combes, B and Boué, F (2014) Echinococcus multilocularis infections in dogs from urban and peri-urban areas in France. Parasitology Research 113, 2219–2222.CrossRefGoogle Scholar
Umur, S and Arslan, MO (1998) The prevalence of helminths in stray dogs in Kars district. Acta Parasitologica Turcica 22, 188–193.Google Scholar
Utuk, AE, Simsek, S, Koroglu, E and McManus, DP (2008) Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta Tropica 107, 192–194.CrossRefGoogle Scholar
Vaniscotte, A, Raoul, F, Poulle, ML, Romig, T, Dinkel, A, Takahashi, K, Guislain, MH, Moss, J, Tiaoying, L, Wang, Q, Qiu, J, Craig, PS and Giraudoux, P (2011) Role of dog behaviour and environmental fecal contamination in transmission of Echinococcus multilocularis in Tibetan communities. Parasitology 138, 1316–1329.CrossRefGoogle ScholarPubMed
Vuitton, DA, 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, 87–107.CrossRefGoogle ScholarPubMed
Vuitton, DA, McManus, DP, Rogan, MT, Romig, T, Gottstein, B, Naidich, A, Tuxun, T, Wen, H and Menezes da Silva, A and the World Association of Echinococcosis (2020) International consensus on terminology to be used in the field of echinococcoses. Parasite 27, 41.CrossRefGoogle ScholarPubMed
Vural, G, Baca, AU, Gauci, CG, Bagci, O, Gicik, Y and Lightowlers, MW (2008) Variability in the Echinococcus granulosus cytochrome C oxidase 1 mitochondrial gene sequence from livestock in Turkey and a re-appraisal of the G1–G3 genotype cluster. Veterinary Parasitology 154, 347–350.CrossRefGoogle Scholar
Yamamoto, N, Morishima, Y, Kon, M, Yamaguchi, M, Tanno, S, Koyama, M, Maeno, N, Azuma, H, Mizusawa, H, Kimura, H, Sugiyama, H, Arakawa, K and Kawanaka, M (2006) The first reported case of a dog infected with Echinococcus multilocularis in Saitama prefecture. Japanese Journal of Infectious Diseases 59, 351–352.Google ScholarPubMed
Yang, YR, McManus, DP, Huang, Y and Heath, DD (2009) Echinococcus granulosus infection and options for control of cystic echinococcosis in Tibetan communities of Western Sichuan Province, China. PLOS Neglected Tropical Diseases 3, 426.CrossRefGoogle ScholarPubMed
Zhang, Y, Bart, JM, Giraudoux, P, Craig, P, Vuitton, D and Wen, H (2006) Morphological and molecular characteristics of Echinococcus multilocularis and Echinococcus granulosus mixed infection in a dog from Xinjiang, China. Veterinary Parasitology 139, 244–248.CrossRefGoogle Scholar
Ziadinov, I, Mathis, A, Trachsel, D, Rysmukhambetova, A, Abdyjaparov, TA, Kuttubaev, OT, Deplazes, P and Torgerson, PR (2008) Canine echinococcosis in Kyrgyzstan: using prevalence data adjusted for measurement error to develop transmission dynamics models. International Journal for Parasitology 38, 1179–1190.CrossRefGoogle ScholarPubMed