Skip to main content Accessibility help

Genetic diversity of Echinococcus spp. in Russia



In Russia, both alveolar and cystic echinococcoses are endemic. This study aimed to identify the aetiological agents of the diseases and to investigate the distribution of each Echinococcus species in Russia. A total of 75 Echinococcus specimens were collected from 14 host species from 2010 to 2012. Based on the mitochondrial DNA sequences, they were identified as Echinococcus granulosus sensu stricto (s.s.), E. canadensis and E. multilocularis. E. granulosus s.s. was confirmed in the European Russia and the Altai region. Three genotypes, G6, G8 and G10 of E. canadensis were detected in Yakutia. G6 was also found in the Altai region. Four genotypes of E. multilocularis were confirmed; the Asian genotype in the western Siberia and the European Russia, the Mongolian genotype in an island of Baikal Lake and the Altai Republic, the European genotype from a captive monkey in Moscow Zoo and the North American genotype in Yakutia. The present distributional record will become a basis of public health to control echinococcoses in Russia. The rich genetic diversity demonstrates the importance of Russia in investigating the evolutionary history of the genus Echinococcus.


Corresponding author

*Corresponding author. Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, 078-8510, Japan. Tel.: +81 166 68 2421. Fax: +81 166 68 2429. E-mail:


Hide All
Abuladze, K. I. (1964). Taeniata of Animals and Man and Diseases Caused by Them. Essentials of Cestodology, Vol. 4 (ed. Skrjabin, K. I.), pp. 549. Akademiya Nauk SSSR, Moscow, 1964 (in Russian); English transl.: Israel Program for Scientific Translations, Jerusalem 1970.
Alperovich, B. I. (1972) Alvoecoccosis and its Treatment. Medicina, Moscow, Russia (in Russian).
Bacciarini, L. N., Gottstein, B., Pagan, O., Rehmann, P. and Gröne, A. (2004). Hepatic alveolar echinococcosis in cynomolgus monkeys (Macaca fascicularis). Veterinary Pathology 41, 229234.
Bagrade, G., Šnábel, V., Romig, T., Ozoliņš, J., Hüttner, M., Miterpáková, M., Ševcová, D. and Dubinský, P. (2009). Echinococcus multilocularis is a frequent parasite of red foxes (Vulpes vulpes) in Latvia. Helminthologia 45, 157161.
Bessonov, A. S. (2002). Echinococcoses of animals and humans in the Russian Federation. In Cestode Zoonose: Echinococcosis and Cysticercosis (ed. Craig, P. and Pawlowski, Z.), pp. 9198. IOS Press, Amsterdam.
Bessonov, A. S. (2003). Alveolar Echinococcosis and Hydatidosis. Rosselkhozacademia Press, Moscow, Russia (in Russian).
Boĭtsov, V. D., Telushkin, A. V., Tumol'skaia, N. I. and Iarotskiĭ, L. S. (1992). The characteristics of the clinical course of hydatid pulmonary echinococcosis in the native inhabitants of Chukotka. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 61, 1214 (in Russian).
Boufana, B., Stidworthy, M. F., Bell, S., Chantrey, J., Masters, N., Unwin, S., Wood, R., Lawrence, R. P., Potter, A., McGarry, J., Redrobe, S., Killick, R., Foster, A. P., Mitchell, S., Greenwood, A. G., Sako, Y., Nakao, M., Ito, A., Wyatt, K., Lord, B. and Craig, P. S. (2012). Echinococcus and Taenia spp. from captive mammals in the United Kingdom. Veterinary Parasitology 190, 95103.
Bowles, J., Blair, D. and McManus, D. P. (1994). Molecular genetic characterization of the cervid strain (‘northern form’) of Echinococcus granulosus. Parasitology 109, 215221.
Brack, M., Tackmann, K., Conraths, F. J. and Rensing, S. (1997). Alveolar hydatidosis (Echinococcus multilocularis) in a captive rhesus monkey (Macaca mulatta) in Germany. Tropical Medicine and International Health 2, 754759.
Bryan, H. M., Darimont, C. T., Hill, J. E., Paquet, P. C., Thompson, R. C. A., Wagner, B. and Smits, J. E. G. (2012). Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago. Parasitology 139, 781790.
Cardona, G. A. and Carmena, D. (2013). A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Veterinary Parasitology 192, 1032.
Casulli, A., Interisano, M., Sreter, T., Chitimia, L., Kirkova, Z., La Rosa, G. and Pozio, E. (2012). Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infection, Genetics and Evolution 12, 377383.
Clement, M., Posada, D. and Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571659.
Eckert, J., Gemmell, M. A., Meslin, F.-X. and Pawlowski, Z. S. (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. World Organization for Animal Health, Paris, France.
Foreyt, W. J., Drew, M. L., Atkinson, M. and McCauley, D. (2009). Echinococcus granulosus in gray wolves and ungulates in Idaho and Montana, USA. Journal of Wildlife Diseases 45, 12081212.
Gaenko, G. P. (1958). Spreading of echinococcosis in the Altai Territory. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 27, 148150. (in Russian).
Gubanov, N. M. (1964). Helminth Fauna of Economically Important Mammals in Yakutia. Nauka, Moscow, Russia (in Russian).
Gubanov, N. M. and Fedorov, K. P. (1970). Helminth fauna of rodents in Yakutia. In Fauna of Siberia, (ed. Cherepanov, A. I.), pp. 1847. Nauka, Novosibirsk, Russia (in Russian).
Hailemariam, Z., Nakao, M., Menkir, S., Lavikainen, A., Yanagida, T., Okamoto, M. and Ito, A. (2012). Molecular identification of unilocular hydatid cysts from domestic ungulates in Ethiopia: implications for human infections. Parasitology International 61, 375377.
Himsworth, C. G., Jenkins, E., Hill, J. E., Nsungu, M., Ndao, M., Thompson, R. C. A., Covacin, C., Ash, A., Wagner, B. A., McConnell, A., Leighton, F. A. and Skinner, S. (2010). Emergence of sylvatic Echinococcus granulosus as a parasitic zoonosis of public health concern in an indigenous community in Canada. American Journal of Tropical Medicine and Hygiene 82, 643645.
Hüttner, M., Nakao, M., Wassermann, T., Siefert, L., Boomker, J., Dinkel, A., Sako, Y., Mackenstedt, U., Romig, T. and Ito, A. (2008). Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. International Journal for Parasitology 38, 861868.
Ito, A., Agvaandaram, G., Bat-Ochir, O. E., Chuluunbaatar, B., Gonchigsenghe, N., Yanagida, T., Sako, Y., Myadagsuren, N., Dorjsuren, T., Nakaya, K., Nakao, M., Ishikawa, Y., Davaajav, A. and Dulmaa, N. (2010). Histopathological, serological, and molecular confirmation of indigenous alveolar echinococcosis cases in Mongolia. American Journal of Tropical Medicine and Hygiene 82, 266269.
Ito, A., Chuluunbaatar, G., Yanagida, T., Davaasuren, A., Sumiya, B., Asakawa, M., Ki, T., Nakaya, K., Davaajav, A., Dorjsuren, T., Nakao, M. and Sako, Y. (2013). Echinococcus species from red foxes, corsac foxes and wolves in Mongolia. Parasitology 140, in press.
Jabbar, A., Narankhajid, M., Nolan, M. J., Jex, A. R., Campbell, B. E. and Gasser, R. B. (2011). A first insight into the genotypes of Echinococcus granulosus from humans in Mongolia. Molecular and Cellular Probes 25, 4954.
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.
Knapp, J., Nakao, M., Yanagida, T., Okamoto, M., Saarma, U., Lavikainen, A. and Ito, A. (2011). Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes. Molecular Phylogenetics and Evolution 61, 628638.
Kondo, H., Wada, Y., Bando, G., Kosuge, M., Yagi, K. and Oku, Y. (1996). Alveolar hydatidosis in a gorilla and ring-tailed lemur in Japan. Journal of Veterinary Medical Science 58, 447449.
Konyaev, S. V., Yanagida, T., Ingovatova, G. M., Shoikhet, Y. N., Nakao, M., Sako, Y., Bondarev, A. Y. and Ito, A. (2012 a). Molecular identification of human echinococcosis in the Altai region of Russia. Parasitology International 61, 711714.
Konyaev, S. V., Yanagida, T., Ivanov, M. V., Ruppel, V. V., Sako, Y., Nakao, M. and Ito, A. (2012 b). The first report on cystic echinococcosis in a cat caused by Echinococcus granulosus sensu stricto (G1). Journal of Helminthology 86, 391394.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 29472948.
Lavikainen, A., Lehtinen, M., Meri, T., Hirvelä-Koski, V. and Meri, S. (2003). Molecular genetic characterization of the Fennoscandian cervid strain, a new genotypic group (G10) of Echinococcus granulosus. Parasitology 127, 207215.
Lukashenko, N. M. (1975). Alveolar Echinococcosis. Medicina, Moscow (in Russian).
Lukmanova, G. I., Tuigunov, M. M., Nartailakov, M. A., Bilalov, F. S. and Gumerov, A. A. (2008). Genotyping of Echinococcus spp. isolates in the South Urals. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 1, 2627. (in Russian).
Lymbery, A. J. (1995). Genetic diversity, genetic differentiation and speciation in the genus Echinococcus Rudolphi 1801. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 5188. CAB International, Wallingford, UK.
Martynenko, V. B. (1984). Ecological and epidemiological characteristic of alveococcosis foci in Yakutsukaya ASSR. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 53, 7378. (in Russian).
Martynenko, V. B., Zorihina, V. I., Shcherbakov, A. M., Starkov, T. V. and Suvorin, V. I. (1984). Seroepidemiological study of foci of echinococcosis in northern Yakutia. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 53, 5456. (in Russian).
Moks, E., Jogisalu, I., Valdmann, H. and Saarma, U. (2008). First report of Echinococcus granulosus G8 in Eurasia and a reappraisal of the phylogenetic relationships of “genotypes” G5-G10. Parasitology 135, 647654.
Moks, E., Saarma, U. and Valdmann, H. (2005). Echinococcus multilocularis in Estonia. Emerging Infectious Diseases 11, 19731974.
Nakao, M., Lavikainen, A., Iwaki, T., Haukisalmi, V., Konyaev, S., Oku, Y., Okamoto, M. and Ito, A. (2013 a). Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria. International Journal for Parasitology 43, 427437.
Nakao, M., Li, T., Han, X., Ma, X., Xiao, N., Qiu, J., Wang, H., Yanagida, T., Mamuti, W., Wen, H., Moro, P. L., Giraudoux, P., Craig, P. S. and Ito, A. (2010 a). Genetic polymorphisms of Echinococcus tapeworms in China as determined by mitochondrial and nuclear DNA sequences. International Journal for Parasitology 40, 379385.
Nakao, M., Xiao, N., Okamoto, M., Yanagida, T., Sako, Y. and Ito, A. (2009). Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitology International 58, 384389.
Nakao, M., Yanagida, T., Konyaev, S., Lavikainen, A., Odnokurtsev, V. A., Zaikov, V. A. and Ito, A. (2013 b). Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology 140, in press.
Nakao, M., Yanagida, T., Okamoto, M., Knapp, J., Nkouawa, A., Sako, Y. and Ito, A. (2010 b). State-of-the-art Echinococcus and Taenia: phylogenetic taxonomy of human-pathogenic tapeworms and its application to molecular diagnosis. Infection, Genetics and Evolution 10, 444452.
Nikulina, N. A., Garaev, M. M., Odoevskaya, I. M. and Benediktov, I. I. (2003). The genotyping of Echinococcus granulosus and E. multilocularis from different regions of Russia. In Theory and Practice in Control of Parasitic Diseases (ed. Uspenskiy, A. V.), pp. 285287. Rosselhozacademia, Moscow, Russia (in Russian).
Odnokurtsev, V. A. and Sedalishchev, V. T. (2012). Helminthic fauna of wild canids in Yakutia. In Diseases and parasites of wildlife in Siberia and the Russian Far East (ed. Seryodkin, I. V. and Miquelle, D. G.), pp. 202217. Dalnauka Press, Vladivostok, Russia.
Omer, R. A., Dinkel, A., Romig, T., Mackenstedt, U., Elnahas, A. A., Aradaib, I. E., Ahmed, M. E., Elmalik, K. H. and Adam, A. (2010). A molecular survey of cystic echinococcosis in Sudan. Veterinary Parasitology 169, 340346.
Rausch, R. L. (1995). Life cycle patterns and geographic distribution of Echinococcus species. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 89134. CAB International, Wallingford, UK.
Rehmann, P., Gröne, A., Lawrenz, A., Pagan, O., Gottstein, B. and Bacciarini, L. N. (2003). Echinococcus multilocularis in Two Lowland Gorillas (Gorilla g. gorilla). Journal of Comparative Pathology 129, 8588.
Sato, C., Kawase, S., Yano, S., Nagano, H., Fujimoto, S., Kobayashi, N., Miyahara, K., Yamada, K., Sato, M. and Kobayashi, Y. (2005). Outbreak of larval Echinococcus multilocularis infection in Japanese monkey (Macaca fuscata) in a zoo, Hokkaido: western blotting patterns in the infected monkeys. Journal of Veterinary Medical Science 67, 133135.
Schurer, J., Shury, T., Leighton, F. and Jenkins, E. (2013). Surveillance for Echinococcus canadensis genotypes in Canadian ungulates. International Journal for Parasitology: Parasites and Wildlife 2, 97101.
Shakhmatova, V. I. (1981). On natural foci alveococcosis in Siberia. In Biological Problem of Natural Foci of Disease (ed. Maksimov, A. A.), pp. 123134. Nauka, Novosibirsk, Russia.
Soriano, S. V., Pierangeli, N. B., Pianciola, L., Mazzeo, M., Lazzarini, L. E., Saiz, M. S., Kossman, A. V., Bergagna, H. F. J., Chartier, K. and Basualdo, J. A. (2010). Molecular characterization of Echinococcus isolates indicates goats as reservoir for Echinococcus canadensis G6 genotype in Neuquén, Patagonia Argentina. Parasitology International 59, 626628.
Storandt, S. T., Virchow, D. R., Dryden, M. W., Hygnstrom, S. E. and Kazacos, K. R. (2002). Distribution and prevalence of Echinococcus multilocularis in wild predators in Nebraska, Kansas, and Wyoming. Journal of Parasitology 88, 420422.
Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis using Parsimony (and other Methods) 4·0 Meta. Sinauer Associates, Massachusetts.
Tang, C., Cui, G., Qian, Y., Kang, Y., Wang, Y., Peng, W., Lu, H. and Chen, D. (2007). Studies on the alveolar Echinococcus species in northward daxingan mountains, Inner Mongolia, China. III. Echinococcus russicensis sp. nov. Chinese Journal of Zoonoses 23, 957963. (in Chinese).
Taniyama, H., Morimitsu, Y., Fukumoto, S. I., Asakawa, M. and Ohbayashi, M. (1996). A natural case of larval echinococcosis caused by Echinococcus multilocularis in a zoo orangutan (Pongo pygmaeus). In Alveolar Echinococcosis. Strategy for Eradication of Alveolar Echinococcosis of the Liver (ed. Uchino, J. and Sato, N.), pp. 6567. Fuji Shoin, Sapporo, Japan.
Templeton, A. R., Crandall, K. A. and Sing, C. F. (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619633.
Thompson, R. C. A., Boxell, A. C., Ralston, B. J., Constantine, C. C., Hobbs, R. P., Shury, T. and Olson, M. E. (2006). Molecular and morphological characterization of Echinococcus in cervids from North America. Parasitology 132, 439447.
Vol'fson, A. G. (1968). Incidence of echinococcosis among the population of the Chukotka District of the Chukotskiĭ National Region according to data of an immunologic survey. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 37, 686691. (in Russian).
Wilson, J. F., Diddams, A. C. and Rausch, R. L. (1968). Cystic hydatid disease in Alaska. A review of 101 autochthonous cases of Echinococcus granulosus infections. American Reviews of Respiratory Disease 98, 115.
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P., Craig, P. and Ito, A. (2005). Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693701.
Yamasaki, H., Nakao, M., Nakaya, K., Schantz, P. M. and Ito, A. (2008). Genetic Analysis of Echinococcus multilocularis originating from a patient with alveolar echinococcosis occurring in Minnesota in 1977. American Journal of Tropical Medicine and Hygiene 79, 245247.
Yanagida, T., Mohammadzadeh, T., Kamhawi, S., Nakao, M., Sadjjadi, S. M., Hijjawi, N., Abdel-Hafez, S. K., Sako, Y., Okamoto, M. and Ito, A. (2012). Genetic polymorphisms of Echinococcus granulosus sensu stricto in the Middle East. Parasitology International 61, 599633.
Yastreb, V. B. (2010). Strains of Echinococcus granulosus (Batsch, 1786). Russia Parasitological Journal 3, 1226 (in Russian).



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed