Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-30T14:24:30.687Z Has data issue: false hasContentIssue false

Echinococcus species from red foxes, corsac foxes, and wolves in Mongolia

Published online by Cambridge University Press:  19 August 2013

AKIRA ITO*
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
GANTIGMAA CHULUUNBAATAR
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan Laboratory of Entomology, Mongolian Academy of Science, Ulaanbaatar, Mongolia
TETSUYA YANAGIDA
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
ANU DAVAASUREN
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan Department of Parasitology, National Center for Communicable Diseases, Ulaanbaatar, Mongolia
BATTULGA SUMIYA
Affiliation:
Laboratory of Entomology, Mongolian Academy of Science, Ulaanbaatar, Mongolia
MITSUHIKO ASAKAWA
Affiliation:
Department of Parasitology, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido, Japan
TOSHIAKI KI
Affiliation:
Department of Parasitology, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido, Japan
KAZUHIRO NAKAYA
Affiliation:
Animal Laboratory for Medical Research, Center for Advanced Research and Education, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
ABMED DAVAAJAV
Affiliation:
Department of Parasitology, National Center for Communicable Diseases, Ulaanbaatar, Mongolia
TEMUULEN DORJSUREN
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan Department of Medical Biology, School of Biomedicine, Health Science University of Mongolia, Ulaanbaatar, Mongolia
MINORU NAKAO
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
YASUHITO SAKO
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
*
*Corresponding author. Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido 078-8510, Japan. Tel.: +81 166 68 2686. Fax: +81 166 68 2429. E-mail: akiraito@asahikawa-med.ac.jp

Summary

The small intestines of 420 wild canids (111 corsac foxes, 191 red foxes and 118 wolves) from Mongolia, were examined for adult worms of the genus Echinococcus. The Mongolian genotype of Echinococcus multilocularis was found in fifteen red foxes and four wolves, whereas two genotypes (G6/7 and G10) of Echinococcus canadensis were found in two and three wolves, respectively. No adult Echinococcus worms were found in the corsac foxes examined. The genotypes of E. multilocularis and E. canadensis are discussed in terms of host specificity and distribution in Mongolia. The importance of wolves in the completion of the life cycle of Echinococcus spp. is also discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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

Abdybekova, A. M. and Torgerson, P. R. (2012). Frequency distributions of helminths of wolves in Kazakhstan. Veterinary Parasitology 184, 348351.CrossRefGoogle ScholarPubMed
Abuladze, K. I. (1964). Taeniata of Animals and Man and Diseases Caused by Them. Essentials of Cestodology, Vol. 4 (ed. Skrjabin, K. I.). Akademiya Nauk SSSR, Moscow (in Russian); English transl.: Israel Program for Scientific Translations, Jerusalem 1970, 549 pp.Google Scholar
Bagrade, G., Kirjusina, M., Vismanis, K. and Ozolins, J. (2009). Helminth parasites of the wolf Canis lupus from Latvia. Journal of Helminthology 83, 6368.CrossRefGoogle ScholarPubMed
Beiromvand, M., Akhlaghi, L., Massom, S. H. F., Mobedi, I., Meamar, A. R., 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
Bretagne, S., Assouline, B., Vidaud, D., Houin, R. and Vidaud, M. (1996). Echinococcus multilocularis: microsatellite polymorphism in U1 snRNA genes. Experimental Parasitology 82, 324328.CrossRefGoogle ScholarPubMed
Breyer, I., Georgieva, D., Kurdova, R. and Gottstein, B. (2004). Echinococcus granulosus strain typing in Bulgaria: the G1 genotype is predominant in intermediate and definitive wild hosts. Parasitology Research 93, 127130.CrossRefGoogle ScholarPubMed
Bryan, H. M., Darimont, C. T., Hill, J. E., Paquet, P. C., Thompson, R. C. A., Wagner, B. and Smits, J. G. (2012). Seasonal and biogeographical patterns of gastrointestinal parasites in large carnivores: wolves in a coastal archipelago. Parasitology 139, 781790.CrossRefGoogle Scholar
Budke, C., Deplazes, P. and Torgerson, P. R. (2006). Global socioeconomic impact of cystic echinococcosis. Emerging Infectious Diseases 12, 296303.CrossRefGoogle ScholarPubMed
Combes, B., Comte, S., Raton, V., Raoul, F., Boué, F., Umhang, G., Favier, S., Dunoyer, C., Woronoff, N. and Giraudoux, P. (2012). Westward spread of Echinococcus multilocularis in foxes, France, 2005–2010. Emerging Infectious Diseases 18, 20592062.CrossRefGoogle ScholarPubMed
Craig, P. S., Budke, C. M., Schantz, P. M., Li, T., Qiu, J., Yang, Y., Zeyhle, E., Rogan, M. T. and Ito, A. (2007). Human echinococcosis: a neglected disease? Tropical Medicine and Health 35, 283292.CrossRefGoogle Scholar
Davaatseren, N., Otogondalai, A., Nyamkhuu, G. and Susher, A. H. (1995). Management of echinococcosis in Mongolia. Journal of the Arkansas Medical Society 92, 122125.Google ScholarPubMed
Dzhabarova, V. I., Zbarskii, A. I. and Bulanova, T. E. (1993). Differences in the infectivity and chemotherapy susceptibility of Kamchatka and Kazakhstan isolates of Echinococcus multilocularis in laboratory animals (a study of echinococcosis on Kamchatka Peninsula. Meditsinskaia parazitologiia I parazitornye bolezni Jul–Sept, 11–15 (in Russian).Google Scholar
Ebright, J. R., Altantsetseg, T. and Oyungerel, R. (2003). Emerging infectious diseases in Mongolia. Emerging Infectious Diseases 9, 15091515.CrossRefGoogle ScholarPubMed
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, pp. 1265. World Organization for Animal Health, Paris.Google Scholar
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.CrossRefGoogle ScholarPubMed
Fuglei, E., Stien, A., Yoccoz, N. G., Ims, R. A., Eide, N. E., Prestrud, P., Deplazes, P. and Oksanen, A. (2008). Spatial distribution of Echinococcus multilocularis, Svalbard, Norway. Emerging Infectious Diseases 14, 7375.CrossRefGoogle ScholarPubMed
Guberti, V., Bolognini, M., Lanfranchi, P. and Battelli, G. (2004). Echinococcus granulosus in the wolf in Italy. Parasitologia 46, 425427.Google ScholarPubMed
Guerra, D., Armua-Fernandez, M. T., Silva, M., Bravo, I., Santos, N., Deplazes, P. and Madeira de Carvalho, L. M. (2013). Taeniid species of the Iberian wolf (Canis lupus signatus) in Portugal with special focus on Echinococcus spp. International Journal for Parasitology: Parasites and Wildlife 2, 5053.Google ScholarPubMed
Gurbadam, A., Nyamkhuu, D., Nyamkhuu, G., Tsendjav, A., Sergelen, O., Narantuya, B., Batsukh, Z., Battsetseg, G., Oyun-Erdene, B., Uranchimeg, B., Otgonbaatar, D., Temuulen, D., Bayarmaa, E., Abmed, D., Tsogtsaikhan, S., Usukhbayar, A., Smirmaul, K., Gereltuya, J. and Ito, A. (2010). Mongolian and Japanese joint conference on “Echinococcosis: diagnosis, treatment and prevention in Mongolia” June 4, 2009. Parasites and Vectors 3, 8.CrossRefGoogle Scholar
Hirvelä-Koski, V., Haukisalmi, V., Kilpelä, S-S, Nylund, M and Koski, P. (2003). Echinococcus granulosus in Finland. Veterinary Parasitology 111, 175192.CrossRefGoogle ScholarPubMed
Hüttner, M., Nakao, M., Wassermann, T., Siefert, L., Boomker, J. D., 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.CrossRefGoogle ScholarPubMed
Ito, A., Agvaandaram, G., Bat-Ochir, O. E., Chuluunbaatar, B., Gonchingsenghe, 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 alveolar echinococcosis cases in Mongolia. American Journal of Tropical Medicine and Hygiene 82, 266269.CrossRefGoogle ScholarPubMed
Ito, A., Okamoto, M., Li, T., Wandra, T., Dharmawan, N. S., Swastika, K. I., Dekumyoy, P., Kusolsuk, T., Davajav, A., Davaasuren, A., Dorjsuren, T., Mekonnen, S. M., Negashi, Z. H., Yanagida, T., Sako, Y., Nakao, M., Nakaya, K., Lavikainen, A. J., Nkouawa, A. and Mohammadzadeh, T. (2011 b). The first workshop on towards the control of cestode zoonoses in Asia and Africa. Parasites and Vectors 4, 114.CrossRefGoogle ScholarPubMed
Ito, A., Yanagida, T., Sako, Y., Nakao, M., Nakaya, K., Knapp, J. and Ishikawa, Y. (2011 a). Echinococcus and echinococcosis. In Molecular Detection of Human Parasitic Pathogens (ed. Liu, D.), pp. 249263. CRC Press, Boca Raton, USA.Google Scholar
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.CrossRefGoogle ScholarPubMed
Jenkins, E. J., Peregrine, A. S., Hill, J. E., Somers, C., Gesy, K., Barnes, B., Gottstein, B. and Polley, L. (2012). Detection of European strain of Echinococcus multilocularis in North America. Emerging Infectious Diseases 18, 10101012.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kongaev, S. V., Yanagida, T., Ingovatova, G. M., Shoiknet, Y. N., Nakao, M., Sako, Y., Bondarev, A. Y. and Ito, A. (2012). Molecular identification of human echinococcosis in the Altal region of Russia. Parasitology International 61, 711714.CrossRefGoogle Scholar
Konyaev, S. V., Yanagida, T., Nakao, M., Ingovatova, G. M., Shoykhet, Y. N., Bondarev, A. Y., Odnokurtsev, V. A., Loskutoba, K. S., Lukmanova, G. I., Dokuchaev, N. E., Spiridonov, S., Alshinecky, M. V., Tatyana, S. N., Andreyanov, O. N., Abramov, S. A., Krivopalov, A. V., Karpenko, S. V., Lopatina, N. V., Dupal, T. A., Sako, Y. and Ito, A. (2013). Genetic diversity of Echinococcus spp. in Russia. Parasitology 140, in press.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mamuti, W., Yamasaki, H., Sako, Y., Nakao, M., Xiao, N., Nakaya, K., Sato, N., Vuitton, D. A., Piarroux, R., Lightowlers, M. W., Craig, P. S. and Ito, A. (2004). An 8 kDa-subunit of Antigen B from Echinococcus multilocularis: molecular cloning, expression and serological evaluation. Journal of Clinical Microbiology 42, 10821088.CrossRefGoogle ScholarPubMed
Martínek, K., Kolářová, L., Hapl, E., Literák, I. and Uhrin, M. (2001). Echinococcus multilocularis in European wolves (Canis lupus). Parasitology Research 87, 838839.Google ScholarPubMed
Matoba, Y., Yamada, D., Asano, M., Oku, Y., Kitaura, K., Yagi, K., Tenora, F. and Asakawa, M. (2006). Parasitic helminths from feral raccoons (Procyon lotor) on Hokkaido and Kyushu Islands, Japan. Helminthologia 43, 139146.CrossRefGoogle Scholar
Mohammadzadeh, T., Sako, Y., Sadjjadi, S. M., Sarkari, B. and Ito, A. (2012). Comparison of the usefulness of hydatid cyst fluid, native antigen B and recombinant antigen B8/1 for serological diagnosis of cystic echinococcosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 106, 371375.CrossRefGoogle ScholarPubMed
Moks, E., Jõgisalu, I., Saarma, U., Talvik, H., Järvis, T. and Valdmann, H. (2006). Helminthological survey of the wolf (Canis lupus) in Estonia, with an emphasis on Echinococcus granulosus. Journal of Wildlife Diseases 42, 359365.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007). A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713722.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Nakao, M., Yanagida, T., Konyaev, S., Lavikainen, A., Odnokurtsev, V. A., Vladimir, A., Zaikoy, 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.CrossRefGoogle ScholarPubMed
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. CABI Press, Wallingford, UK.Google Scholar
Rausch, R. L. (2003). Cystic echinococcosis in the Arctic and Sub-Arctic. Parasitology 127, S73S85.CrossRefGoogle ScholarPubMed
Rausch, R. L. and Schiller, E. L. (1951). Hydatid disease (echinococcosis) in Alaska and the importance of rodent intermediate hosts. Science 113, 5758.CrossRefGoogle ScholarPubMed
Schantz, P. M. (2006). Progress in diagnosis, treatment and elimination of echinococcosis and cysticercosis. Parasitology International 55, S7S13.CrossRefGoogle ScholarPubMed
Schneider, R., Aspöck, H. and Auer, H. (2013). Unexpected increase of alveolar echinococcosis, Austria, 2011. Emerging Infectious Diseases 19, 475477.CrossRefGoogle ScholarPubMed
Schweiger, A., Ammann, R. W., Candinas, D., Clavien, P. A., Eckert, J., Gottstein, B., Halkic, N., Muellhaupt, B., Prinz, B. M., Reichen, J., Tarr, P. E., Torgerson, P. R. and Deplazes, P. (2007). Human alveolar echinococcosis after fox population increase, Switzerland. Emerging Infectious Diseases 13, 878882.CrossRefGoogle ScholarPubMed
Sobrino, R., Gozalez, L. M., Vicente, J., Fernández de Luco, D., Garate, T. and Gontázar, C. (2006). Echinococcus granulosus (Cestoda, Taeniidae) in the Iberian wolf. Parasitology Research 99, 753756.CrossRefGoogle ScholarPubMed
Spira, A. M. (1995). Saturday, May 13, 1995. Ulaanbaatar: Infectious Disease Department, National Medical University of Mongolia. Journal of the Citizen Ambassador Program Parasitology Delegation to the People's Republic of China and Mongolia May 7 to 20, 78.Google Scholar
Swofford, D. L. (2002). PAUP*: Phylogenetic Analysis using Parsimony (and other Methods) 4·0 Beta.Sinauer Associates, Massachusetts.Google Scholar
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).Google Scholar
Tang, C., Quian, Y. C., Kang, Y. M., Cui, G. W., Lu, H. C., Shu, L. M., Wang, Y. H. and Tang, L. (2004). Study on the ecological distribution of alveolar Echinococcus in Hulunbeier pasture of Inner Mongolia, China. Parasitology 128, 187194.CrossRefGoogle Scholar
Thompson, R. C. A. (2008). The taxonomy, phylogeny and transmission of Echinococcus. Experimental Parasitology 119, 439446.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. and McManus, D. P. (2002). Towards a taxonomic revision of the genus Echinococcus. Trends in Parasitology 18, 452457.CrossRefGoogle ScholarPubMed
Torgerson, P. R. (2013). The emergence of echinococcosis in central Asia. Parasitology 140, in press.CrossRefGoogle ScholarPubMed
Torgerson, P. R. and Budke, C. (2003). Echinococcosis – an international public health challenge. Research in Veterinary Science 74, 191202.CrossRefGoogle ScholarPubMed
Torgerson, P. R., Keller, K., Magnotta, M. and Ragland, N. (2010). The global burden of alveolar echinococcosis. PLoS Neglected Tropical Diseases 22, e722.CrossRefGoogle Scholar
Torgerson, P. R., Oguijahan, B., Muminov, A. E., Karaeva, R. R., Kuttbaev, O. T., Aminjianov, M. and Shaikenov, B. (2006). Present situation of cystic echinococcosis in Central Asia. Parasitology International 55, S253S258.CrossRefGoogle ScholarPubMed
Wang, W., Wu, Y. and Ding, Z. (1989). The occurrence of Echinococcus multilocularis Leuckart, 1863 in fox and wolf in Tacheng District, Xinjiang. Endemic Diseases Bulletin 4, 812.Google Scholar