Skip to main content

Transmission ecosystems of Echinococcus multilocularis in China and Central Asia


From continental to regional scales, the zoonosis alveolar echinococcosis (AE) (caused by Echinococcus multilocularis) forms discrete patches of endemicity within which transmission hotspots of much larger prevalence may occur. Since the late 80s, a number of hotspots have been identified in continental Asia, mostly in China, wherein the ecology of intermediate host communities has been described. This is the case in south Gansu, at the eastern border of the Tibetan plateau, in south Ningxia, in the western Tian Shan of Xinjiang, and in the Alay valley of south Kyrgyzstan. Here we present a comparative natural history and characteristics of transmission ecosystems or ecoscapes. On this basis, regional types of transmission and their ecological characteristics have been proposed in a general framework. Combining climatic, land cover and intermediate host species distribution data, we identified and mapped 4 spatially distinct types of transmission ecosystems typified by the presence of one of the following small mammal ‘flagship’ species: Ellobius tancrei, Ochotona curzoniae, Lasiopodomys brandtii or Eospalax fontanierii. Each transmission ecosystem had its own characteristics which can serve as a reference for further in-depth research in the transmission ecology of E. multilocularis. This approach may be used at fine spatial scales to characterize other poorly known transmission systems of the large Eurasian endemic zone, and help in consideration of surveillance systems and interventions.

    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Transmission ecosystems of Echinococcus multilocularis in China and Central Asia
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Transmission ecosystems of Echinococcus multilocularis in China and Central Asia
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Transmission ecosystems of Echinococcus multilocularis in China and Central Asia
      Available formats
The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution license .
Corresponding author
*Corresponding author: Chrono-environment Lab, University of Franche-Comté, place Leclerc, F-25030 Besançon, France. Tel: +33 381 665 745. Fax: +33 381 665 797. E-mail:
Hide All
Barua M. (2011). Mobilizing metaphors: the popular use of keystone, flagship and umbrella species concepts. Biodiversity and Conservation 20, 14271440.
Bessonov A. S. (1998). Echinococcus multilocularis infection in Russia and neighbouring countries. Helminthologia 35, 7378.
Budke C. M., Campos-Ponce M., Qian W. and Torgerson P. R. (2005 a). A canine purgation study and risk factor analysis for echinococcosis in a high endemic region of the Tibetan plateau. Veterinary Parasitology 127, 4349.
Budke C. M., Jiamin Q., Craig P. S. and Torgerson P. R. (2005 b). Modeling the transmission of Echinococcus granulosus and Echinococcus multilocularis in dogs for a high endemic region of the Tibetan plateau. International Journal for Parasitology 35, 163170.
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. Parasites and Vectors 4, 19.
Chautan M., Pontier D. and Artois M. (2000). Role of rabies in recent demographic changes in Red Fox (Vulpes vulpes) populations in Europe. Mammalia 64, 391410.
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.
Craig P. S., Giraudoux P., Shi D., Bartholomot B., Barnish G., Delattre P., Quéré J. P., Harraga S., Bao G., Wang Y. H., Lu F., Ito A. and Vuitton D. A. (2000). An epidemiological and ecological study of human alveolar echinococcosis transmission in south Gansu, China. Acta Tropica 77, 167177.
Craig P. S., Liu D. S., Macpherson C. N. L., Shi D. Z., Reynolds D., Barnish G., Gottstein B. and Wang Z. R. (1992). A large focus of alveolar echinococcosis in central China. Lancet 340, 826831.
Danson F. M., Graham A. J., Pleydell D. R. J., Campos-Ponce M., Giraudoux P. and Craig P. S. (2003). Multi-scale spatial analysis of human alveolar echinococcosis risk in China. Parasitology 127, 133141.
Danson F. M., Craig P. S., Man W., Shi D. and Giraudoux P. (2004). Landscape dynamics and risk modeling of human alveolar echinococcosis. Photogrammetric Engineering and Remote Sensing 70, 359366.
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.
Feng X. H. (2013). Immunodiagnosis of human and canine echinococcosis and community studies in northwestern China. Ph.D. University of Salford, Salford (in prep).
Giraudoux P., Craig P. S., Delattre P., Bartholomot B., Bao G., Barnish G., Harraga S., Quéré J. P., Raoul F., Wang Y. H., Shi D. and Vuitton D. (2003). Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127, 121131.
Giraudoux P., Delattre P., Takahashi K., Raoul F., Quere J. P., Craig P. and Vuitton D. (2002). Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multiscale approaches? In Cestode Zoonoses: Echinococcosis and Cysticercosis: an Emergent and Global Problem (ed. Craig P. and Pawlowski Z.), pp. 251266. IOS Press, Amsterdam.
Giraudoux P., Pleydell D., Raoul F., Quere J. P., Qian W., Yang Y., Vuitton D. A., Qiu J. M., Yang W. and Craig P. S. (2007). Echinococcus multilocularis: why are multidisciplinary and multiscale approaches essential in infectious disease ecology? Tropical Medicine and Health 55, S237S246.
Giraudoux P., Pleydell D., Raoul F., Quere J. P., Wang Q., Yang Y. R., Vuitton D. A., Qiu J. M., Yang W. and Craig P. S. (2006). Transmission ecology of Echinococcus multilocularis: what are the ranges of parasite stability among various host communities in China? Parasitology International 55, S237S246.
Giraudoux P., Pradier B., Delattre P., Deblay S., Salvi D. and Defaut R. (1995). Estimation of water vole abundance by using surface indices. Acta Theriologica 40, 7796.
Giraudoux P., Quere J. P., Delattre P., Bao G. S., Wang X. M., Shi D. Z., Vuitton D. and Craig P. S. (1998). Distribution of small mammals along a deforestation gradient in southern Gansu, central China. Acta Theriologica 43, 349362.
Giraudoux P., Raoul F., Pleydell D. and Craig P. S. (2008 a). Multidisciplinary studies, systems approaches and parasite eco-epidemiology: something old, something new. Parasite – Journal de la Societe francaise de parasitologie 15, 469476.
Giraudoux P., Raoul F., Pleydell D., Li T. Y., Han X. M., Qiu J. M., Xie Y., Wang H., Ito A. and Craig P. S. (2013). Drivers of Echinococcus multilocularis transmission in China: host biodiversity, landscape or climate? PLOS Neglected Tropical Diseases 7, e2045.
Giraudoux P., Zhou H., Quere J. P., Raoul F., Delattre P., Volobouev V., Déforêt T., Ito A., Mamuti W., Scheifler R. and Craig P. (2008 b). Small mammal assemblages and habitat distribution in the northern Junggar basin, Xinjiang, China: a pilot survey. Mammalia 72, 309319.
Heywood V. H. (ed.) (1995). Global Biodiversity Assessment. Cambridge University Press, Cambridge.
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 Zürich, Switzerland. Parasitology 120, 135142.
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 indigenous alveolar echinococcosis cases in Mongolia. American Journal of Tropical Medicine and Hygiene 82, 266269.
Ito A., Urbani C., Qiu J., Vuitton D. A., Qiu D., Heath D. D., Craig P. S., Zheng F. and Schantz P. M. (2003). Control of echinococcosis and cysticercosis: a public health challenge to international cooperation in China. Acta Tropica 86, 317.
IUCN (2012). The IUCN Red List of Threatened Species.
Jiang W. B., Liu N., Zhang G. T., Renqing P. C., Xie F., Li T. Y., Wang Z. H. and Wang X. M. (2012). Specific detection of Echinococcus spp. from the Tibetan fox (Vulpes ferrilata) and the red fox (V. vulpes) using copro-DNA PCR analysis. Parasitology Research 111, 15311539.
Komonen M., Komonen A. and Otgonsuren A. (2003). Daurian pikas (Ochotona daurica) and grassland condition in eastern Mongolia. Journal of Zoology 259, 281288.
Konyaev S. V., Yanagida T., Ingovatova G. M., Shoikhet Y. N., Nakao M., Sako Y., Bondarev A. Y. and Ito A. (2012). Molecular identification of human echinococcosis in Altai region, Russia. Parasitology International 61, 711714.
Leemans R. and Cramer W. (1991). The IIASA Database for Mean Monthly Values of Temperature, Precipitation and Cloudiness on a Global Terrestrial Grid. Research Report RR-91-18. November 1991. pp. 61. International Institute of Applied Systems Analyses, Laxenburg.
Li M., Wang H., Yin Y. C. and Li W. X. (1990). B-ultrasound diagnosis of hepatic alveolar echinococcosis in 141 cases. Gansu Medical Journal, 989990.
Li T. Y., Chen X. W., Zhen R., Qiu J. M., Qiu D. C., Xiao N., Ito A., Wang H., Giraudoux P., Sako Y., Nakao M. and Craig P. S. (2010). Widespread co-endemicity of human cystic and alveolar echinococcosis on the eastern Tibetan Plateau, northwest Sichuan/southeast Qinghai, China. Acta Tropica 113, 248256.
Li T. Y., Qiu J. M., Yang W., Craig P. S., Chen X. W., Xiao N., Ito A., Giraudoux P., Wulamu M., Yu W. and Schantz P. M. (2005). Echinococcosis in Tibetan populations, Western Sichuan Province, China. Emerging Infectious Diseases 11, 18661873.
Lidicker W. Z. (2000). A food web/landscape interaction model for microtine rodent density cycles. Oikos 91, 435445.
Lidicker W. Z. (2008). Levels of organization in biology: on the nature and nomenclature of ecology's fourth level. Biological Reviews 83, 7178.
Miterpakova M., Dubinsky P., Reiterova K. and Stanko M. (2006). Climate and environmental factors influencing Echinococcus multilocularis occurrence in the Slovak Republic. Annals of Agricultural and Environmental Medicine 13, 235242.
Patz J. A., Daszak P., Tabor G. M., Aguirre A. A., Pearl M., Epstein J., Wolfe N. D., Kilpatrick A. M., Foufopoulos J., Molyneux D. and Bradley D. J. (2004). Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Enviromental Health Perspectives 112, 10921098.
Pleydell D., Yang Y., Wang Q., Raoul F., Danson M., Craig P., Vuitton D. and Giraudoux P. (2008). Landscape composition and spatial prediction of a zoonosis: the case of alveolar echinococcosis in southern Ningxia, China. PLOS Neglected Tropical Diseases 2, e287.
Pleydell D. R. J., Raoul F., Danson F. M., Graham A., Craig P. S., Tourneux F. and Giraudoux P. (2004). Modelling the spatial distribution of Echinococcus multilocularis infection in foxes. Acta Tropica 91, 253265.
Qiu J. M., Liu F. J., Schantz P., Ito A., Carol D. and He J. G. (1999). Epidemiological Survey of Hydatidosis in Tibetan Areas of Western Sichuan Province. Archivos Internacionales de la Hidatidosis 33, 211213.
Quéré J. P., Raoul F., Giraudoux P. and Delattre P. (2000). An index method applicable at landscape scale to estimate relative population densities of the common vole (Microtus arvalis). Revue d'Écologie, Terre et Vie 55, 2532.
Raoul F., Deplazes P., Nonaka N., Piarroux R., Vuitton D. A. and Giraudoux P. (2001). Assessment of the epidemiological status of Echinococcus multilocularis in foxes in France using ELISA coprotests on fox faeces collected in the field. International Journal for Parasitology 31, 15791588.
Raoul F., Deplazes P., Rieffel D., Lambert J. C. and Giraudoux P. (2010). Predator dietary response to prey density variation and consequences for cestode transmission. Oecologia 164, 129139.
Raoul F., Pleydell D., Quere J. P., Vaniscotte A., Rieffel D., Takahashi K., Bernard N., Wang J. L., Dobigny T., Galbreath K. E. and Giraudoux P. (2008). Small-mammal assemblage response to deforestation and afforestation in central China. Mammalia 72, 320332.
Raoul F., Quere J. P., Rieffel D., Bernard N., Takahashi K., Scheifler R., Wang Q., Qiu J., Yang W., Craig P. S., Ito A. and Giraudoux P. (2006). Distribution of small mammals along a grazing gradient on the Tibetan plateau of western Sichuan, China. Mammalia 42, 214225.
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.
Shaikenov B. S. and Torgerson P. R. (2002). Distribution of Echinococcus multilocularis in Kazakhstan. In Cestode Zoonoses: Echinococcosis and Cysticercosis: an Emergent and Global Problem (ed. Craig P. and Pawlowski Z.), pp. 299307. IOS Press, Amsterdam.
Smith A. and Xie Y. (2008). A Guide to the Mammals of China, Princeton University Press, Princeton.
Tang C. T., 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.
Tang C. T., Wang Y. H., Peng W. F., Tang L. and Chen D. (2006). Alveolar Echinococcus species from Vulpes corsac in Hulunbeier, Inner Mongolia, China, and differential development of the metacestodes in experimental rodents. Journal of Parasitology 92, 719724.
Tokobaev M. M. (1959). Helminths of rodents in Kyrgyzia. Works of the Institute Zoology and Parasitology of the Kyrgyz SSR Academy of Sciences 7, 133142.
Torgerson P. R., 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 and International Health 14, 341348.
Tougard C., Montuire C., Volobouev V., Markova E., Contet J. and Quéré J. P. (2013). Exploring phylogeography and species limits in the Altaï vole (Rodentia: Cricetidae). Biological Journal of the Linnean Society 108, 434452.
Vaniscotte A., Pleydell D. R. J., Raoul F., Quere J. P., Qiu J. M., Qian W., Li T. Y., Bernard N., Coeurdassier M., Delattre P., Takahashi K., Weidmann J. C. and Giraudoux P. (2009). Modelling and spatial discrimination of small mammal assemblages: an example from western Sichuan (China). Ecological Modelling 220, 12181231.
Vaniscotte A., Raoul F., Poulle M. L., Romig T., Dinkel A., Takahashi K., Guislain M. H., Moss J., Tiaoying L., Wang Q., Qiu J., Craig P. S. and Giraudoux P. (2011). Role of dog behaviour and environmental fecal contamination in transmission of Echinococcus multilocularis in Tibetan communities. Parasitology 138, 13161329.
Veit P., Bilger B., Schad V., Schäfer J., Frank W. and Lucius R. (1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 7986.
Viel J. F., Giraudoux P., Abrial V. and Bresson-Hadni S. (1999). Water vole (Arvicola terrestris scherman) density as risk factor for human alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 61, 559565.
Vuitton D. A., 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, S87S107.
Wang H. L., Yin Y. C., Ma C., Zhang C. Y., Zhang X. P., Cheng R. P., Jiang R. F. and Li M. (1991). Preliminary investigation of liver alveolar echinococcosis and liver cystic echinococcosis in Xiji County, Ningxia. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 9, 143145.
Wang Q., Raoul F., Budke C. M., Craig P. S., Xiao Y. F., Vuitton D. A., Campos-Ponce M., Qiu D. C., Pleydell D. and Giraudoux P. (2010). Grass height and transmission ecology of Echinococcus multilocularis in Tibetan communities, China. Chinese Medical Journal 123, 6167.
Wang Q., Vuitton D. A., Qiu J. M., Giraudoux P., Xiao Y. F., Schantz P. M., Raoul F., Li T. Y., Yang W. and Craig P. S. (2004). Fenced pasture: a possible risk factor for human alveolar echinococcosis in Tibetan pastoralist communities of Sichuan, China. Acta Tropica 90, 285293.
Wang Q., Vuitton D. A., Xiao Y. F., Budke C. M., Campos-Ponce M., Schantz P. M., Raoul F., Yang W., Craig P. S. and Giraudoux P. (2006). Pasture types and Echinococcus multilocularis, Tibetan communities. Emerging Infectious Diseases 12, 10081010.
Wang Z. H., Wang X. M. and Chmura A. A. (2008). Den habitat characteristics of Tibetan foxes (Vulpes ferrilata) in Shiqu County, Sichuan Province, China. Zoological Studies 47, 445454.
Wang Z. H., Wang X. M. and Lu Q. B. (2007). Selection of land cover by the Tibetan fox Vulpes ferrilata on the eastern Tibetan plateau, western Sichuan Province, China. Acta Theriologica 52, 215223.
Wilson D. E. and Mittermeier R. A. (2009). Handbook of the Mammals of the World. Lynx Edicions, Barcelona.
Wilson D. E. and Reeder D. M. (2005). Mammal Species of the World. Johns Hopkins University Press, Baltimore.
Winters A. M., Rumbeiha W. K., Winterstein S. R., Fine A. E., Munkhtsog B. and Hickling G. J. (2010). Residues in Brandt's voles (Microtus brandti) exposed to bromadiolone-impregnated baits in Mongolia. Ecotoxicology and Environmental Safety 73, 10711077.
Wood S. N. (2006). Generalized Additive Models: An Introduction with R. Chapman & Hall/CRC, London.
Xiao N., Li T. Y., Qiu J. M., Nakao M., Chen X. W., Nakaya K., Yamasaki H., Schantz P. M., Craig P. S. and Ito A. (2004). The Tibetan hare Lepus oiostolus: a potential novel intermediate host for Echinococcus multilocularis. Parasitology Research 92, 352353.
Xie Y., Mackinnon J. and Li D. (2004). Study on biogeographical divisions of China. Biodiversity and Conservation 13, 13911417.
Xu X. Y., Liance M., Lin Y. G., Li W. X. and Houin R. (1992). Present data about alveolar echinococcosis in the popular republic of China. Bulletin De La Societe De Pathologie Exotique 85, 241246.
Yang Y. R., Clements A. C. A., Gray D. J., Atkinson J. A. M., Williams G. M., Barnes T. S. and McManus D. P. (2012). Impact of anthropogenic and natural environmental changes on Echinococcus transmission in Ningxia Hui Autonomous Region, the People's Republic of China. Parasites and Vectors 5, 146.
Yang Y. R., Sun T., Li Z. Z., Zhang J. Z., Teng J., Liu X. Z., Liu R. Q., Zhao R., Jones M. K., Wang Y. H., Wen H., Feng X. H., Zhao Q., Zhao Y. M., Shi D. Z., Bartholomot B., Vuitton D. A., Pleydell D., Giraudoux P., Ito A., Danson M. F., Boufana B., Craig P. S., Williams G. M. and McManus D. P. (2006). Community surveys and risk factor analysis of human alveolar and cystic echinococcosis in Ningxia Hui Autonomous Region, China. Bulletin of the World Health Organization 84, 714721.
Zhou H. X. (2001). Epidemiologie et écologie de la transmission d'Echinococcus multilocularis au Xinjang, Republique Populaire de Chine: étude preliminaire. Ph.D. University of Franche-Comté, Besançon.
Zhou H. X., Chai S. X., Craig P. S., Delattre P., Quere J. P., Raoul F., Vuitton D. A., Wen H. and Giraudoux P. (2000). Epidemiology of alveolar echinococcosis in Xinjiang Uygur autonomous region, China: a preliminary analysis. Annals of Tropical Medicine and Parasitology 94, 715729.
Zhou H. X., Wen H., Wang Y. H., Delattre P., Quere J. P., Vuitton D. A., Craig P. and Giraudoux P. (1998). Experimental susceptibility of Spermophilus erythrogenys to Echinococcus multilocularis. Annals of Tropical Medicine and Parasitology 93, 335337.
Ziadinov I., Deplazes P., Mathis A., Mutunova B., Abdykerimov K., Nurgaziev R. and Torgerson P. R. (2011). Frequency distribution of Echinococcus multilocularis and other helminths of foxes in Kyrgyzstan. Veterinary Parasitology 171, 286292.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 2
Total number of PDF views: 182 *
Loading metrics...

Abstract views

Total abstract views: 243 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 16th January 2018. This data will be updated every 24 hours.