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Epidemiology of alveolar echinococcosis with particular reference to China and Europe

Published online by Cambridge University Press:  04 March 2004

D. A. VUITTON
Affiliation:
WHO Collaborating Centre for the Prevention and Treatment of Alveolar Echinococcosis, SERF and LBE Usc INRA research units, Université de Franche-Comté, 25030 – Besançon, France
H. ZHOU
Affiliation:
WHO Collaborating Centre for the Prevention and Treatment of Alveolar Echinococcosis, SERF and LBE Usc INRA research units, Université de Franche-Comté, 25030 – Besançon, France Xinjiang Medical University, 83000 Urumqi, Xinjiang, PR China Present address: Public Health College, Guanxi Medical University, Nanning city, PR China.
S. BRESSON-HADNI
Affiliation:
WHO Collaborating Centre for the Prevention and Treatment of Alveolar Echinococcosis, SERF and LBE Usc INRA research units, Université de Franche-Comté, 25030 – Besançon, France
Q. WANG
Affiliation:
WHO Collaborating Centre for the Prevention and Treatment of Alveolar Echinococcosis, SERF and LBE Usc INRA research units, Université de Franche-Comté, 25030 – Besançon, France Sichuan Institute of Parasitic Diseases, Chengdu, Sichuan, PR China
M. PIARROUX
Affiliation:
WHO Collaborating Centre for the Prevention and Treatment of Alveolar Echinococcosis, SERF and LBE Usc INRA research units, Université de Franche-Comté, 25030 – Besançon, France
F. RAOUL
Affiliation:
WHO Collaborating Centre for the Prevention and Treatment of Alveolar Echinococcosis, SERF and LBE Usc INRA research units, Université de Franche-Comté, 25030 – Besançon, France
P. GIRAUDOUX
Affiliation:
WHO Collaborating Centre for the Prevention and Treatment of Alveolar Echinococcosis, SERF and LBE Usc INRA research units, Université de Franche-Comté, 25030 – Besançon, France

Abstract

Human alveolar echinococcosis (AE), caused by the metacestode of the fox tapeworm Echinococcus multilocularis, is the most pathogenic zoonosis in temperate and arctic regions of the northern hemisphere. Prospective collection of human cases in some areas and mass screenings using ultrasound imaging and confirmation with serological techniques have markedly improved our knowledge of the epidemiology of the disease in humans during the past two decades. Transmission occurs when eggs of the tapeworm, excreted by the final hosts (usually foxes but also dogs, wolves and cats), are ingested accidentally by humans or during normal feeding by a variety of rodents and small lagomorphs. However, the species of host animals differ according to regional changes in mammalian fauna. This review mostly focuses on epidemiology of alveolar echinococcosis in those parts of the world where new and more accurate epidemiological data are now available, i.e. China and Europe, as well as on new epidemiological trends that can be suspected from recent case reports and/or from recent changes in animal epidemiology of E. multilocularis infection. The People's Republic of China (PRC) is a newly recognized focus on AE in Asia. Human AE cases were firstly recognized in Xinjiang Uygur Autonomous Region and Qinghai Provinces at the end of 1950s and infected animals were first reported from Ningxia in central China and north-east of Inner Mongolia in the 1980s. E. multilocularis (and human cases of AE) appears to occur in three areas: (1) Northeastern China (northeast focus): including Inner Mongolia Autonomous region and Heliongjiang Province (2) Central China (central focus): including Gansu Province, Ningxia Hui Autonomous Region, Sichuan Province, Qinghai Province and Tibet Autonomous Region and (3) Northwestern China: including Xinjiang Uygur Autonomous Region, bordered with Mongolia, Russia, Kazakhstan and Kyrgyzstan. The highest prevalence of the disease, up to 15 per cent of the population in some villages, is reached in China. In Europe, data from the European Echinococcosis Registry (EurEchinoReg: 1982–2000) show 53 autochthonous cases of AE in Austria, 3 in Belgium, 235 in France, 126 in Germany, 1 in Greece, and 112 in Switzerland, and 15 ‘imported’ cases, especially from central Asia; 14 cases were collected in Poland, a country not previously considered endemic for AE. Improved diagnostic technology, as well as a real increase in the infection rate and an extension to new areas, can explain that more than 500 cases have been reported for these 2 decades while less than 900 cases were published for the previous 7 decades. New epidemiological trends are related to an unprecedented increase in the fox population in Europe, to the unexpected development of urban foxes in Japan and in Europe, and to changes in the environmental situation in many countries worldwide due to climatic or anthropic factors which might influence the host–predator relationship in the animal reservoir and/or the behavioural characteristics of the populations in the endemic areas.

Type
Research Article
Copyright
© 2003 Cambridge University Press

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References

REFERENCES

ALTINTAS, N. (1997). Alveolar echinococcosis in Turkey and Middle-East countries. In Archivos Internacionales de la Hidatidosis ( ed. Menezes Da Silva, A. & Nunes, J. L.), pp. 150154. Lisbon, International Society of Hydatidology.
AMMANN, R. W. & ECKERT, J. (1995). Clinical diagnosis and treatment of Echinococcus in humans. In Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A. & Lymbery A. L.), pp. 411463. Wallingford, Cab International.
ARTOIS, M. (1997). Managing problem wildlife in the ‘Old World’: A veterinary perspective. Reproduction Fertility and Development 9, 1725.CrossRefGoogle Scholar
BARTHOLOMOT, B., VUITTON, D. A., HARRAGA, S., SHI, D. Z., GIRAUDOUX, P., BARNISH, G., WANG, Y. H., MACPHERSON, N. & CRAIG, P. (2002). Combined ultrasonographic and serological screening of hepatic alveolar echinococcosis in central China. American Journal of Tropical Medicine and Hygiene 66, 2329.CrossRefGoogle Scholar
BESSONOV, A. S. (1998). Echinococcus multilocularis infection in Russia and neighboring countries. Helminthologia 35, 7378.Google Scholar
BESSONOV, A. S. (2002). Echinococcoses of animals and humans in the Russian federation. In Cestode Zoonoses: An Emergent and Global Problem ( ed. Craig, P. S. & Pawlowski, Z. ), pp. 9198. Amsterdam, NATO Science Series, IOS Press, Vol. 341.
BRESSON-HADNI, S., BARTHOLOMOT, B., MIGUET, J. P., MANTION, G. & VUITTON, D. A. (1997). L'échinococcose alvéolaire hépatique. Hepato-Gastro 4, 151159.Google Scholar
BRESSON-HADNI, S., KURTZ, S., BEURTON, I., BARTHOLOMOT, B., KRATZER, W., MIGUET, J. P., VUITTON, D. A. & KERN, P. (1999). Classification of alveolar echinococcosis: a bicentric European proposal. Journal of Hepatology 30 (Suppl. 1), 166.Google Scholar
BRESSON-HADNI, S., LAPLANTE, J. J., LENYS, D., ROHMER, P., GOTTSTEIN, B., JACQUIER, P., MERCET, P., MEYER, J. P. & VUITTON, D. A. (1994). Seroepidemiological screening of Echinococcus multilocularis in a European area endemic for alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 51, 837846.CrossRefGoogle Scholar
BRESSON-HADNI, S., MIGUET, J. P., VUITTON, D. A., MEYER, J. P., BECKER, M. C., DIDIER, J. P., COCHE, G., WEILL, F., CARBILLET, J. P., LANDECY, G., MANTION, G. & GILLET, M. (1988). L'échinococcose alvéolaire hépatique humaine. Revue générale à propos de 80 cas. Semaine des hôpitaux de Paris 64, 26912699.Google Scholar
BRESSON-HADNI, S., VUITTON, D. A., BARTHOLOMOT, B., HEYD, B., GODARD, D., MEYER, J. P., HRUSOVSKY, S., BECKER, M. C., MANTION, G., LENYS, D. & MIGUET, J. P. (2000). A twenty-year history of alveolar echinococcosis: analysis of a series of 117 patients from Eastern France. European Journal of Gastroenterology and Hepatology 12, 327336.CrossRefGoogle Scholar
CHAUTAN, M., PONTIER, D. & ARTOIS, M. (2000). Role of rabies in recent demographic changes in Red Fox (Vulpes vulpes) populations in Europe. Mammalia 64, 391410.CrossRefGoogle Scholar
CLAUDON, M. (1983). Place actuelle des méthodes d'imagerie dans le diagnostic et la surveillance de l'échinococcose alvéolaire (à props de 62 observations recueillies en Lorraine). MD Thesis. Faculty of medicine, University of Nancy, France.
COROIU, Z., RUSU, G. & STEFANOIU, V. (1992). Occurrence and distribution of hydatidosis in men in three transylvanian countries. Revista Romania Parazitologia 2, 39.Google Scholar
CRAIG, P. S., DESHAN, L., MacPHERSON, C. N. L., DAZHONG, S., REYNOLDS, D., BARNISH, G., GOTTSTEIN, B. & ZHIRONG, W. (1992). A large focus of alveolar echinococcosis in central China. The Lancet 340, 826831.CrossRefGoogle Scholar
CRAIG, P. S., GIRAUDOUX, P., SHI, D. Z., BARTHOLOMOT, B., BARNISH, G., DELATTRE, P., QUERE, J. P., HARRAGA, S., BAO, G., WANG, Y. H., LU, F., ITO, A. & VUITTON, D. A. (2000). An epidemiological and ecological study of human alveolar echinococcosis transmission in south Gansu, China. Acta Tropica 77, 167177.CrossRefGoogle Scholar
CRAIG, P., SHI, D. Z., BARTHOLOMOT, B., VUITTON, D. A., WANG, W., BARNISH, G., MacPHERSON, C., HARRAGA, S., WANG, Y., GIRAUDOUX, P., LIU, J. & SHI, P. (1997). China, the highest prevalence country for alveolar echinococcosis in human? In Archivos Internacionales de la Hidatidosis ( ed. Menezes Da Silva, A. & Nunes, J. L.), pp. 154156. Lisbon, International Society of Hydatidology.
DEPLAZES, P. & ECKERT, J. (2001). Veterinary aspects of alveolar echinococcosis – a zoonosis of public health significance. Veterinary Parasitology 98, 6587.CrossRefGoogle Scholar
ECKERT, J. (1996). Echinococcus multilocularis and alveolar echinococcosis in Europe. In Alveolar Echinococcosis of the Liver ( ed. Uchino, J. & Sato, N.), pp. 2743. Sapporo, Fuji-Shoin.
ECKERT, J. (1997). Epidemiology of Echinococcus multilocularis and E. granulosus in Central Europe. Parassitologia 39, 337344.Google Scholar
ECKERT, J., CONRATHS, F. J. & TACKMANN, K. (2000). Echinococcosis: an emerging or re-emerging zoonosis? International Journal for Parasitology 30, 12831294.Google Scholar
ECKERT, J. & DEPLAZES, P. (1996). Methods for surveys on Echinococcus multilocularis infections in final hosts. In Alveolar Echinococcosis of the Liver ( ed. Uchino, J. & Sato, N.), pp. 151163. Sapporo, Fuji-Shoin.
ECKERT, J. & DEPLAZES, P. (1999). Alveolar echinococcosis in humans: the current situation in Central Europe and the need for countermeasures. Parasitology Today 15, 315319.CrossRefGoogle Scholar
ECKERT, J., SCHANTZ, P. M., GASSER, R. B., TORGERSON, P. R., BESSONOV, A. S., MOVSESSIAN, S. O., THAKUR, A., GRIMM, F. & NIKOGOSSIAN, M. A.(2001). Echinococcosis. Geographic distribution and prevalence. In WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern (ed. Eckert, J., Gemmell, M. A., Meslin, F. & Pawlowski, Z. S.), pp. 100142. Paris, OIE/WHO.
EIERMANN, T., BETTENS, F., TIBERGHIEN, P., SCHMITZ, K., BEURTON, I., BRESSON-HADNI, S., AMMANN, R., GOLDMANN, S., VUITTON, D., GOTTSTEIN, B. & KERN, P. (1998). HLA and alveolar echinoccosis. Tissue Antigens 52, 124129.CrossRefGoogle Scholar
EPSNR (Prevention Station of Ningxia Hui Autonomous Region) (1999). Current status of echinococcosis in Ningxia, China. In Proceedings of the Workshop on Echinococcosis Control Strategy in China, pp. 16. Institute for Endemic Disease Research and Control, Urumqi. (In Chinese.)
FESSELER, M. (1990). Vergleich der Endemiegebiete von Echinococcus multilocularis und Tollwut in Mitteleuropa. Veterinary dissertation, University of Zurich.
GENOV, T. P., SILENOV, D. K. & POLYAKOVA-KRUSTEVA, P. T. (1980). The natural occurrence of Alveococcus multilocularis in the Microtus nivalis in Bulgaria. Comptes Rendus de l'Académie Bulgare des Sciences 38, 981984.Google Scholar
GIRAUDOUX, P., DELATTRE, P., TAKAHASHI, K., RAOUL, F., QUÉRÉ, J. P., CRAIG, P. & VUITTON, D. (2002). Transmission ecology of Echinococcus multilocularis in wildlife: what can be learnt from comparative studies and multi-scale approaches? In Cestode Zoonoses: An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 251262. Amsterdam, NATO Sciences Series, IOS press.
GIRAUDOUX, P., QUERE, J. P., DELATTRE, P., BAO, G., WANG, X., SHI, D., VUITTON, D. A. & CRAIG, P. (1998). Distribution of small mammals along a deforestation gradient in southern Gansu, central China. Acta Theriologica 43, 349362.CrossRefGoogle Scholar
GIRAUDOUX, P., RAOUL, F., BARDONNET, K., VUILLAUME, P., TOURNEUX, F., CLIQUET, F., DELATTRE, P. & VUITTON, D. A. (2001). Alveolar echinococcosis: characteristics of a possible emergence and new perspectives in epidemiosurveillance. Médecine et Maladies Infectieuses 31, 247256.CrossRefGoogle Scholar
GLOOR, S. (1988). Echinokokkose beim Menschen in der Schweiz 1970–1983. Medical Dissertation, Zurich.
GLOOR, S., BONTADINA, F., HEGGLIN, D., DEPLAZES, P. & BREITENMOSER, U. (2001). The rise of urban fox population in Switzerland. Mammal Biology 66, 155164.Google Scholar
GODOT, V., HARRAGA, S., BEURTON, I., DESCHASEAUX, M., SARCIRON, E., GOTTSTEIN, B. & VUITTON, D. A. (2000 a). Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. I. Comparison of patients with progressive and abortive lesions. Clinical and Experimental Immunology 121, 484490.Google Scholar
GODOT, V., HARRAGA, S., BEURTON, I., TIBERGHIEN, P., SARCIRON, E., GOTTSTEIN, B. & VUITTON, D. A. (2000 b). Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. II. Influence of the HLA B8, DR3, DQ2 haplotype. Clinical and Experimental Immunology 121, 491498.Google Scholar
GODOT, V., HARRAGA, S., DESCHASAUX, M., BRESSON-HADNI, S., GOTTSTEIN, B., EMILIE, D. & VUITTON, D. A. (1997). Role of IL-10 in alveolar echinococcosis: mRNA expression by CD4+ and CD8+ T-cells and increased basal production by PBMC. European Cytokine Network 8, 401408.Google Scholar
GOTTSTEIN, B., LENGELER, C., BACHMANN, P., HAGEMANN, P., KOCHER, P., BROSSARD, M., WITASSEK, F. & ECKERT, J. (1987). Sero-epidemiological survey for alveolar echinococcosis (by Em2-ELISA) of blood donors in an endemic area of Switzerland. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 960964.CrossRefGoogle Scholar
GOTTSTEIN, B., SAUCY, F., DEPLAZES, P., REICHEN, J., DEMIERRE, G., BUSATO, A., ZUERCHER, C. & PUGIN, P. (2001). Is high prevalence of E. multilocularis in wild and domestic animals associated with disease incidence in humans? Emerging Infectious Diseases 7, 408412.Google Scholar
GUO, Z. X. (1986). Survey of Echinococcus spp. in wildlife: an evidence of Ochotona curzoniae as intermediate host of E. multilocularis in Qinghai-Tibet Plateau. Endemic Disease Bulletin 1, 128130. (In Chinese.)Google Scholar
HE, D. L., HAN, S. M. & WU, X. H. (1994). Epidemiology and parasitology survey of hydatidosis in Chengduo of Qinghai Province. Chinese Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih 12, 185. (In Chinese.)Google Scholar
HOFER, S., GLOOR, S., MÜLLER, U., MATHIS, A., HEGGLIN, D. & 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.CrossRefGoogle Scholar
HONG, L. X. & LIN, Y. G. (1987). Studies on the development and histopathology of alveolar cestode of Echinococcus multilocularis in human and animal hosts. Endemic Disease Bulletin 2, 5159. (In Chinese.)Google Scholar
HOU, X. M. (2001). The current situation of rodents and its control methods in resource area of Qingnan pasture. Sichuan Grassland 1, 2831.Google Scholar
ITO, A., URBANI, C., QIU, J. M., VUITTON, D. A., QIU, D., HEATH, D. D., CRAIG, P. S., FENG, Z. & SCHANTZ, P. (2003). Control of echinococcosis and cysticercosis: a public health challenge to international cooperation in PR China. Acta Tropica 86, 317.CrossRefGoogle Scholar
JAKAB, F. & FALLER, J. (1988). Echinococcus alveolaris treated by right trisegmentectomy. Acta Chirurgica Hungarica 29, 223230.Google Scholar
JENSEN, B., REUTER, S., KRATZER, W., NASER, K., KACHELE, V., KIMMIG, P. & KERN, P. (2001). Long-term seropositivity against Echinococcus multilocularis in an epidemiological follow-up study in southwestern Germany (Romerstein). Infection 29, 310314.CrossRefGoogle Scholar
JI, X. L., XING, Z. H. & XU, H. M. (1987). A report of human AE case from Hulunbeier Meng, Inner Mongolia. Medical Journal of Inner Mongolia 7, 129. (In Chinese.)Google Scholar
KAMIYA, M. (1988). Infectious diseases transmitted by dogs to humans. Asian Medical Journal 31, 8793.Google Scholar
KERN, P., BARDONNET, K., RENNER, E., AUER, H., PAWLOWSKI, Z., AMMANN, R. W., VUITTON, D. A. & KERN, P. (2003). European Echinococcosis Registry: assessment of human alveolar echinococcosis in Europe from 1982 to 2000. Emerging Infectious Diseases 9, 343349. http://www.cdc.gov/ncidod/EID/vol19no3/02-0341.htmCrossRefGoogle Scholar
KOLAROVA, L. (1999). Echinococcus multilocularis: new epidemiological insights in Central and Eastern Europe. Helminthologia 36, 193200.Google Scholar
KRCMERY, V., BELAN, V., CERNAK, P., SOBOTA, K., BORUTA, P., HRUSOVSKY, S., SOBOVOTA, O., SORF, M. & SILAN, I. (1989). CT picture of the liver in patients with tissue parasitoses. Czech Gastroenterology 42, 175182.Google Scholar
KREIDL, P., ALLERSBERGER, F., JUDMAIER, G., AUER, H., ASPOCK, H. & HALL, A. J. (1998). Domestic pets as risk factors of alveolar hydatid disease in Austria. American Journal of Epidemiology 147, 978981.CrossRefGoogle Scholar
LI, W. X., ZHANG, G. C., LIN, Y. G. & HONG, L. X. (1985). The occurrence of Echinococcus multilocularis Leuckart, 1863, the natural animal hosts in China and its morphological study. Acta Zoologica Sinica 31, 365371. (In Chinese.)Google Scholar
LIN, Y. G. & HONG, L. X. (1991). The biology and the geographical distribution of Echinococcus multilocularis infection in China. Endemic Disease Bulletin 6, 117127. (In Chinese.)Google Scholar
LIU, F. J. (1993). Prevalence of Echinococcus granulosus in dogs in the Xinjiang Uygur Autonomous Region, PRC. In Compendium on Cystic Echinococcosis with Special Reference to the Xinjiang Uygur Autonomous Region, The People's Republic of China ( ed. Andersen, F. L. ), pp. 168176. Provo, Utah, Brigham Young University.
LIU, F. J., QIU, J. M. & SCHANTZ, P. (1998). Epidemiology and transmission of alveolar echinococcosis in East Tibetan Plateau. In Proceedings of the First National Hydatidology Conference of Imaging and Therapeutics and International Symposium on Transmission and Control of Echinococcus Infection, pp. 104108. Urumqi, Xinjiang Medical University. ( In Chinese.)
LIU, R. C. & QU, Z. Y. (1964). A case report: alveolar echinococcosis infection in brain. Zhong Hua Sheng Jing Jing Sheng Ke Za Zhi 8, 174. (In Chinese.)Google Scholar
LOSSON, B., MIGNON, B., BROCHIER, B., BAUDIEN, B. & PASTORET, P. P. (1997). Echinococcus multilocularis infection in the red fox (Vulpes vulpes) in the province of Luwembourg (Belgium): results of a survey conducted between 1993–1995. Annales de Médecine Vétérinaire 141, 149155.Google Scholar
LUCIUS, R. & BILGER, B. (1995). Echinococcus multilocularis in Germany: increased awareness or spreading of a parasite. Parasitology Today 11, 430434.CrossRefGoogle Scholar
LUKASHENKO, N. P. (1968). Comparative biologic and pathologic studies of Alveococcus multilocularis. Archives of Environmental Health 17, 676680.CrossRefGoogle Scholar
LUO, Y. G. (1993). Clinical analysis of 12 AE cases in Tibet. Chinese Chi Sheng Chung Ping Fang Zhi Tsa Chih 6, 62. (In Chinese.)Google Scholar
MACPHERSON, C. N. L., BARTHOLOMOT, B. & FRIDER, B. (2003). Application of ultrasound in diagnosis, treatment, epidemiology, public health and control of Echinococcus (E.) granulosus and E. multilocularis. Parasitology 127, S21S35.Google Scholar
MANFREDI, M. T., GENCHI, C., DEPLAZES, P., TREVISIOL, K. & FRAQUELLI, C. (2002). Echinococcus multilocularis infection in red foxes in Italy. The Veterinary Record 150, 757757.CrossRefGoogle Scholar
MU, Y. & SUENG, Z. G. (1991). Alveolar hydatid disease of liver: clinical analysis of 113 cases. Endemic Disease Bulletin 6, 6468. (In Chinese.)Google Scholar
NOTHDURFT, H. D., JELINEK, T., MA, A., SIGL, B., VON SONNENBURG, G. F. & LOSCHER, T.(1995). Epidemiology of alveolar echinococcosis in Southern Germany (Bavaria). Infection 23, 8588.CrossRefGoogle Scholar
PAWLOWSKI, Z. (1996). Alveolar echinococcosis in humans in Poland. In Alveolar Echinococcosis of the Liver ( ed. Uchino, J. & Sato, N.), pp. 4548. Sapporo, Fuji-Shoin.
PENG, S. G. (1988). Report of two AE cases from the Changdu, Tibet Autonomous Region. Chinese Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih 6, 288. (In Chinese.)Google Scholar
PETERSEN, E. & KAPEL, C. (2000). Dvaergbaendelorm hos raeve. Epi-Nyt 21, 5.Google Scholar
PU, Z. (1999). A case report of Echinococcus multilocularis in brain. Chinese Journal of Neurosurgery 15, 338. (In Chinese.)Google Scholar
QIU, J. M., LIU, F. J. & SCHANTZ, P. M. (1999). Epidemiology of echinococcosis in a Tibetan community in western Sichuan. In Proceedings of the Workshop of Echinococcosis Control Strategy in China. Urumqi, Institute for Endemic Disease Research and Control. (In Chinese.)
QU, Z. Y. & ZHANG, Z. Z. (1965). Clinical analysis of 15 cases of alveolar echinococcosis. Chinese Medical Journal 51, 2829. (In Chinese.)Google Scholar
RAOUL, F., DEPIERRE, V., SCHEIFLER, R., MASS, R., PETAVY, A. F., VUITTON, D. A. & GIRAUDOUX, P. (1999). Landscape effect on Echinococcus multilocularis winter prevalence in foxes in the Jura massif, France. Helminthologia 36, 48.Google Scholar
RAOUL, F., DEPLAZES, P., NONAKA, N., PIARROUX, R., VUITTON, D. A. & GIRAUDOUX, P. (2002). Assessement of the epidemiological status of Echinococcus multilocularis in foxes using ELISA coprotests on fox faeces collected in the field. International Journal for Parasitology 31, 15791588.Google Scholar
RAUSCH, R. L. (1995). Life-cycle patterns and geographic distribution of Echinococcus species. In Echinococcus and Hydatid disease (ed. Thompson, R. C. A. & Lymbery, A. J.), pp. 89119. Wallingford, Cab International.
RAUSCH, R. L. & FAY, F. H. (2002). Epidemiology of alveolar echinococcosis with reference to St Lawrence island, Bering sea. In Cestode Zoonoses: An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 309325. Amsterdam, NATO Sciences Series, IOS press.
RAUSCH, R. L., FAY, F. H. & WILLIAMSON, F. S. L. (1990). The ecology of Echinococcus multilocularis (cestoda: Taeniidae) on St Lawrence Island, Alaska. II. Helminth populations in the definitive host. Annales de Parasitologie Humaine et Comparée 65, 131140.CrossRefGoogle Scholar
RAUSCH, R. L. & SCHILLER, E. L. (1956). Studies on the helminth fauna of Alaska XXV. The ecology and public health significance of Echinococcus sibiricensis Rausch and Schiller, 1954, on St. Lawrence Island. Parasitology 46, 395419.Google Scholar
RAUSCH, R. L., WILSON, J. F. & SCHANTZ, P. M.(1990). A programme to reduce the risk of infection by Echinococcus multilocularis: the use of praziquantel to control the cestode in a village in the hyperendemic region of Alaska. Annals of Tropical Medicine and Parasitology 84, 239250.CrossRefGoogle Scholar
RAUSCH, R. L., WILSON, J. F., SCHANTZ, J. F. & McMAHON, B. J. (1987). Spontaneous death of Echinococcus multilocularis: cases diagnosed serologically (by Em2-ELISA) and clinical significance. American Journal of Tropical Medicine and Hygiene 36, 576585.CrossRefGoogle Scholar
ROBBANA, M., RACHID, B. M. S., ZITOUNA, M. M. & HAFSIA, M. (1981). Première observation d'échinococcose alvéolaire autochtone en Tunisie. Archives d'Anatomie et Cytologie Pathologique 29, 311312.Google Scholar
ROMIG, T. (for EurEchinoReg) (2002). Spread of Echinococcus multilocularis in Europe? In Cestode Zoonoses: An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 6580. Amsterdam, NATO Sciences Series, IOS press.
ROMIG, T., BILGER, B., KINKEL, A., MERLI, M. & MACKENSTEDT, U. (1999). Echinococcus multilocularis in animal hosts: new data from Western Europe. Helminthologia 36, 185191.Google Scholar
ROMIG, T., KRATZER, W., KIMMIG, P., FROSCH, M., GAUS, W., FLEGEL, W. A., GOTTSTEIN, B., LUCIUS, R., BECKH, K. & KERN, P. (1999). An epidemiologic survey of human alveolar echinococcosis in southwestern Germany. Romerstein Study Group. American Journal of Tropical Medicine and Hygiene 61, 566573.CrossRefGoogle Scholar
SAEED, I. & KAPEL, C. M. O. (2001). Echinococcus multilocularis in Scandinavia: results of helminthological study of Danish red foxes. XXth International Congress of Hydatidology, Kusadasi, Turkey ( ed. Altintas, N., Yolasigmaz, A., Coskun, E. & Gunes, K.), p. 245, Izmir, International Archives of the Hydatidosis.
SEILER, M., SOELDER, B., ALLERBERGER, F., ZAKNUN, D., FEICHTINGER, H. & GOTTSTEIN, B. (1997). Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. Journal of Pediatrics 130, 320.CrossRefGoogle Scholar
SCHALLER, G. B. (1998). Wildlife of the Tibetan Steppe, pp. 178211. Chicago, University of Chicago.
SCHANTZ, P. M. (1998). A survey of hydatid disease (echinococcosis) in Tibetan populations in China: preliminary results. In Proceedings of The First National Hydatidology Conference of Imaging and Therapeutics, and International Symposium on Transmission and Control of Echinococcus Infection, pp. 152. Urumqi, Xinjiang Medical University.
SCHANTZ, P. M., CHAI, J., CRAIG, P. S., ECKERT, J., JENKINS, D. J., MacPHERSON, C. N. L. & THAKUR, A. (1995). Epidemiology and control of hydatid disease. In Echinococcus and Hydatid Disease ( ed. Thompson, R. C. A. & Lymbery, A. J.), pp. 233302. Wallingford, Cab International.
SHAIKENOV, B. S. & TORGERSON, P. R. (2002). Distribution of Echinococcus multilocularis in Kazakhstan. In Cestode Zoonoses: An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 299305. Amsterdam, NATO Science Series, IOS Press.
SHI, D. Z. (1995). The first report of Echinococcus multilocularis in domestic dogs in Zhang Country of Gansu Province. Chinese Medical Journal 108, 615617.Google Scholar
SLAIS, J., MADLE, A., VANKA, K., JELINEK, F., CERNIK, V., PRUCHOVA, M. & JINDRA, J. (1979). Alveolarni hydatidoza (Echinokokkosa) diagnostikovana punkcni jaterni biopsii. Casopis Lekaru Ceskych 118, 472475. (In Czech.)Google Scholar
STEHR-GREEN, J. A., STEHR-GREEN, P. A., SCHANTZ, P. M., WILSON, J. F. & LANIER, A. (1988). Risk factors for infection with Echinococcus multilocularis in Alaska. American Journal of Tropical Medicine and Hygiene 38, 380385.CrossRefGoogle Scholar
STORANDT, S. T. & KAZACOS, K. R. (1993). Echinococcus multilocularis identified in Indiana, Ohio, and east-central Illinois. Journal of Parasitology 79, 301315.CrossRefGoogle Scholar
STORANDT, S. T., VIRCHOW, D. R., DRYDEN, M. W., HYGNSTROM, S. E. & KAZACOS, K. R. (2002). Distribution and prevalence of Echinococcus multilocularis in wild predators in Nebraska, Kansas, and Wyoming. Journal of Parasitology 88, 420422.CrossRefGoogle Scholar
STÖSSEL, T. (1989). Literaturubersicht zur Haufigkeit und geographischen Verbreitung der Echinokokkose in Landern der EG und EFTA. Medical dissertation, University of Zurich.
SRETER, T., SZELL, Z., EGYED, Z. & VARGA, I. (2003). Echinococcus multilocularis: an emerging pathogen in Hungary and Central Eastern Europe? Emerging Infectious Diseases 9, 384386.Google Scholar
SUZUKI, K., SATO, N. & UCHINO, J. (1993). I. Epidemiology. In Alveolar Echinococcosis of the Liver ( ed. Uchino, J. & Sato, N.), pp. 19. Sapporo, Fuji-Shoin.
TAKAHASHI, K. & NAKATA, K. (1995). Note on the first occurrence of larval Echinococcocus multilocularis in Clethrionomys rex in Hokkaido, Japan. Journal of Helminthology 69, 265266.CrossRefGoogle Scholar
TAKAHASHI, K., YAGI, K., URAGUCHI, K. & KONDO, N. (1989). Infection of larval Echinococcus multilocularis in red-backed vole, Clethrionomys rufocanus bedfordiae, captured around fox dens. Report of the Hokkaido Institute of Public Health 39, 58.Google Scholar
TANG, C. X., CUI, G. W., QIAN, Y. C., LU, S. M. & LU, H. C. (1988). On the occurrence of Echinococcus multilocularis in Hulunbeier Pasture, Inner Mongolia Autonomous Region. Acta Zoologica Sinica 34, 172179. (In Chinese.)Google Scholar
THEODOROPOULOS, G., KOLISOPOULOS, A., ARCHIMANDRITIS, A. & MELISSINOS, K. (1978). Echinococcose alvéolaire hépatique. Trois observations en Grèce. Nouvelle Presse Médicale 37, 3056.Google Scholar
TSUKADA, H., MORISHIMA, Y., NONAKA, N., OKU, Y. & KAMIYA, M. (2000). Preliminary study of the role of red foxes in Echinococcus multilocularis transmission in the urban area of Sapporo, Japan. Parasitology 120, 423428.CrossRefGoogle Scholar
TUNODA, I., MIKAMI, J. & AOKI, T. (1937). The recently discovered first case of typical hepatic multilocular “Echinococcosis” in Japan. Gerenz Gebeit 11, 10931100.Google Scholar
UYSAL, V. & PAKSOY, N. (1986). Echinococcus multilocularis in Turkey. Journal of Tropical Medicine and Hygiene 89, 249255.Google Scholar
VAN DER GIESSEN, J., ROMBOUT, Y., FRANCHIMONT, H., LIMPER, L. & HOMAN, W. (1999). Detection of Echinococcus multilocularis in foxes in the Netherlands. Veterinary Parasitology 82, 4957.CrossRefGoogle Scholar
VIEL, F., GIRAUDOUX, P., ABRIAL, V. & BRESSON-HADNI, S. (1999). Water vole (Arvicola terrestris Sheman) density as risk factor for human alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 61, 559565.CrossRefGoogle Scholar
VUILLEMIN, I. (1997). Facteur de risque de contamination humaine par Echinococcus multilocularis étude cas-témoins dans le département du Doubs. Pharm. D. Thesis, Université de Bourgogne, France.
VUITTON, D. A. (1990). Alveolar echinococcosis of the liver: a parasitic disease in search of a treatment. Hepatology 12, 617618.CrossRefGoogle Scholar
VUITTON, D. A. (2003). The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Tropica 85, 119132.Google Scholar
VUITTON, D. A., BRESSON-HADNI, S., LIANCE, M., MEYER, J. P., GIRAUDOUX, P. & LENYS, D. (1990). Human alveolar echinococcosis. Epidemiologic hazard or immunologic incident? Gastroentérologie Clinique et Biologique 14, 124130. (In French.)Google Scholar
VUITTON, D. A., GODOT, V., SHAOLING, ZHANG, HARRAGA, S., PENFORNIS, A., BEURTON, I., GOTTSTEIN, B., GIRAUDOUX, P., KERN, P. V. & EURECHINOREG NETWORK (2002). Host immunogenetics and role in epidemiology of larval cestodoses. In Cestode Zoonoses: An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 183194. Amsterdam, NATO Science Series, IOS Press.
WANG, C. X. (1996). Rodent pests and public health. In Theory and Practice of Rodent Pest Management ( ed. Wang, Z. W. & Zhang, Z. B.), pp. 3853. Beijing, Science Press. (In Chinese.)
WANG, H., MA, S. M., CAO, D. P., ZHAO, H. L. & WU, H. Y. (1999). General review of echinococcosis in Qinghai. In Proceedings of the Workshop on Echinococcosis Control Strategy in China, pp. 711. Urumqi, Institute for Endemic Disease Research and Control. (In Chinese.)
WANG, H. L., YI, Y. C., MA, Z., ZHANG, X. P., CHENG, R. P., JING, R. F. & LI, M. (1991). A report of a mass screening on alveolar and cystic echinococcosis in Xiji County, Ningxia, China. Chinese Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih 9, 143145. (In Chinese.)Google Scholar
WANG, M. Y. (1978). Histopathology description on alveolar echinococcosis in the liver. Acta Academiae Medicinae Xinjiang 2, 125129. (In Chinese.)Google Scholar
WANG, Q., QIU, J. M., SCHANTZ, P. M. S., HE, J. G., ITO, A. & LIU, F. J. (2001). Risk factors for development of human hydatidosis among people whose family is raising livestock in Western Sichuan Province, China. Chinese Journal of Parasitology and Parasitic Diseases 19, 289293.Google Scholar
WANG, Q., VUITTON, D. A., QIU, J., GIRAUDOUX, P., XIAO, Y., SCHANTZ, P., RAOUL, F., LI, T., WEN, Y. & CRAIG, P. S. (2003). Fenced pasture: A possible risk factor for human alveolar echinococcosis in Tibetan pastoral communities of Sichuan, China. Acta Tropica (in press).Google Scholar
WANG, X. T. (1989). Scientific Investigation in Liupan Mountains, Ningxia ( ed. Wang, X. T. ), pp. 248251. Yingchuang, Ningxia People's Press.
WEN, G. Z. (1990). A case report of human alveolar hydatid disease in Jamusi city. In Proceedings of China Third Academic Workshop of Parasitology and Parasite Disease, pp. 235236. Beijing, Science Press. (In Chinese.)
WILSON, J. F. & RAUSCH, R. L. (1980). Alveolar hydatid disease. A review of clinical features of 33 indigenous cases of Echinococcus multilocularis infection in Alaskan eskimos. American Journal of Tropical Medicine and Hygiene 29, 13401355.CrossRefGoogle Scholar
XIA, W. P. (1996). Rodent-like pests and ecological equilibrium. In Theory and Practice of Rodent Pest Management ( ed. Wang, Z. W. & Zhang, Z. B. ), pp. 218. Beijing, Science Press. (In Chinese.)
YAMASHITA, J. (1973). Echinococcus and echinococcosis. Progress of Medical Parasitology in Japan 5, 65123.Google Scholar
YAO, B. L., FU, L. M., XIU, D. Z., ZOU, P. F., LI, J. & WANG, Y. H. (1986). Hepatic alveolar hydatidosis: experience in the clinical treatment of 52 cases. Acta Academiae Medicinae Xinjiang 9, 309317. (In Chinese.)Google Scholar
YAO, B. L., HUANG, N. Q., FU, L. M. & FANG, K. H. (1965). Hepatic alveolar echinococcosis. Chinese Surgery Journal 13, 460461.Google Scholar
YAROTSKII, L. S., MARTYNENKO, V. B., KOLESNIDOV, N. M., YURASEV, N. G., NIKKIFOROVA, T. F., TUMOLSKAYA, N. I., BLIZNYUK, V. G., BOJIN, N. M., LOSEVA, T. A., VEDEJINA, L. I., SMIRNOV, V. A., POLOSMAK, L. P., KOLOGRIVOVA, Z. A., VOROPANOV, T. V., BLOTSKY, V. Y., PAPIKO, V. P., CHUIKO, A. G. & SAVINKIN, V. V. (1988). Echinococcosis in the Kamchatka region: scientific and practical aspects of their control activation. Moscow Medical Parasitology 3, 6064.Google Scholar
YIXI, J. Q. (1992). Histopathological analysis of 10 cases of hepatic alveolar echinococcosis. Chinese Journal of Pathology 21, 363. (In Chinese.)Google Scholar
YU, S. H., XU, L. Q., JIANG, Z. X., XU, S. H., HAN, J. J., ZHU, Y. G., CHANG, J., LIN, J. X. & XU, F. N. (1994). Report on the first national wide survey of the distribution of human parasites in China 1. Regional distribution of parasite species. Chinese Journal of Parasitology and Parasitic Diseases 12, 241247. (In Chinese.)Google Scholar
ZARRIFAR, M. R. (1997). Observations on E. multilocularis in Iran. In Archivos Internacionales de la Hidatidosis ( ed. Menezes Da Silva, A. & Nunes, J. L. ), p. 243. Lisbon, International Society of Hydatidology.
ZHANG, S. L., PENFORNIS, A., HARRAGA, S., BRESSON-HADNI, S., TIBERGHIEN, P., KERN, P. & VUITTON, D. A. (2003). Polymorphism of TAP1 and TAP2 genes in human alveolar echinococcosis. European Journal of Immunogenetics 30, 133139.CrossRefGoogle Scholar
ZHANG, Y. Z. (1997). Distribution of Mammalian Species in China. Beijing, Science Press.
ZHOU, H. X. (2001). Epidemiologie et écologie de la transmission d'Echinococcus multilocularis au Xinjiang, République Populaire de Chine: étude préliminaire. PhD Thesis, University of Franche-Comté, N°25-01-08, 190 pp.
ZHOU, H. X., CHAI, S. X., CRAIG, P. S., DELATTRE, P., QUERE, J. P., RAOUL, F., VUITTON, D. A., WEN, H. & GIRAUDOUX, P. (2000). Epidemiology of alveolar echinococcosis (AE) in northwest China: Xinjiang Uygur Autonomous Region (XUAR): a preliminary analysis. Annals of Tropical Medicine and Parasitology 94, 715729.CrossRefGoogle Scholar
ZHOU, H. X., WEN, H., WANG, Y. H., DELATTRE, P., QUERE, P., VUITTON, D. A., CRAIG, P. & GIRAUDOUX, P. (1998). Experimental susceptibility of Spermophilus erythrogenys to Echinococcus multilocularis. Annals of Tropical Medicine and Parasitology 93, 335337.CrossRefGoogle Scholar