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Perspective on control options for Echinococcus multilocularis with particular reference to Japan

Published online by Cambridge University Press:  04 March 2004

A. ITO ,
T. ROMIG  and
K. TAKAHASHI
A. ITO
Affiliation:
Department of Parasitology, Asahikawa Medical College, Asahikawa, Japan
T. ROMIG
Affiliation:
Section Infectiology, University Clinic, Ulm, Germany
K. TAKAHASHI
Affiliation:
Division of Medical Zoology, Hokkaido Institute of Public Health, Sapporo, Japan
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Abstract

Following a brief introduction of recent advances in molecular and immunological technology for detection of persons and animals infected with Echinococcus multilocularis and an overview of the current situation of alveolar echinococcosis (AE) in Japan, perspectives on control options are discussed with reference to different epidemiological situations. AE is considered the most serious parasitic zoonosis in temperate and arctic regions of the northern hemisphere. The number of human cases differs drastically among regions. While high numbers of patients are apparently associated with high E. multilocularis prevalence in domestic dogs, e.g. in parts of Alaska and western China, the number of cases is moderate or low in areas where the parasite is mainly transmitted by wild canid species (e.g. in central Europe or temperate North America). However, the severity of the disease, the absence of curative treatment for most cases, the high cost of long-term chemotherapy and the anxiety caused for the population in highly endemic areas call for the development of preventive strategies even in regions where human AE is rare. Furthermore, in view of (1) drastically increasing numbers and infection rates of foxes involved in transmission of E. multilocularis, and (2) increasingly close contact between humans and foxes e.g. in Europe and Japan, there is considerable concern that AE incidences may in future increase in these regions. Control options depend on a variety of factors including the species of canid principally responsible for transmission and the socio-economic situation in the region. Where domestic dogs (stray or owned) are the principal hosts for E. multilocularis, control options can include those applicable to E. granulosus, i.e. reduction of the number of stray dogs, registration and regular preventive chemotherapy of owned dogs, and information campaigns for the population promoting low-risk behaviour for man and dogs. Where E. multilocularis is mainly transmitted by wild canids, the situation is far more difficult with preventive strategies still being in trial stage. Integrated control measures could include prevention information campaigns, restricting access of pet animals (dogs and cats) to rodents, chemotherapy of foxes on local or regional scales, and strategies to minimize contacts between people and foxes.

Keywords

Alveolar echinococcosisEchinococcus multilocularisepidemiologycontrolJapan
Type
Research Article
Information
Parasitology , Volume 127 , Issue S1 , October 2003 , pp. S159 - S172
Copyright
© 2003 Cambridge University Press

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References

REFERENCES

ABE, H. (1975). Winter food of the red fox, Vulpes vulpes schrencki Kishida (Carnivora: Canidae), in Hokkaido, with special reference to vole populations. Applied Entomology and Zoology 10, 40–51.CrossRefGoogle Scholar
ALLAN, J. C., CRAIG, P. S., GARCIA-NOVAL, J., MENCOS, F., LIU, D., WANG, Y., WEN, H., ZHOU, P., STRINGER, R., ROGAN, M. & ZEYHLE, E. (1992). Coproantigen detection for immunodiagnosis of echinococcosis and taeniasis in dogs and humans. Parasitology 104, 347–356.CrossRefGoogle Scholar
AMBO, H., ICHIKAWA, K., IIDA, H. & ABE, N. (1954). On echinococcosis alveolaris, endemic parasitosis in Rebun Island. Special Report of Hokkaido Institute of Public Health 4, 1–19 (in Japanese).Google Scholar
ANDREWS, P. & THOMAS, H. (1983). Praziquantel. Medical Research Review 3, 147–200.CrossRefGoogle Scholar
BRESSON-HADNI, S., LAPLANTE, J. J., LENYS, D., ROHMER, P., GOTTSTEIN, B., JACQUIER, P., MERCET, P., MEYER, J. P., MIGUET, J. P. & VUITTON, D. A. (1994). Seroepidemiologic screening of Echinococcus multilocularis infection in a European area endemic for alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 51, 837–846.CrossRefGoogle Scholar
BRETAGNE, S., ASSOULINE, B., VIDAUD, D., HOUIN, R. & VIDAUD, M. (1996). Echinococcus multilocularis: microsatellite polymorphism in U1 snRNA genes. Experimental Parasitology 82, 324–328.CrossRefGoogle Scholar
CRAIG, P. S., GIRAUDOUX, P., SHI, D., BARTHOLOMOT, B., GARNISH, G., DELATTRE, P., QUÉRE, J. P., HARRAGA, S., BAO, G., WNAG, W., 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, 167–177.CrossRefGoogle Scholar
CRAIG, P. S. & PAWLOWSKI, Z. S. (2002). Cestode Zoonoses: Echinococcosis and Cysticercosis An Emergent and Global Problem. 395 pp. NATO Science Series, IOS Press, Amsterdam.
DAI, W. J., HEMPHILL, A., WALDVOGEL, A., INGOLD, K., DEPLAZES, P., MOSSMANN, H. & GOTTSTEIN, B. (2001). Major carbohydrate antigen of Echinococcus multilocularis induces an immunoglobulin G response independent of alphabeta+ CD4+ T cells. Infection and Immunity 69, 6074–6083.CrossRefGoogle Scholar
DEPLAZES, P., ALTHER, P., TANNER, I., THOMPSON, R. C. & ECKERT, J. (1999). Echinococcus multilocularis coproantigen detection by enzyme-linked immunosorbent assay in fox, dog and cat populations. Journal of Parasitology 85, 115–121.CrossRefGoogle Scholar
DINKEL, A., NICKISCH-ROSENEGK, M., BILGER, B., MERLI, M., LUCIUS, R. & ROMIG, T. (1998). Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. Journal of Clinical Microbiology 36, 1871–1876.Google Scholar
DOI, M., KANDA, E., NIHEI, N. & UCHIDA, A. (2000 a). Occurrence of alveolar hydatid disease (multilocular echinococcosis) outside of Hokkaido and a proposal for its prevention. Japanese Journal of Public Health 47, 111–126 (in Japanese with English summary).Google Scholar
DOI, M., NAKAO, M., INAOKA, T., OHNISHI, K., KUTSUMI, H., ARAKAWA, K., AMOH, K., ISHIMARU, O., SEO, H. & FUKUYAMA, Y. (1987). Epidemiology of multilocularis echinococcosis in Hokkaido (1) a sero-epidemiological study of hunters. Japanese Journal of Public Health 34, 357–365 (in Japanese with English summary).Google Scholar
DOI, M., NAKAO, M., NIHEI, N. & KUTSUMI, H. (2000 b). Epidemiology of alveolar hydatid disease (AHD) and estimation of infected period of AHD in Rebun Island, Hokkaido. Japanese Journal of Public Health 47, 145–152 (in Japanese with English summary).Google Scholar
ECKERT, J., GEMMELL, M. A., MESLIN, F.-X. & PAWLOWSKI, Z. S. (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. Office International des Epizooties, Paris, 265 pp.
FELLEISEN, R. & GOTTSTEIN, B. (1994). Echinococcus multilocularis: molecular and immunochemical characterization of diagnostic antigen II/3–10. Parasitology 107, 335–342.Google Scholar
FROSCH, P. M., FROSCH, M., PFISTER, T., SCHAAD, V. & BITTER-SUERMANN, D. (1991). Cloning and characterization of an immunodominant major surface antigen of Echinococcus multilocularis. Molecular and Biochemical Parasitology 48, 121–130.CrossRefGoogle Scholar
FROSCH, P. M., MUHLSCHEGEL, F., SYGULLA, L., HARTMANN, M. & FROSCH, M. (1994). Identification of a cDNA clone from the larval stage of Echinococcus granulosus with homologies to the E. multilocularis antigen EM10-expressing cDNA clone. Parasitology Research 80, 703–705.Google Scholar
FURUYA, K., SASAKI, S., HONMA, H., KUMAGAI, M., SATO, N., TAKAHASHI, M. & UCHINO, J. (1989). Serologic investigations of human alveolar hydatid disease by western blotting and indirect histo-immunoperoxidase techniques. Japanese Journal of Parasitology 38, 184–193.Google Scholar
GAUCI, C., MERLI, M., MULLER, V., CHOW, C., YAGI, K., MACKENSTEDT, U. & LIGHTOWLERS, M. W. (2002). Molecular cloning of a vaccine antigen against infection with the larval stage of Echinococcus multilocularis. Infection and Immunity 70, 3969–3972.CrossRefGoogle Scholar
GIRAUDOUX, P., DELATTRE, P., TAKAHASHI, K., RAOUL, F., QUÉRE, 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. 251–262. NATO Science Series, IOS Press, Amsterdam.
GOTTSTEIN, B. (1985). Purification and characterization of a specific antigen from Echinococcus multilocularis. Parasite Immunology 7, 201–212.CrossRefGoogle Scholar
GOTTSTEIN, B., JACQUIER, P., BRESSON HADNI, S. & ECKERT, J. (1993). Improved primary immunodiagnosis of alveolar echinococcosis in humans by an enzyme-linked immunosorbent assay using Em2plus antigen. Journal of Clinical Microbiology 31, 373–376.Google Scholar
GOTTSTEIN, B., SAUCY, F., DEPLAZES, P., REICHEN, J., DEMIERRE, G., BUSATO, A., ZUERCHER, C. & PUGIN, P. (2001). Is high prevalence of Echinococcus multilocularis in wild and domestic animals associated with disease incidence in humans? Emerging Infectious Diseases 7, 408–412.Google Scholar
HANSEN, F., TACKMANN, K., JELTSCH, F., STAUBACH, C. & THULKE, H. H. (2001). If space changes all – the small-scale epidemiology of the fox tapeworm. Proceedings, SVEPM conference, pp. 73–85. Nordwijkerhout.
HATAKEYAMA, Y., SATO, N., OYAMA, Y., INOUE, N., TAKENOSITA, S., TAKEUCHI, S. & ITO, A. (2002). A surgical case report of hepatic cystic echinococcosis. Shujutsu 56, 819–823 (in Japanese).Google Scholar
HELBIG, M., FROSCH, P., KERN, P. & FRSOCH, M. (1993). Serological differentiation between cystic and alveolar echinococcosis by use of recombinant larval antigens. Journal of Clinical Microbiology 31, 3211–3215.Google Scholar
HEMMINGS, L. & McMANUS, D. P. (1991). The diagnostic value and molecular characterisation of an Echinococcus multilocularis antigen gene clone. Molecular and Biochemical Parasitology 44, 56–62.CrossRefGoogle Scholar
HILDRETH, M. B., JOHNSON, M. D. & KAZACOS, K. R. (1991). Echinococcus multilocularis: A zoonosis of increasing concern in the United States. Compendium on Continuing Education for the Practising Veterinarian 13, 727–740.Google Scholar
HILDRETH, M. B., SRIRAM, S., GOTTSTEIN, B., WILSON, M. & SCHANTZ, P. M. (2000). Failure to identify alveolar echinococcosis in trappers from South Dakota in spite of high prevalence of Echinococcus multilocularis in wild canids. Journal of Parasitology 86, 75–77.CrossRefGoogle 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, 135–142.CrossRefGoogle Scholar
HULSMEIER, A. J., GEHRIG, P. M., GEYER, R., SACK, P., GOTTSTEIN, B., DEPLAZES, P. & KOHLER, P. (2002). A major Echinococcus multilocularis antigen is a mucin-type glycoprotein. Journal of Biological Chemistry 277, 5742–5748.CrossRefGoogle Scholar
INAOKA, T., NAKAO, M., OHNISHI, K., DOI, M. & KUTSUMI, H. (1987). Epidemiological survey of multilocularis echinococcosis intended for tanners and taxidermists in Hokkaido, Japan. Journal of Northern Occupational Health 36, 9–12 (in Japanese with English summary).Google Scholar
ISHIGE, M. (1984). Incidence of swine multilocular echinococcosis in Hokkaido. Report of the Hokkaido Institute of Public Health 34, 70–71 (in Japanese).Google Scholar
ITO, A. (2001 a). Introduction of ongoing research projects on echinococcosis at Asahikawa Medical College and some comments on the surveillance, prevention and control of alveolar echinococcosis in Japan. Hokkaido Journal of Medical Science 76, 3–8 (in Japanese with English summary).Google Scholar
ITO, A. (2001 b). Problems on echinococcosis. Asahikawa Medical Forum 2, 13–19 (in Japanese with English summary).Google Scholar
ITO, A. (2002 a). Serologic and molecular diagnosis of zoonotic larval cestode infections. Parasitology International 51, 221–235.Google Scholar
ITO, A. (2002 b). Up-to-date situation and problems of cysticercosis and echinococcosis in the world as emerging and re-emerging parasitic diseases. Japanese Journal of Clinical Environment 10, 59–66 (in Japanese with English summary).Google Scholar
ITO, A. & CRAIG, P. S. (2003). Immunodiagnostic and molecular approaches for the detection of taeniid cestode infections. Trends in Parasitology 19, 377–381.CrossRefGoogle Scholar
ITO, A., MA, L., SCHANTZ, P. M., GOTTSTEIN, B., LIU, Y. H., CHAI, J. J., ABDEL-HAFEZ, S. K., ALTINTAS, N., JOSHI, D. D., LIGHTOWLERS, M. W. & PAWLOWSKI, Z. S. (1999). Differential serodiagnosis for cystic and alveolar echinococcosis using fractions of Echinococcus granulosus cyst fluid (antigen B) and E. multilocularis protoscolex (Em18). American Journal of Tropical Medicine and Hygiene 60, 188–192.CrossRefGoogle Scholar
ITO, A., NAKAO, M., KUTSUMI, H., LIGHTOWLERS, M. W., ITOH, M. & SATO, S. (1993). Serodiagnosis of alveolar hydatid disease by western blotting. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 170–172.CrossRefGoogle Scholar
ITO, A., SAKO, Y., ISHIKAWA, Y., NAKAO, M., NAKAYA, K. & YAMASAKI, H. (2002 a). Differential serodiagnosis for alveolar echinococcosis by Em18-immunoblot and Em18-ELISA in Japan and China. In Cestode Zoonoses: Echinococcosis and Cysticercosis – An Emergent and Global Problem ( ed. Craig, P. S. & Pawlowski, Z. ), pp. 147–155. NATO Science Series, IOS Press, Amsterdam.
ITO, A., SAKO, Y., YAMASAKI, H., MAMUTI, W., NAKAYA, K., NAKAO, M. & ISHIKAWA, Y. (2003 a). Development of Em18-immunoblot and Em18-ELISA for specific diagnosis of alveolar echinococcosis. Acta Tropica 85, 173–182.Google Scholar
ITO, A., SCHANTZ, P. M. & WILSON, J. F. (1995). Em18, a new serodiagnostic marker for differentiation of active and inactive cases of alveolar hydatid disease. American Journal of Tropical Medicine and Hygiene 52, 41–44.CrossRefGoogle Scholar
ITO, A., URBANI, C., QIU, J. M., VUITTON, D. A., QIU, D. C., HEATH, D. D., CRAIG, P. S., FENG, Z. & SCHANTZ, P. M. (2003 b). Control of echinococcosis and cysticercosis: a public health challenge to international cooperation in China. Acta Tropica 86, 3–17.Google Scholar
ITO, A., XIAO, N., LIANCE, M., SATO, M. O., SAKO, Y., MAMUTAI, W., ISHIKAWA, Y., NAKAO, M., YAMASAKI, H., NAKAYA, K., BARDONNET, K., BRESSOPN-HADNI, S. & VUITTON, D. A. (2002 b). Evaluation of an enzyme-linked immunosorbent assay (ELISA) with affinity-purified Em18 and an ELISA with recombinant Em18 for differential diagnosis of alveolar echinococcosis: results of a blind test. Journal of Clinical Microbiology 40, 4161–4165.Google Scholar
KAJI, Y., TANIYAMA, H., MATSUKAWA, K., OKADA, H., TSUNODA, S., TAGAMI, M. & AKITA, H. (1993). First incidence of multilocular echinococcosis in a race horse in Japan. Japanese Journal of Veterinary Medical Science 55, 869–870.CrossRefGoogle Scholar
KAMIYA, H. & KANAZAWA, T. (1999). The first detection of Echinococcus infection among pigs on the main island of Japan, August 1998 – Aomori. Infectious Agents Surveillance Report 20, 248–249 (in Japanese).Google Scholar
KERN, P., BARDONNET, K., RENNER, E., AUER, H., PAWLOWSKI, Z., AMMANN, R. W., VUITTON, D. A., KERN, P. & EUROPEAN ECHINOCOCCOSIS REGISTRY (2003). European echinococcosis registry: human alveolar echinococcosis, Europe, 1982–2000. Emerging Infectious Diseases 9, 343–349.CrossRefGoogle Scholar
KONDO, N., TAKAHASHI, K. & YAGI, K. (1986). Winter food of the red fox, Vulpes vulpes schrencki Kishida in the endemic area of multilocular echinococcosis. The Bulletin of Preparative Office of Nemuro Municipal Museum 1, 23–31 (in Japanese with English summary).Google Scholar
KOSUGE, M. & BANDO, G. (2003). A case report of alveolar echinococcosis of a Gorilla at Asahikawa Zoo and strategy for prevention of accidental infection of zoo animals and visitors from wild foxes. Japan Veterinary Medical Association 56, 46–51 (in Japanese).Google Scholar
LAWTON, P., HEMPHILL, A., DEPLAZES, P., GOTTSTEIN, B. & SARCIRON, M. E. (1997). Echinococcus multilocularis metacestodes: immunological and immunocytochemical analysis of the relationships between alkaline Phosphatase and the Em2 antigen. Experimental Parasitology 87, 142–149.CrossRefGoogle Scholar
LIGHTOWLERS, M. W., JENSEN, O., FERNANDEZ, E., IRIATE, J. A., WOOLARD, D. J., GAUCI, C. G., JENKINS, D. J. & HEATH, D. D. (1999). Vaccination trials in Australia and Argentina confirm the effectiveness of the EG95 hydatid vaccine in sheep. International Journal for Parasitology 29, 531–534.CrossRefGoogle Scholar
MATHIS, A., DEPLAZES, P. & ECKERT, J. (1996). An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. Journal of Helminthology 70, 219–222.CrossRefGoogle Scholar
McMANUS, D. P., ZHANG, W. & BARTLEY, P. B. (2003). Echinococcosis. Lancet (in press).CrossRefGoogle Scholar
MINAGAWA, N. (1997). Survey of echinococcosis in Hokkaido and measure against it. Hokkaido Journal of Medical Science 72, 569–581 (in Japanese with English summary).Google Scholar
MINAGAWA, N. (1999). The reconsideration of natural history of echinococcosis on Rebun Island. Hokkaido Journal of Medical Science 74, 113–134 (in Japanese with English summary).Google Scholar
MIYAUCHI, T., SAKUI, M., ISHIGE, M., FUKUMOTO, S., UEDA, A. & OHBAYASHI, M. (1984). A case of multilocular echinococcosis in a horse. Japanese Journal of Veterinary Research 32, 171–173.Google Scholar
NAKAO, M., INAOKA, T., DOI, M., KUTSUMI, H., ARAKAWA, K. & OHNISHI, K. (1988). Epidemiology of multilocular echinococcosis in Hokkaido (2) Seroepidemiological survey of residents in hog raising areas in Asahikawa city. Japanese Journal of Public Health 35, 184–192 (in Japanese with English summary).Google Scholar
NAKAO, M., SAKO, Y. & ITO, A. (2003). Isolation of polymorphic microsatellite loci from the tapeworm Echinococcus multilocularis. Infection, Genetics and Evolution 3, 159–163.CrossRefGoogle Scholar
NAKAO, M., YOKOYAMA, N., SAKO, Y., FUKUNAGA, M. & ITO, A. (2002). The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae). Mitochondrion 1, 497–509.CrossRefGoogle Scholar
NATIONAL INSTITUTE OF INFECTIOUS DISEASES AND TUBERCULOSIS AND INFECTIOUS DISEASES CONTROL DIVISION, MINISTRY OF HEALTH, LABOUR AND WELFARE (1999). Multilocular echinococcosis in Hokkaido, Japan. Infectious Agents Surveillance Report 20, 1′–2′.
NONAKA, N., IIDA, M., YAGI, K., ITO, T., OOI, H. K., OKU, Y. & KAMIYA, M. (1996). Time course of coproantigen excretion in Echinococcus multilocularis infection in foxes and alternative host, golden hamsters. International Journal for Parasitology 26, 1271–1278.CrossRefGoogle Scholar
OHBAYASHI, M. (1996). Host animals of Echinococcus multilocularis in Hokkaido. In Alveolar Echinococcosis: Strategy for Eradication of Alveolar Echinococcosis of the Liver (ed. Uchino, J. & Sato, N. ), pp. 59–64. Sapporo, Fujishoin.
PAWLOWSKI, Z. S., ECKERT, J., VUITTON, D. A., AMMANN, R. W., KEMP, P., CRAIG, P. S., DAR, K. F., DE ROSA, F., FILICE, C., GOTTSTEIN, B., GRIMM, F., MACPHERSON, C. N. L., SATO, N., TODOROV, T., UCHINO, J., VON SINNER, W. & WEN, H. (2001). Chapter 2 Echinococcosis in humans: clinical aspects, diagnosis and treatment. 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.-X. & Pawlowski, Z. S. ), pp. 20–66. Paris, Office International des Epizooties.
RAOUL, F., DEPLAZES, P., NONAKA, N., PIARROUX, R., VUITTON, D. A. & 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, 1579–1588.CrossRefGoogle Scholar
RAUSCH, R. L. (1954). Studies on the helminth fauna of Alaska. XX. The histogenesis of the alveolar larva of Echinococcus species. Journal of Infectious Diseases 94, 178–186.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. 88–134. Wallingford, CAB International.
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, 239–250.CrossRefGoogle Scholar
REUTER, S., KRATZER, W., KURZ, S., WELLINGHAUSEN, N. & KERN, P. (1998). Chemotherapie der alveolären Echinokokkose mit Benzimidazolen. Medizinische Klinik 93, 463–467 (in German).CrossRefGoogle Scholar
ROMIG, T. (2002). Spread of Echinococcus multilocularis in Europe? In Cestode Zoonoses: Echinococcosis and Cysticercosis – An Emergent and Global Problem (ed. Craig, P. & Pawlowski, Z. ), pp. 65–80. NATO Science Series, Amsterdam, IOS Press.
ROMIG, T., BILGER, B., DINKEL, A., MERLI, M. & MACKENSTEDT, U. (1999 a). Echinococcus multilocularis in animal hosts: new data from western Europe. Helminthologia 36, 185–191.Google Scholar
ROMIG, T., BILGER, B., MERLI, M., DINKEL, A., LUCIUS, R. & MACKENSTEDT, U. (1999 c). Bekämpfung von Echinococcus multilocularis in einem Hochendemiegebiet Süddeutschlands. In Neuere Methoden und Ergebnisse zur Epidemiologie von Parasitosen, pp. 172–183. Giessen, Deutsche Veterinärmedizinische Gesellschaft (in German).
ROMIG, T., KRATZER, W., KIMMIG, P., FROSCH, M., GAUS, W., FLEGEL, W. A., GOTTSTEIN, B., LUCIUS, R., BECKH, K. & KERN, P. (1999 b). An epidemiologic survey of human alveolar echinococcosis in southwestern Germany. American Journal of Tropical Medicine and Hygiene 61, 566–573.Google Scholar
SAITOH, T., STENSETH, N. C. & BJORNSTAD, O. N. (1998). The population dynamics of the vole Clethrionomys rufocanus in Hokkaido, Japan. Research in Population Ecology 40, 61–76.CrossRefGoogle Scholar
SAITOH, T. & TAKAHASHI, K. (1998). The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes. Research in Population Ecology 40, 97–105.CrossRefGoogle Scholar
SAKO, Y., NAKAO, M., NAKAYA, K., YAMASAKI, H., GOTTSTEIN, B., LIGHTOWLERS, M. W., SCHANTZ, P. M. & ITO, A. (2002). Alveolar echinococcosis: characterization of diagnostic antigen Em18 and serological evaluation of recombinant Em18. Journal of Clinical Microbiology 40, 2760–2765.CrossRefGoogle Scholar
SAKUI, M., ISHIGE, M., FUKUMOTO, S., UEDA, A. & OHBAYASHI, M. (1984). Spontaneous Echinococcus multilocularis infection in swine in north-eastern Hokkaido, Japan. Japanese Journal of Parasitology 33, 291–296.Google Scholar
SATO, C. & FURUYA, K. (1994). Isolation and characterization of a diagnostic polysaccharide antigen from larval Echinococcus multilocularis. Japanese Journal of Medical Science and Biology 47, 65–71.CrossRefGoogle Scholar
SATO, C., NAGANO, H. & FURUYA, K. (1996). A polysaccharide antigen diagnostic in human alveolar hydatid disease. In Alveolar Echinococcosis: Strategy for Eradication of Alveolar Echinococcosis of the Liver ( ed. Uchino, J. & Sato, N. ), pp. 129–134. Sapporo, Fujishoin.
SATO, H., MITAMURA, H., ARAI, J. & KUMAGAI, M. (1983). Serological diagnosis of human hydatid disease by enzyme-linked immunosorbent assay (part 1) enzyme-linked immunosorbent assay by multilocular echinococcus antigen. Report of the Hokkaido Institute of Public Health 33, 8–15 (in Japanese with English summary).Google Scholar
SATO, N., OGASAWARA, K., KAMIYAMA, T., MATSUSHITA, M. & TODO, S. (2003). Echinococcosis. Nippon Rinsho 61 (Suppl. 2), 636–643 (in Japanese).Google Scholar
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. 233–331. Wallingford, CAB International.
SCHELLING, U., FRANK, W., WILL, R., ROMIG, T. & LUCIUS, R. (1997). Chemotherapy with praziquantel has the potential to reduce the prevalence of Echinococcus multilocularis in wild foxes (Vulpes vulpes). Annals of Tropical Medicine and Parasitology 91, 179–186.CrossRefGoogle Scholar
SILES-LUCAS, M. & GOTTSTEIN, B. (2001). Molecular tools for the diagnosis of cystic and alveolar echinococcosis. Tropical Medicine and International Health 6, 463–475.CrossRefGoogle Scholar
SILES-LUCAS, M., MERLI, M., MACKENSTEDT, U. & GOTTSTEIN, B. (2003). The Echinococcus multilocularis 14-3-3 protein protects mice against primary but not secondary alveolar echinococcosis. Vaccine 21, 431–439.CrossRefGoogle Scholar
STIEGER, C., HEGGLIN, D., SCHWARZENBACH, G., MATHIS, A. & DEPLAZES, P. (2002). Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitology 124, 631–640.CrossRefGoogle Scholar
STORANDT, S. T. & KAZACOS, K. R. (1993). Echinococcus multilocularis identified in Indiana, Ohio, and east-central Illinois. Journal of Parasitology 79, 301–305.CrossRefGoogle Scholar
STORANDT, S. T., VIRCHOW, D. R., DRYDEN, M. W., HUGNSTOROM, S. E. & KAZACOS, K. R. (2002). Distribution and prevalence of Echinococcus multilocularis in wild predators in Nebraska, Kansas, and Wyoming. Journal of Parasitology 88, 420–422.CrossRefGoogle Scholar
SUZUKI, K., UCHINO, J., SATO, N. & TAKAHASHI, H. (1996). Development and efficacy of mass screening of alveolar echinococcosis in Hokkaido. In Alveolar Echinococcosis: Strategy for Eradication of Alveolar Echinococcosis of the Liver (ed. Uchino, J. & Sato, N. ), pp. 213–217. Sapporo, Fujishoin.
TACKMANN, K., LÖSCHNER, U., MIX, H., STAUBACH, C., THULKE, H.-H., ZILLER, M. & CONRATHS, F. J. (2001). A field study to control Echinococcus multilocularis-infections of the red fox (Vulpes vulpes) in an endemic focus. Epidemiology and Infection 127, 577–587.CrossRefGoogle Scholar
TAKAHASHI, K. & MORI, C. (2001). Host animals and prevalence of Echinococcus multilocularis in Hokkaido. Public Health in Hokkaido 27, 73–80 (in Japanese).Google Scholar
TAKAHASHI, K. & URAGUCHI, K. (1996). Ecological factors influencing prevalence of larval E. multilocularis in vole. In Alveolar Echinococcosis: Strategy for Eradication of Alveolar Echinococcosis of the Liver (ed. Uchino, J. & Sato, N. ), pp. 75–77. Sapporo, Fujishoin.
TAKAHASHI, K., URAGUCHI, K., ROMIG, T., HATAKEYAMA, H. & TAMURA, M. (2002). Preliminary report on Echinococcus multilocularis control by fox baiting with praziquantel. Report of the Hokkaido Institute of Public Health 52, 61–63 (in Japanese).Google Scholar
TAKAHASHI, K., URAGUCHI, K. & YAGI, K. (1999). Prevalence of Echinococcus multilocularis in animals in Hokkaido. Alveolar Echinococcosis in Hokkaido – a Fiftieth-anniversary Publication – Hokkaido Institute of Public Health, pp. 24–38 (in Japanese).
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, 5–9 (in Japanese with English summary).Google Scholar
TAKAHASHI, A., YAMAGUCHI, T. & INABA, T. (1986). A review of multilocularis echinococcosis cases reported from Honshu, Japan, during a period from 1926 to 1984. Japanese Journal of Parasitology 35, 95–107 (in Japanese with English summary).Google Scholar
TANIYAMA, H., MORIMITSU, Y., FUKUMOTO, S., ASAKAWA, M. & 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. & Sato, N. ), pp. 65–67. Sapporo, Fujishoin.
TSUKADA, H., HAMAZAKI, K., GANZORIG, S., IWAKI, T., KONNO, K., LAGAPA, J. T., MATSUO, K., ONO, A., SHIMIZU, M., SAKAI, H., MORISHIMA, Y., NONAKA, N., OKU, Y. & KAMIYA, M. (2002). Potential remedy against Echinococcus multilocularis in wild red foxes using baits with anthelmintic distributed around fox breeding dens in Hokkaido, Japan. Parasitology 125, 1–11.CrossRefGoogle 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, 423–428.CrossRefGoogle Scholar
URAGUCHI, K. & TAKAHASHI, K. (1998). Den site selection and utilization by the red fox in Hokkaido, Japan. Mammal Study 23, 31–40.CrossRefGoogle Scholar
URAGUCHI, K. & TAKAHASHI, K. (1999). Ecology of the red fox in Hokkaido. Alveolar Echinococcosis in Hokkaido – A Fiftieth-Anniversary Publication – Hokkaido Institute of Public Health, pp. 39–48 (in Japanese).
VOGEL, H. (1957). Studies on the Echinococcus multilocularis of South Germany. I. The tapeworm stage of strains of human and animal origin. Zeitschrift für Tropenmedizin und Parasitologie 8, 404–456 (in German).Google Scholar
XIAO, N., MAMUTI, W., YAMASAKI, H., SAKO, Y., NAKAO, M., NAKAYA, K., GOTTSTEIN, B., SCHANTZ, P. M., LIGHTOWLERS, M. W., CRAIG, P. S. & ITO, A. (2003). Evaluation of recombinant Em18 and affinity-purified Em18 for serological differentiation of alveolar echinococcosis from cystic echinococcosis and other parasitic infections. Journal of Clinical Microbiology 41, 3351–3353.CrossRefGoogle Scholar
YAGI, K., TAKAHASHI, K. & HATTORI, K. (1984). A case of immature Echinococcus multilocularis in a domestic cat in Nemuro, eastern Hokkaido, Japan. Report of the Hokkaido Institute of Public Health 34, 68–69 (in Japanese).Google Scholar
YAMASHITA, J. (1978). Echinococcus. Sapporo, Hokkaido University Press, 246 pp. (in Japanese).
YIMAM, A. E., NONAKA, N., OKU, Y. & KAMIYA, M. (2002). Prevalence and intensity of Echinococcus multilocularis in red foxes (Vulpes vulpes schrencki) and raccoon dogs (Nyctereutes procyonoides albus) in Otaru city, Hokkaido, Japan. Japanese Journal of Veterinary Research 49, 287–296.Google Scholar
YOSHIMURA, K. (2000). A confirmation of fascioliasis for a case reported as echinococcosis in October 1999 – Akita. Infectious Agents Surveillance Report 21, 170–171 (in Japanese).Google Scholar
ZHANG, W., LI, J. & McMANUS, D. P. (2003). Concepts in immunology and diagnosis of hydatid disease. Clinical Microbiology Reviews 16, 18–36.CrossRefGoogle Scholar