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

  • A. ITO (a1), T. ROMIG (a2) and K. TAKAHASHI (a3)

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.

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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, 347356.

ANDREWS, P. & THOMAS, H. (1983). Praziquantel. Medical Research Review 3, 147200.

BRETAGNE, S., ASSOULINE, B., VIDAUD, D., HOUIN, R. & VIDAUD, M. (1996). Echinococcus multilocularis: microsatellite polymorphism in U1 snRNA genes. Experimental Parasitology 82, 324328.

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, 167177.

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, 60746083.

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, 115121.

FELLEISEN, R. & GOTTSTEIN, B. (1994). Echinococcus multilocularis: molecular and immunochemical characterization of diagnostic antigen II/3–10. Parasitology 107, 335342.

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, 121130.

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, 703705.

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, 39693972.

GOTTSTEIN, B. (1985). Purification and characterization of a specific antigen from Echinococcus multilocularis. Parasite Immunology 7, 201212.

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, 408412.

HEMMINGS, L. & McMANUS, D. P. (1991). The diagnostic value and molecular characterisation of an Echinococcus multilocularis antigen gene clone. Molecular and Biochemical Parasitology 44, 5662.

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, 7577.

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.

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, 57425748.

ITO, A. (2002a). Serologic and molecular diagnosis of zoonotic larval cestode infections. Parasitology International 51, 221235.

ITO, A. & CRAIG, P. S. (2003). Immunodiagnostic and molecular approaches for the detection of taeniid cestode infections. Trends in Parasitology 19, 377381.

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, 170172.

ITO, A., SAKO, Y., YAMASAKI, H., MAMUTI, W., NAKAYA, K., NAKAO, M. & ISHIKAWA, Y. (2003a). Development of Em18-immunoblot and Em18-ELISA for specific diagnosis of alveolar echinococcosis. Acta Tropica 85, 173182.

ITO, A., URBANI, C., QIU, J. M., VUITTON, D. A., QIU, D. C., HEATH, D. D., CRAIG, P. S., FENG, Z. & SCHANTZ, P. M. (2003b). Control of echinococcosis and cysticercosis: a public health challenge to international cooperation in China. Acta Tropica 86, 317.

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. (2002b). 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, 41614165.

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, 869870.

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, 343349.

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, 142149.

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, 531534.

MATHIS, A., DEPLAZES, P. & ECKERT, J. (1996). An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. Journal of Helminthology 70, 219222.

McMANUS, D. P., ZHANG, W. & BARTLEY, P. B. (2003). Echinococcosis. Lancet (in press).

NAKAO, M., SAKO, Y. & ITO, A. (2003). Isolation of polymorphic microsatellite loci from the tapeworm Echinococcus multilocularis. Infection, Genetics and Evolution 3, 159163.

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, 497509.

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, 12711278.

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, 15791588.

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, 178186.

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.

REUTER, S., KRATZER, W., KURZ, S., WELLINGHAUSEN, N. & KERN, P. (1998). Chemotherapie der alveolären Echinokokkose mit Benzimidazolen. Medizinische Klinik 93, 463467 (in German).

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, 6176.

SAITOH, T. & TAKAHASHI, K. (1998). The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes. Research in Population Ecology 40, 97105.

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, 27602765.

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, 6571.

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, 179186.

SILES-LUCAS, M. & GOTTSTEIN, B. (2001). Molecular tools for the diagnosis of cystic and alveolar echinococcosis. Tropical Medicine and International Health 6, 463475.

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, 431439.

STIEGER, C., HEGGLIN, D., SCHWARZENBACH, G., MATHIS, A. & DEPLAZES, P. (2002). Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitology 124, 631640.

STORANDT, S. T. & KAZACOS, K. R. (1993). Echinococcus multilocularis identified in Indiana, Ohio, and east-central Illinois. Journal of Parasitology 79, 301305.

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, 420422.

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, 577587.

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, 111.

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.

URAGUCHI, K. & TAKAHASHI, K. (1998). Den site selection and utilization by the red fox in Hokkaido, Japan. Mammal Study 23, 3140.

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, 33513353.

ZHANG, W., LI, J. & McMANUS, D. P. (2003). Concepts in immunology and diagnosis of hydatid disease. Clinical Microbiology Reviews 16, 1836.

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