Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T09:32:02.416Z Has data issue: false hasContentIssue false
  • English
  • Français

Echinococcosis: disease, detection and transmission

Published online by Cambridge University Press:  04 March 2004

P. S. CRAIG ,
M. T. ROGAN  and
M. CAMPOS-PONCE
P. S. CRAIG
Affiliation:
Cestode Zoonoses Research Group, Bioscience Research Institute and School of Environment and Life Sciences, University of Salford, Salford, M54WT, UK
M. T. ROGAN
Affiliation:
Cestode Zoonoses Research Group, Bioscience Research Institute and School of Environment and Life Sciences, University of Salford, Salford, M54WT, UK
M. CAMPOS-PONCE
Affiliation:
Cestode Zoonoses Research Group, Bioscience Research Institute and School of Environment and Life Sciences, University of Salford, Salford, M54WT, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Echinococcosis is one of the world's most geographically widespread parasitic zoonoses, with transmission occurring in tropical, temperate and arctic biomes. Most human infections are due to Echinococcus granulosus transmitted between domestic dogs and livestock, but this cosmopolitan species also cycles between wild carnivores (principally canids) and wild ungulates. The other species with significant zoonotic potential is E. multilocularis that occurs naturally in fox definitive hosts and small mammal intermediate hosts. These two species cause human cystic or alveolar echinococcosis respectively, which may be considered serious public health problems in several regions including developed countries. This review provides an introductory overview to the Supplement and summarises the biology and epidemiology of these two related cestodes with an emphasis on applied aspects relating to detection, diagnosis and surveillance in animal and human populations, and includes aspects of transmission ecology, and also considers aspects of community epidemiology and potential for control.

Keywords

Echinococcus granulosusE. multilocularisdiagnosisepidemiologytransmission
Type
Research Article
Information
Parasitology , Volume 127 , Issue S1 , October 2003 , pp. S5 - S20
Copyright
© 2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ABBASI, I., BRANZBURG, A., CAMPOS-PONCE, M., ABDEL-HAFEZ, S. K., RAOUL, F., CRAIG, P. S. & HAMBURGER, J. (2003). Coprodiagnosis of Echinococcus granulosus infection in dogs by amplification of a newly identified repeated DNA sequence. American Journal of Tropical Medicine and Hygiene 69, 324–330.Google Scholar
ALLAN, J. C., CRAIG, P. S., GARCIA NOVAL, J., MENCOS, F., LIU, D., WANG, Y., WEN, H., ZHOU, P., STRINGER, R., ROGAN, M. T. & ZEYHLE, E. (1992). Coproantigen detection for immunodiagnosis of echinococcosis and taeniasis in dogs and humans. Parasitology 104, 347–356.CrossRefGoogle Scholar
BARONET, D., WALTNER-TOEWS, D., CRAIG, P. S. & JOSHI, D. D. (1994). Echinococcus granulosus infections in the dogs of Kathmandu, Nepal. Annals of Tropical Medicine and Parasitology 88, 485–492.CrossRefGoogle Scholar
BARTHOLOMOT, B., VUITTON, D. A., HARRAGA, S., SHI, D., GIRAUDOUX, P., BARNISH, G., WANG, Y. H., MacPHERSON, C. N. L. & CRAIG, P. S. (2002). Combined ultrasound and serologic screening for hepatic alveolar echinococcosis in central China. American Journal of Tropical Medicine and Hygiene 66, 23–29.CrossRefGoogle Scholar
BCHIR, A., LAROUZE, B., SOLTAMI, M. A., HAMDI, A., BOUHAOUALA, H., DUCI, S., BOUDEN, L., GANOVNI, A., ACHOUR, A., GANDEBOUT, C., ROUSSET, J. J. & JEMALI, M. (1991). Echotomographic and serological population based study of hydatidosis in central Tunisia. Acta Tropica 49, 149–153.CrossRefGoogle Scholar
BELDING, D. L. (1965). Textbook of Parasitology. New York: Appleton-Century-Crofts.
BERKE, O. (2001). Choropleth mapping of regional count data of Echinococcus multilocularis among red foxes in Lower Saxony, Germany. Preventative Veterinary Medicine 52, 119–131.CrossRefGoogle Scholar
BOWLES, J., BLAIR, D. B. & McMANUS, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 169–174.CrossRefGoogle Scholar
BRETAGNE, S., GUILLOI, J. P., MORAND, M. & HOUIN, R. T. (1993). Detection of Echinococcus multilocularis DNA in fox faeces using DNA amplification. Parasitology 106, 193–199.CrossRefGoogle Scholar
CABRERA, M., CANOVA, S., ROSENZVIT, M. & GUARENA, E. (2002). Identification of Echinococcus granulosus eggs. Diagnostic Microbiology and Infectious Diseases 44, 29–34.CrossRefGoogle Scholar
CABRERA, P. A., HARAN, G., BENAVIDEZ, V., VALLEDOR, S., PERERA, G., LLOYD, S., GEMMELL, M. A., BARAIBAR, M., MORANA, A., MAISSONAVE, J. & CARBALLO, M. (1995). Transmission dynamics of Echinococcus granulosus, Taenia hydatigena and Taenia ovis in sheep in Uruguay. International Journal for Parasitology 25, 807–813.CrossRefGoogle Scholar
CHENG, T. C. (1981). General Parasitology. Orlando, Florida: Academic Press.
CHRISTOFI, G., DEPLAZES, P., CHRISTOFI, N., TANNER, I., ECONOMIDES, P. & ECKERT, J. (2002). Screening of dogs for Echinococcus granulosus coproantigen in a low endemic situation in Cyprus. Veterinary Parasitology 104, 299–306.CrossRefGoogle Scholar
COHEN, H., PAOLILLO, E., BONIFACINO, R., BOTTA, B., PARADA, L., CABRERA, P., SNOWDEN, K., GASSER, R., TESSIER, R., DIBARBOURE, L., WEN, H., ALLAN, J. C., SOTO DE ALFARO, H., ROGAN, M. T. & CRAIG, P. S. (1998). Human cystic echinococcosis in a Uruguayan community: a sonographic, serologic, and epidemiological study. American Journal of Tropical Medicine and Hygiene 59, 620–627.CrossRefGoogle Scholar
COMBES, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. Chicago, The University of Chicago Press.
CRAIG, P. S., BAILEY, W. & NELSON, G. S. (1986). A specific test for the identification of cyst fluid samples from suspected human hydatid infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 256–257.CrossRefGoogle Scholar
CRAIG, P. S., GASSER, R. B., PARADA, L., CABRERA, P., PARIETTI, S., BORGUES, C., ACUTTIS, A., GULLA, J., SNOWDEN, K. & PAOLILLO, E. (1995). Diagnosis of canine echinococcosis: comparison of coproantigen and serum antibody tests with arecoline purgation in Uruguay. Veterinary Parasitology 56, 293–301.CrossRefGoogle Scholar
CRAIG, P. S., GIRAUDOUX, P., SHI, D., BARTHOLOMOT, B., BARNISH, G., DELATTRE, P., QUERE, J. P., HARRAGA, S., BAO, G., WANG, Y., 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., LIU, D., MACPHERSON, C. N. L., SHI, D., REYNOLDS, D., BARNISH, G., GOTTSTEIN, B. & WANG, Z. (1992). A large focus of alveolar echinococcosis in central China. Lancet 340, 826–831.CrossRefGoogle Scholar
CRAIG, P. S., MACPHERSON, C. N. L., WATSON-JONES, D. L. & NELSON, G. S. (1988). Immunodetection of Echinococcus eggs from naturally infected dogs and from environmental contamination sites in settlements in Turkana, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 268–274.CrossRefGoogle Scholar
CRAIG, P. S., ROGAN, M. T. & ALLAN, J. C. (1996). Detection, screening and community epidemiology of taeniid cestode zoonoses in cystic echinococcosis, alveolar echinococcosis and neurocysticercosis. Advances in Parasitology 38, 169–250.CrossRefGoogle Scholar
DAEKI, A., CRAIG, P. S. & SHAMBESH, M. K. (2000). IgG-subclass antibody responses and the natural history of hepatic cystic echinococcosis in asymptomatic patients. Annals of Tropical Medicine and Parasitology 94, 319–328.CrossRefGoogle Scholar
D'ALESSANDRO, A. (1997). Polycystic echinococcosis in tropical America: Echinococcus vogeli and E. oligarthrus. Acta Tropica 67, 43–65.CrossRefGoogle Scholar
DANSON, F. M., CRAIG, P. S., MAN, W., SHI, D., PLEYDELL, D. R. J. & GIRAUDOUX, P. (2002). Satellite remote sensing and geographical information systems for risk modelling of alveolar echinococcosis. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem ( ed. Craig, P. S. & Pawlowski, Z.), pp. 237–248. Nato Science Series, Vol. 341, Amsterdam, IOS Press.
DEPLAZES, P., ALTHER, P., TANNER, I., THOMPSON, R. C. A. & 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
DEPLAZES, P. & ECKERT, J. (1996). Diagnosis of the Echinococcus multilocularis infection in final hosts. Applied Parasitology 37, 245–252.Google Scholar
DEPLAZES, P., GOTTSTEIN, B., ECKERT, J., EWALD, D., JENKINS, D. J., JIMENEZ-PALACIOS, S. & EWALD, D. (1992). Detection of Echinococcus coproantigens by enzyme-linked immunosorbent assay in dogs, dingoes and foxes. Parasitology Research 78, 303–308.CrossRefGoogle Scholar
DEPLAZES, P., JIMENEZ-PALACIOS, S., GOTTSTEIN, B., SKAGGS, J. & ECKERT, J. (1994). Detection of Echinococcus coproantigens in stray dogs of Northern Spain. Applied Parasitology 35, 297–301.Google Scholar
DE RYCKE, P. H. & PENNOIT-DE COOMAN, E. (1978). Serial passages of larval Echinococcus granulosus from equine origin in mice. Zeitschrift für Parasitenkunde 57, 251–254.CrossRefGoogle Scholar
DEW, H. R. (1927). Observations on the encysted stage of Taenia echinococcus. Medical Journal of Australia 2, 497.Google Scholar
DINKEL, A., VON 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
DOWLING, P. M., ABO-SHEHADA, M. N. & TORGERSON, P. R. (2000). Risk factors associated with human cystic echinococcosis in Jordan; results of a case-control study. Annals of Tropical Medicine and Parasitology 94, 69–75.CrossRefGoogle Scholar
EL-ON, J. & HOIDA, G. (2002). Echinococcosis/hydatidosis in Israel: A disease of ethnic behaviour. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 57–64. Nato Science Series, Vol. 341, Amsterdam, IOS Press.
EL-SHEHABI, F. S., KAMHAWI, S. A., SCHANTZ, P. M., CRAIG, P. S. & ABDEL-HAFEZ, S. K. (2000). Diagnosis of canine echinococcosis: comparison of coproantigen detection with necropsy in stray dogs and red foxes from northern Jordan. Parasite 7, 83–90.CrossRefGoogle Scholar
FRENCH, C. M. & NELSON, G. S. (1982). Hydatid disease in the Turkana District of Kenya, II. A study in medical geography. Annals of Tropical Medicine and Parasitology 76, 425–437.CrossRefGoogle Scholar
FRENCH, C. M., NELSON, G. S. & WOOD, M. (1982). Hydatid disease in Turkana Districk of Kenya, I. The background to the problem with hypotheses to account for the remarkably high prevalence of the disease in man. Annals of Tropical Medicine and Parasitology 76, 425–437.Google Scholar
GASSER, R. B., JENKINS, D. J., PAOLILLO, E., PARADA, L., CABRERA, P. & CRAIG, P. S. (1993). Serum antibodies in canine echinococcosis. International Journal for Parasitology 23, 579–586.CrossRefGoogle Scholar
GASSER, R. B., LIGHTOWLERS, M. W., OBENDORF, D. L., JENKINS, D. J. & RICKARD, M. D. (1988). Evaluation of a serological test system for the diagnosis of natural Echinococcus granulosus infection in dogs using E. granulosus protoscolex and oncosphere antigens. Australian Veterinary Journal 65, 369–373.Google Scholar
GEMMELL, M. A. (1990). Australian contributions to an understanding of the epidemiology and control of hydatid disease caused by Echinococcus granulosus – past, present and future. International Journal for Parasitology 20, 431–456.CrossRefGoogle Scholar
GEMMELL, M. A., LAWSON, J. R., ROBERTS, M. G., KERIN, B. R. & MASON, C. J. (1986). Population dynamics in echinococcosis and cysticercosis: comparison of the dynamics of transmission of Echinococcus granulosus, Taenia hydatigena and T. ovis during control programmes. Parasitology 93, 357–369.Google Scholar
GEMMELL, M. A. & ROBERTS, M. G. (1998). Cystic echinococcosis (Echinococcus granulosus). In Zoonoses ( ed. Palmer, S. R., Lord Soulsby & Simpson, D. I. H.), pp. 665–688. Oxford Medical Publications, OUP.
GHARBI, H. A., HASSINE, B., BRAUNER, M. W. & DUPUCH, K. (1981). Ultrasound examination of hydatid liver. Radiology 139, 459–463.Google Scholar
GIRAUDOUX, P., DELATTRE, P., HABERT, M., QUERE, J. P., DEBLAY, S., DEFAUT, R., DUHAMEL, R., MOISSENET, M. F., SALVI, D. & TRUCHETET, D. (1997). Population dynamics of fossorial water vole (Arvicola terrestris scherman): A land usage and landscape perspective. Agriculture Ecosystems and Environment 66, 47–60.CrossRefGoogle Scholar
GIRAUDOUX, P., QUERE, J. P., DELATTRE, P., BAO, G., WANG, X., SHI, D., VUITTON, D. A. & CRAIG, P. S. (1998). Distribution of small mammals along a deforestation gradient in southern Gansu, central China. Acta Theriologica 43, 349–362.CrossRefGoogle Scholar
GIRAUDOUX, P., VUITTON, D., BRESSON-HADNI, S., CRAIG, P., BARTHOLOMOT, B., BARNISH, G., LAPLANTE, J. J., ZHONG, S. D., WANG, Y. H. & LENYS, D. (1996). Mass screening and epidemiology of alveolar echinococcosis in France, western Europe, and in Gansu, central China: from epidemiology towards transmission biology. In Alveolar Echinococcosis: Strategy for Eradication of Alveolar Echinococcosis of the Liver (ed. Ito, J. & Sato, N. ), pp. 197–211. Sapporo 060, Japan: Fuji Shoin.
GOLDSMITH, R., NAHMIAS, J., SCHANTZ, P., PELEG, H., SHTAMLER, B. & EL-ON, J. (1991). Resurgence of hydatid disease (echinococcosis) in communities in northern Israel. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 98–118.CrossRefGoogle Scholar
GOTTSTEIN, B., DEPLAZES, P., ECKERT, J., MULLER, B., SCHOTT, E., HELLE, O., BOUJON, P., WOLFF, K., WANDELER, A., SCHWIETE, U. & MOEGLE, H. (1991). Serological (Em2-ELISA) and parasitological examinations of fox populations for Echinococcus multilocularis infections. Journal of Veterinary Medicine 38, 161–168.CrossRefGoogle Scholar
GUARNERA, E. A., ZANZOTTERA, E. M., PEREYRA, H. & FRANCO, A. J. (2000). Ultrasonographic diagnosis of ovine cystic echinococcosis. Veterinary Radiology and Ultrasound 42, 352–354.Google Scholar
HEMPHILL, A., STETTLER, M., WALKER, M., SILES-LUCAS, M., FINK, R. & GOTTSTEIN, B. (2003). In vitro culture of Echinococcus multilocularis and Echinococcus vogeli metacestodes: studies on the host–parasite interface. Acta Tropica 85, 145–155.CrossRefGoogle Scholar
HIRVELA-KOSKI, V., HAUKISALMI, V., KILPELA, S., NYLUND, M. & KOSKI, P. (2003). Echinococcus granulosus in Finland. Veterinary Parasitology 111, 175–192.CrossRefGoogle Scholar
HOFER, S., GLOOR, S., MULLER, 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 Zurich, Switzerland. Parasitology 120, 135–142.CrossRefGoogle Scholar
ITO, A., SCHANTZ, P. M. & WILSON, J. F. (1995). EM18, a new serodiagnostic marker for differentiation of active and inactive cases of alveolar hydtid disease American Journal of Tropical Medicine and Hygiene 52, 41–44.Google Scholar
ITO, A., URBANI, C., QIU, J., VUITTON, D. A., QIU, D., HEATH, D. D., CRAIG, P. S., FENG, Z. & SCHANTZ, P. M. (2003). Control of echinococcosis and cysticercosis: a public health challenge to international coopertion in China. Acta Tropica 86, 3–17.CrossRefGoogle Scholar
JENKINS, D. J., FRASER, A., BRADSHAW, H. & CRAIG, P. S. (2000). Detection of Echinococcus granulosus coproantigens in Australian canids with natural or experimental infection. Journal of Parasitology 86, 140–145.CrossRefGoogle Scholar
JENKINS, D. J. & RICKARD, M. D. (1985). Specific antibody responses to Taenia hydatigena, Taenia pisiformis and Echinococcus granulosus infection in dogs. Australian Veterinary Journal 62, 72–78.CrossRefGoogle Scholar
JENKINS, D. J. & RICKARD, M. D. (1986). Specific antibody responses in dogs experimentally infected with Echinococcus granulosus. American Journal of Tropical Medicine and Hygiene 35, 345–349.CrossRefGoogle Scholar
JIANG, C. (1981). Liver alveolar echinococcosis in the northwest: report of 15 patients and collective analysis of 90 cases. Chinese Medical Journal 94, 771–778.Google Scholar
KAMHAWI, S. (1995). A retrospective study of human cystic echinococcosis in Jordan. Annals of Tropical Medicine and Parasitology 89, 409–414.CrossRefGoogle Scholar
KERN, P., BARDONNET, K., RENNER, E., AYER, H., PAWLOWSKI, Z., AMMANN, R. W., VUITTON, D. A., KERN, P. & The European Echinococcosis Registry (2003). European echinococcosis registry: human alveolar echinococcosis, Europe, 1982–2000. Emerging Infectious Diseases 9, 343–349.CrossRefGoogle Scholar
KITTLEBERGER, R., REICHEL, M. P., JENNER, J., HEATH, D. D., LIGHTOWLERS, M. W., MORO, P., IBRAHEM, M. M., CRAIG, P. S. & O'KEEFE, J. (2002). Evaluation of three enzyme-linked immunosorbant assays (ELISAs) for the detection of serum antibodies in sheep infected with Echinococcus granulosus. Veterinary Parasitology 110, 57–76.CrossRefGoogle Scholar
KOHNO, H., SAKAI, H., OKAMOTO, M., ITO, M., OKU, Y. & KAMIYA, M. (1995). Development and characterisation of murine monoclonal antibodies to Echinococcus multilocularis adult worms and its use for the coproantigen detection. Japanese Journal for Parasitology 44, 404–412.Google Scholar
LE, T. H., PEARSON, M. S., BLAIR, D., DAI, N., ZHANG, L. H. & McMANUS, D. P. (2002). Complete mitochondrial genomes confirm the distinctiveness of the horse–dog and sheep–dog strains of Echinococcus granulosus. Parasitology 124, 97–112.CrossRefGoogle Scholar
LIGHTOWLERS, M. W. & GAUCI, C. G. (2001). Vaccines against cysticercosis and hydatidosis. Veterinary Parasitology 101, 337–352.CrossRefGoogle Scholar
LUCIUS, R. & BILGER, B. (1995). Echinococcus multilocularis in Germany: increased awareness or spreading of a parasite? Parasitology Today 11, 430–434.Google Scholar
MACPHERSON, C. N. L. & CRAIG, P. S. (2000). Dogs and cestode zoonoses. In Dogs, Zoonoses and Public Health ( ed. Macpherson, C. N. L., Meslin, F. X. & Wandeler, A. I.), pp. 177–211. Wallingford, Oxon, UK: CABI Publishing.CrossRef
MACPHERSON, C. N. L. & MILNER, R. (2003). Performance characteristics and quality control of community based ultrasound surveys for cystic and alveolar echinococcosis. Acta Tropica 85, 203–209.CrossRefGoogle Scholar
MACPHERSON, C. N. L., SPOERRY, A., ZEYHLE, E., ROMIG, T. & GORFE, M. (1989). Pastoralists and hydatid disease: an ultrasound scanning prevalence survey in East Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 243–247.CrossRefGoogle Scholar
MACPHERSON, C. N. L. & WACHIRA, T. W. M. (1997). Cystic echinococcosis in Africa south of the Sahara. In Compendium on Cystic Echinococcosis in Africa and in Middle Eastern Countries with Special Reference to Morocco (ed. Andersen, F. L., Ouhelli, H. & Kachoni, M. ), pp. 245–277. Provo, UT 84602, USA: Brigham Young University Print Services.
MAFF (Ministry of Agriculture, Fisheries and Food) (1998). Summary of Recommendations – Quarantine & Rabies. A Reappraisal. Report by Advisory Group on Quarantine. MAFF Publications, Admail 6000, London, SW1A 2XX.
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
MAXSON, A. D., WACHIRA, T. M., ZEYHLE, E. E., FINE, A., MWANGI, T. W. & SMITH, G. (1996). The use of ultrasound to study the prevalence of hydatid cysts in the right lung and liver of sheep and goats in Turkana, Kenya. International Journal for Parasitology 26, 1335–1338.CrossRefGoogle Scholar
McVIE, A., ERSFELD, K., ROGAN, M. T. & CRAIG, P. S. (1997). Expression and immunological characterisation of Echinococcus granulosus recombinant antigen B, for serodiagnosis of human cystic echinococcosis. Acta Tropica 67, 19–35.CrossRefGoogle Scholar
MESSIER, F., RAU, M. E. & McNEILL, M. A. (1989). Echinococcus granulosus (Cestoda: Taeniidae): Infections and moose-wolf population dynamics in southwestern Quebec. Canadian Journal of Zoology 67, 216–219.CrossRefGoogle Scholar
MONNIER, P. H., CLIQUET, F., AUBERT, M. & BRETAGNE, S. (1996). Improvement of a polymerase chain reaction assay for the detection of Echinococcus multilocularis in faecal samples of foxes. Veterinary Parasitology 67, 185–195.CrossRefGoogle Scholar
MORO, P. L., BONIFACIO, N., GILMAN, R. H., LOPERA, L., SILVA, B., TAKUMOTO, R., VERASTEGUI, M. & CABRERA, L. (1999). Field diagnosis of Echinococcus granulosus infection among intermediate and definitive hosts in an endemic focus of human cystic echinococcosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 611–615.CrossRefGoogle Scholar
MULLER-GRAF, C. D. M. (1995). A coprological survey of the intestinal parasites of wild lions (Panthera leo) in the Serengeti and the Ngorongoro Crater, Tanzania, East Africa. Journal of Parasitology 8, 812–814.CrossRefGoogle Scholar
NAKAO, M., OKAMOTO, M., SAKO, Y., YAMASAKI, H., NAKAYA, K. & ITO, A. (2002). A phylogenetic hypothesis for the distribution of two genotypes of the pig tapeworm Taenia solium worldwide. Parasitology 124, 657–662.CrossRefGoogle Scholar
NELSON, G. S. (1986). Hydatid disease: research and control in Turkana, Kenya I. Epidemiological observations. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 177–182.CrossRefGoogle Scholar
NONAKA, N., IIDA, M., YAGI, K., ITO, T., OOI, H. K., OKU, Y. & KAMIYA, M. (1996). Time course of coproantigen excretion in Echinococcus multilocularis infections in foxes and an alternative definitive host, golden hamsters. International Journal for Parasitology 26, 1271–1278.CrossRefGoogle Scholar
PALMER, S. R., BIFFIN, A. H., CRAIG, P. S. & WALTERS, T. M. (1996). Control of hydatid disease in Wales. British Medical Journal 312, 674–675.CrossRefGoogle Scholar
PAUL, M. & STEFANIAK, J. (1997). Detection of specific Echinococcus granulosus antigen 5 in liver cyst bioptate from human patients. Acta Tropica 64, 65–77.CrossRefGoogle Scholar
PAWLOWSKI, Z. (1997). Critical points in the clinical management of cystic echinococcosis: a revised review. In Compendium on Cystic Echinococcosis in Africa and in Middle Eastern Countries with Special Reference to Morocco (ed. Anderson, F. L., Ouhelli, H. & Kachani, M.), pp. 119–135. Provo, Utah, USA: Brigham Young University Print Services.
PEARSON, M., LE, T. H., ZHANG, L. H., BLAIR, D., DAI, T. H. N. & McMANUS, D. P. (2002). Molecular taxonomy and strain analysis in Echinococcus. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem (ed. Craig, P. & Pawlowski, Z.), pp. 205–219. NATO Science Series, Vol. 341, Amsterdam: IOS Press, Ohmsha.
RAOUL, F., DEPLAZES, P., NONAKA, N., PIARROUX, R., VUITTON, D. A. & GIRAUDOUX, P. (2001). Assessment of the epidemiological status of Echinococcus multilocularis in 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 histiogenesis of the alveolar larva of Echinococcus species. Journal of Infectious Diseases 94, 178–186.Google Scholar
RAUSCH, R. L. (1997). Echinococcus granulosus: Biology and Ecology. In Compendium on Cystic Echinococcosis in Africa and in Middle Eastern Countries with special reference to Morocco ( ed. Andersen, F. L., Ouhelli, H. and Kachani, M.), pp. 18–53. Provo, UT, USA: Brigham Young University Print Services.
RAUSCH, R. L. & NELSON, G. S. (1963). A review of the genus Echinococcus Rudolphi, 1801. Annals of Tropical Medicine and Parasitology 57, 127–135.CrossRefGoogle Scholar
RAUSCH, R. L., RAUSCH, V. R. & D'ALESSANDRO, A. (1978). Discrimination of the larval stages of Echinococcus oligarthrus (Diesing 1863) and E. vogeli Rausch and Bernstein, 1972 (Cestoda: Taeniidae). American Journal of Tropical Medicine and Hygiene 27, 1195–1202.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, 239–250.CrossRefGoogle Scholar
REUTER, S., WUSSLE, K., KOLOKYTHAS, O., HAUG, U., RIEBER, A., KERN, P. & KRATZER, W. (2001). Alveolar liver echinococcosis: A comparative study of three imaging techniques. Infection 29, 119–125.CrossRefGoogle Scholar
RINDER, H., RAUSCH, R. L., TAKAHASHI, K., KOPP, H., THOMSCHKE, A. & LOSCHER, T. (1997). Limited range of genetic variation in Echinococcus multilocularis. Journal of Parasitology 83, 1045–1050.CrossRefGoogle Scholar
ROBERTS, M. G. & AUBERT, M. F. A. (1994). A model for the control of Echinococcus multilocularis in France. Veterinary Parasitology 56, 67–74.Google Scholar
ROGAN, M. T. (1988). Observations on the origin of daughter cysts within hydatid cysts of Echinococcus granulosus. Annals of Tropical Medicine and Parasitology 82, 1045–1050.Google Scholar
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., KRATZNER, 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 south western Germany. American Journal of Tropical Medicine and Hygiene 61, 566–573.Google Scholar
ROTT, M. B., FERNANDEZ, V., FARIAS, S., CENI, J., FERRERA, H. B., HAAG, K. L. & ZAHA, A. (2000). Comparative analysis of two different subunits of antigen B from Echinococcus granulosus: gene sequences expression in Escherichia coli and serological evaluation. Acta Tropica 75, 331–340.CrossRefGoogle Scholar
SASKI, F., HAYTA, Y., SATO, N., HAMADA, H., TAKASHASHI, H. & UCHINO, J. (1994). Alveolar echinococcosis of the liver in children. Paediatric Survery International 9, 32–34.CrossRefGoogle Scholar
SCHELLING, U., FRANK, W., WILL, B., ROMIG, T. & LUCIUS, R. (1997). Chemotherapy with praziquantel has potential to reduce prevalence of Echinococcus multilocularis in wild foxes (Vulpes vulpes). Annals of Tropical Medicine and Parasitology 91, 179–186.CrossRefGoogle Scholar
SCHMIDT, G. D. & ROBERTS, L. S. (2000). Foundations of Parasitology. Boston and London: McGraw-Hill.
SHAMBESH, M. K., CRAIG, P. S., MACPHERSON, C. N. L., ROGAN, M. T., GUSBI, A. M. & ECHTUISH, E. F. (1999). An extensive mass ultrasound and serological study to investigate the prevalence of human cystic echinococcosis in Libya. American Journal of Tropical Medicine and Hygiene 60, 462–468.CrossRefGoogle Scholar
SHAIKENOV, B. S., VAGANOV, T. F. & TORGERSON, P. R. (1999). Cystic echinococcosis in Kazakhstan: An emerging disease since independence from the Soviet Union. Parasitology Today 15, 172–174.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
SMITH, G. C., GANGADHARAN, B., TAYLOR, Z., LAURENSON, K., BRADSHAW, H., HIDE, G., HUGHES, J. M., DINKEL, A., ROMIG, T. & CRAIG, P. S. (2003). Prevalence of zoonotic important parasites in the red fox (Vulpes vulpes) in Great Britain. Veterinary Parasitology. In press.CrossRefGoogle Scholar
TACKMANN, T., LOSCHNER, 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
TEGGI, A. & DI VICO, B. (2002). The natural history of human cystic echinococcosis (CE) by imaging methods. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 125–134. Nato Science Series, Vol. 341, Amsterdam: IOS Press.
THATCHER, V. E. & SOUSA, O. E. (1966). Echinococcus oligarthrus Diesing, 1863, in Panama and a comparison with a recent human hydatid. Annals of Tropical Medicine and Parasitology 60, 405–416.CrossRefGoogle Scholar
THOMPSON, R. C. A. & LYMBERY, A. J. (1988). The nature, extent and significance of variation within the genus Echinococcus. Advances in Parasitology 27, 209–263.CrossRefGoogle Scholar
TODOROV, T. & BOEVA, V. (1999). Human echinococcosis in Bulgaria: a comparative epidemiological analysis. Bulletin of the World Health Organisation 77, 110–118.Google Scholar
TORGERSON, P. (2002). Transmission dynamics of taeniid parasites in animal hosts. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 221–235. Nato Science Series, Vol. 341, Amsterdam: IOS Press.
TORGERSON, P., SHAIKENOV, B. & KUTTYBAEV, O. (2002). Cystic echinococcosis in Central Asia: new epidemic in Kazakhstan and Kyrgystan. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 99–105. Nato Science Series, Vol. 341, Amsterdam: IOS Press.
VAN DER GIESSEN, J. W. B., ROMBOUT, Y. B., FRANCHIMONT, J. H., LIMPER, L. P. & HOMAN, W. L. (1999). Detection of Echinococcus multilocularis in foxes in the Netherlands. Veterinary Parasitology 82, 49–57.CrossRefGoogle Scholar
VEIT, P., BILGER, B., SCHAD, V., SCHAFER, J., FRANK, W. & LUCIUS, R. (1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 79–86.CrossRefGoogle Scholar
VISCIDI, R., LAUGHTON, B. E., HANVANICH, M., BARTLETT, J. G. & YOLKEN, R. H. (1984). Improved enzyme immunoassays for the detection of antigens in faecal specimens. Investigation and correction of interfering factors. Journal of Immunological Methods 67, 129–143.Google Scholar
VOGEL, H. (1957). Uber den Echinococcus multilocularis Suddentschlands. Das Bandwurmstadium von stamen menschlicher und tierischt Herkunft. Zeitschrift für Tropendmedizin und Parasitologie 8, 404–456.Google Scholar
VUITTON, D. A. (2002). Host immunogenetics and role in epidemiology of larval cestodes. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem (ed. Craig, P. S. & Pawlowski, Z.), pp. 183–194. Nato Science Series, Vol. 341, Amsterdam: IOS Press.
WANG, Q., QIU, J. M., SCHANTZ, P., HE, J. G., ITO, A. & LIU, F. J. (2001). Investigation of risk factors for development of human hydatidosis among households raising livestock in Tibetan areas of western Sichuan Province. Chinese Journal of Parasitology and Parasitic Diseases 19, 93–96.Google Scholar
WANG, Y. H., BRADSHAW, H., ROGAN, M. T. & CRAIG, P. S. (2002). Rapid dot-ELISA for the detection of specific antigens in the cyst fluid from human cases of cystic echinococcosis. Annals of Tropical Medicine and Parasitology 96, 691–694.CrossRefGoogle Scholar
WANG, Y. H., ROGAN, M. T., VUITTON, D. A., WEN, H., BARTHOLOMOT, B., MACPHERSON, C. N. L., ZOU, P. F., DING, Z. X., ZHOU, H. X., ZHANG, X. F., LUO, J., XIONG, H. B., FU, Y., McVIE, A., GIRAUDOUX, P., YANG, W. G. & CRAIG, P. S. (2000). Cystic echinococcosis in semi-nomadic pastoral communities in northwest China. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 153–158.Google Scholar
WANG, Y. H., ZHANG, X., BARTHOLOMOT, B., LIU, B., LUO, J., LI, T., WEN, X., ZHENG, H., ZHOU, H., WEN, H., DAVAADORJ, N., GAMBOLT, L., MUKHAR, T., AL-QAOUD, K., ABDEL-HAFEZ, S., GIRAUDOUX, P., VUITTON, D. A., FRASER, A., ROGAN, M. T. & CRAIG, P. S. (2003). Classification, follow-up and recurrence of hepatic cystic echinococcosis using ultrasound images. Transactions of the Royal Society of Tropical Medicine and Hygiene. 97, 203–211.CrossRefGoogle Scholar
WEN, H. & CRAIG, P. S. (1994). IgG subclass responses in human cystic and alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 51, 741–748.CrossRefGoogle Scholar
WHO/OIE (2001). 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.), p. 265. World Organisation for Animal Health: Paris.
WYN-JONES, G. & CLARKSON, M. J. (1984). Radiologic detection of ovine hydatidosis. Veterinary Radiology 25, 182–186.CrossRefGoogle Scholar
YAMAMOTO, N., KATAKURA, K. Y. & MIYAKE, H. (2001). Risk factors for human alveolar echinococcosis: a case-control study in Hokkaido, Japan. Annals of Tropical Medicine and Parasitology 95, 689–696.CrossRefGoogle Scholar
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 in Xinjiang Uygur autonomous region, China: a preliminary analysis. Annals of Tropical Medicine and Parasitology 94, 715–729.CrossRefGoogle Scholar