Hostname: page-component-7c8c6479df-p566r Total loading time: 0 Render date: 2024-03-28T03:59:04.428Z Has data issue: false hasContentIssue false

Molecular tools for studies on the transmission biology of Echinococcus multilocularis

Published online by Cambridge University Press:  04 March 2004

P. DEPLAZES
Affiliation:
Institute of Parasitology, University of Zürich, 8057 Zürich, Switzerland
A. DINKEL
Affiliation:
Department of Parasitology, University of Hohenheim, 70599 Stuttgart, Germany
A. MATHIS
Affiliation:
Institute of Parasitology, University of Zürich, 8057 Zürich, Switzerland

Abstract

Two novel approaches for diagnosis of intestinal Echinococcus multilocularis infection, the detection of E. multilocularis-specific coproantigens in ELISA and of copro-DNA by PCR, have been successfully implemented. These methods have proven their value for the post mortem and the intra vitam diagnosis of E. multilocularis in definitive hosts. They have also made novel approaches possible to study the transmission biology of the parasite as they allow detection of the infection in faecal samples collected in the environment. Coproantigen detection is the diagnostic method of choice as it is sensitive, fast and cheap. Studies on faecal samples collected in the field revealed that coproantigen detection did reflect the different prevalences in fox populations as assessed from foxes at necropsy and also the effect of deworming efforts in foxes as achieved by long-term distribution of praziquantel-containing baits. The use of PCR for routine diagnostic or large-scale purposes is hampered by the fact that DNA extraction from faecal material is a very laborious task. Therefore, PCR is rationally used for confirmatory purposes of copro-antigen-positive samples. As taeniid eggs cannot further be differentiated morphologically, PCR is the method of choice to identify E. multilocularis infections in faecal or environmental samples containing taeniid eggs. In intermediate rodent hosts, PCR is routinely used in epidemiological studies for identifying E. multilocularis from liver lesions which are often very small, atypical or calcified.

Type
Research Article
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

ALLAN, J. C., CRAIG, P. S., GARCIA, N. J., MENCOS, F., LIU, D., WANG, Y., WEN, H., ZHOU, P., STRINGER, R. & ROGAN, M. (1992). Coproantigen detection for immunodiagnosis of echinococcosis and taeniasis in dogs and humans. Parasitology 104, 347356.CrossRefGoogle Scholar
BOWLES, J., BLAIR, D. & McMANUS, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.CrossRefGoogle Scholar
BOWLES, J. & McMANUS, D. P. (1993). Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Molecular and Biochemical Parasitology 57, 231239.CrossRefGoogle Scholar
BRETAGNE, S., ASSOULINE, B., VIDAUD, D., HOUIN, R. & VIDAUD, M. (1996). Echinococcus multilocularis: microsatellite polymorphism in U1 snRNA genes. Experimental Parasitology 82, 324328.CrossRefGoogle Scholar
BRETAGNE, S., GUILLOU, J. P., MORAND, M. & HOUIN, R. (1993). Detection of Echinococcus multilocularis DNA in fox faeces using DNA amplification. Parasitology 106, 193199.CrossRefGoogle Scholar
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, 299306.CrossRefGoogle Scholar
CRAIG, P. S., ROGAN, M. T. & ALLAN, J. C. (1996). Detection, screening and community epidemiology of taeniid cestode zoonoses: cystic echinococcosis, alveolar echinococcosis and neurocysticercosis. Advances in Parasitology 38, 169250.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, 115121.CrossRefGoogle Scholar
DEPLAZES, P. & ECKERT, J. (1996). Diagnosis of the Echinococcus multilocularis infection in final hosts. Applied Parasitology 37, 245252.Google Scholar
DEPLAZES, P. & ECKERT, J. (2001). Veterinary aspects of alveolar echinococcosis – a zoonosis of public health significance. Veterinary Parasitology 98, 6587.CrossRefGoogle Scholar
DEPLAZES, P. & GOTTSTEIN, B. (1991). A monoclonal antibody against Echinococcus multilocularis Em2 antigen. Parasitology 103, 4149.CrossRefGoogle Scholar
DEPLAZES, P., GOTTSTEIN, B., ECKERT, J., JENKINS, D. J., EWALD, D. & JIMENEZ-PALACIOS, S. (1992). Detection of Echinococcus coproantigens by enzyme-linked immunosorbent assay in dogs, dingoes and foxes. Parasitology Research 78, 303308.CrossRefGoogle Scholar
DEPLAZES, P., GOTTSTEIN, B., STINGELIN, Y. & ECKERT, J. (1990). Detection of Taenia hydatigena copro-antigens by ELISA in dogs. Veterinary Parasitology 36, 91103.CrossRefGoogle Scholar
DINKEL, A. (1998). Diagnostik von Echinococcus multilocularis im End- und Zwischenwirt mit Hilfe der PCR. Verlag Ulrich E. Grauer, Stuttgart, Germany.
DINKEL, A., VON NICKISCH-ROSENEGK, M., BILGER, B., MERLI, M., KÖDER, M., LOOS-FRANK, B., LUCIUS, R. & ROMIG, T. (1996). Spezifischer Nachweis von Echinococcus multilocularis-DNA aus End- und Zwischenwirt mit Hilfe der PCR. 17th Congress of the German Society for Parasitology, München, Germany.
DINKEL, A., VON NICKISCH-ROSENEGK, M., BILGER, B., MERLI, M., LUCIUS, R. & ROMIG, I. (1998). Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. Journal of Clinical Microbiology 36, 18711876.Google Scholar
ECKERT, J., GEMMELL, M. A., MESLIN, F.-X. & PAWLOWSKI, J. (eds) (2001 a). Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Manual of the World Health Organization, Geneva, and the Office International des Epizooties, Paris.
ECKERT, J., THOMPSON, R. C., BUCKLAR, H., BILGER, B. & DEPLAZES, P. (2001 b). Efficacy evaluation of epsiprantel (Cestex) against Echinococcus multilocularis in dogs and cats. Berliner und Munchener Tierarztliche Wochenschrift 114, 121126.Google Scholar
GASSER, R. B. & CHILTON, N. B. (1995). Characterisation of taeniid cestode species by PCR-RFLP of ITS2 ribosomal DNA. Acta Tropica 59, 3140.CrossRefGoogle Scholar
GOTTSTEIN, B. & MOWATT, M. R. (1991). Sequencing and characterization of an Echinococcus multilocularis DNA probe and its use in the polymerase chain reaction. Molecular and Biochemical Parasitology 44, 183193.CrossRefGoogle 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, 408412.Google Scholar
HAAG, K. L., ZAHA, A., ARAUJO, A. M. & GOTTSTEIN, B. (1997). Reduced genetic variability within coding and non-coding regions of the Echinococcus multilocularis genome. Parasitology 115, 521529.CrossRefGoogle Scholar
HEGGLIN, D., WARD, P. & DEPLAZES, P. (2003). Small-scale anthelmintic baiting of foxes reduces urban Echinococcus multilocularis egg contamination. Emerging Infectious Diseases (in press).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, 135142.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, 140145.CrossRefGoogle Scholar
KERN, P., FROSCH, P., HELBIG, M., WECHSLER, J. G., USADEL, S., BECKH, K., KUNZ, R., LUCIUS, R. & FROSCH, M. (1995). Diagnosis of Echinococcus multilocularis infection by reverse-transcription polymerase chain reaction. Gastroenterology 109, 596600.CrossRefGoogle Scholar
KOHNO, H., SAKAI, H., OKAMOTO, M., ITO, M., OKU, Y. & KAMIYA, M. (1995). Development and characterization of murine monoclonal antibodies to Echinococcus multilocularis adult worms and its use. Japanese Journal of Parasitology 44, 404412.Google Scholar
MAJOR, M., JOHNSON, M. K., DAVIS, W. S. & KELLOGG, T. F. (1980). Identifying scats by recovery of bile acids. Journal of Wildlife Management 44, 290293.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, 219222.CrossRefGoogle Scholar
MERLI, M., DINKEL, A., LOOS-FRANK, B., LUCIUS, R. & ROMIG, T. (1996). Untersuchungen zum Vorkommen von Echinococcus multilocularis in Feld- und Schermäusen in Baden-Württemberg. 17th Congress of the German Society for Parasitology, München, Germany.
MERLI, M., ROMIG, T., DINKEL, A., BILGER, B. & MACKENSTEDT, U. (2001). Developmental aspects of Echinococcus multilocularis metacestodes in the common vole (Microtus arvalis). XXth International Congress of Hydatidology, Kusadasi, Turkey.
MONNIER, P., CLIQUET, F., AUBERT, M. & BRETAGNE, S. (1996). Improvement of a polymerase chain reaction assay for the detection of Echinococcus multilocularis DNA in faecal samples of foxes. Veterinary Parasitology 67, 185195.CrossRefGoogle Scholar
MORISHIMA, Y., TSUKADA, H., NONAKA, N., OKU, Y. & KAMIYA, M. (1999). Coproantigen survey for Echinococcus multilocularis prevalence of red foxes in Hokkaido, Japan. Parasitology International 48, 121134.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, 12711278.CrossRefGoogle Scholar
NONAKA, N., TSUKADA, H., ABE, N., OKU, Y. & KAMIYA, M. (1998). Monitoring of Echinococcus multilocularis infection in red foxes in Shiretoko, Japan, by coproantigen detection. Parasitology 117, 193200.CrossRefGoogle Scholar
PALOMARES, F., GODOY, J. A., PIRIZ, A. & O'BRIEN, S. J. (2002). Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Molecular Ecology 11, 21712182.CrossRefGoogle Scholar
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.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, 10451050.CrossRefGoogle Scholar
SAKAI, H., NONAKA, N., YAGI, K., OKU, Y. & KAMIYA, M. (1998). Coproantigen detection in a survey of Echinococcus multilocularis infection among red foxes, Vulpes vulpes schrencki, in Hokkaido, Japan. Journal of Veterinary Medical Science 60, 639641.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, 631640.CrossRefGoogle Scholar
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, 119129.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, 423428.CrossRefGoogle Scholar
VAN DER GIESSEN, J. W., 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, 4957.CrossRefGoogle Scholar
VAN HERWERDEN, L., GASSER, R. B. & BLAIR, D. (2000). ITS-1 ribosomal DNA sequence variants are maintained in different species and strains of Echinococcus. International Journal for Parasitology 30, 157169.CrossRefGoogle Scholar
VON NICKISCH-ROSENEGK, M., LUCIUS, R. & LOOS-FRANK, B. (1999). Contributions to the phylogeny of the Cyclophyllidea (Cestoda) inferred from mitochondrial 12S rDNA. Journal of Molecular Evolution 48, 586596.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION/OFFICE INTERNATIONAL DES EPIZOOTIES (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals ( ed. J. Eckert, M. A. Gemmell, F.-X. Meslin & Z. Pawlowski ). Office International des Epizooties, Paris.
YAGI, K., OHYAMA, T., OKAMOTO, M., KUROSAWA, T. & KAMIYA, M. (1996). The application of PCR for the identification of Echinococcus multilocularis eggs in Hokkaido. In Alveolar Echinococcosis. Strategy for the Eradication of Alveolar Echinococcosis in the Liver ( ed. J. Uchini & N. Sato ), pp. 165170. Fuji Shoin, Sapporo, Japan.