Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-22T23:14:21.106Z Has data issue: false hasContentIssue false
  • English
  • Français

An experimental field approach to parasitism and immune defence in voles

Published online by Cambridge University Press:  10 June 2004

G. A. SCHWARZENBACH ,
D. HEGGLIN ,
C. STIEGER ,
P. DEPLAZES  and
P. I. WARD
G. A. SCHWARZENBACH
Affiliation:
Zoological Museum, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
D. HEGGLIN
Affiliation:
Institute of Parasitology, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
C. STIEGER
Affiliation:
Institute of Parasitology, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
P. DEPLAZES
Affiliation:
Institute of Parasitology, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
P. I. WARD
Affiliation:
Zoological Museum, University of Zürich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland
Get access Rights & Permissions [Opens in a new window]

Abstract

The fox tapeworm Echinococcus multilocularis is typically perpetuated in a cycle with red foxes as definitive hosts and various rodent species as intermediate hosts. In this study, foxes were baited with a highly efficient drug against cestodes (praziquantel) in 5 blocks of 1 km2. Voles, Arvicola terrestris, the most abundant intermediate host species, were trapped in the 5 baited blocks and in 5 non-baited control blocks. Baiting the foxes reduced the prevalence of E. multilocularis in fox faecal samples in the baited blocks, but voles trapped in the two blocks did not differ in their infection rates. However, voles from the baited blocks had significantly smaller spleen masses and were more likely to be infested with mites than those from the control blocks, possibly reflecting different immunological activities. Our study suggests that the environmental contamination with E. multilocularis eggs, and perhaps those of other tapeworms, influences the immune system of the intermediate host species A. terrestris in the wild.

Keywords

Arvicola terrestrisEchinococcus multilocularisurban foxrodentinfection pressure
Type
Research Article
Information
Parasitology , Volume 129 , Issue 1 , July 2004 , pp. 93 - 99
Copyright
© 2004 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

ALI-KHAN, Z. (1974). Host–parasite relationship in echinococcosis. I. Parasite biomass and antibody response in three strains of inbred mice against graded doses of Echinococcus multilocularis cysts. Journal of Parasitology 60, 231–235.Google Scholar
ALI-KHAN, Z. (1978 a). Cellular changes in lymphoreticular tissues of C57/J mice infected with Echinococcus multilocularis cysts. Immunology 34, 831–839.Google Scholar
ALI-KHAN, Z. (1978 b). Echinococcus multilocularis cell mediated immune responses in early and chronic alveolar murine hydatiosis. Experimental Parasitology 46, 157–165.Google Scholar
AMMAN, R. & ECKERT, J. (1995). Clinical diagnosis and treatment of echinococcosis in humans. In Echinococcus and Hydatid Disease (ed. Thompson, R. C. A. & Lymbery, A. J. ), pp. 411–463. CAB International, Walingford.
BARON, R. & TANNER, C. (1976). The effect of immunosuppression on the secondary E. multilocularis infections in mice. International Journal for Parasitology 6, 37–42.Google Scholar
BREITENMOSER, U., MÜLLER, U., KAPPELER, A. & ZANONI, R. G. (2000). The final phase of the rabies epizootic in Switzerland. Schweizer Archiv für Tierheilkunde 142, 447–454.Google Scholar
CHRISTENSEN, H. (1985). Urban fox populations in Oslo. Revue d'écologie de la terre et la vie 40, 185–186.Google Scholar
CONTESSE, P., HEGGLIN, D., GLOOR, S., BONTADINA, F., BREITENMOSER, U. & DEPLAZES, P. (2004). The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zurich, Switzerland. Mammalian Biology 69, 81–95.CrossRefGoogle Scholar
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., GLOOR, S., STIEGER, C. & HEGGLIN, D. (2002). Urban transmission of Echinococcus multilocularis. In Cestode Zoonoses: Echinococcosis and Cysticercosis (ed. Craig, P. & Pawloski, Z.), pp. 287–297. IOS Press, Amsterdam, Netherlands.
DEVOUGE, M. & ALI-KHAN, Z. (1983). Intraperitoneal murine alveolar hyaditosis: relationship between the size of larval cyst mass, immigrant inflammatory cells, splenomegaly and thymus involution. Tropenmedizin und Parasitologie 34, 15–20.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
ECKERT, J. (1998). Echinococcus multilocularis, Echinococcus oligarthrus and Echinococcus vogeli. In Zoonoses: Biology, Clinical Practice, and Public Health Control (ed. Palmer, S. R. & Simpson, D. I. H.), pp. 689–716. Oxford University Press, Oxford.
ECKERT, J. & DEPLAZES, P. (1999). Alveolar echinococcosis in humans: the current situation in central Europe and the need for countermeasures. Parasitology Today 15, 315–319.CrossRefGoogle Scholar
ECKERT, J., RAUSCH, R. L., GEMMELL, M. A., GIRADOUX, P., KAMIYA, M., LIU, F-J., SCHANTZ, P. M. & ROMIG, T. (2001 a). Epidemology of Echinococcus multilocularis, Echinococcus vogeli and Echinococcus oligarthrus. In WHO/OIE Manual on Echinococcus in Humans and Animals: A Public health Problem of Global Concern (ed. Eckert, J., Gemmell, M. A., Meslin, F.-X. & Pawlowski, Z. S.), pp. 164–194. World Organization for Animal Health, Paris.
ECKERT, J., SCHANTZ, P. M., GASSER, R. B., TORGERSON, P. R., BRESSONOV, A. S., MOVSESSIAN, S. O., THAKUR, A., GRIMM, F. & NIKOGOSSIAN, M. A. (2001 b). Geographic distribution and prevalence. In WHO/OIE Manual on Echinococcus in Humans and Animals: A Public health Problem of Global Concern (ed. Eckert, J., Gemmell, M. A., Meslin, F.-X. & Pawlowski, Z. S. ), pp. 100–142. World Organization for Animal Health, Paris.
FOTIADIS, C., SERGIOU, C., KIROU, J., TROUPIS, T. G., TSELENTIS, J., DOUSSAITOU, P., GORGOULIS, V. G. & SECHAS, M. N. (1999). Experimental Echinococcus infection in the mouse model: pericystic cellular immunity reaction and effects on the lymphoid organs of immunocompetent and thymectomized mice. In vivo 13, 541–546.Google Scholar
GIRADOUX, P., DELATTRE, P., HABERT, M., QUERE, J. P., DEBLAY, S., DEFAUT, R., DUHAMEL, R., MOISSENET, M. F., SALVI, D. & DRUCHET, D. (1997). Population dynamics of fossorial water vole (Arvicola terrestris scherman): a land usage and landscape perspective. Agriculture, Ecosystem and Environment 66, 47–60.CrossRefGoogle Scholar
GIRADOUX, P., PRADIER, B., DELATTRE, P., DEBLAY, S., SALVI, D. & DEFAUT, R. (1995). Estimation of water vole abundance by using surface indices. Acta Theriologica 40, 77–96.CrossRefGoogle Scholar
GLOOR, S. (2002). The rise of urban foxes (Vulpes vulpes) in Switzerland and ecological and parasitological aspects of afox population in the recently colonised city of Zurich. Dissertation. University of Zurich, Zurich, Switzerland.
GOTTSTEIN, B. (1992). Echinococcus multilocularis infection: immunology and immunodiagnosis. Advances in Parasitology 31, 321–380.CrossRefGoogle Scholar
GOTTSTEIN, B., SAUCY, F., WYSS, C., SIEGENTHALER, M., JACQUIER, P., SCHMITT, M., BROSSHARD, M. & DEMIERRE, G. (1996). Investigations on a Swiss area highly endemic for Echinococcus multilocularis. Applied Parasitology 37, 129–136.Google Scholar
HEGGLIN, D., BONTADINA, F., GLOOR, S., MÜLLER, U., BREITENMOSER, U. & DEPLAZES, P. (2004). Baiting red foxes in an urban area: a camera trap study. Jouranl of wildlife management (in the Press).CrossRefGoogle Scholar
HEGGLIN, D., WARD, P. I. & DEPLAZES, P. (2003). Small scale anthelminitc baiting of foxes reduces urban Echinococcus multilocularis egg contamination. Emerging Infectious Diseases 9, 1266–1272.CrossRefGoogle Scholar
HESKE, E. J. & OSTFIELD, R. S. (1990). Sexual dimorphism in size, relative size of testes, and mating systems in north american voles. Journal of Mammalogy 71, 510–519.CrossRefGoogle Scholar
HOFER, S., GLOOR, S., MÜLLER, U., HEGGLIN, D. & DEPLAZES, P. (2000). High prevalences of Echinococcus multlocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich. Parasitology 120, 135–142.CrossRefGoogle Scholar
HOUIN, R., DENIEU, M., LIANCE, M. & PUEL, F. (1982). Arvicola terrestris an intermediate host of Echinococcus multilocularis in France: epidemiological consequences. International Journal for Parasitology 12, 593–600.CrossRefGoogle Scholar
JOHN, J. L. (1995). Parasites and the avian spleen. Biological Journal of the Linnean Society 54, 87–106.CrossRefGoogle Scholar
KAMIYA, H., KAMIYA, M., OHBAYASHI, M. & NOMURA, T. (1980). Studies on the host resistance to infections with Echinococcus multilocularis. 1. Difference of susceptibility of various rodents, especially of congenitally athymic nude mice. Japanese Journal of Veterinary Research 29, 87–100.Google Scholar
KOPP, W. C. (1990). The immune functions of the spleen. In The Spleen: Structure, Function and Clinical Significance (ed. Bowdler, A. J. ), pp. 261–265. Chapman and Hall, London.
MØLLER-NIELSEN, S. M. (1990). The food of rural and suburban woodland foxes Vulpes vulpes in Denmark. Natura Jutlandica 23, 25–32.Google 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
O'BRIEN, R. M., MAY, O., CLARKE, A. H. & THOMAS, W. R. (1996). Immunologic responses following respiratory sensitization to house dust mite allergens in mice. Immunlogy and Cell Biology 74, 174–179.CrossRefGoogle Scholar
PÉTAVY, A. F. & DEBLOCK, S. (1983). Connaissance du foyer auvergnant d'échinococcose alvéolaire. Annales de Parasitologie Humaine et Comparée 58, 439–453.CrossRefGoogle Scholar
PLAYFORD, M. C. & KAMIYA, M. (1992). Immune-response to Echinococcus multilocularis infection in the house mouse model – A review. Japanese Journal of Veterinary Research 40, 113–130.Google Scholar
SCHANTZ, P. M. & GOTTSTEIN, B. (1986). Echinococcus (hyaditosis). In Immunodiagnosis of Parasitic Diseases (ed. Walls, K. M. & Schantz, P. M.), pp. 69–107. Academic Press, Orlando, USA.
SCHELLING, U. & FRANK, W. (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
SKARSTEIN, F., FOLSTRAD, I. & LILJEDAL, S. (2001). Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Canadian Journal of Zoology 79, 271–278.CrossRefGoogle Scholar
STEININGER, B. & BARTH, P. (1999). Microanatomy and function of the spleen. Advances in Anatomy, Embryology and Cell Biology 151, 1–112.Google 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
SPSS Statistical Package for PC, SPSS PC-Version, 1999, Chicago.
TACKMAN, K., LOSCHNER, U., MIX, H., STAUBACH, C., THULKE, H., ZILLER, M. & CONRATHS, F. (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
TRAVI, B., OSORIO, Y., MELBY, P., CHANDRASEKAR, B., ARTEAGA, L. & SARAVIA, N. (2002). Gender is a major determinant of the clinical evolution and immune response in hamsters infected with Leishmania spp. Infection and Immunity 70, 2288–2296.CrossRefGoogle Scholar
VEIT, P., BILGER, B., SCHAD, V., SCHÄFER, J., FRANK, W. & LUCIUS, R. (1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 79–86.CrossRefGoogle Scholar
WEBER, J. M. & AUBRY, S. (1993). Predation by foxes, Vulpes vulpes, on the fossorial form of the water vole, Arvicola terrestris Scherman, in western Switzerland. Journal of Zoology, London 229, 553–559.CrossRefGoogle Scholar
ZUK, M. & McKEAN, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.CrossRefGoogle Scholar