Skip to main content
×
×
Home

Rodents as shared indicators for zoonotic parasites of carnivores in urban environments

  • L. A. REPERANT (a1), D. HEGGLIN (a1), I. TANNER (a1), C. FISCHER (a2) and P. DEPLAZES (a1)...
Summary

Rodents are shared intermediate or paratenic hosts for Echinococcus multilocularis, Toxocara spp. and Toxoplasma gondii, and may serve as valuable indicators for assessing the occurrence and the level of environmental contamination and infection pressure with free-living stages of these zoonotic parasites. We investigated 658 non-commensal rodents for parasite infections in the canton of Geneva, Switzerland. The prevalence of infection with E. multilocularis was highest in Arvicola terrestris captured in the north-western area (16·5%, CI: 10·1%–24·8%), possibly reflecting a higher red fox density due to the low incidence of sarcoptic mange in this part of the canton. The exposure rate to Toxocara spp. was highest in the urban area (13·2%, CI: 7·9%–20·3%), and may account for higher densities of domestic carnivore and red fox definitive hosts within the city. Exposure to T. gondii was widespread (5·0%, CI: 3·2–7·4%), indicating a ubiquitous distribution of infected cat definitive hosts. Interestingly, a widespread distribution of Taenia taeniaeformis, a parasite mainly transmitted by cats, was similarly evidenced in A. terrestris. Distinct spatial patterns for the different zoonotic parasites likely reflected differences in distribution, abundance, and habitat use of the respective definitive hosts. These results highlight the potential value of rodents as shared indicators for these pathogens.

Copyright
Corresponding author
*Corresponding author: Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057Zurich, Switzerland. Tel: +41 44 63 58 501. Fax: +41 44 63 58 907. E-mail: deplazesp@access.uzh.ch
References
Hide All
Afonso, E., Thulliez, P. and Gilot-Fromont, E. (2006). Transmission of Toxoplasma gondii in an urban population of domestic cats (Felis catus). International Journal for Parasitology 36, 13731382.
Antolova, D., Reiterova, K., Miterpakova, M., Stanko, M. and Dubinsky, P. (2004). Circulation of Toxocara spp. in suburban and rural ecosystems in the Slovak Republic. Veterinary Parasitology 126, 317324.
Aramini, J. J., Stephen, C., Dubey, J. P., Engelstoft, C., Schwantje, H. and Ribble, C. S. (1999). Potential contamination of drinking water with Toxoplasma gondii oocysts. Epidemiology and Infection 122, 305315.
Bonnin, J. L., Delattre, P., Artois, M., Pascal, M., Aubert, M. F. and Petavy, A. F. (1986). [Intermediate hosts of Echinococcus multilocularis in northeastern France. Description of lesions found in 3 naturally infested rodent species]. Annales de Parasitologie Humaine et Comparée 61, 235243.
Brohmer, P. (1988). Fauna von Deutschland. Quelle and Meyer Verlag, Heidelberg – Wiesbaden, Germany.
Calhoon, R. E. and Haspel, C. (1989). Urban cat populations compared by season, subhabitat and supplemental feeding. The Journal of Animal Ecology 58, 321328.
Childs, J. E., Glass, G. E. and Korch, G. W. Jr. (1988). The comparative epizootiology of Capillaria hepatica (Nematoda) in urban rodents from different habitats of Baltimore, Maryland. Canadian Journal of Zoology 66, 27692775.
Clopper, C. J. and Pearson, E. S. (1934). The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26, 404413.
Contesse, P., Hegglin, D., Gloor, S., Bontadina, F. and Deplazes, P. (2003). The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zürich, Switzerland. Mammalian Biology 69, 8195.
Cuéllar, C., Fenoy, S. and Guillén, J. L. (1995). Cross-reactions of sera from Toxascaris leonina and Ascaris suum infected mice with Toxocara canis, Toxascaris leonina and Ascaris suum antigens. International Journal for Parasitology 25, 731739.
Danson, F. M., Giraudoux, P. and Craig, P. S. (2006). Spatial modelling and ecology of Echinococcus multilocularis transmission in China. Parasitology International 55, S227S231.
Deplazes, P., Hegglin, D., Gloor, S. and Romig, T. (2004). Wilderness in the city, the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 7784.
Deplazes, P., Grimm, F., Sydler, T., Tanner, I. and Kapel, C. M. (2005). Experimental alveolar echinococcosis in pigs, lesion development and serological follow up. Veterinary Parasitology 130, 213222.
Despommier, D. (2003). Toxocariasis, clinical aspects, epidemiology, medical ecology, and molecular aspects. Clinical Microbiology Reviews 16, 265272.
Dickman, C. R. (1987). Habitat fragmentation and vertebrate species richness in an urban environment. The Journal of Applied Ecology 24, 337351.
Dickman, C. R. and Doncaster, C. P. (1987). The ecology of small mammals in urban habitats. I. Populations in a patchy environment. The Journal of Animal Ecology 56, 629640.
Dubinsky, P., Havasiova-Reiterova, K., Petko, B., Hovorka, I. and Tomasovicova, O. (1995). Role of small mammals in the epidemiology of toxocariasis. Parasitology 110, 187193.
Dubna, S., Langrova, I., Jankovska, I., Vadlejch, J., Pekar, S., Napravnik, J. and Fechtner, J. (2007). Contamination of soil with Toxocara eggs in urban (Prague) and rural areas in the Czech Republic. Veterinary Parasitology 144, 8186.
Dumetre, A. and Darde, M. L. (2003). How to detect Toxoplasma gondii oocysts in environmental samples? FEMS Microbiology Reviews 27, 651661.
Eckert, J. and Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107135.
Fischer, C., Reperant, L. A., Weber, J. M., Hegglin, D. and Deplazes, P. (2005). Echinococcus multlocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite 12, 339346.
Giacometti, A., Cirioni, O., Fortuna, M., Osimani, P., Antonicelli, L., Del Prete, M. S., Riva, A., D'Errico, M. M., Petrelli, E. and Scalise, G. (2000). Environmental and serological evidence for the presence of toxocariasis in the urban area of Ancona, Italy. European Journal of Epidemiology 16, 10231026.
Greiner, M., Franke, C. R., Bohning, D. and Schlattmann, P. (1994). Construction of an intrinsic cut-off value for the sero-epidemiological study of Trypanosoma evansi infections in a canine population in Brazil: a new approach towards an unbiased estimation of prevalence. Acta Tropica 56, 97109.
Habluetzel, A., Traldi, G., Ruggieri, S., Attili, A. R., Scuppa, P., Marchetti, R., Menghini, G. and Esposito, F. (2003). An estimation of Toxocara canis prevalence in dogs, environmental egg contamination and risk of human infection in the Marche region of Italy. Veterinary Parasitology 113, 243252.
Harris, S. (1981). An estimation of the number of foxes (Vulpes vulpes) in the city of Bristol, and some possible factors affecting their distribution. The Journal of Applied Ecology 18, 455465.
Hegglin, D. , D., Bontadina, F., Contesse, P., Gloor, S. and Deplazes, P. (2007). Plasticity of predation behaviour as a putative driving force for parasite life-cycle dynamics, the case of urban foxes and Echinococcus multilocularis tapeworm. Functional Ecology 21, 552560.
Hill, D. and Dubey, J. P. (2002). Toxoplasma gondii, transmission, diagnosis and prevention. Clinical Microbiology and Infection 8, 634640.
Hofer, S., Gloor, S., Müller, U., Mathis, A., Hegglin, D. and 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.
Kapel, C. M., Torgerson, P. R., Thompson, R. C. A. and Deplazes, P. (2006). Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon, dogs and cats. International Journal for Parasitology 36, 7986.
Loos-Frank, B. and Zeyhle, E. (1982). The intestinal helminths of the red fox and some other carnivores in southwest Germany. Zeitschrift für Parasitenkunde 67, 99113.
Matter, H. C. and Daniels, T. J. (2001). Dog ecology and population biology. In Dogs, Zoonoses and Public Health (ed. MacPherson, C. N. L., Meslin, F. X. and Wandeler, A. I., CABI Publishing, Wallingford, Oxon., UK.
McKinney, M. L. (2002). Urbanization, biodiversity, and conservation. BioScience 52, 883890.
Mizgajska, H. (1997). The role of some environmental factors in the contamination of soil with Toxocara spp. and other geohelminth eggs. Parasitology International 46, 4672.
Mizgajska, H. (2001). Eggs of Toxocara spp. in the environment and their public health implications. Journal of Helminthology 75, 147151.
Müller, N., Zimmermann, V., Hentrich, B. and Gottstein, B. (1996). Diagnosis of Neospora caninum and Toxoplasma gondii infection by PCR and DNA hybridization immunoassay. Journal of Clinical Microbiology 34, 28502852.
O'Lorcain, P. (1994). Epidemiology of Toxocara spp. in stray dogs and cats in Dublin, Ireland. Journal of Helminthology 68, 331336.
Pence, D. B. and Ueckermann, E. (2002). Sarcoptic mange in wildlife. Revue Scientifique et Technique de l'Office International des Epizooties 21, 385398.
Pleydell, D. R., Raoul, F., Tourneux, F., Danson, F. M., Graham, A. J., Craig, P. S. and Giraudoux, P. (2004). Modelling the spatial distribution of Echinococcus multilocularis infection in foxes. Acta Tropica 91, 253265.
Raoul, F., Michelat, D., Ordinaire, M., Decote, Y., Aubert, M., Delattre, P., Deplazes, P. and Giraudoux, P. (2003). Echinococcus multilocularis, secondary poisoning of fox population during a vole outbreak reduces environmental contamination in a high endemicity area. International Journal for Parasitology 33, 945954.
Reperant, L. A. and Deplazes, P. (2005). Cluster of Capillaria hepatica infections in non-commensal rodents from the canton of Geneva, Switzerland. Parasitology Research 96, 340342.
Reperant, L. A., Hegglin, D., Fischer, C., Kohler, L., Weber, J. M. and Deplazes, P. (2007). Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland. Parasitology Research 101, 605611.
Robardet, E., Giraudoux, P., Caillot, C., Boue, F., Cliquet, F., Augot, D. and Barrat, J. (2008). Infection of foxes by Echinococcocus multilocularis in urban and suburban areas of Nancy, France: influence of feeding habits and environment. Parasite 15, 7785.
Speiser, F. and Gottstein, B. (1984). A collaborative study on larval excretory/secretory antigens of Toxocara canis for the immunodiagnosis of human toxocariasis with ELISA. Acta Tropica 41, 361372.
Stieger, C., Hegglin, D., Schwarzenbach, G., Mathis, A. and Deplazes, P. (2002). Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitology 124, 631640.
Viel, J. F., Giraudoux, P., Abrial, V. and Bresson-Hadni, S. (1999). Water vole (Arvicola terrestris scherman) density as risk factor for human alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 61, 559565.
Vuitton, D. A., Zhou, H., Bresson-Hadni, S., Wang, Q., Piarroux, M., Raoul, F. and Giraudoux, P. (2003). Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127, S87S107.
Weber, J. M. and 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, 553559.
Wyss, R., Sager, H., Müller, N., Inderbitzin, F., König, M., Audigé, L. and Gottstein, B. (2000). [The occurrence of Toxoplasma gondii and Neospora caninum as regards meat hygiene]. Schweizer Archiv für Tierheilkunde 142, 95108.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed