Hostname: page-component-745bb68f8f-grxwn Total loading time: 0 Render date: 2025-01-26T22:57:13.942Z Has data issue: false hasContentIssue false
  • English
  • Français

Stability of the southern European border of Echinococcus multilocularis in the Alps: evidence that Microtus arvalis is a limiting factor

Published online by Cambridge University Press:  16 June 2014

DIOGO GUERRA ,
DANIEL HEGGLIN ,
LUCA BACCIARINI ,
MANUELA SCHNYDER  and
PETER DEPLAZES
DIOGO GUERRA
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland
DANIEL HEGGLIN
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland
LUCA BACCIARINI
Affiliation:
Cantonal Veterinary Office, Via Dogana 16, CH-6500 Bellinzona, Switzerland
MANUELA SCHNYDER
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland
PETER DEPLAZES*
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland
*
*Corresponding author: Institute of Parasitology, Winterthurerstrasse 266a, CH-8057 Zurich, Switzerland. E-mail: deplazesp@access.uzh.ch
Get access Rights & Permissions [Opens in a new window]

Summary

The known range of the zoonotic fox tapeworm Echinococcus multilocularis has expanded since the 1990s, and today this parasite is recorded in higher abundances throughout large parts of Europe. This phenomenon is mostly attributed to the increasing European fox populations and their invasion of urban habitats. However, these factors alone are insufficient to explain the heterogeneous distribution of the parasite in Europe. Here, we analysed the spatial interrelationship of E. multilocularis with the known distribution of seven vole species in Ticino, southern Switzerland. Among 404 necropsied foxes (1990–2006) and 79 fox faecal samples (2010–2012), E. multilocularis was consistently found in the north of the investigated area. No expansion of this endemic focus was recorded during the 22 years of the study period. This stable endemic focus is coincident with the known distribution of the vole species Microtus arvalis but not, or only partly, with the distribution of the other autochthonous vole species. Our results give evidence that this vole species plays a crucial role in the maintenance of the parasite's life cycle and that its absence could be a limiting factor for the spread of E. multilocularis in this region.

Keywords

distributionEchinococcus multilocularisfoxMicrotus arvalisrodentsSwitzerland
Type
Research Article
Information
Parasitology , Volume 141 , Issue 12 , October 2014 , pp. 1593 - 1602
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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

Alther, P. (1996). Beitrag zur Epidemiologie und Diagnose der Echinococcus multilocularis – Infektion bei Endwirten. Vet Med thesis. University of Zurich, Zurich, Switzerland.Google Scholar
Berke, O., Romig, T. and von Keyserlingk, M. (2008). Emergence of Echinococcus multilocularis among red foxes in northern Germany, 1991–2005. Veterinary Parasitology 155, 319–322.Google Scholar
Bonnin, J., Delattre, P., Artois, M., Pascal, M., Aubert, M. and Petavy, A. (1986). Contribution à la connaissance des hôtes intermédiaires d'Echinococcus multilocularis dans le nord-est de la France. Annales de Parasitologie Humaine et Comparée 61, 235–243.Google Scholar
Braaker, S. and Heckel, G. (2009). Transalpine colonisation and partial phylogeographic erosion by dispersal in the common vole (Microtus arvalis). Molecular Ecology 18, 2518–2531.Google Scholar
Brossard, M., Andreutti, C. and Siegenthaler, M. (2007). Infection of red foxes with Echinococcus multilocularis in western Switzerland. Journal of Helminthology 81, 369–376.Google Scholar
Bružinskaitė, R., Marcinkutė, A., Strupas, K., Sokolovas, V., Deplazes, P., Mathis, A., Eddi, C. and Šarkūnas, M. (2007). Alveolar echinococcosis, Lithuania. Emerging Infectious Diseases 13, 1618–1619.Google Scholar
Burlet, P., Deplazes, P. and Hegglin, D. (2011). Age, season and spatio-temporal factors affecting the prevalence of Echinococcus multilocularis and Taenia taeniaeformis in Arvicola terrestris. Parasites and Vectors 4, 1–9.Google Scholar
Casulli, A., Manfredi, M. T., La Rosa, G., Di Cerbo, A. R., Dinkel, A., Romig, T., Deplazes, P., Genchi, C. and Pozio, E. (2005). Echinococcus multilocularis in red foxes (Vulpes vulpes) of the Italian Alpine region: is there a focus of autochthonous transmission? International Journal for Parasitology 35, 1079–1083.CrossRefGoogle Scholar
Casulli, A., Bart, J. M., Knapp, J., La Rosa, G., Dusher, G., Gottstein, B., Di Cerbo, A., Manfredi, M. T., Genchi, C., Piarroux, R. and Pozio, E. (2009). Multi-locus microsatellite analysis supports the hypothesis of an autochthonous focus of Echinococcus multilocularis in northern Italy. International Journal for Parasitology 39, 837–842.Google Scholar
Combes, B., Comte, S., Raton, V., Raoul, F., Boué, F., Umhang, G., Favier, S., Dunoyer, C., Woronoff, N. and Giraudoux, P. (2012). Westward spread of Echinococcus multilocularis in foxes, France, 2005–2010. Emerging Infectious Diseases 18, 2059–2062.Google Scholar
Deblock, S., Pétavy, A. F. and Gilot, B. (1988). Helminthes intestinaux du renard commun (Vulpes vulpes L.) dans le Massif central (France). Canadian Journal of Zoology 66, 1562–1569.CrossRefGoogle Scholar
Delattre, P., Giraudoux, P. and Quéré, J.-P. (1990). Conséquences épidémiologiques de la réceptivité d'un nouvel hôte intermédiaire du Taenia multiloculaire (Echinococcus multilocularis) et de la localisation spatiotemporelle des rongeurs infestés. Comptes rendus de l'Académie des Sciences 310, 339–344.Google Scholar
Delattre, P., Clarac, R., Melis, J.-P., Pleydell, D. and Giraudoux, P. (2006). How moles contribute to colonization success of water voles in grassland: implications for control. Journal of Applied Ecology 43, 353–359.Google Scholar
Deplazes, P., Hegglin, D., Gloor, S. and Romig, T. (2004). Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 77–84.CrossRefGoogle ScholarPubMed
Di Cerbo, A. R., Manfredi, M. T., Trevisiol, K., Bregoli, M., Ferrari, N., Pirinesi, F. and Bazzoli, S. (2008). Intestinal helminth communities of the red fox (Vulpes vulpes L.) in the Italian Alps. Acta Parasitologica 53, 302–311.Google Scholar
Duscher, G., Pleydell, D., Prosl, H. and Joachim, A. (2006). Echinococcus multilocularis in Austrian foxes from 1991 until 2004. Journal of Veterinary Medicine, Series B 53, 138–144.CrossRefGoogle ScholarPubMed
Eckert, J., Gemmell, M., Meslin, F. and Pawlowski, Z. (2001). WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern, Vol. 32. World Organisation for Animal Health, Paris, France.Google Scholar
Eckert, J., Deplazes, P. and Kern, P. (2011). Alveolar echinococcosis (Echinococcus multilocularis) and neotropical forms of echinococcosis (Echinococcus vogeli and Echinococcus oligarthrus). In Oxford Textbook of Zoonoses: Biology, Clinical Practice, and Public Health Control, 2nd Edn (ed. Palmer, S. R., Soulsby, E. J. L., Torgerson, P. R. and Brown, D. W. G.), pp. 668–699. Oxford University Press, Oxford, UK.Google Scholar
Ewald, D. (1993). Prävalenz von Echinococcus multilocularis bei Rotfüchsen (Vulpes vulpes L.) in der Nord-, Ost- und Südschweiz sowie im Fürstentum Liechtenstein. Ph.D. thesis, Phil. II. University of Zurich, Zurich, Switzerland.Google Scholar
Fischer, C., Reperant, L., Weber, J., Hegglin, D. and Deplazes, P. (2005). Echinococcus multilocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite 12, 339–346.Google Scholar
Genov, T., Svilenov, D. and Polyakova-Krusteva, O. (1980). The natural occurrence of Alveococcus multilocularis in the Microtus nivalis in Bulgaria. Doklady Bolgarskoi Akademii Nauk 33, 981–984.Google Scholar
Giraudoux, P., Craig, P., Delattre, P., Bao, G., Bartholomot, B., Harraga, S., Quéré, J., Raoul, F., Wang, Y. and Shi, D. (2003). Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127, S121–S132.CrossRefGoogle ScholarPubMed
Giraudoux, P., Raoul, F., Afonso, E., Ziadinov, I., Yang, Y., Li, L., Li, T., Quéré, J.-P., Feng, X. and Wang, Q. (2013 a). Transmission ecosystems of Echinococcus multilocularis in China and Central Asia. Parasitology 140, 1655–1666.CrossRefGoogle Scholar
Giraudoux, P., Raoul, F., Pleydell, D., Li, T., Han, X., Qiu, J., Xie, Y., Wang, H., Ito, A. and Craig, P. S. (2013 b). Drivers of Echinococcus multilocularis transmission in china: small mammal diversity, landscape or climate? PLOS Neglected Tropical Diseases 7, e2045. doi: 10.1371/journal.pntd.0002045.Google Scholar
Guislain, M.-H., Raoul, F., Giraudoux, P., Terrier, M.-E., Froment, G., Ferté, H. and Poulle, M.-L. (2008). Ecological and biological factors involved in the transmission of Echinococcus multilocularis in the French Ardennes. Journal of Helminthology 82, 143–151.CrossRefGoogle ScholarPubMed
Hansen, F., Jeltsch, F., Tackmann, K., Staubach, C. and Thulke, H.-H. (2004). Processes leading to a spatial aggregation of Echinococcus multilocularis in its natural intermediate host Microtus arvalis. International Journal for Parasitology 34, 37–44.Google Scholar
Hausser, J. (1995). Säugetiere der Schweiz. Birkhauser, Basel, Switzerland.Google Scholar
Hegglin, 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, 552–560.Google Scholar
Hofer, S., Gloor, S., Muller, 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 Zurich, Switzerland. Parasitology 120, 135–142.Google Scholar
Hosemann, G., Schwarz, E., Lehmann, J. C. and Posselt, A. (1928). Die Echinokokken Krankheit. In Neue Deutsche Chirurgie, Vol. 40 (ed. Küttner, H.), pp. 103–107. Ferdinand Enke Verlag, Stuttgart, Germany.Google Scholar
Houin, R., Deniau, M., Liance, M. and Puel, F. (1982). Arvicola terrestris, an intermediate host of Echinococcus multilocularis in France: epidemiological consequences. International Journal for Parasitology 12, 593–600.Google Scholar
Jones, A. and Pybus, M. J. (2001). Taeniasis and echinococcosis. In Parasitic Diseases of Wild Mammals (ed. Samuel, W. M., Pybus, M. J. and Kocan, K. K.), pp. 150–192. Iowa State University Press, Iowa, USA.Google Scholar
Kharchenko, V. A., Kornyushin, V. V., Varodi, E. I. and Malega, O. M. (2008). Occurrence of Echinococcus multilocularis (Cestoda, Taeniidae) in red foxes (Vulpes vulpes) from Western Ukraine. Acta Parasitologica 53, 36–40.Google Scholar
Lind, E. O., Juremalm, M., Christensson, D., Widgren, S., Hallgren, G., Ågren, E., Uhlhorn, H. and Lindberg, A. (2011). First detection of Echinococcus multilocularis in Sweden, February to March 2011. Euro Surveillance 16, 696–705.Google Scholar
Macdonald, D. (1977). On food preference in the red fox. Mammal Review 7, 7–23.Google Scholar
Maddalena, T., Maurizio, R. and Moretti, M. (2000). Zone di contatto fra Talpa caeca Savi e Talpa europaea L. in Val Leventina, Valle di Blenio, Val Mesolcina, e Val San Giacomo (Cantoni Ticino e Grigioni, Svizzera / provicina di Sondrio, Italia). Bolletino dela Società Ticinese di Scienze Naturali 88, 13–18.Google Scholar
Magi, M., Macchioni, F., Dell'Omodarme, M., Prati, M., Calderini, P., Gabrielli, S., Iori, A. and Cancrini, G. (2009). Endoparasites of red fox (Vulpes vulpes) in central Italy. Journal of Wildlife Diseases 45, 881–885.Google Scholar
Manfredi, M., Genchi, C., Deplazes, P., Trevisiol, K. and Fraquelli, C. (2002). Echinococcus multilocularis infection in red foxes in Italy. Veterinary Record 150, 757.Google Scholar
Mathis, A., Deplazes, P. and Eckert, J. (1996). An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. Journal of Helminthology 70, 219–222.Google Scholar
Meia, J.-S. and Weber, J.-M. (1995). Home ranges and movements of red foxes in central Europe: stability despite environmental changes. Canadian Journal of Zoology 73, 1960–1966.Google Scholar
Moks, E., Saarma, U. and Valdmann, H. (2005). Echinococcus multilocularis in Estonia. Emerging Infectious Diseases 11, 1973–1974.Google Scholar
Nonaka, N., Sano, T., Inoue, T., Teresa Armua, M., Fukui, D., Katakura, K. and Oku, Y. (2009). Multiplex PCR system for identifying the carnivore origins of faeces for an epidemiological study on Echinococcus multilocularis in Hokkaido, Japan. Parasitology Research 106, 75–83.CrossRefGoogle ScholarPubMed
Rajković-Janje, R., Marinculić, A., Bosnić, S., Benić, M., Vinković, B. and Mihaljević, Ž. (2002). Prevalence and seasonal distribution of helminth parasites in red foxes (Vulpes vulpes) from the Zagreb County (Croatia). Zeitschrift für Jagdwissenschaft 48, 151–160.Google Scholar
Raoul, F., Deplazes, P., Rieffel, D., Lambert, J.-C. and Giraudoux, P. (2010). Predator dietary response to prey density variation and consequences for cestode transmission. Oecologia 164, 129–139.Google Scholar
Rataj, A. V., Bidovec, A., Žele, D. and Vengušt, G. (2010). Echinococcus multilocularis in the red fox (Vulpes vulpes) in Slovenia. European Journal of Wildlife Research 56, 819–822.Google Scholar
Rausch, R. L. (1967). On the ecology and distribution of Echinococcus spp. (Cestoda: Taeniidae), and characteristics of their development in the intermediate host. Annales de Parasitologie Humaine et Comparée 42, 19–63.CrossRefGoogle ScholarPubMed
Reperant, L., 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, 605–611.Google Scholar
Reperant, L., Hegglin, D., Tanner, I., Fischer, C. and Deplazes, P. (2009). Rodents as shared indicators for zoonotic parasites of carnivores in urban environments. Parasitology 136, 329–337.Google Scholar
Rietschel, G. (1981). Beitrag zur Kenntnis von Taenia crassiceps (Zeder, 1800) Rudolphi, 1810 (Cestoda, Taeniidae). Zeitschrift für Parasitenkunde 65, 309–315.Google Scholar
Said-Ali, Z., Grenouillet, F., Knapp, J., Bresson-Hadni, S., Vuitton, D. A., Raoul, F., Richou, C., Millon, L. and Giraudoux, P. (2013). Detecting nested clusters of human alveolar echinococcosis. Parasitology 140, 1693–1700.Google Scholar
Schaerer, O. (1987). Die Metacestoden der Kleinsäuger (Insectivora und Rodentia) und ihre Wirtsarten Verbreitung und Häufigkeit im Kanton Thurgau (Schweiz). Ph.D. thesis, Phil. II. University of Zurich, Zurich, Switzerland.Google Scholar
Schneider, R., Aspöck, H. and Auer, H. (2013). Unexpected increase of alveolar echinococcosis, Austria, 2011. Emerging Infectious Diseases 19, 475–477.Google Scholar
Schweiger, A., Ammann, R. W., Candinas, D., Clavien, P.-A., Eckert, J., Gottstein, B., Halkic, N., Muellhaupt, B., Prinz, B. M., Reichen, J., Tarr, P. E., Torgerson, P. R. and Deplazes, P. (2007). Human alveolar echinococcosis after fox population increase, Switzerland. Emerging Infectious Diseases 13, 878–882.Google Scholar
Sikó, S. B., Deplazes, P., Ceica, C., Tivadar, C., Bogolin, I., Popescu, S. and Cozma, V. (2011). Echinococcus multilocularis in south-eastern Europe (Romania). Parasitology Research 108, 1093–1097.Google Scholar
Sommer, R. and Nadachowski, A. (2006). Glacial refugia of mammals in Europe: evidence from fossil records. Mammal Review 36, 251–265.Google Scholar
Sreter, T., Szell, Z., Egyed, Z. and Varga, I. (2003). Echinococcus multilocularis: an emerging pathogen in Hungary and Central Eastern Europe? Emerging Infectious Diseases 9, 384–386.Google Scholar
Staubach, C., Hoffmann, L., Schmid, V. J., Ziller, M., Tackmann, K. and Conraths, F. J. (2011). Bayesian space–time analysis of Echinococcus multilocularis-infections in foxes. Veterinary Parasitology 179, 77–83.Google Scholar
Štefanić, S., Shaikenov, B., Deplazes, P., Dinkel, A., Torgerson, P. and Mathis, A. (2004). Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (“sheep strain”) in naturally infected dogs. Parasitology Research 92, 347–351.Google Scholar
Stieger, C., Hegglin, D., Schwarzenbach, G., Mathis, A. and Deplazes, P. (2002). Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitology 124, 631–640.Google Scholar
Takumi, K., de Vries, A., Chu, M. L., Mulder, J., Teunis, P. and van der Giessen, J. (2008). Evidence for an increasing presence of Echinococcus multilocularis in foxes in the Netherlands. International Journal for Parasitology 38, 571–578.Google Scholar
Tanner, F., Hegglin, D., Thoma, R., Brosi, G. and Deplazes, P. (2006). Echinococcus multilocularis in Grisons: distribution in foxes and presence of potential intermediate hosts. Schweizer Archiv fur Tierheilkunde 148, 501–510.CrossRefGoogle ScholarPubMed
Trachsel, D., Deplazes, P. and Mathis, A. (2007). Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911–920.Google Scholar
Trewhella, W., Harris, S. and McAllister, F. (1988). Dispersal distance, home-range size and population density in the red fox (Vulpes vulpes): a quantitative analysis. Journal of Applied Ecology 25, 423–434.Google Scholar
Van Gucht, S., Van Den Berge, K., Quataert, P., Verschelde, P. and Le Roux, I. (2010). No emergence of Echinococcus multilocularis in foxes in Flanders and Brussels anno 2007–2008. Zoonoses and Public Health 57, e65–e70.Google Scholar
Veit, P., Bilger, B., Schad, V., Schäfer, J., Frank, W. and Lucius, R. (1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 79–86.Google Scholar
Weber, J. M. and Aubry, S. (2009). Predation by foxes, Vulpes vulpes, on the fossorial form of the water vole, Arvicola terrestris scherman, in western Switzerland. Journal of Zoology 229, 553–559.Google Scholar
Wilson, D. E. and Reeder, D. M. (2005). Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd Edn. Johns Hopkins University Press, Baltimore, MD, USA.Google Scholar