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

Parasitology

Volumn 141, Issue 12, 2014, Pages 1593-1602

  Guerra, Diogo ^a   Hegglin, Daniel ^a   Bacciarini, Luca ^b   Schnyder, Manuela ^a   Deplazes, Peter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b Cantonal Veterinary Office   (Switzerland)

Author keywords

distribution; Echinococcus multilocularis; fox; Microtus arvalis; rodents; Switzerland

Indexed keywords

ARTICLE; ECHINOCOCCUS MULTILOCULARIS; GEOGRAPHIC DISTRIBUTION; HOME RANGE; LATITUDE; MICROTUS ARVALIS; MORPHOLOGICAL TRAIT; MULTIPLEX POLYMERASE CHAIN REACTION; NONHUMAN; PRIORITY JOURNAL; SWITZERLAND;

CANIDAE; ECHINOCOCCUS MULTILOCULARIS; MICROTUS ARVALIS; MURIDAE; RODENTIA;

EID: 84906793886     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182014000730     Document Type: Article

References (67)

1. Alther, P. (1996). Beitrag zur Epidemiologie und Diagnose der Echinococcus multilocularis - Infektion bei Endwirten. Vet Med thesis. University of Zurich, Zurich, Switzerland.
2. 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.
3. 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.
4. 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.
5. Brossard, M., Andreutti, C. and Siegenthaler, M. (2007). Infection of red foxes with Echinococcus multilocularis in western Switzerland. Journal of Helminthology 81, 369-376.
6. 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.
7. Burlet, P., Deplazes, P. and Hegglin, D. (2011). Age, season and spatiotemporal factors affecting the prevalence of Echinococcus multilocularis and Taenia taeniaeformis in Arvicola terrestris. Parasites and Vectors 4, 1-9.
8. 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.
9. 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.
10. 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.
11. 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.
12. Delattre, P., Giraudoux, P. and Quéré, J.-P. (1990). Conséquences épidémiologiques de la ré ceptivité 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. Giraudoux, P., Raoul, F., Afonso, E., Ziadinov, I., Yang, Y., Li, L., Li, T., Quéré, J.-P., Feng, X. and Wang, Q. (2013a). Transmission ecosystems of Echinococcus multilocularis in China and Central Asia. Parasitology 140, 1655-1666.
24. Giraudoux, P., Raoul, F., Pleydell, D., Li, T., Han, X., Qiu, J., Xie, Y., Wang, H., Ito, A. and Craig, P. S. (2013b). 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.
25. 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.
26. 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.
27. Hausser, J. (1995). Säugetiere der Schweiz. Birkhauser, Basel, Switzerland.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. Macdonald, D. (1977). On food preference in the red fox. Mammal Review 7, 7-23.
36. 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.
37. 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.
38. Manfredi, M., Genchi, C., Deplazes, P., Trevisiol, K. and Fraquelli, C. (2002). Echinococcus multilocularis infection in red foxes in Italy. Veterinary Record 150, 757.
39. 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.
40. 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.
41. Moks, E., Saarma, U. and Valdmann, H. (2005). Echinococcus multilocularis in Estonia. Emerging Infectious Diseases 11, 1973-1974.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. Rietschel, G. (1981). Beitrag zur Kenntnis von Taenia crassiceps (Zeder, 1800) Rudolphi, 1810 (Cestoda, Taeniidae). Zeitschrift für Parasitenkunde 65, 309-315.
50. 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.
51. 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.
52. Schneider, R., Aspöck, H. and Auer, H. (2013). Unexpected increase of alveolar echinococcosis, Austria, 2011. Emerging Infectious Diseases 19, 475-477.
53. 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.
54. 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.
55. Sommer, R. and Nadachowski, A. (2006). Glacial refugia of mammals in Europe: evidence from fossil records. Mammal Review 36, 251-265.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.