Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T22:54:18.210Z Has data issue: false hasContentIssue false
  • English
  • Français

Ecological and biological factors involved in the transmission of Echinococcus multilocularis in the French Ardennes

Published online by Cambridge University Press:  01 June 2008

Marie-Hélène Guislain ,
Francis Raoul ,
Patrick Giraudoux ,
Marie-Eve Terrier ,
Guillaume Froment ,
Hubert Ferté  and
Marie-Lazarine Poulle
Marie-Hélène Guislain
Affiliation:
Department of Environmental Biology, EA 3184-usc INRA, University of Franche-Comté, 1 place Leclerc, 25030Besançon, France 2C2A-CERFE, 5 rue de la Héronnière, 08240Boult-aux-Bois, France
Francis Raoul
Affiliation:
Department of Environmental Biology, EA 3184-usc INRA, University of Franche-Comté, 1 place Leclerc, 25030Besançon, France
Patrick Giraudoux
Affiliation:
Department of Environmental Biology, EA 3184-usc INRA, University of Franche-Comté, 1 place Leclerc, 25030Besançon, France
Marie-Eve Terrier
Affiliation:
AFSSA-LERRPAS, Technopôle Agricole et Vétérinaire, B.P. 40 009, 54220Malzeville, France
Guillaume Froment
Affiliation:
EA 3800, UFR de Pharmacie-Médecine, IFR 53, 51 rue Cognac-Jay, 51096Reims Cedex, France
Hubert Ferté
Affiliation:
EA 3800, UFR de Pharmacie-Médecine, IFR 53, 51 rue Cognac-Jay, 51096Reims Cedex, France
Marie-Lazarine Poulle*
Affiliation:
2C2A-CERFE, 5 rue de la Héronnière, 08240Boult-aux-Bois, France EA 3800, UFR de Pharmacie-Médecine, IFR 53, 51 rue Cognac-Jay, 51096Reims Cedex, France
*
*Fax: +33 (0) 324 30 67 81 E-mail: marielazarine.poulle@cerfe.com
Get access Rights & Permissions [Opens in a new window]

Abstract

In order to identify the respective importance of the ecological and biological factors involved in the transmission of Echinococcus multilocularis, we estimated grassland vole intermediate host (Microtus sp. and Arvicola terrestris) population densities, in relation to the diet of the definitive host (red fox, Vulpes vulpes) and with the prevalence of E. multilocularis in the fox population. The study was conducted in the Ardennes, north-eastern France, which is an area with a high incidence of alveolar echinococcosis. Surface index methods showed that Microtus was the most abundant intermediate host in the area. Furthermore, Microtus was present in one-third of the 144 faeces and 98 stomach content samples examined and represented more than two-thirds of the rodent occurrences. Red fox predation on Microtus was significantly correlated with Microtus relative abundance. In contrast, the relative abundance of A. terrestris was very low. This species, as well as Clethrionomys glareolus and Apodemus sp., was little consumed. E. multilocularis prevalence in foxes was determined from carcasses and reached 53% (95% confidence interval 45–61%). Intensity of infection varied from 2 to 73,380 worms per fox, with 72% of the sampled worm burden harboured by 8% of the sampled foxes. The selected explanatory variables (sex, year, age class, health and nutritional condition, and season) failed to predict prevalence rate and worm burden. The high prevalence rate in foxes indicates the possibility of intense E. multilocularis transmission, apart from periods, or in landscapes, favourable to large population outbreaks of grassland rodents.

Type
Research Papers
Information
Journal of Helminthology , Volume 82 , Issue 2 , June 2008 , pp. 143 - 151
Copyright
Copyright © Cambridge University Press 2008

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

Anderson, D.R., Link, W.A., Johnson, D.H. & Burnham, K.P. (2001) Suggestions for presenting the results of data analyses. Journal of Wildlife Management 65, 373–378.CrossRefGoogle Scholar
Artois, M. (1989) Le renard roux (Vulpes vulpes Linneaus, 1758). 90 pp. Société Française pour l'Étude et la Protection des Mammifères.Google Scholar
Bart, J.M., Breyer, I., Gottstein, B., Romig, T. & Piarroux, R. (2003) Development of molecular tools to explore genetic diversity in Echinococcus multilocularis. Helminthologia 40, 117–121.Google Scholar
Berke, O. (2001) Choropleth mapping of regional count data of Echinococcus multilocularis among red foxes in Lower Saxony, Germany. Preventive Veterinary Medicine 52, 119–131.CrossRefGoogle ScholarPubMed
Bresson-Hadni, S., Laplante, J.J., Lenys, D., Rohmer, P., Gottstein, B., Jacquier, P., Mercet, P., Meyer, J.P., Miguet, J.P. & Vuitton, D.A. (1994) Seroepidemiologic screening of Echinococcus multilocularis infection in an European area endemic for alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 51, 837–846.CrossRefGoogle Scholar
Burnham, K.P. & Anderson, D.R. (2002) Model selection and multimodel inference: a practical information-theoretic approach. 496 pp. 2nd edn.New York, Springer.Google Scholar
Chalon, P.X., Brochier, B., Bauduin, B., Mosselmands, F. & Pastoret, P.P. (1998) Structure d'âge et sexe ratio d'une population de renards roux (Vulpes vulpes) en Belgique. Cahiers d'éthologie 18, 17–38.Google Scholar
Ciucci, P., Boitani, L., Pelliccioni, E.R., Rocco, M. & Guy, I. (1996) A comparison of scat-analysis methods to assess the diet of the wolf Canis lupus. Wildlife Biology 2, 37–48.CrossRefGoogle Scholar
Craig, P. (2003) Echinococcus multilocularis. Current Opinion in Infectious Diseases 16, 437–444.CrossRefGoogle ScholarPubMed
Debrot, S., Fivaz, G., Mermod, C. & Weber, J.M. (1982) Atlas des poils de mammifères d'Europe. 208 pp. Neuchâtel, Université de Neuchâtel.Google Scholar
Delattre, P., Giraudoux, P., Baudry, J., Quéré, J.P. & Fichet, E. (1996) Effect of landscape structure on Common Vole (Microtus arvalis) distribution and abundance at several space scales. Landscape Ecology 11, 279–288.CrossRefGoogle Scholar
Delattre, P., de Sousa, B., Fichet-Calvet, E., Quéré, J.P. & Giraudoux, P. (1999) Vole outbreaks in a landscape context: evidence from a six year study of Microtus arvalis. Landscape Ecology 14, 401–412.CrossRefGoogle Scholar
Depaquit, J., Gallego, A., Usseglio, F., Liance, M. & Favriel, J.M. (1998) L'échinococcose alvéolaire dans le département français des Ardennes: cas isolés ou nouveau foyer? Parasite 5, 285–287.CrossRefGoogle Scholar
Duscher, G., Pleydell, D., Prosl, H. & Joachim, A. (2006) Echinococcus multilocularis in Austrian foxes from 1999 until 2004. Journal of Veterinary Medicine Series B 53, 138–144.CrossRefGoogle ScholarPubMed
Eckert, J. (2003) Predictive values and quality control of techniques for the diagnosis of Echinococcus multilocularis in definitive hosts. Acta Tropica 85, 157–163.CrossRefGoogle ScholarPubMed
Eckert, J., Gottstein, B., Heath, D. & Liu, F.J. (2001a) Prevention of echinococcosis in humans and safety precautions. pp. 238–247in Eckert, J., Gemmell, M.A., Meslin, F.X. & Pawloswki, Z.S. (Eds) WHO/OIE manual on echinococcosis in humans and animals: A public health problem of global concern. Paris, Office International des Epizooties.Google Scholar
Eckert, J., Rausch, R.L., Gemmell, M.A., Giraudoux, P., Kamiya, M., Liu, F.J., Schantz, P.M. & Romig, T. (2001b) Epidemiology of Echinococcus multilocularis, Echinococcus vogeli and Echinococcus oligarthrus. pp. 164–182in Eckert, J., Gemmell, M.A., Meslin, F.X. & Pawloswki, Z.S. (Eds) WHO/OIE manual on echinococcosis in humans and animals: A public health problem of global concern. Paris, Office International des Epizooties.Google Scholar
Erome, G. & Aulagnier, S. (1982) Contribution à l'identification des proies des rapaces. Bièvre 4, 129–135.Google Scholar
Ferrari, N. & Weber, J.M. (1995) Influence of the abundance of food resources on the feeding habits of the red fox, Vulpes vulpes, in western Switzerland. Journal of Zoology (London) 236, 117–129.CrossRefGoogle Scholar
Fichet-Calvet, E., Jomaa, I., Giraudoux, P. & Ashford, W. (1999) Estimation of sand rat abundance by using surface indices. Acta Theriologica 44, 353–362.CrossRefGoogle Scholar
Fischer, C., Reperant, L.A., Weber, J.M., Hegglin, D. & Deplazes, P. (2005) Echinococcus multilocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite 12, 339–346.CrossRefGoogle Scholar
Fromont, E., Sager, A., Léger, F., Bourgmestre, F., Jouquelet, E., Stahl, P., Pontier, D. & Artois, M. (2000) Prevalence and pathogenicity of retroviruses in wildcats in France. Veterinary Record 146, 317–319.CrossRefGoogle ScholarPubMed
Gemmell, M.A., Roberts, M.G., Beard, T.C. & Lawson, J.R. (2001) Quantitative epidemiology and transmission dynamics with special reference to Echinococcus granulosus. pp. 143–156in Eckert, J., Gemmell, M.A., Meslin, F.X. & Pawloswki, Z.S. (Eds) WHO/OIE manual on echinococcosis in humans and animals: A public health problem of global concern. Paris, Office International des Epizooties.Google Scholar
Giraudoux, P. (2006) pgirmess: data analysis in ecology. R package version 1.2.2. Available athttp://lbe.univ-fcomte.fr/telechar/div.html.Google Scholar
Giraudoux, 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
Giraudoux, P., Delattre, P., Takahashi, K., Raoul, F., Quéré, J.P., Craig, P. & Vuitton, D. (2002) Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multiscale approaches? pp. 251–266in Craig, P.S. & Pawlowski, Z.S. (Eds) Cestode zoonoses: Echinococcosis and cysticercosis. Amsterdam, IOS Press.Google Scholar
Giraudoux, P., Craig, P.S., Delattre, P., Bao, G., Bartholomot, B., Harraga, S., Quéré, J.P., Raoul, F., Wang, Y., Shi, D. & Vuitton, D.A. (2003) Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127, S1–S11.CrossRefGoogle ScholarPubMed
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, 408–412.CrossRefGoogle ScholarPubMed
Guislain, M.H., Raoul, F., Poulle, M.L. & Giraudoux, P. (2007) Fox faeces and vole distribution on a local range: ecological data in a parasitological perspective for Echinococcus multilocularis. Parasite 14, in press.CrossRefGoogle Scholar
Hansen, F., Tackmann, K., Jeltsch, F., Wissel, C. & Thulke, H.H. (2003) Controlling Echinococcus multilocularis – ecological implications of field trials. Preventive Veterinary Medicine 60, 91–105.CrossRefGoogle ScholarPubMed
Hansson, L. (1979) Field signs as indicators of vole abundance. Journal of Applied Ecology 16, 339–347.CrossRefGoogle Scholar
Hegglin, D., Bontadina, F., Contesse, P., Gloor, S. & 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.CrossRefGoogle Scholar
Henry, C., Poulle, M.L. & Roeder, J.-J. (2005) Effect of sex and female reproductive status on seasonal home range size and stability in rural red foxes (Vulpes vulpes). Ecoscience 12, 2002–2009.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 Zurïch, Switzerland. Parasitology 120, 135–142.CrossRefGoogle ScholarPubMed
Hudson, P.J., Rizzoli, A., Grenfell, B.T., Heersterbeek, H. & Dobson, A.P. (2002) The ecology of wildlife disease. 197 pp. New York, Oxford University Press.CrossRefGoogle Scholar
Knapp, J., Bart, J.M., Glowatzki, M.L., Ito, A., Gerard, S., Maillard, S. & Piarroux, R. (2007) Assessment of microsatellite polymorphism for improving the spatial distribution tracking of Echinococcus multilocularis. Journal of Clinical Microbiology 45, 2943–2950.CrossRefGoogle ScholarPubMed
König, A., Romig, T., Thoma, D. & Kellermann, K. (2005) Drastic increase of the prevalences of Echinococcus multilocularis in fox (Vulpes vulpes) in southern Bavaria, Germany. European Journal of Wildlife Research 51, 277–282.CrossRefGoogle Scholar
Kritsky, D.C. & Leiby, P.D. (1978) Studies on sylvatic echinococcosis. V. Factors influencing prevalence of Echinococcus multilocularis Leuckart 1863, in red foxes from North Dakota, 1965–1972. Journal of Parasitology 64, 625–634.CrossRefGoogle ScholarPubMed
Losson, B., Kervyn, T., Detry, J., Pastoret, P.P., Mignon, B. & Brochier, B. (2003) Prevalence of Echinococcus multilocularis in the red fox (Vulpes vulpes) in southern Belgium. Veterinary Parasitology 117, 23–28.CrossRefGoogle ScholarPubMed
MacDonald, D.W. (1977) On food preference in the red fox. Mammal Revue 7, 7–23.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, 121–134.CrossRefGoogle ScholarPubMed
Petavy, A.F. & Deblock, S. (1980) Helminthes du renard commun (Vulpes vulpes L.) dans la région du Massif Central (France). Annales de Parasitologie Paris 40, 191–197.Google Scholar
Piarroux, M., Bresson-Hadni, S., Capek, I., Knapp, J., Watelet, J., Dumortier, J., Abergel, A., Minello, A., Gérard, A., Beytout, J., Piarroux, R., Kantelop, B., Delabrousse, E., Vaillant, V. & Vuitton, D.A. for FrancEchino, . (2006) Surveillance de l'échinococcose alvéolaire en France: bilan de cinq années d'enregistrement, 2001–2005. Bulletin d'Épidémiologie Hebdomadaire 27–28, 11–12.Google Scholar
Pleydell, D.R.J., Raoul, F., Vaniscotte, A., Craig, P.S. & Giraudoux, P. (2006) Towards understanding the impacts of environmental variation on Echinococcus multilocularis transmission. pp. 545–654in Morand, S., Krasnov, B. & Poulin, R. (Eds) Micromammals and macroparasites. Berlin, Springer.CrossRefGoogle Scholar
Poulle, M.L. (1991) Eco-éthologie du renard roux (Vulpes vulpes L.) en Lorraine: influence du mode de distribution des ressources sur le partage de l'espace et les relations interindividuelles. PhD thesis, University Louis Pasteur, Strasbourg.Google Scholar
Quéré, J.P., Raoul, F., Giraudoux, P. & Delattre, P. (2000) An index method of estimating relative population densities of the common vole (Microtus arvalis) at landscape scale. Revue d'Ecologie (Terre Vie) 55, 25–31.CrossRefGoogle Scholar
Raoul, F. (2001) Écologie de la transmission d'Echinococcus multilocularis chez le renard dans l'Est de la France: dépendance au paysage et à la relation proie-prédateur? PhD thesis, University of Franche-Comté.Google Scholar
Raoul, F., Nonaka, N., Piarroux, R., Vuitton, D.A. & Giraudoux, P. (2001a) 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, 1579–1588.CrossRefGoogle ScholarPubMed
Raoul, F., Defaut, R., Michelat, D., Montadert, M., Pépin, D., Quéré, J.P., Tissot, B., Delattre, P. & Giraudoux, P. (2001b) Landscape effects on the population dynamics of small mammal communities: a preliminary analysis of prey–resource variations. Revue d'Ecologie (Terre Vie) 56, 339–351.CrossRefGoogle Scholar
Raoul, F., Michelat, D., Ordinaire, M., Décoté, Y., Aubert, M., Delattre, P., Deplazes, P. & 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, 945–954.CrossRefGoogle Scholar
Rausch, R.L. (1995) Life-cycle patterns and geographic distribution of Echinococcus species. pp. 88–134in Thompson, R.C.A. & Lymbery, A.J. (Eds) Echinococcus and hydatid disease. Wallingford, CAB International.Google Scholar
Romig, T., Bilger, B., Dinkel, A., Merli, M. & Mackenstedt, U. (1999a) Echinococcus multilocularis in animal hosts: a new data from western Europe. Helminthologia 36, 185–191.Google Scholar
Romig, T., Kratzer, W., Kimmig, P., Frosch, M., Gaus, W., Flegel, W.A., Gottstein, B., Lucius, R., Beckh, K. & Kern, P. (1999b) An epidemiologic survey of human alveolar echinococcosis in southwestern Germany. American Journal of Tropical Medicine and Hygiene 61, 566–573.CrossRefGoogle ScholarPubMed
Romig, T., Dinkel, A. & Mackenstedt, U. (2006) The present situation of echinococcosis in Europe. Parasitology International 55, S187–S191.CrossRefGoogle ScholarPubMed
Saitoh, T. & Takahashi, K. (1998) The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes. Research in Population Ecology 40, 97–105.CrossRefGoogle Scholar
Siegel, S. & Castellan, N.J.J. (1988) Non parametric statistics for the behavioural sciences. 399 pp. New York, McGraw-Hill International Editions.Google Scholar
Tackmann, K., Löschner, U., Mix, H., Staubach, C., Thulke, H.H. & Conraths, F.J. (1998) Spatial distribution patterns of Echinococcus multilocularis (Leukart 1863) (Cestoda: Cyclophyllidea: Taeniidae) among red foxes in an endemic focus in Brandenburg, Germany. Epidemiology and Infection 120, 101–109.CrossRefGoogle Scholar
Tanner, F., Hegglin, D., Thoma, R., Brosi, G. & Deplazes, P. (2006) Echinococcus multilocularis in Graubünden: verbreitung bei Füchsen und Vorkommen potentieller Zwischenwirte. Schweizer Archiv für Tierheilkunde 148, 501–510.CrossRefGoogle Scholar
Viel, J.F., Giraudoux, P., Abrial, V. & 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, 559–565.CrossRefGoogle ScholarPubMed
Vuitton, D.A., Zhou, H., Bresson-Hadni, S., Wang, Q., Piarroux, R., Raoul, F. & Giraudoux, P. (2003) Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127, S87–S107.CrossRefGoogle ScholarPubMed
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
Wilson, K., Bjørnstad, O.N., Dobson, A.P., Merler, S., Poglayen, G., Randolph, S.E., Read, A.F. & Skorping, A. (2002) Heterogeneities in macroparasite infections: patterns and processes. pp. 6–44in Hudson, P.J., Rizzoli, A., Grenfell, B.T., Heesterbeek, H. & Dobson, A.P. (Eds) The ecology of wildlife diseases. Oxford, Oxford University Press.CrossRefGoogle Scholar
Yimam, A.E., Nonaka, N., Oku, Y. & Kamiya, M. (2002) Prevalence and intensity of Echinococcus multilocularis in red foxes (Vulpes vulpes schrencki) and raccoon dogs (Nyctereutes procyonoides albus) in Otaru city, Hokkaïdo, Japan. Japanese Journal of Veterinary Research 49, 287–296.Google ScholarPubMed