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Completed research project

Title / Titel Surveillance of alveolar echinococcosis and control of Echinococcus multilocularis in Switzerland
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Summary / Zusammenfassung Fox population densities strongly increased in Switzerland in the 1990ies, possibly due to the successful rabies vaccination campaigns which eliminated a main cause of mortality of foxes, and foxes started to colonize urban habitats. The IPZ is involved in parasitological and epidemiological investigations of this phenomenon in the framework of an interdisciplinary project (Integrated Fox Project IFP). It was shown that E. multilocularis is present in urban habitats, and especially in urban peripheries an extraordinarily high environmental contamination with parasite eggs was recorded (Stieger et al. 2002, Fischer et al. 2005, Reperant et al. 2007). In these areas, high urban fox densities overlap with the habitat of the most susceptible intermediate hosts Arvicola terrestris and Microtus arvalis that live on meadows and pastures (Deplazes et al. 2004, Hegglin et al. 2007). It could be demonstrated that E. multilocularis profits from high fox densities sustained in urban settings by a high supply of anthropogenic food (Contesse et al. 2004) and that in the transition zone from urban to rural habitats extraordinary high prevalences can be detected in both the fox populations (Hegglin et al. 2007) and the intermediate hosts (Stieger et al. 2002, Burlet et al. 2011). Thus the force of infection is highest in the urban periphery (Lewis et al. 2014).
E. multilocularis is a widespread and common parasite in red fox populations north of the Alps and the adjacent lowlands. South of the Alps, the parasite has been recorded only occasionally. Climatic conditions that adversely affect the survival of E. multilocularis eggs and the lack of suitable intermediate hosts are thought to be the primary causes limiting the parasite distribution. In the Canton Grisons, local prevalences in foxes varied significantly between 0 and 40% and correlated with the predation rate on voles by foxes. Our results suggest that the life cycle of E. multilocularis in the Alps is confined to mainly small scale hot spots which may persist for decades. This could explain why some human cases of alveolar echinococcosis were recorded in endemic areas whereas no such cases were registered in areas free of E. multilocularis (Tanner et al., 2006). The existence of such stable foci has been confirmed by an ongoing study in the Canton Ticino of southern Switzerland, where the parasite has been regularly confirmed in the North of the Canton and did not spread further south during more the 20 years. The endemic area corresponded with the distribution of the vole Microtus arvalis but not with the distributions of five other vole species, giving evidence that this vole species plays a key role in the maintenance of the parasite life cycle in this region.
The actual epidemiological situation gave reason for a retrospective study on the incidence of human alveolar echinococcosis (AE) in Switzerland. As hypothesised, the incidence has increased and was 2.6 times higher between 2001 and 2005 than in the 1990ies. This increase correlates with the general increase and the urbanisation of the Swiss fox populations (Schweiger et al., 2007). On the other hand, survival analysis revealed a strongly improved prognosis for AE patients over the last 30 years. Mean life expectancy of patients was reduced by 18.2 and 21.3 years for men and women, respectively, in 1970ies whereas these values were 3.5 and 2.6 years in 2005 (Torgerson et al., 2008). The better survival and the higher incidence caused a steady increase of the prevalence. The actual annual burden of disease in Switzerland is approximately 77.6 DALYs and yearly costs amount to approximately €108,762 per patient or a total of € 2.0 million (Torgerson et al., 2008).
In experimental field studies, the feasibility of E. multilocularis control were tested in urban peripheries. The monthly delivery of Praziquantel-containing baits in six areas of 1 km2 and one 2 km2 area for two years successfully reduced the contamination of defined small urban patches with a high E. multilocularis egg contamination to a very low level (Hegglin et al. 2003). A follow-up study revealed also a significant effect when anthelmintic baits were delivered in 3-months intervals only. However, the effect was much less pronounced. Furthermore it was demonstrated that 2 years after finishing a baiting campaign, the infection pressure had returned to the same level as before baiting started (Hegglin and Deplazes, 2008).
Eradication of the parasite is unlikely and long-term baiting campaigns are actually the most effective tool to significantly lower the infection pressure with parasite eggs. As it has been shown that intermediate hosts get more frequently infected during winter season, it can be assumed that reducing the infection pressure on intermediate host by the delivery of anthelmintic baits for foxes is more effective during this season than during the rest of the year (Burlet et al. 2011). Regarding the long latency of 5-15years of alveolar echinococcosis, such measures can only be cost effective if they are pursued for several decades and concentrate on restricted areas which are most relevant for the transmission of alveolar echinococcosis such as highly endemic areas in densely populated zones (Hegglin and Deplazes, 2013).
Considering the high reproduction of E. multilocularis in domestic dogs which live in close contact to humans, a monthly deworming scheme for domestic dogs with access to rodents is likely to be of high importance. This holds true if only low prevalences in domestic dogs are recorded, as high densities of these pets can easily outweigh low infections rates. Thus, in central Europe their estimated contribution to environmental contamination with E. multilocularis eggs ranges between 4% and 19% (Hegglin & Deplazes 2013).
For the planning of locally adapted information campaigns, a survey of public knowledge about the risk and the prevention of alveolar echinococcosis was carried out in the Czech Republic, France, Germany and Switzerland (Hegglin et al. 2008). Fewer people had heard of E. multilocularis in the Czech Republic (14%) and France (18%) compared to Germany (63%) and Switzerland (70%). In France, only 17% of the interviewees who knew the parasite felt reasonably informed in contrast to other countries where the corresponding percentages ranged from 54 to 60%. Promising measures such as deworming dogs were frequently not recognized as prevention options. These results and the actual epidemiological circumstances of AE call for proactive information programs.
Current investigations focus on the transmission potential of common European rodents. In the framework of a European Research program, we investigate the occurrence, frequency and development stages of E. multilocularis in natural occurring rodent populations of different regions and elucidate the ecological and behavioural mechanisms affecting the transmission dynamic of E. multilocularis (e.g. predation and egg distribution of foxes in relation to intermediate host populations).
Publications / Publikationen Hegglin, D., & Deplazes, P.: Control of Echinococcus multilocularis: Strategies, feasibility and cost-benefit analyses. International Journal for Parasitology 43: 327–337 (2013)

Comte, S., Raton, V., Raoul, F., Hegglin, D., Giraudoux, P., Deplazes, P., Favier, S., Gottschek, D., Boué, F., Combes, B.: Fox baiting against Echinococcus multilocularis: Contrasted achievements among two medium size cities. Preventive veterinary medicine 11: 147–155 (2013).

Takumi, K., Hegglin, D., Deplazes, P., Gottstein, B., Teunis, P., Van der Giessen, J.: Mapping the increasing risk of human alveolar echinococcosis in Limburg, The Netherlands. Epidemiology and infection 140: 867-871 (2012).

Schweiger, A., Grimm, F., Tanner, I., Müllhaupt, B., Bertogg, K., Müller, N., Deplazes, P.: Serological diagnosis of echinococcosis: the diagnostic potential of native antigens. Infection: 40: 139-152 (2012).

Deplazes, P., van Knapen, F., Schweiger, A., Overgaauw, P.AM.: Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Veterinary parasitology 182: 41-53 (2011).

Nagy, A., Ziadinov, I., Schweiger, A., Schnyder, M.: Fellkontamination mit Eiern von zoonotischen Helminthen bei Hof- und Haushunden sowie bei Füchsen [Hair coat contamination with zoonotic helminth eggs of farm and pet dogs and foxes]. Berliner und Munchener Tierarztliche Wochenschrift 124: 503-511 (2011).

Burlet, P., Deplazes, P., Hegglin, D.: Age, season and spatio-temporal factors affecting the prevalence of Echinococcus multilocularis and Taenia taeniaeformis in Arvicola terrestris. Parasites & Vectors 56: 685-688 (2011).

Francis, R., Deplazes, P., Rieffel, P., Vuitton, D., Lambert, JC., Giradoux, G. : Predator dietary response to prey density variation and consequences for cestode transmission. Oecologia 164: 129-139 (2010).

Burlet, Pierre, Peter Deplazes, and Daniel Hegglin. 2010. Efficient age determination: how freezing affects eye lens weight of the small rodent species Arvicola terrestris. European Journal of Wildlife Research 56, no. 4 (April): 685-688.

Reperant, L.A., Hegglin, D., Tanner, I., Fischer, C., Deplazes, P.: Rodents as shared indicators for zoonotic parasites of carnivores in urban environments. Parasitology 136: 329-337 (2009).

Knapp, J., Bart, J-M., Giraudoux, P., Glowatzki, M-L., Breyer, I., Raoul, F., Deplazes, P., Duscher, G., Martinek, K., Dubinsky, P., Guislain, M-H., Cliquet, F., Romig, T., Malczweski, A., Gottstein, B., Piarroux, R.: Genetic diversity of the cestode Echinococcous multilocularis in red foxes at a continental scale in Europe. PLoS Negl Trop Dis 3(6): e452 (2009).

Torgerson, P.R., Deplazes, P.: Echinococcosis: diagnosis and diagnostic interpretation in population studies. Trends Parasitol. 25 4: 164-170 (2009).

Torgerson, P.R., Schweiger, A., Deplazes, P., Pohar, M., Reichen, J., Ammann, R.W., Tarr, P.E., Halkik, N., Müllhaupt, B.: Alveolar echinococcosis: From a deadly disease to a well-controlled infection. Relative survival and economic analysis in Switzerland over the last 35 years. J. of Hepatol. 49: 72-77 (2008).

Hegglin, D., Bontadina, F., Gloor, S., Romig, T., Deplazes, P., Kern, P.: Survey of public knowledge about Echinococcus multilocularis in four European countries: Need for proactive information. BMC Public Health 8: 247 (2008).

Hegglin, D., Deplazes, P.: Control strategy for Echinococcus multilocularis. Emerg. Infect. Dis. 14: 1626-1628 (2008).

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., Deplazes, P.: Human alveolar echinococcosis after fox population increase, Switzerland. Emerging Infectious Disease 6: 878-882 (2007).

Trachsel, D., Deplazes, P., Mathis, A.: Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134: 911-920 (2007).

Staebler, S., Steinmetz, H., Keller, S., Deplazes, P.: First description of natural Echinococcus multilocularis infections in chinchilla (Chinchilla laniger) and Prevost’s squirrel (Callosciurus prevostii borneoensis). Parasitol. Res. 101: 1725-1727 (2007).

Reperant, L.A., Hegglin, D., Fischer, C., Kohler, L., Weber J-M., Deplazes, P.: Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland. Parasitol. Res. 101: 605-611 (2007).

Hegglin, D., Bontadina, F., Contesse, P., Gloor, S., Deplazes, P.: Plasticity of predation behaviour as a putative driving force for parasite life-cycle dynamics: the case of urban foxes and Echinococcus multilocularis tapeworm. Funtional Ecology (2007).

Tanner, F., Hegglin, D., Thoma, R., Brosi, G., Deplazes, P.: Echinococcus multilocularis in Graubünden: Verbreitung bei Füchsen und Vorkommen potentieller Zwischenwirte. Schweiz. Arch. Tierheilk. 148: 501-510 (2006).

Fischer, C., Reperant, L.A., Weber, J.M., Hegglin, D., Deplazes, P.: Echinococcus multilocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite 12: 339-346 (2005).

Hegglin, D.. Bontadina, F., Gloor, S., Romer, J., Müller, U., Breitenmoser, U., Deplazes, P.: Baiting red foxes in an urban area: a camera trap study. J. Wildl. Manage. 68: 1010-1017 (2004).

Deplazes, P., Hegglin, D., Gloor, S., Romig, Th.: Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol. 20: 77-84 (2004).

Hegglin, D., Ward, P.I., Deplazes, P.: Anthelmintic baiting of foxes against urban contamination with Echinococcus multilocularis. Emerg. Infect. Dis. 9: 1266-1272 (2003).

Stieger, C., Hegglin, D., Schwarzenbach, G., Mathis, A., Deplazes, P.: Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitology 124: 631-640 (2002).

Gloor, S., Bontadina, F., Hegglin, D., Deplazes, P., Breitenmoser, U.: The rise of urban fox populations in Switzerland. Mamm. Biol. 66: 155-164 (2001).

Hofer, S., Gloor, S., Müller-Doblies, U., Mathis, A., Hegglin, D., Deplazes, P.: 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 (2000).

Conraths F J, Peter Deplazes P (2015). Echinococcus multilocularis: epidemiology, surveillance and state-of-the-art diagnostics from a veterinary public health perspective. Vet. Parasitol. In press.

Hegglin D, Bontadina F, Deplazes P. (2015)Human-wildlife interactions and zoonotic transmission of Echinococcus multilocularis. Trends Parasitol. 2015 Jan 16. pii: S1471-4922(14)00207-4. doi: 10.1016/ [Epub ahead of print].

Guerra D, Hegglin D, Bacciarini L, Schnyder M, Deplazes P. Stability of the southern European border of Echinococcus multilocularis in the Alps: evidence that Microtus arvalis is a limiting factor. Parasitology. 2014 Jun 16:1-10.

Isaksson M, Hagström Å, Armua-Fernandez M, Wahlström H, Ågren E, Miller A, Holmberg A, Lukacs M, Casulli A, Deplazes P, Juremalm M. A semi-automated magnetic capture probe based DNA extraction and real-time PCR method applied in the Swedish surveillance of Echinococcus multilocularis in red fox ( Vulpes vulpes ) faecal samples. Parasit Vectors. 2014 Dec 19;7(1):583. [Epub ahead of print].

Keywords / Suchbegriffe Alveolar echinococcosis, control, Echinococcus multilocularis, epidemiology, Switzerland
Project leadership and contacts /
Projektleitung und Kontakte
Prof. Peter Deplazes (Project Leader)
Dr. Daniel Hegglin
Dr. Maria Teresa Armua-Fernandez
Diogo Ribeiro Almeida Guerra
Olivia Beerli
Funding source(s) /
Unterstützt durch
Federal Veterinary Office, Grün Stadt Zürich, Stiftung Echinococcose; EU-Project EMIDA (Emerging and Major Infectious Diseases of Livestock)
In collaboration with /
In Zusammenarbeit mit
PD Dr. Beat Müllhaupt, Klinik für Gastroenterologie und Hepatologie, Universitätsspital Zürich Switzerland
Dr. S. Gloor and Dr. F. Bontadina, WILD, Urban Ecology and Wildlife Research, Zurich Switzerland
Prof. Paul R. Torgerson, Leitung der Abteilung Veterinärepidemiologie, Vetsuisse-Fakultät, Universität Zürich Switzerland
Duration of Project / Projektdauer Jan 2000 to Dec 2016