Echinococcus multilocularis (Leuckart, 1863)

Mackenstedt, Ute, Jenkins, David & Romig, Thomas, 2015, The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas, International Journal for Parasitology: Parasites and Wildlife 4 (1), pp. 71-79 : 73-74

2.2. E. multilocularis in urban and peri-urban areas of Europe

Until the 1990s, AE in central Europe was considered to be a disease associated with rural areas and farming activities ( Auer and Aspöck, 1991). Since then, the annual incidence of human AE has increased at least in parts of the region ( Schweiger et al., 2007), a development which seems to be correlated with the general increase of European fox populations beginning in the early 1990s ( Chautan et al., 2000). In addition, human cases are being reported increasingly from urban areas (cit. in Deplazes et al., 2011), which appear to be a consequence of the urbanization of the E. multilocularis life cycle.

For most of the 20th century, foxes outside Britain were not known to occur in larger towns and cities, and the principal intermediate hosts, M. arvalis and Arvicola scherman , are typical rodents of meadows, pastures and orchards in rural landscapes. From that time onwards, however, habitat preferences of some red fox populations have changed. Regular sightings of foxes inside larger human settlements were first reported from the middle of the 1990s, and by the early 2000s several larger cities of central Europe were known to support resident fox populations ( Deplazes et al., 2004). The most obvious characteristic of these ‘urban foxes’ is tolerance of disturbing factors like traffic and the immediate vicinity of humans and pet animals. Initially, this phenomenon was thought to be the result of population pressure from rural areas to less suitable urban habitats in the wake of general fox population increases in the 1990s (probably aided by reduced mortality after successful rabies vaccinations – Chautan et al., 2000). Genetic studies, however, showed that populations of ‘urban foxes’ are self-sustaining and show reduced gene flow to and from surrounding rural populations ( Wandeler et al., 2003). Typically, these synanthropic foxes live in higher population densities than their rural counterparts, aided by sufficient and seasonally stable food from anthropogenic sources ( Contesse et al., 2004). For urban and suburban areas in Switzerland and southern Germany, radio-tracking data suggest densities of> 10 resident adult foxes per km 2 ( Deplazes et al., 2004), compared with <3 per km 2 in rural areas ( Heydon et al., 2000; Thoma, 2008; Janko et al., 2012).

Relatively few studies have been conducted on the infection of such foxes with E. multilocularis . Reported prevalences in different cities and towns vary drastically, being e.g. 4% in Nancy ( France) and 44% in Zurich ( Switzerland) ( Deplazes et al., 2004; Robardet et al., 2008). ‘Urban’ E. multilocularis life cycles are assumed to result from the establishment of these synanthropic fox populations. However, earlier presence of the parasite in urban areas cannot be excluded, since relevant studies were only initiated after the urban fox phenomenon was recognized. At least in the periphery of cities and towns, rural (‘shy’) foxes are known to utilize anthropogenic food sources and might be able to maintain a certain level of transmission inside the settlement area. The same applies for domestic dogs, whose generally low E. multilocularis prevalence is compensated by their extremely large numbers in urban and peri-urban areas ( Deplazes et al., 2011; Hegglin and Deplazes, 2013). In any case, the prevalence of E. multilocularis in synanthropic foxes is the only practically available indicator for presence and frequency of the parasite. Data suggest that, even as fox population densities increase from rural through peri-urban to urban areas, E. multilocularis frequency shows the opposite trend, e.g. in the cities of Zurich, Geneva, Stuttgart and Nancy ( Deplazes et al., 2004; Robardet et al., 2008; Reperant et al., 2009). This is usually explained by decreased availability of suitable intermediate hosts in highly urbanized areas, which either depend on extensively managed grassland which becomes increasingly rare towards city centers ( M. arvalis ), or which are not as easily accessible as prey for foxes due to low density, burrowing habits or size ( A. scherman , M. glareolus, Ondatra zibethicus ) ( Robardet et al., 2011). Based on population densities of both foxes and rodents, peri-urban areas appear to be focal points for transmission of E. multilocularis . Such areas are characterized by (1) higher population densities of foxes compared to strictly rural landscapes (as foxes are able to supplement their ‘natural’ food sources with anthropogenic sources like waste or pet food), (2) presence of intermediate host species at sufficient frequency to serve as regular fox prey (even though at reduced densities or with patchy distribution compared to strictly rural landscapes), and (3) high density of humans and their pet animals. E. multilocularis prevalence of foxes in such areas is usually lower than in adjacent rural habitats (reflecting the reduced availability of intermediate hosts), but this is counteracted by the larger fox densities. Such peri-urban areas are a contact zone between humans and infected foxes and therefore – hypothetically – more important than rural (few humans) or highly urbanized areas (few infected animals). In addition, dogs and cats can complement the life cycle of E. multilocularis when preying on rodents, e.g. in the city periphery or in parks and gardens ( Deplazes et al., 2004). Although cats are known to be inferior hosts for this parasite, and dogs are generally rarely infected, dogs in particular are thought to be an important conduit for human infection due to their frequent and close contact (compared to foxes) with people ( Kapel et al., 2006). In addition, even at very low prevalences, dogs may also contribute substantially to transmission due to their large number: it has been estimated that, under urban conditions, dogs may contribute 6.8–18.9% of the total egg output of all definitive hosts combined ( Hegglin and Deplazes, 2013).

A definition of ‘urban’ or ‘peri-urban’ life cycless for E.multilocularis is difficult to formulate for a number of reasons. Even within a region like central Europe, the character of urbanization varies considerably. Size, distribution and management of ‘green’ areas inside human settlements differ, which has an impact on the suitability of these areas as habitats for host species. At the periphery of cities, there is necessarily a contact zone between typical synanthropic fox populations and those from surrounding rural areas that also exploit anthropogenic food sources using different strategies. The dependency of urban E. multilocularis life cycles on these ‘periphery’ foxes (whose home ranges can include both agricultural grassland and urban parts) is not known. Likewise, it is unclear which species of intermediate hosts can maintain the life cycle in urban/peri-urban areas. For open landscapes of central Europe, stable populations of common voles ( M. arvalis ) seem to be more important for the parasite than any other rodent species ( Guerra et al., 2014), and some data from France suggest that this may also be the case for cities and towns ( Robardet et al., 2011). Water voles ( A. sherman ) can be frequently infected in city parks and gardens (e.g. 9.1% in Zurich - Stieger et al., 2002), although their role in transmission is less clear. Likewise, 15.2% of 46 muskrats ( O. zibethicus ) were found to be infected at a recreational lake within the city of Stuttgart, Germany (Romig, unpublished), but their impact on transmission may be marginal due to localized occurrence and low predation by foxes. There are considerable gaps of knowledge concerning such basic epidemiological parameters. Better understanding of urban/periurban life cycles and their link with the surrounding ‘rural’ landscape, however, is crucial for the development of countermeasures against the parasite which have been specifically recommended for peri-urban areas with increased fox–human contact ( Hegglin and Deplazes, 2013). Various deworming schemes using anthelmintic fox baits have been described from Europe and Japan ( Ito et al., 2003; Hegglin and Deplazes, 2013). In urban areas, they were conducted with different degrees of success, and comparative data from two French studies indicate that failure in one area is linked to parasite infection pressure from surrounding landscapes ( Comte et al., 2013). In conclusion, it is apparent that even within Europe, there is no uniform pattern of urban/peri-urban transmission of E. multilocularis , and even less so when comparing areas (e.g. in Japan or North America) where other host species with different ecological requirements occur.