Daniel Hegglin

High prevalence of Echinococcus multilocularis in urban red foxes ( Vulpes vulpes ) and voles ( Arvicola terrestris ) in the city of Zürich, Switzerland

Over a period of 26 months from January 1996 to February 1998, 388 foxes from the city of Zürich, Switzerland, were examined for intestinal infections with Echinococcus multilocularis and other helminths. The prevalence of E. multilocularis in foxes sampled during winter increased significantly from 47% in the urban to 67% in the adjacent recreational area, whereas prevalence rates of other helminths were similar in both areas. Seasonal differences in the prevalence of E. multilocularis were only found in urban subadult male foxes which were significantly less frequently infected in summer than in winter. The distribution of the Echinococcus biomass, as expressed by worm numbers per fox was overdispersed in 133 infected foxes randomly sampled in winter. Ten of these foxes (8%) were infected with more than 10,000 specimens and carried 72% of the total biomass of E. multilocularis (398,653 worms). Prevalences did not differ significantly in these foxes in regard to age and sex but worm burdens were significantly higher in subadult foxes as compared with adult foxes. In voles (Arvicola terrestris) trapped in a city park of Zürich, E. multilocularis metacestodes were identified by morphological examination and by PCR. The prevalence was 20% among 60 rodents in 1997 and 9% among 75 rodents in 1998. Protoscoleces occurred in 2 of the cases from 1997. The possible risk for human infection is discussed with respect to the established urban E. multilocularis cycle.

The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zurich, Switzerland

Summary The diet of urban foxes and the availability of anthropogenic food were studied in the city of Zurich, Switzerland. A stomach analysis of 402 foxes, which were shot or found dead between January 1996 and March 1998, showed a broad variety in the diet of urban foxes, with a dominance of scavenged meat, other scavenge and cultivated fruit and crops. More than half of an average stomach content was anthropogenic. The proportion of anthropogenic food was increased in stomachs from the city centre – mainly due to the increasing proportion of scavenged meat – compared with stomachs from the periurban area. Significant seasonal variations in the diet were found for invertebrates, birds and for cultivated fruit and crops, which were all most frequently consumed in summer. A written survey among the inhabitants of three municipal districts showed that 85% of the households provided anthropogenic food which was accessible to foxes. This food supply consisted of three quarters of rubbish and compost, completed by fruit and berries and, to a lesser extent, food provisions for pets, birds, and other wild animals. In contrast, the anthropogenic food supply of allotment gardens mainly consisted of berries, completed by fruit, compost and birdseed. The anthropogenic food supply in public areas was determined by transects. The overall food supply of households, allotment gardens and public areas would be sufficient to feed a much higher number of foxes than currently present. This overabundance of food resources could explain the continual increase of urban population densities. A possible further exploitation of anthropogenic food sources is discussed considering its specific characteristics and the necessary behavioural adaptations.

Spatial and temporal aspects of urban transmission of Echinococcus multilocularis

High prevalences of Echinococcus multilocularis have been reported from foxes of the city of Zurich, Switzerland. In order to characterize transmission in urban areas, a coproantigen ELISA was evaluated for diagnosing the infection in fox faecal samples collected in the environment. In addition, trapped rodents were investigated for the presence of metacestodes. Faecal samples could reliably be classified as being of fox origin by assessing physical properties as shown by the different parasite spectra of putative fox and dog faecal specimens. From the total of 604 tested putative fox faecal samples 156 (25.8%) were positive in the ELISA with a distinct increase in the proportion of positive samples from the urban to the periurban zone. Furthermore, samples collected in the border zone had significantly more coproantigen-positive results during winter. Prevalence of E. multilocularis in rodents was 9.1% (81/889) for Arvicola terrestris (with 3.5% of the animals harbouring between 14 and 244400 protoscoleces) and 2.4% (2/83) for Clethrionomys glareolus. E. multilocularis-infected A. terrestris were found in 9 of 10 trapping sites in the border zone. The high infection pressure in the periphery of urban areas might pose a risk for infection with E. multilocularis for both domestic carnivores as well as for urban inhabitants. Interventions into the cycle aiming at reducing the infection pressure should therefore focus on these areas.

The invasive mosquito Aedes japonicus in Central Europe

Complaints about a biting pest led to the recognition of invasive Aedes (Finlaya) japonicus japonicus (Theobald) (Diptera: Culicidae) in Central Europe. Larval collections from cemetery vases revealed a colonized area of approximately 1400 km2 in northern Switzerland spreading into bordering Germany, suggesting that the mosquito has been established in this region for several years. Within this range, larvae of Ae. japonicus were recovered from more containers than the most common resident culicid species Culex pipiens. Possible introduction sites (used tyre yards and international airports) revealed few or no larvae, and the mode of introduction remains unclear. Given the vector potential of this species for arboviruses, implementation of surveillance and control measures should be considered.

Anthelmintic Baiting of Foxes against Urban Contamination with Echinococcus multilocularis

In recent years, increases in the urban fox population have been observed in many countries of the Northern Hemisphere. As a result, Echinococcus multilocularis has entered the urban environment. Because of a possible increased risk for alveolar echinococcosis, intervention strategies need to be evaluated. In Zürich, Switzerland, 50 praziquantel-containing baits per km2 were distributed monthly in six 1-km2 bait areas and one 6-km2 bait area from April 2000 through October 2001. The proportion of E. multilocularis coproantigen–positive fox fecal samples collected remained unchanged in six control areas but decreased significantly in the 1-km2 bait areas (from 38.6% to 5.5%) and in the 6-km2 bait area (from 66.7% to 1.8%). E. multilocularis prevalence in the intermediate host Arvicola terrestris also decreased significantly in baited areas. This controlled baiting study shows that a pronounced reduction of E. multilocularis egg contamination is feasible in urban areas where the organism is highly endemic.

Rodents as shared indicators for zoonotic parasites of carnivores in urban environments

Rodents are shared intermediate or paratenic hosts for Echinococcus multilocularis, Toxocara spp. and Toxoplasma gondii, and may serve as valuable indicators for assessing the occurrence and the level of environmental contamination and infection pressure with free-living stages of these zoonotic parasites. We investigated 658 non-commensal rodents for parasite infections in the canton of Geneva, Switzerland. The prevalence of infection with E. multilocularis was highest in Arvicola terrestris captured in the north-western area (16.5%, CI: 10.1%-24.8%), possibly reflecting a higher red fox density due to the low incidence of sarcoptic mange in this part of the canton. The exposure rate to Toxocara spp. was highest in the urban area (13.2%, CI: 7.9%-20.3%), and may account for higher densities of domestic carnivore and red fox definitive hosts within the city. Exposure to T. gondii was widespread (5.0%, CI: 3.2-7.4%), indicating a ubiquitous distribution of infected cat definitive hosts. Interestingly, a widespread distribution of Taenia taeniaeformis, a parasite mainly transmitted by cats, was similarly evidenced in A. terrestris. Distinct spatial patterns for the different zoonotic parasites likely reflected differences in distribution, abundance, and habitat use of the respective definitive hosts. These results highlight the potential value of rodents as shared indicators for these pathogens.

Emergence of canine ocular thelaziosis caused by Thelazia callipaeda in southern Switzerland

In Europe, Thelazia callipaeda has been reported in Italy and France in the eyes of dogs, cats and foxes and, recently, also in humans. In southern Switzerland (Ticino), the first case of T. callipaeda in a dog was detected in 2000 and because of an increasing number of dog thelaziosis, a survey in veterinary practices was carried out. A total of 106 Thelazia-positive dogs from a retrospective analysis and from ongoing cases between 2005 and 2007 as well as five positive cats were reported. For a cross-sectional study, 529 randomly selected dogs (from six veterinary practices), to which anaesthesia was given for other medical reasons, were additionally checked for the presence of adult specimens of Thelazia in 2006: 28 dogs were found positive indicating an overall prevalence of 5.3%. Thelazia-infection was furthermore diagnosed in 7 of 126 foxes (5.6%) shot in Ticino in winter 2005-2006. Affected foxes, dogs and cats originated from the same regions up to 863m of altitude. The cats and 57.9% (55/95) of the infected dogs had never crossed the Swiss border. Collected nematodes were morphologically identified as T. callipaeda, and this diagnosis was confirmed by the analysis of a part of the sequence of the mitochondrial cytochrome c oxidase subunit 1 gene (cox1), revealing haplotype 1, the only one so far found in Europe. Animals harboured 1-23 eye worms. The most common symptoms were conjunctivitis and epiphora, while keratitis was present only in a low number of animals. Young and small sized dogs were significantly less involved than large animals and over 3 years of age. The results indicate that thelaziosis is endemic in that area.

Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva, Switzerland

Dixenous helminths that depend on rodent intermediate hosts are supposed to be negatively affected by urbanization due to lower supply of rodents in urbanized environments. Prevalence rates of dixenous, non-strictly monoxenous, and monoxenous helminths in 228 red foxes (Vulpes vulpes) along a gradient of increasing urbanization were assessed by morphological parasite identification in the city of Geneva, Switzerland. Multivariate analyses for the five most prevalent helminth species or genera revealed a significant decrease of prevalence rates for the dixenous helminths Echinococcus multilocularis and Taenia spp. from the rural (52.1 and 54.3%, respectively) to the urban area (30.0 and 20.0%, respectively), but not for the monoxenous nematode Uncinaria stenocephala (overall prevalence of 78.2%) and the non-strictly monoxenous nematode Toxocara canis (overall prevalence of 44.3%). The lower prevalence of Toxascaris leonina in the urban area (8.0%) compared to the rural area (59.6%) raises the question of whether rodent paratenic hosts play a major role for the population dynamics of this species.

Control of Echinococcus multilocularis: Strategies, feasibility and cost-benefit analyses

Echinococcus multilocularis, the zoonotic agent of human alveolar echinococcosis, has considerably extended its range and became more prevalent in many parts of the endemic areas. Accordingly, there is an increasing demand for measures to prevent human infections. Rising public awareness of this zoonosis and individual protective actions should be part of every prevention program. 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%. The estimated contribution of domestic cats is insignificant (<0.3%) due to low parasite reproduction in this species. Control of the parasite by reducing its main wildlife hosts (foxes, vole species) is barely achievable on a larger scale and is generally not well accepted due to ecological considerations and animal welfare concerns. In general, the frequency of the parasite sharply decreases when anthelmintic baits are regularly distributed to foxes. However, 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. Regarding the long latency of 5-15 years of alveolar echinococcosis, however, 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. Thus, the implementation of this approach strongly depends on factors such as public attitude, available financial resources and priority setting of political decision-makers.

BAITING RED FOXES IN AN URBAN AREA: A CAMERA TRAP STUDY

Abstract Baiting red foxes (Vulpes vulpes) is an established method of vaccinating foxes against rabies in rural environments. Furthermore, anthelmintic baiting has been demonstrated to reduce the prevalence of the zoonotic tapeworm Echinococcus multilocularis in foxes. The recent invasion of foxes into urban areas on continental Europe represents a considerable health risk that calls for the evaluation of baiting strategies adapted to the urban environment. We investigated bait uptake by urban foxes using camera traps in Zurich, Switzerland. Baits with and without the anthelmintic praziquantel were placed in several arrangements (exposed, covered, buried), at different locations (fox dens, compost heaps, fox tracks) and in different seasons (early summer, summer, winter). Ninety-one of 252 baits (36%) disappeared within 3 days. Most of the baits consumed near cameras were consumed by foxes (44 of 91). The remaining baits were consumed by hedgehogs (Erinaceus europaeus), snails (Arion sp.), dogs, rodents (Apodemus sp.), and unidentified animals. Bait uptake by foxes was significantly higher during summer than winter (P = 0.022), and foxes accepted baits most frequently at fox dens during early summer (52.8%). Burying baits reduced bait removal by species other than foxes (P < 0.01). For rabies control in urban areas, avoiding contact of nontarget species with the rabies vaccine is particularly important. Greater selection of the fox population can be achieved by distributing baits in winter, burying baits, and choosing sites that are less accessible to non-target species. However, with anthelmintic treatment, uptake by nontarget species is of lesser importance; hence, the effort to bury the bait is unnecessary.