The impact of socio-cultural factors on transmission of Taenia spp. and Echinococcus granulosus in Kosovo.

Echinococcus granulosus sensu latu (s.l.) and Taenia hydatigena are common parasites of ruminant intermediate hosts in the Balkans. Transmission is linked mainly to home slaughtering and the feeding of infected organs to dogs. In Kosovo, many old sheep are slaughtered particularly during Eid al-Adha (Feast of Sacrifice). To determine whether this tradition could affect parasite transmission, we compared the probability of 504 dogs to contract taenid infections after deworming during one period before Eid al-Adha and a similar period beginning with this event. Initially, taeniid eggs were detected in 6·2% (CI 4·2-8·6) of the dogs. The prevalence before Eid al-Adha was significantly lower (1·2%, CI 0·4-2·6) as compared with the prevalence after the event (4·3%, CI 2·6-6·3). A comparable trend was apparent at species level for T. hydatigena and E. granulosus. These results indicate that the pronounced increase of taeniid infections, including E. granulosus s.l., after Eid al-Adha is linked to traditional home slaughtering that occurs during this celebration. This particular epidemiological situation provides an opportunity for implementing focussed control activities.

Echinococcosis: Control and Prevention.

Human cystic echinococcosis (CE) has been eliminated or significantly reduced as a public health problem in several previously highly endemic regions. This has been achieved by the long-term application of prevention and control measures primarily targeted to deworming dogs, health education, meat inspection, and effective surveillance in livestock and human populations. Human CE, however, remains a serious neglected zoonotic disease in many resource-poor pastoral regions. The incidence of human alveolar echinococcosis (AE) has increased in continental Europe and is a major public health problem in parts of Eurasia. Better understanding of wildlife ecology for fox and small mammal hosts has enabled targeted anthelmintic baiting of fox populations and development of spatially explicit models to predict population dynamics for key intermediate host species and human AE risk in endemic landscapes. Challenges that remain for echinococcosis control include effective intervention in resource-poor communities, better availability of surveillance tools, optimal application of livestock vaccination, and management and ecology of dog and wildlife host populations.

Seroepidemiological survey and spatial analysis of the occurrence of Angiostrongylus vasorum in Swiss dogs in relation to biogeographic aspects.

Angiostrongylus vasorum is a metastrongyloid nematode living in the pulmonary arteries and in the right heart causing potentially fatal respiratory distress, coagulopathies and a wide range of other clinical signs in dogs. The aim of this study was to investigate the seroprevalence and distribution of A. vasorum in Swiss dogs and to identify correlations with biogeographic aspects. A total of 6136 dog sera from all over the country submitted by veterinarians for haematological or chemical analyses were examined for the presence of circulating A. vasorum parasite antigen and specific antibodies against A. vasorum by ELISA. The combined seroprevalence for both specific antibodies and antigen was 0.96% (95% confidence intervals: 0.7-1.2%), while the overall antibody prevalence was 3.08% (CI: 2.7-3.5%) and the antigen prevalence 2.17% (CI: 1.8-2.6%). The highest prevalence for dogs identified as positive in both ELISAs was detected in Western Switzerland (around Geneva, 2.21%, CI: 0.7-5.1%), representing a new endemic area. Known endemic regions in Southern Switzerland (Ticino, 2.17%, CI: 1.0-4.0%) and in the High Rhine area (northern Switzerland, 1.11%, CI: 0.4-2.4%) were confirmed. Spatial analysis identified a cluster with a radius of approximately 30 km in Sisseln, located in this latter region at the German border, for antibody positive dogs, which interestingly corresponded to the location of historical cases of canine angiostrongylosis diagnosed 12-16 years previously. In total 96.6% (57/59) of the antigen- and antibody positive samples originated from areas with a mean temperature warmer than -2 °C in January. Correspondingly, most of the samples (53/59, 89.8%) positive in both ELISAs originated from areas below 700 meters above sea level (m asl), suggesting the altitude being a limiting factor for A. vasorum transmission in Switzerland. This study confirms previously known endemic areas for A. vasorum in Switzerland, and additionally identifies positive dogs in virtually all bioregions. As asymptomatic dogs may suddenly develop a critical clinical status with potentially fatal outcome, disease awareness has to be maintained for dogs from across Switzerland at altitudes below 700 m asl.

Trophic ecology, behaviour and host population dynamics in Echinococcus multilocularis transmission.

The life cycle of the cestode Echinococcus multilocularis primarily involves canids and small mammals (rodents, lagomorphs) as definitive and intermediate hosts, respectively. Several surveys have identified marked temporal and geographical variations at different scales in the parasite's prevalence in both types of hosts, suggesting variations in the biological and ecological factors that control transmission processes. The parasite transmission from intermediate to definitive hosts is determined by the predator-prey relationship, which theoretically depends on prey population dynamics and the complex dietary response of predators to varying densities of prey species and other food items. Parasite eggs are transmitted to intermediate hosts via carnivore faeces, whose distribution in the environment is driven by the defecating behaviour of final hosts. We reviewed field-based studies that address issues related to the trophic ecology and behaviour of definitive hosts, interactions between definitive and intermediate hosts, and E. multilocularis transmission both in wild and domestic animals in rural and urban environments. Two density-dependent mechanisms control the transmission dynamics in definitive hosts: one is based on the variations in the availability of intermediate hosts, and the other is based on the variations in the density of the definitive host and its faeces. Non-linearity and the direct and delayed responses of definitive host contamination in relation to intermediate host population variations were recorded. The dietary response of the red fox was shown to be complex when abundant alternative resources were available (anthropogenic food, multiple intermediate host prey species). Micro-local hotspots of parasite transmission to intermediate hosts in a landscape, as well as areas of higher risk for human contamination in village and urban settings, may be explained by the definitive hosts' activity patterns and defecation behaviour.

Fox baiting against Echinococcus multilocularis: contrasted achievements among two medium size cities.

In Europe, most cities are currently colonized by red foxes (Vulpes vulpes), which are considered to be the main definitive host of the zoonotic cestode Echinococcus multilocularis. The risk of transmission to humans is of particular concern where high fox populations overlap with high human populations. The distribution of baits containing praziquantel has successfully reduced the infection pressure in rural areas and in small plots within large cities. The purpose of this study was to assess its efficiency in two medium size cities (less than 100,000 inhabitants) in areas of high human alveolar echinococcosis incidence. From August 2006 to March 2009, 14 baiting campaigns of praziquantel treatment were run in Annemasse and Pontarlier (Eastern France), each of which encompassed 33 km(2), with a density of 40 baits/km(2). The bait consumption appeared to be lower in strictly urban context compared to suburban areas (78.9% vs. 93.4%) and lower in Annemasse than in Pontarlier (82.2% vs. 89.5%). During our study, the prevalence of E. multilocularis, as assessed by EM-ELISA on fox faeces collected in the field in Annemasse, was lower within the treated area than in the rural control area. A "before/during" treatment comparison revealed a significant decrease of spring prevalence from 13.3% to 2.2%. No significant change in prevalence was detected in Pontarlier (stable prevalence: 9.1%) where the contamination of the treated area followed the temporal trend observed in the control area. There, a greater resilience of the parasite's life cycle, probably due to a strong pressure of recontamination from outside the treated area, may have counteracted the prophylaxis treatment. These contrasted outcomes suggest that the frequency of fox anthelmintic treatment should be adapted to the local situation.

Mapping the increasing risk of human alveolar echinococcosis in Limburg, The Netherlands.

The parasite Echinococcus multilocularis was first detected in The Netherlands in 1996 and repeated studies have shown that the parasite subsequently spread in the local population of foxes in the province of Limburg. It was not possible to quantify the human risk of alveolar echinococcosis because no relationship between the amount of parasite eggs in the environment and the probability of infection in humans was known. Here, we used the spread of the parasite in The Netherlands as a predictor, together with recently published historical records of the epidemiology of alveolar echinococcosis in Switzerland, to achieve a relative quantification of the risk. Based on these analyses, the human risk in Limburg was simulated and up to three human cases are predicted by 2018. We conclude that the epidemiology of alveolar echinococcosis in The Netherlands might have changed from a period of negligible risk in the past to a period of increasing risk in the forthcoming years.

Intestinal parasites of endangered orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia.

Faecal samples from 163 captive and semi-captive individuals, 61 samples from wild individuals and 38 samples from captive groups of Bornean orangutans (Pongo pygmaeus) in Kalimantan, Indonesia, were collected during one rainy season (November 2005-May 2006) and screened for intestinal parasites using sodium acetate-acetic acid-formalin-concentration (SAFC), sedimentation, flotation, McMaster- and Baermann techniques. We aimed to identify factors influencing infection risk for specific intestinal parasites in wild orangutans and individuals living in captivity. Various genera of Protozoa (including Entamoeba, Endolimax, Iodamoeba, Balantidium, Giardia and Blastocystis), nematodes (such as Strongyloides, Trichuris, Ascaris, Enterobius, Trichostrongylus and hookworms) and one trematode (a dicrocoeliid) were identified. For the first time, the cestode Hymenolepis was detected in orangutans. Highest prevalences were found for Strongyloides (individuals 37%; groups 58%), hookworms (41%; 58%), Balantidium (40%; 61%), Entamoeba coli (29%; 53%) and a trichostrongylid (13%; 32%). In re-introduction centres, infants were at higher risk of infection with Strongyloides than adults. Infection risk for hookworms was significantly higher in wild males compared with females. In groups, the centres themselves had a significant influence on the infection risk for Balantidium. Ranging patterns of wild orangutans, overcrowding in captivity and a shift of age composition in favour of immatures seemed to be the most likely factors leading to these results.

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 km(2) 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.

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.

[Echinococcus multilocularis in Grisons: distribution in foxes and presence of potential intermediate hosts]. / Echinococcus multilocularis in Graubünden: Verbreitung bei Füchsen und Vorkommen potentieller Zwischenwirte.

The southern border of the European endemic area of Echinococcus multilocularis runs along the alpine crest. This endemic transition area was analysed in the canton Grisons on a small spatial scale. A total of 543 foxes originating from 10 areas north and 4 areas south of the main alpine divide were investigated. Parasites were isolated using the sedimentation and counting technique on intestinal contents. The mean prevalence of E. multilocularis was 6.4% with significant differences between different areas. In the southern valleys, only foxes from the Val Müstair were infected (14.3%). On the northern side of the main alpine divide, prevalences varied between 0 and 40%. The predation habits of foxes on potential intermediate hosts was investigated by means of stomach content analyses (n=530). Rodents of the genera Microtus/Pitymys were found in 19.6% of fox stomachs, Clethrionomys glareolus in 8.0% and Arvicola terrestris in 0.4%. A small scale analysis based on a 10 x 10 km grid suggested that the predation rate on the genera Microtus/Pitymys significantly correlated with the prevalence of E. multilocularis in foxes (Spearman's r = 0.51). Hence, E. multilocularis appears to occur in the alpine study area on a very small spatial scale. These local sources of infection may persist for decades. This may partly explains why, during the last 34 years, some human cases of alveolar echinococcosis occurred in areas of the Canton Grisons where the parasite is presently endemic in foxes. No such human cases have been recorded in other areas free of E. multilocularis.

Echinococcus multlocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland.

We examined 267 red foxes (Vulpes vulpes) from the canton of Geneva, Switzerland, for intestinal infections with Echinococcus multilocularis. This region is situated in the core area of the endemic range of this zoonotic cestode in Central Europe. Several factors were taken into account and urbanisation level appeared to be the most explicative to describe observed differences. The prevalence decreased significantly from rural and residential areas (prevalence of 52%, CI 43-62%, and 49%, CI 38-59 %, respectively) to the urban area (prevalence of 31%, CI 19-42%). A few juvenile foxes harboured very high burdens up to more than 120,000 worms and were significantly more heavily infected than adults. The intensity of infection decreased from rural and residential areas to the city, suggesting a lower contamination of the urban environment.

An experimental field approach to parasitism and immune defence in voles.

The fox tapeworm Echinococcus multilocularis is typically perpetuated in a cycle with red foxes as definitive hosts and various rodent species as intermediate hosts. In this study, foxes were baited with a highly efficient drug against cestodes (praziquantel) in 5 blocks of 1 km2. Voles, Arvicola terrestris, the most abundant intermediate host species, were trapped in the 5 baited blocks and in 5 non-baited control blocks. Baiting the foxes reduced the prevalence of E. multilocularis in fox faecal samples in the baited blocks, but voles trapped in the two blocks did not differ in their infection rates. However, voles from the baited blocks had significantly smaller spleen masses and were more likely to be infested with mites than those from the control blocks, possibly reflecting different immunological activities. Our study suggests that the environmental contamination with E. multilocularis eggs, and perhaps those of other tapeworms, influences the immune system of the intermediate host species A. terrestris in the wild.

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.

Comparison of heavy metal concentrations in tissues of red foxes from adjacent urban, suburban, and rural areas.

The red fox (Vulpes vulpes) is a representative of the canid family with wide distribution in the Northern Hemisphere and Australia. The increasing utilization of urbanized habitats by red foxes prompted us to test whether this species may be used to monitor the presence of anthropogenic pollutants in cities or suburbs. For that purpose, we compared the concentrations of heavy metals (Cd, Pb, Cu, Zn) in foxes from urban, suburban, and rural areas within the municipality of Zürich (Switzerland). The kidney and liver of suburban and rural foxes contained the highest Cd concentrations, whereas urban foxes contained the highest Pb levels. In the kidney of suburban foxes, Cd concentrations increased from a median value of 0.73 mg/kg in juvenile animals to 1.82 mg/kg in adults. Similarly, the liver of suburban foxes contained increasing Cd levels from a median of 0.21 mg/kg in juvenile animals to 0.94 mg/kg in adults. An age-dependent storage of Cd was also found in foxes from the rural surroundings, but no such accumulation occurred in urban foxes from the city center, where even adult animals contained very low Cd levels. Conversely, foxes from the urban center were characterized by elevated Pb concentrations during the first 2 years of life, but this transient Pb accumulation was absent in suburban or rural animals. The liver of juvenile foxes contained a median Pb concentration of 0.99 mg/kg in the city compared to only 0.47 and 0.37 mg/kg in the suburban and rural area, respectively. Thus, we found that animals from separate environmental compartments contain different patterns of tissue residues, implying that red foxes may serve as a bioindicator species to detect certain toxic hazards in urbanized habitats.

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.