Emergence of Echinococcus multilocularis among Red Foxes in northern Germany, 1991--2005

The parasite Echinococcus multilocularis is currently of great concern in Europe because of its spreading behavior, which has public health implications. This study investigates the spatiotemporal distribution of Echinococcus multilocularis in Red Foxes. The infection status of 8459 foxes was sampled from 43 regions in the north German province of Lower Saxony over three investigation periods 1991--1994, 1994--1997 and 2003--2005. Linear empirical Bayesian smoothing within the binomial model was used to produce smoothed choropleth maps. Geostatistical kriging was applied to generate prevalence risk maps. Further geostatistical modeling of the prevalence difference between study periods facilitated spatiotemporal trend investigations. The spatial scan statistic was used for cluster detection analysis. The average prevalence risk for Lower Saxony increased from about 12 to 20% during 1991--2005. Specifically the increases from first to second and to third study periods were estimated by 3.3% (CI 95%: 0.6%-5.9%) and 8.5% (CI 95%: 5.2%-11.8%), respectively. Infections in foxes were clustering and a location stable disease cluster was detected in the south of the province. This study is the first showing evidence for steady emergence of Echinococcus multilocularis in Red Foxes. First cases of human Alveolar Echinococcosis were recorded recently.     

The occurrence of Echinococcus multilocularis in red foxes in lower Saxony: identification of a high risk area by spatial epidemiological cluster analysis

There is considerable interest in the spatial distribution of Echinococcus multilocularis in red foxes (Vulpes vulpes L.), because this parasite causes the zoonoses of alveolar echinococcosis which is potentially of high fatality rate. High risk areas are known from France, Switzerland and the Swabian Alb in Germany for a long time. In this work, the spatial scan statistic is introduced as an instrument for identification and localisation of high risk areas, so called disease clusters in spatial epidemiology. The use of the spatial scan statistic along with data about the distribution of the parasite in 5365 red foxes in Lower Saxony, that were collected during 1991 to 1997, led to the identification of another high risk area. The relative risk for this disease cluster is approximated by RR = 5.03 (CI0.95(RR) = [4.27; 6.58]) for the period of 1991 to 1994 and by RR = 4.45 (CI0.95(RR) = [3.53; 5.59]) for the period of 1994 to 1997, respectively.     

Choropleth mapping of regional count data of Echinococcus multilocularis among red foxes in Lower Saxony, Germany.

In this paper, choropleth maps display the geographical distribution of Echinococcus multilocularis in red foxes in Lower Saxony. Areas of high prevalence of the infection in foxes and with high fox population density pose high risk for the human population for alveolar echinococcosis. Spatial statistical methods were used to analyse regional count data obtained from 5365 hunted or found-dead foxes. Spatial smoothing (of raw estimates of regional prevalences based on count data before mapping) was used because raw estimates can give an erratic impression of the spatial pattern of the infection. For smoothing, empirical Bayesian methods are used as an explorative spatial epidemiological tool. The resulting map showed the geographical variation of the estimated prevalences around a median at 9% and indicated the presence of spatial-trend effects. Based on this finding, conditional autoregressive spatial modelling for Freeman-Tukey transformed data was used as an inferential spatial epidemiological tool. There were significant additive linear and quadratic spatial-trend effects with elevated prevalences in the north and south and extreme values (prevalences>38%) for the south of Lower Saxony.     

Echinococcus multilocularis in Belgium: prevalence in red foxes (Vulpes vulpes) and in different species of potential intermediate hosts

Echinococcus multilocularis causes a rare but potentially lethal zoonotic infection in humans. This tapeworm is known to be endemic in foxes in several countries of Western and Central Europe. In Western Europe, the common vole (Microtus arvalis) and the water vole (Arvicola terrestris) are considered to be the most important intermediate host species of this cestode whereas the red fox is by far the most important final host. The purpose of this study was to provide data on the prevalences in Wallonia (Southern part of Belgium) both in the red fox and in different potential intermediate hosts. A total of 990 red foxes were examined between January 2003 and December 2004 for the presence of E. multilocularis. The average prevalence was 24.55% (22.38-27.87). Out of 1249 rodents or insectivores belonging to the species Apodemus sylvaticus, Arvicola terrestris, Clethrionomys glareolus, Microtus arvalis, Microtus agrestris and Sorex araneus, only one M. arvalis (out of 914-0.11% (0.003-0.61) and one C. glareolus (out of 23-4.3% (0.1-21.9) were found to be infected. However, the muskrat (Ondatra zibethicus) seems to be a good intermediate host as 11.18% (9.72-12.76) of the animals (n=1718) were found to be infected. A positive correlation was found between the prevalences in foxes and in muskrats in each of the different geological regions. This study indicates that the muskrat is highly sensitive to this zoonotic tapeworm and could perhaps represent a good bioindicator when studying the epidemiology of this parasitic infection in Belgium and in other countries where the muskrat is present.     

Prevalence and intensity of Echinococcus multilocularis in red foxes (Vulpes vulpes schrencki) and raccoon dogs (Nyctereutes procyonoides albus) in Otaru City, Hokkaido, Japan

A survey was done in an attempt to investigate the epidemiological status of Echinococcus multilocularis in red foxes and raccoon dogs in Otaru city from June to September 1999. Sixty-seven red foxes (Vulpes vulpes schrencki) and 13 raccoon dogs (Nyctereutes procyonoides albus) were captured, and postmortem examinations were conducted with them. Thirty-eight red foxes (56.7%) and 3 raccoon dogs (23.1%) were found to be infected with E. multilocularis. The total biomass of E. multilocularis in all infected red foxes and raccoon dogs were 2,817,000 and 1,515 worms, respectively. Nine of the infected red foxes harboring more than 100,000 worms accounted for 90.6% of the total biomass. No significant differences in the prevalence were observed between male and female, and juvenile and adult. However, the worm burden was higher in juvenile than in adult foxes. In one of the infected raccoon dogs, mature worms and eggs of E. multilocularis were found in the intestine and fecal sample, respectively. This result suggested that the raccoon dogs are probably playing a small role in the egg contamination of the environment. The validity of coproantigen ELISA for diagnosis of foxes was confirmed by comparing the results of autopsy, egg examination and coproantigen ELISA using rectal fecal samples.     

Echinococcus multilocularis in Grisons: distribution in foxes and presence of potential intermediate hosts

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 multilocularis in dogs from two French endemic areas: no evidence of infection but hazardous deworming practices

The life cycle of the zoonotic parasite Echinococcus multilocularis is predominantly sylvatic, involving foxes as definitive hosts infected by predation of rodents, the intermediate hosts. The North-Eastern French departments of Meuse and Haute-Sa?ne are highly endemic, with an estimated fox prevalence of 41% and 36% respectively. Although most of the parasites' biomass occurs in foxes, domestic dogs can also be infected, leading to a major risk of human infection due to the close proximity of dogs and owners. In the present study, dog faeces were collected after praziquantel treatment provided by veterinarians. In all, 860 faecal samples were collected throughout Meuse (n=493) and Haute-Sa?ne (n=367). Intestinal helminth eggs were isolated from the faeces using a flotation technique and observed by microscopy. Parasite species were identified in samples positive for taeniid eggs by sequence analysis after PCR amplification. To study the factors associated with infestation, each sample was linked to a questionnaire filled in by the dog owners. Taeniid eggs were observed in seven faecal samples (0.8%) but none of them were positive for E. multilocularis. Thus, the apparent prevalence of E. multilocularis in dog populations is lower than 1.00% for Haute-Sa?ne and lower than 0.75% for Meuse. In Haute-Sa?ne, a high proportion of dogs observed suspected preying on rodents were not dewormed monthly. In endemic areas, these dogs must be considered at risk of transmitting E. multilocularis to humans.     

Controlling Echinococcus multilocularis-ecological implications of field trials

Two field trials to reduce the prevalence of Echinococcus multilocularis in foxes have been conducted in recent years. Although both trials reduced prevalence considerably, they failed to eradicate the parasite in the study region. Following the control trial in northern Germany, prevalence recovered unexpectedly and rapidly, reaching pre-control levels five quarters (15 months) after the end of control. To understand the internal dynamics of the parasite-host system's reaction to control, we developed a spatially explicit simulation model, Echi. The simulation model incorporates the information available concerning fox tapeworm population dynamics.Using epidemiological parameters to adjust pre-control prevalence, the model predicts the temporal evolution of the prevalence of E. multilocularis in controlled foxes without departing from the range of uncertainty of the field data. However, the model does not predict the rapid pre-control recovery observed in the field trial.The deviation of the model's prediction from field data indicates the involvement of processes not yet taken into account. We modified the model step by step to mimic processes with the potential to cause the rapid post-control recovery of the prevalence of E. multilocularis in foxes.Neither the longevity of tapeworm eggs nor the migratory behaviour of foxes showed any influence on the post-control reaction of the parasite-host system. However, landscape structures leading to a heterogeneous distribution of infected foxes have the potential to alter the system's reaction to control. If infected foxes are concentrated in multiple clusters in the landscape, the model prediction tallied with the range of uncertainty of the field data. Such spatial distribution of infected foxes may be caused by differential abiotic conditions influencing the survival of tapeworm eggs.The model was found to comply best with field data if the foxes acquire partial immunity by being exposed to the fox tapeworm.Both hypotheses explaining the rapid post-control recovery of the prevalence of E. multilocularis observed in the fox population were supported by field data.Both hypotheses have far-reaching consequences for future control trials. The spatial aggregation of infected foxes would enable control efforts to be concentrated on these highly infected areas. However, the acquisition of immunity acts as a buffer to control, necessitating intensified control measures.     

Serological (Em2-ELISA) and parasitological examinations of fox populations for Echinococcus multilocularis infections

Serum or body fluid samples of 1,006 foxes were investigated in an ELISA for antibodies against a highly sensitive and specific antigen (Em2-antigen) of Echinococcus multilocularis. Parasitological examinations of the intestines and simultaneous serological examinations were carried out in 505 foxes: A group of 98 blue foxes (Alopex lagopus) from Norwegian fox farms did not contain intestinal stages of E. multilocularis and was clearly sero-negative in Em2-ELISA. On the other hand in red foxes (Vulpes vulpes) originating from European areas known to be endemic for E. multilocularis the following average prevalence rates were found: 244 foxes from Southern Germany, E. multilocularis prevalence 55% and sero-prevalence 60%; 139 foxes from Austria, E. multilocularis prevalence 4% and sero-prevalence 12%. Serological identification of individual foxes with or without intestinal E. multilocularis infection was not possible. Only serological (no parasitological) examination in 402 foxes originating from endemic areas in Switzerland resulted in a sero-prevalence rate of 37%. Sero-prevalence was only 6% and 4% in 54 and 26 other foxes, respectively, originating from Swiss and German areas where E. multilocularis has not yet been reported. Negative control Norwegian (farmed) silver foxes (n = 43) were all sero-negative. The specificity of the Em2-ELISA was confirmed by negative Em2-serologies with sera from dogs infected with intestinal and tissue dwelling helminth species (with the exception of two from 24 dogs infected with E. granulosus).(ABSTRACT TRUNCATED AT 250 WORDS)     

Environmental hygienic aspects of echinococcosis]

A literature review on the current situation of echinococcosis in Central Europe is given. The only final host for Echinococcus granulosus in this region ist the dog. The infection rate of dogs with E. granulosus in Central Europe is less than 1%. According to meat inspection statistics in Germany less than 0.008% of sheep, pigs and horses carry larval stages of E. granulosus. Parasitologically confirmed is the occurrence of a cattle-dog strain, the cysts of which were found in 0.26% of slaughter cattle. It is not known whether this strain infects also man as does the sheep-dog strain. Cases of cystic echinococcosis (E. granulosus) diagnosed in Central Europe are often imported from mediterranean countries. In Baden-Wurtemberg, the only state where human cases of echinococcosis are recorded, 50-100 cases are diagnosed per year. In areas with endemic E. multilocularis infection also dogs and cats may be infected with the adult worm besides the red fox. Recent investigations have revealed that not only in classical endemic areas (Switzerland, Austria, Baden-Wurtemberg, Rhineland-Palatinate) foxes have infection rates of up to 67% but that E. multilocularis-infection is also wide-spread in Thuringia, Hesse, Northrhine-Westphalia and in the southern parts of Lower Saxony. The most northern infested area seems to be the region of Detmold (infection rate of foxes 9%). The infection rates with alveolar echinococcosis (E. multilocularis) in humans even in endemic areas are low. In Baden-Wurtemberg 140 new cases became known during the past ten years.(ABSTRACT TRUNCATED AT 250 WORDS)     

Base line prevalence and spatial distribution of Echinococcus multilocularis in a newly recognized endemic area in the Netherlands

The base line prevalence of Echinococcus multilocularis in foxes was determined in the eastern part of the province of Groningen in the Netherlands adjacent to the German border. This region has been identified in a previous study in 1998 as one of the westernmost border areas of E. multilocularis. Base line prevalence data are important for a better insight in the possible spread of the parasite and its changes in time. As fox feces containing E. multilocularis eggs are an important source for human exposure this base line prevalence is also an indicator for the potential risk for public health. The base line prevalence was estimated at 9.4% (95% CI: 5.2-16.5%). These results confirm previous findings of E. multilocularis in the same region. The spatial distribution of the infected foxes has been analyzed as a spatial gradient using a logistic model. The prevalence appeared to change strongest in east-western direction and was highest near the German border, adjacent to a German endemic area. These results suggest that the border areas in the Netherlands are the most margin of E. multilocularis territory.     

The use of tetracycline in anthelmintic baits to assess baiting rate and drug efficacy against Echinococcus multilocularis in foxes

Anthelmintic (praziquantel) baiting of wild red foxes against Echinococcus multilocularis infection was studied in a highly epizootic suburban area of Otaru, Hokkaido (the northern island of Japan) during the summer and autumn in the years 1999-2004. Acceptance of baits containing the biomarker tetracycline (TC) was evaluated. The prevalence of E. multilocularis infection in foxes before baiting (1999-2000) was 58% (88/153), whereas in the fourth year of bait distribution year (2004), it decreased to 11% (5/45). Analysis of TC marking in the teeth of foxes showed that 39% (77/195) of those captured after baiting were estimated to have consumed baits in the year of capture. Importantly, more juvenile (56%, 49/87) than adult foxes (26%, 28/108) were marked, indicating efficient baiting of juveniles, which tended to have a higher worm burden of E. multilocularis. Of 77 marked foxes, E. multilocularis and Alaria alata (monitored as the second indicator species of deworming) were not detected in 70 (90%) and 76 (99%) foxes, respectively. The results suggest effective deworming by bait consumption. However, it was also demonstrated that 9% of the marked foxes were infected or re-infected after bait consumption, suggesting high infection pressure and the importance of frequent baiting.     

Detection of Echinococcus multilocularis in foxes: evaluation of a protocol of the intestinal scraping technique

The intestinal scraping technique (IST) is widely used for the detection of definitive hosts infected with Echinococcus multilocularis. The sensitivity of the method has been questioned in recent years. Several variations of the technique are used that may differ in their performance. We therefore estimated the diagnostic sensitivity and specificity of the IST protocol used in our lab by examining the small intestines of 210 E. multilocularis-infected foxes and 294 foxes that had tested negative for this parasite. To this end, IST was first performed on 48 and 294 intestines from infected and uninfected foxes respectively, followed by an examination of the entire remaining mucosa of the small intestine to discover any infections with E. multilocularis that had not been detected by IST. The point estimate for diagnostic sensitivity was 100%. Five different classes of infection intensities were formed. The lower limits of the 95% confidence intervals ranged between 76.8% and 92.6% depending on the number of samples analysed per class. When the small intestines of another 162 infected foxes were examined by IST and the results recorded separately for the anterior, middle and posterior third of the small intestine, a strong preference of E. multilocularis for the posterior third was observed. For epidemiological purposes, it may thus be possible to restrict routine investigations to the posterior portion of the small intestine. By contrast, a reduction of the number of slides examined per infected animal may lead to a considerable loss in sensitivity in animals with a low intensity of infection.     

Combining information from surveys of several species to estimate the probability of freedom from Echinococcus multilocularis in Sweden,Finland and mainland Norway

Background

The fox tapeworm Echinococcus multilocularis has foxes and other canids as definitive host and rodents as intermediate hosts. However, most mammals can be accidental intermediate hosts and the larval stage may cause serious disease in humans. The parasite has never been detected in Sweden, Finland and mainland Norway. All three countries require currently an anthelminthic treatment for dogs and cats prior to entry in order to prevent introduction of the parasite. Documentation of freedom from E. multilocularis is necessary for justification of the present import requirements.

Methods

The probability that Sweden, Finland and mainland Norway were free from E. multilocularis and the sensitivity of the surveillance systems were estimated using scenario trees. Surveillance data from five animal species were included in the study: red fox (Vulpes vulpes), raccoon dog (Nyctereutes procyonoides), domestic pig, wild boar (Sus scrofa) and voles and lemmings (Arvicolinae).

Results

The cumulative probability of freedom from EM in December 2009 was high in all three countries, 0.98 (95% CI 0.96-0.99) in Finland and 0.99 (0.97-0.995) in Sweden and 0.98 (0.95-0.99) in Norway.

Conclusions

Results from the model confirm that there is a high probability that in 2009 the countries were free from E. multilocularis. The sensitivity analyses showed that the choice of the design prevalences in different infected populations was influential. Therefore more knowledge on expected prevalences for E. multilocularis in infected populations of different species is desirable to reduce residual uncertainty of the results.     

Echinococcus multilocularis and Toxocara canis in urban red foxes (Vulpes vulpes) in Brussels, Belgium

During the last decades, European red foxes (Vulpes vulpes) have been implicated in the transmission of several viral or parasitic pathogenic agents to domestic animals and humans. In urban areas, risks of zoonoses transmission are likely to increase as a result of a higher rate of intra- and inter-species contacts. Foxes occur on 35% of the Brussels-Capital Region area and local densities reach up to 4 family groups per square kilometre. According to the directive 2003/99/ECC, a first survey for the presence in foxes of Echinococcus multilocularis and Toxocara canis was conducted in Brussels from 2001 to 2004. None of 160 foxes were found to be infected with E. multilocularis and 24 of 134 foxes were found to be infected with T. canis. Considering numbers of examined foxes, the sensitivity and the specificity of tests used for diagnosis, the 95% credibility intervals for the true prevalence of E. multilocularis and T. canis were estimated in a Bayesian framework to be 0 to 1.87% (median value of 0%) and 12.7 to 26% (median value of 18.7%), respectively. For T. canis, a significantly higher risk to be a carrier occurs in cubs and a significantly lower risk in adults.     

Field evaluation of an intravital diagnostic test of Echinococcus multilocularis infection in red foxes

Echinococcus multilocularis parasitizes the small intestine of red foxes (Vulpes vulpes) and other carnivores, and has a wide distribution throughout the northern hemisphere. This cestode is the causative agent of human alveolar echinococcosis, a life-threatening helminth zoonosis. In 2000-2002, 2130 red foxes were examined for its presence in Slovakia, with a total prevalence of 30.7%. The data on occurrence were obtained by the combination of necropsy of small intestines from red foxes and coproantigen detection in faecal samples. The correlation between the number of detected specimens and the value of optical density of copro-ELISA test was found. When worm burdens were low (1-25 specimens) the sensitivity of the method was 31.3+/-8.64%, when worm burdens were >50 specimens, 81.8+/-0.66%, and with high worm burdens (>1000 specimens) the sensitivity reached 100+/-0.34%. E. multilocularis presence was detected using the nested PCR method from the eggs in the faecal samples with a 100% specificity. In epidemiological surveys of this zoonosis, it is of crucial importance to detect animals with a high level of infection, which are responsible for the bulk of environmental contamination. The advantage of copro-ELISA test lies in allowing the intravital diagnostics to be employed within the epidemiological survey of E. multilocularis occurrence in the protected and urban areas.     

Veterinary aspects of alveolar echinococcosis--a zoonosis of public health significance

Human alveolar echinococcosis (AE), caused by the metacestode stage of Echinococcus multilocularis, is a serious zoonosis which caused up to 100% lethality in untreated patients before the 1970s, when modern methods of treatment were not yet established. AE occurs in large areas of the northern hemisphere mostly with low country-wide prevalences, but high prevalences of up to 4% have been reported from small population groups in highly endemic foci, e.g. from China. AE includes many veterinary aspects which are the topic of this review. Recent studies have shown that E. multilocularis has a wider geographic range than previously anticipated. There is evidence for growing populations of red foxes (Vulpes vulpes) in some areas, for increasing invasion of cities by foxes and also for establishment of the parasite cycle in urban areas. These and other factors may lead to an increased infection risk for humans. Significant progress has been made in the development of sensitive and specific new techniques for the intra vitam and post mortem diagnosis of intestinal E. multilocularis infection in definitive hosts, notably the detection of coproantigen by enzyme-linked immunosorbent assay and of copro-DNA by PCR. Both tests can also be used for the identification of E. multilocularis in faecal samples collected in the environment. Recommendations are given for chemotherapy and chemoprophylaxis of the intestinal infection in definitive hosts. In recent years, infections with the metacestode stage of E. multilocularis have not only been diagnosed in humans in several regions, including at least eight countries in central Europe, but also in animal species which do not play a role in the transmission cycle (wild and domestic pigs, dogs etc.). From 1987 to 2000 our group in Zurich has diagnosed 10 cases of AE in dogs and 15 in captive monkeys. In 2 dogs, concurrent infections of the intestine and of the liver with adult and larval stages of E. multilocularis, respectively, were observed for the first time. Clinical data are presented, and methods of diagnosis and treatment (surgery, chemotherapy) are described. Furthermore, small liver lesions caused by E. multilocularis were diagnosed in 10% of 90 slaughter pigs, and 2.9% of 522 breeding sows had specific serum antibodies against parasite antigens. In view of the unpredictable epidemiological situation, all possible measures for preventing E. multilocularis infections in humans and in domestic animals should be initiated by the veterinary and health authorities.     

The so-called "fox tapeworm"

The so-called "fox tapeworm" (Echinococcus multilocularis), the causative agent of a severe disease in man (alveolar echinococcosis), is presently under public discussion in Switzerland. Therefore, actual information is provided on the life cycle of the parasite, epidemiology, disease in humans, symptomatology, diagnosis, therapy and prophylaxis. It is recommended that in endemic regions hunters handling foxes should wear protective gloves, dead foxes should be transported in plastic bags and wild fruits, berries and vegetables should be carefully washed and--if possible--heated to more than 70 degrees C for some minutes prior to consumption. After contact with foxes or other final hosts (dogs, cats) infected with E. multilocularis, persons should be monitored with the highly sensitive and specific Em2-ELISA for serum antibodies aiming at an early diagnosis and treatment of a potential infection.     

Reduced egg production of Echinococcus multilocularis in experimentally infected and re-infected red foxes (Vulpes vulpes)

Ingestion of eggs of the small fox tapeworm, Echinococcus multilocularis, causes the severe human disease alveolar echinococcosis. Previously, the dynamics of the egg excretion from infected carnivores have been studied only where the host animals have been exposed to a single experimental infection. In nature, foxes are most likely repeatedly infected. To study the effect of repeated exposure, twenty-one foxes were inoculated with a high dose of E. multilocularis protoscoleces three times over a 1-month period. For comparative purposes, three groups of twenty-one foxes were respectively inoculated with low, medium, or high single dose of protoscoleces. For each group, worm number and morphology were analyzed after necropsy of seven foxes at 1, 2, and 4 months after last inoculation. The establishment of intestinal worms was very low in all foxes, and surprisingly, most of the worms did not produce eggs. Although most reproductive structures were detectable, the genital pore and the cirrus pouch often had abnormal enlargements that spread internally, most likely preventing the reproductive function. The reason for this abnormality could not be determined, but the preparation and storage conditions of the inoculated protoscoleces may have contributed to the stunted development. Physical stress of E. multilocularis at the larval stage in rodents may later adversely affect the reproductive success of the adult tapeworm in the carnivore definitive host; as in the present study where a worm establishment in the definitive host was only followed by a neglectable egg production.     

Helminths of red foxes (Vulpes vulpes) in Denmark

An epidemiological study of helminths in 1040 red foxes collected from various localities in Denmark during 1997-2002, revealed 21 helminth species at autopsy, including nine nematode species: Capillaria plica (prevalence 80.5%), Capillaria aerophila (74.1%), Crenosoma vulpis (17.4%), Angiostrongylus vasorum (48.6% from Northern Zealand (endemic area)), Toxocara canis (59.4%), Toxascaris leonina (0.6%), Uncinaria stenocephala (68.6%), Ancylostoma caninum (0.6%), and Trichuris vulpis (0.5%); seven cestodes: Mesocestoides sp. (35.6%), a number of Taeniid species (Taenia pisiformis, T. hydatigena, T. taeniaeformis, T. crassiceps, and unidentified Taenia spp.) (22.8%), and Echinococcus multilocularis (0.3%); four trematodes: Alaria alata (15.4%), Cryptocotyle lingua (23.8%), Pseudamphystomum truncatum (3.6% from Northern Zealand), and Echinochasmus perfoliatus (2.4% from Northern Zealand); one acanthocephalan: Polymorphus sp. (1.2%). Significant difference in prevalence was found for T. canis and A. vasorum according to host sex, and for T. canis, U. stenocephala, Mesocestoides sp., Taenia spp., A. alata, A. vasorum, and Capillaria spp. according to age groups (adult, young or cub). Prevalence and average worm intensity for each helminth species varied considerably according to geographical locality, season, and year. Aggregated distribution was found for several helminth species. The two species E. multilocularis and E. perfoliatus are first records for Denmark.