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The Z value and clustering of foxes with high parasite burdens in areas with a high prevalence of A. alata infection amongst foxes
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The digenean trematode Alaria alata, an intestinal parasite of wild canids is widely distributed in Europe. The recent finding of the mesocercarial life cycle stage in the paratenic wild boar host suggests that it may potentially infect humans Mohl et al. (Parasitol Res 105:1-15, 2009). Over 500 foxes were examined during a wildlife survey for zoon...
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... foxes examined in 2009 and 2010 were widely distributed throughout the country and originated from 25 of the 26 counties of the Republic of Ireland ( Fig. 1). Adult trematodes resembling Alaria spp. were found in 26% of the foxes in 2009 and 21% in 2010. The mean parasite burden in 2009 was 124 (±11; x ± s.e.m.) and this was slightly lower in 2010 at 48 (±10). The majority of foxes had worm burdens of one to ten parasites. Although over 12% of foxes had more than 200 parasites and 6.5% of them were parasitised with 500 or more Alaria spp. (Fig. 2.), one fox found in east Limerick had a parasite intensity of 981 flukes. Amplification of the 18SrRNA gene in the 42 randomly selected trematodes taken from 42, also randomly selected, foxes produced an amplicon of 381 bp in a stPCR assay. The sequence of these amplicons had 100% homology with A. alata (GenBank accession number AY222091). Analysis of the spatial correlation between foxes and land cover indicated that 79% of infected foxes and 65% of the uninfected foxes were found in areas of pasture (Fig. 1). Parasitised foxes were confined mainly to the central plain and areas of low-lying pasture between the Slieve Bloom and Mitcheltown Mountains in Munster (Fig. 1). The prevalence of infection was highest in foxes from east Limerick, east Galway, mid-Offaly, northeast Laois and the county border between Roscommon and Westmeath. Hot spot analysis indicated that parasite intensity was also highest in foxes from these areas (Fig. 3). Except for the cluster of positive foxes in east Limerick, the majority of parasitised animals were concentrated in the greater Shannon basin and the Corrib catchment (Fig. 1). Results from high to low clustering gave a G index of 0 and a Z score of 1.68 standard deviations. These values complemented the hot spot analysis by showing a statistically significant (at a 10% confi- dence level) clustering of heavily parasitised foxes in these locations. The distribution of the parasite also appeared to be restricted in the south, west and northwest by land with an elevation of >300 m. The analysis of the proximity between frogs and infected foxes showed that over 45% of frog sightings occurred within 10 km of a fox location. The prevalence of circa 25% reported here for A. alata in rural foxes in Ireland compares with a level of infection, ranging from 11% to 88%, recorded for foxes and other carnivores elsewhere in continental Europe and Turkey (Borgsteede 1984; Saeed et al. 2006; Gicik et al. 2009; Mohl et al. 2009). The maximum number of 981 trematodes was found in a fox from east Limerick. This was markedly higher than the previous highest recorded worm burden of 600 (Shimalov et al. 2003). There are no published reports on the pathology of adult A. alata in canidae but it is not unreasonable to assume that a parasite intensity of greater than 500 worms would induce some disturbances in the digestive process. It was not feasible to carry out a histopa- thology examination of the small intestines due the freezing regime used to inactivate any adult Echinococcus spp. that may have been present and thus evidence of pathological change, if any, awaits examination of non-autolysed fox intestines. The prevalence of A. alata is high amongst wildlife definitive and paratenic hosts in wet areas where suitable intermediate hosts such as snails and amphibians are present (Wojcik et al. 2001 cited by Mohl et al. 2009). In Spain, the trematode was present in foxes in the well-irrigated Jarama valley but not in the semiarid regions of southern Spain (Criado-Fernelio et al. 2000). The results of this study confirms this premise as the majority of the parasitised foxes were found in the water-rich areas of the River Shannon basin in the centre of the country and rich grasslands of the main dairy-producing area in north Munster. There are only three amphibian species in Ireland, the common brown frog, natterjack toad ( Epidalea calamita L.) and the smooth newt ( Lissotriton vulgaris L.) (Becart et al. 2007). The brown frog and natterjack toad are known to be intermediate hosts for A. alata (Mohl et al. 2009). The brown frog is widely dispersed throughout the country oc- cupying small ponds and other aquatic milieu and surround- ing grassland (Marnell 1998). The natterjack toad is less widely distributed being confined to the sandy dunes of the coastal areas of Dingle in Co. Kerry (Becart et al. 2007). Despite positive foxes being found in some coastal counties, there was no evidence of A. alata infection in the foxes examined from Dingle. This would suggest that the natterjack toad might not be an important intermediate host for this parasite in Ireland. Foxes habitat and home range can vary from 10 to 2,000 ha depending on the richness or sparseness of the environment and the abundance of food at various times of the year (MacDonald 1983; Lucherini and Lovari 1996). In areas with intensive agriculture, the short-term home range can vary from 500 to 700 ha with dispersal of young foxes up to 30 km (Fairley 1969; Coman et al. 1991). Over 20% and 48% of the reported sightings of R. temporaria were within a 5 and 10 km radius, respectively, of the place of capture of all the foxes infected with A. alata . It is likely that the positive foxes in this study encountered brown frogs at some stage in their life and that R. temporaria may have a role in the life cycle of this trematode in Ireland. The preferential habitat of foxes for foraging is open fields (Kidawa and Kowalczyk 2011). The majority of the A. alata -positive foxes were captured in areas of low-lying pasture in a corridor running in a northeast/southwest direc- tion in the centre of the country and bounded by mountain ranges in the south, west and northwest. In addition, the intensity of infection, as shown by the hot spot and high low clustering analysis, was greatest in foxes from east Limerick an area of intensive dairy and agricultural production. This limited geographical distribution was unexpected as there is no apparent reason why A. alata is not more widely dispersed, although the preference of hunters to hunt in open areas may have introduced some bias into the point positions where foxes were shot (Staubach et al. 2001). Not- withstanding many of the known paratenic and carnivore definitive hosts being present, the spectrum of intermediate hosts for completing the A. alata life cycle may be narrow in Ireland. Genetic diversity making various species unsuitable intermediate hosts maybe a possible explanation for the absence of A. alata in some parts of the country. Populations of R. temporaria genetically distinct from the European common frog haplotypes occur in Ireland as a consequence of survival in a local glacial refugium during the last ice age (Teacher et al. 2009). This study has shown that the prevalence of A. alata in foxes in Ireland is comparable to other countries in continental Europe. It appears to have a restricted distribution, which should aid regulatory public health bodies in target- ing measures preventing the transmission, in free range pig meat, of the parasite to humans. A number of features of the biology and host/parasite relationship of A. alata were identified, such as its limited geographical dispersion, identification and availability of invertebrate and amphibian intermediate hosts and pathological potential of high numbers of parasites in the small intestine of the definitive host, which need further ...
Citations
... Except for D. canis and Cystoisospora spp., all the others have zoonotic potential and, therefore, can parasitize humans. According to Murphy et al. (2012), more than 45% of zoonotic pathogens have a carnivorous host in their life cycle. Thus, wild canids play an important role in the maintenance and transmission of pathogens. ...
Cerdocyon thous is considered the most common wild canid in Rio Grande do Sul, and can serve as a host for several parasites, playing an important role in maintaining the biological cycle. Despite being a widespread and abundant species, they have a relatively little-known fauna of endo and ectoparasites, mainly focusing on the different regions of their occurrence. With this work, the objective was to report the multiparasitism in a specimen of C. thous in the Brazilian Pampa. Using modified Centrifuge-Flotation and Spontaneous Sedimentation techniques, a high taxonomic diversity of parasites was observed, and the finding of eggs compatible with Lagochilascaris spp. in C. thous in Brazil, in addition to Uncinaria spp. eggs and Cystoisospora spp. oocysts in the same host in the south of the country. The presence of eggs of different helminths in the feces of C. thous is extremely important, mainly for public health, but also for the knowledge of the biodiversity of parasites present in wild populations of canids, until then little studied, thus allowing the implementation of control programs.
Keywords:
coproparasitological; endoparasites; wild fauna
... The definitive hosts are carnivores such as canids, felids and mustelids (Wójcik et al., 2001;Takeuchi-Storm et al., 2015). In Europe, the definitive hosts are typically red foxes (Vulpes vulpes), wolves (Canis lupus) and racoon dogs (Nyctereutes procyinoides) (Murphy et al., 2012;Rentería-Solís et al., 2013;Ozoliņ a et al., 2018). ...
... Such areas should be prioritized for constant monitoring of A. alata. Particularly high infections of wild boar in a limited area have been described in Ireland (Murphy et al., 2012). ...
Alaria alata is an emerging parasite that poses a potential risk for those consuming game, pork, snails and frogs. One paratenic host of A. alata that is known to play an important role in its spread through its feeding habitats is the wild boar. However, no statistical analysis of the influence of aquatic environments and carnivores on the occurrence of A. alata in wild boars has yet been performed. The present study combines a small-scale analysis based on hunting districts in the Mazowieckie province with a large-scale analysis based on data for all provinces in Poland. We applied various modeling approaches, including logistic regression and a generalized linear model in order to determine the presence, intensity and prevalence of A. alata. We used the Alaria mesocercariae migration technique (AMT) to estimate the risk of A. alata among wild boar in a given hunting district or province. The small-scale analysis found that mesopredators (red fox (Vulpes vulpes)) and racoon dog (Nyctereutes procyinoides) were likely to influence A. alata infestation of wild boar; however, the effect was weak, probably as a result of the large home range size of these animals. The large-scale analysis found that wetlands influence the prevalence of A. alata in wild boar, with the estimated risk increasing in the north of the country; this finding is consistent with other studies. Our findings indicate that the occurrence of A. alata in wild boar requires analysis on many levels, and environmental factors play a key role in risk assessment.
... We identified a number of parasites which may impact the health of humans and domesticated animals. These include parasites currently considered a risk for zoonotic transmission such as Alaria alata, an intestinal parasite of wild canids-a concern as other Alaria species have been reported to cause fatal illness in humans (Murphy et al., 2012), and Bovine viral diarrhoea virus 1, which is not currently considered to be a human pathogen, but is highly mutable, has the ability to replicate in human cell lines, and has been isolated from humans on rare occasions (Walz et al., 2010). However, there is a large amount of effort that goes into studying infectious diseases of humans and domestic species, and it is likely that most contemporary associations among humans and described parasites have been recorded, even if not included in the aggregated databases because they occur rarely or are difficult to detect. ...
1. Parasites that infect multiple species cause major health burdens globally, but for many, the full suite of susceptible hosts is unknown. Predicting undocumented host–parasite associations will help expand knowledge of parasite host specificities, promote the development of theory in disease ecology and evolution, and support surveillance of multi‐host infectious diseases. The analysis of global species interaction networks allows for leveraging of information across taxa, but link prediction at this scale is often limited by extreme network sparsity and lack of comparable trait data across species.
2. Here we use recently developed methods to predict missing links in global mammal‐parasite networks using readily available data: network properties and evolutionary relationships among hosts. We demonstrate how these link predictions can efficiently guide the collection of species interaction data and increase the completeness of global species interaction networks.
3. We amalgamate a global mammal host–parasite interaction network (>29,000 interactions) and apply a hierarchical Bayesian approach for link prediction that leverages information on network structure and scaled phylogenetic distances among hosts. We use these predictions to guide targeted literature searches of the most likely yet undocumented interactions, and identify empirical evidence supporting many of the top ‘missing’ links.
4. We find that link prediction in global host–parasite networks can successfully predict parasites of humans, domesticated animals and endangered wildlife, representing a combination of published interactions missing from existing global databases, and potential but currently undocumented associations.
5. Our study provides further insight into the use of phylogenies for predicting host–parasite interactions, and highlights the utility of iterated prediction and targeted search to efficiently guide the collection of information on host–parasite interactions. These data are critical for understanding the evolution of host specificity, and may be used to support disease surveillance through a process of predicting missing links, and targeting research towards the most likely undocumented interactions.
... So far, studies have investigated the existence of infection hotspots at large to moderate spatial scales such as hundreds to thousands of metres (e.g. Bousema et al., 2010;Murphy et al., 2012;Poulin & FitzGerald, 1989;Ramirez-Sierra et al., 2010;Thamm et al., 2009 We argue that studies at a very fine spatial scale could improve our understanding of the factors favouring the encounter between infective parasite larvae and hosts, even for parasites not displaying active strategies to increase encounter rate. These very small-scale studies are also crucial to better predict potential infection hotspots, which are key targets for slowing the life cycles of parasites and thus eradicating pathogenic parasites to humans and/or wild animals. ...
For parasites, finding their hosts in vast and heterogeneous environments is a task that can be complex. Some parasite species rely on elaborate strategies to increase encounter rate with their hosts (e.g. behavioural modification of host), but others do not. For these parasites, a key issue is to reveal the processes that enable them to successfully find their hosts and complete their life cycles.
Here, we tested the hypothesis that infective larvae of the freshwater ectoparasite Tracheliastes polycolpus are not homogeneously distributed along the river and preferentially occur in very specific microhabitats that maximize encounter rate, and hence infection rate, with their host fish. To do this, we combined an in situ experiment (caging) with an empirical survey carried out on the same sites to identify potential ‘hotspots’ of infection at the microgeographic scale and their environmental characteristics.
Experimental and empirical results demonstrated that infections were not evenly distributed among microhabitats, and that infections were spatially aggregated in hotspots at a very fine spatial grain.
We further found that certain combinations of environmental variables were consistently and nonlinearly associated with higher infection rate for both caged and wild‐caught fish. Microhabitats characterized by very low or high stream velocities, associated with medium or very small substrate, respectively, and a deep water column were strongly and repeatedly associated with higher infection rates. These microhabitats could concentrate parasites and/or promote physical contact with the hosts.
We conclude that the characteristics of some microhabitats could facilitate contact between hosts and parasites and explain how some parasites manage to find their hosts in complex environments.
A free Plain Language Summary can be found within the Supporting Information of this article.
... Such close contact with foxes may result in the dispersion of invasive eggs into environments that pets and farm animals inhabit; therefore, it may represent a threat to human health [45]. Studies conducted in Spain confirmed that the infection of foxes with A. alata is more common among wild animals that live near moist areas; this fluke was present in foxes that lived near rivers and was absent in foxes that inhabited the desert regions of southern Spain [46]. In addition, in Poland, the percentage of red foxes infected with A. alata varies significantly among different regions, as it depends on the presence of surface water. ...
Alaria alata flukes are cosmopolitan parasites. In Europe, the definitive hosts are red foxes (Vulpes vulpes), wolves (Canis lupus), and raccoon dogs (Nyctereutes procyonoides), as well as animals that belong to the Felidae family. Intermediate hosts, such as snails and frogs, are the sources of infection for definitive hosts. The developmental stages of A. alata mesocercariae may occur in paratenic hosts, including many species of mammals, birds, and reptiles, as well as in wild boars (Sus scrofa), which are important from the zoonotic point of view. Because there are no regulations concerning the detection of A. alata in meat, this fluke is usually detected during official obligatory Trichinella spp. inspections. However, a method dedicated to A. alata detection was developed. The growing popularity of game and organic meat has led to an increased risk of food-associated parasitic infections, including alariosis, which is caused by the mesocercarial stage of A. alata. The aim of this article is to highlight the problem of A. alata as an emerging parasite, especially in the terms of the increasing market for game and organic meats that have been processed with traditional methods, often without proper heat treatment.
... (Al-Sabi et al. 2013;Bruzinskaite- Schmidhalter et al. 2012;Franssen et al. 2014b;Murphy et al. 2012). Additionally, raccoon dogs are very suitable definitive hosts, showing prevalences of up to 68-97%(Al-Sabi et al. 2013;Bruzinskaite-Schmidhalter et al. 2012;Laurimaa et al. 2016). ...
Urbanisation and invasion of wildlife into urban areas as well as human leisure activities create diverse wildlife-domestic animal-human interfaces, increasing the risk of (zoonotic) parasite spillover from sylvatic to domestic and synanthropic cycles. This study investigated the endo- and ectoparasite fauna, emphasising on parasites of One Health Concern, of the most common predators in northern Germany between November 2013 and January 2016. Eighty red foxes (Vulpes vulpes), 18 stone martens (Martes foina) and nine raccoon dogs (Nyctereutes procyonoides) were available for the study. Overall, 79 (73.8%) of the examined predators (n=107) harboured at least one endoparasite. The most frequently detected endoparasites in red foxes were Toxocara canis (43.8% positive individuals), Capillaria spp. (36.3%), Alaria alata (25.0%), Echinococcus multilocularis (26.3%) and Uncinaria stenocephala (25.0%). Furthermore, Toxascaris leonina, Trichuris vulpis, Taenia ssp., Mesocestoides spp. and coccidian oocysts were observed. The endoparasite species richness in raccoon dogs was comparable to red foxes, while in stone martens, only Capillaria spp. were found. Muscle digestion for detection of Trichinella spp. and antigen testing for Giardia spp. did not show positive results. Ectoparasite analyses revealed infestations with ticks species of the genus Ixodes as well as Dermacentor reticulatus. Scabies mites were not present in digested skin samples, while Demodex spp. mites were observed by faecal flotation in one red fox. Furthermore, fleas (Archaeopsylla erinacei and Chaetopsylla globiceps) were observed in the fur of red foxes, while lice were not present in any predator species. However, infestation frequency with ectoparasites was with 19.2% generally low in available predator skins (n=99). Overall, the present study showed that predators in northern Germany serve as reservoirs for parasites of One Health concern, with four of the five most frequent endoparasites being zoonotic, highlighting the need of parasite surveillance in wildlife predators in order to implement measures avoiding spillovers to domestic animals and humans.
... In our opinion, this is related to the scarcity of wetlands in the regions tested which these other authors also highlighted. Similar conclusions were made in studies of red foxes in Spain (Murphy et al. 2012), where A. alata was present in red foxes living in the well-irrigated valley of the Jarama river, but not in the desert regions of southern Spain. ...
Alaria alata is a trematode included among several emerging zoonotic parasites. The mesocercarial larval stage of A. alata named Distomum musculorum suis (DMS) may potentially be infective for humans. In the past, DMS was often observed in wild boar meat during the official Trichinella inspection by artificial digestion before a more specific and effective detection method, the A. alata mesocercariae migration technique (AMT), was introduced. In the present study, the AMT method was used to screen 3589 tissue samples collected from wild boars hunted in Poland during the 2015–2019 period. The survey mainly focused on the southern part of Poland with the majority of samples coming from Małopolskie, Świętokrzyskie, and Dolnoślaskie provinces; samples from ten additional provinces were also included. The total prevalence was 4.2% with mean abundance of 4.7 DMS. Occurrence was dependent upon environmental conditions (i.e., wetland habitats and water reservoirs) rather than on sex of the host or season in which they were hunted. The recovered trematodes were identified as Alaria spp. according to their morphological features. Molecular analysis of 18S rDNA and COI genes confirmed the species identification to be A. alata and documented genetic variability among the isolates.
... The trematodes of the Alaria genus are parasites of many wild and domestic carnivores, mainly foxes, wolves, raccoons, dogs and cats (3,10,12,16,18,34,37). The parasite has a complex life cycle with two intermediate hosts. ...
The study was aimed at assessment of the usefulness of a digestion method, a standard procedure for routine examination of wild boar meat for Trichinella, in detecting the presence of Distomum musculorum suis (DMS) in the population of wild boars from the Eastern Lublin province. The study material included 500 samples collected from the diaphragm pillars of 250 young boars (6-12 months) and 250 boars above one year of age. First, the meat was tested with the digestion method that is a referential procedure for trichinosis detection. Then, the samples in which over ten mesocercariae were found were assessed with an Alaria-Migration Technique (AMT). The digestion method confirmed the presence of Alaria mesocercariae in 42 carcasses of young boars (16.8 %) and 117 samples of animals older than one year (46.8 %). The study showed a diversified intensity of the parasite presence in the carcasses of individual animals. The invasion intensity ranged from 1 to 18 parasites in 50 g of meat in the young animals, and from 1 to 22 larvae in the older individuals. The carcasses of eight young and thirty two older animals contained over 10 parasites per 50 g of the meat, which accounted for 3.2 % and 12.8 % animals per respective age group. AMT analysis also indicated variable intensity of the parasite infestation, amounting to 32-57 mesocercariae in young animals and 31-71 larvae in the older ones. The study demonstrated an almost three times higher efficiency of the AMT method than the digestion method, which made us conclude that the former should be recommended for Alaria detection. The digestion method used for routine detection of Trichinella, despite its lower accuracy in diagnosing Alaria mesocercariae, can be also employed for the detection of DMS in the case of intensive parasite infection. Our study confirmed high prevalence of the parasite among wild boars from the Eastern Lublin Province. We also found that the invasion intensity depended on the animal age and was higher in older individuals. Considering the zoonotic nature of alariosis and its frequency, it poses an increasingly common problem for official veterinarians during the sanitary and veterinary evaluation of wild boar meat.
... Despite the distribution, mean intensity per 100 g of musculature parasites was higher in peritoneum (68), followed by the muscle of larynx (26) and diaphragm (11), which suggested that A. alata mesocercariae preferred muscular tissue containing high amounts of adipose and connective tissue and/or glandular tissues (Riehn et al., 2010). It has been previously discussed, that A. alata presence was closely linked to the wetlands (Möhl et al., 2009;Murphy et al., 2012;Széll et al., 2013), which was related to the complex life cycle including snail (1st intermediate) and amphibian (2nd intermediate) hosts (Möhl et al., 2009). Altitude could have been one of the reasons of comparatively high A. alata prevalence in Latvia. ...
Alaria alata trematode is widely distributed throughout Europe and has a complex life cycle in which wild boar serve as a reservoir host. The primary aims of the present study are to establish the occurrence of A. alata mesocercariae in naturally infected wild boar in Latvia and to assess the risk for humans to acquire A. alata infection via consumption of wild boar meat. By summarizing long-term data using the Trichinella inspection method from 2014 to 2019, the overall A. alata prevalence was 8.3%, of which significantly higher A. alata prevalence was observed during the summer seasons. Additionally, 43.9% (n = 485) of wild boar were found to be infected with A. alata using Alaria mesocercariae migration technique. The present study indicates that the probability for humans to acquire A. alata mesocercariae is possible, yet improbable and varies from 0.2% to 2.2%. Most likely, it depends on both frequency of A. alata presence in wild boar population and of a method of preparing wild boar meat for consumption that will allow for the parasite inactivation.
... Similar correlations connected with regions were observed in different studies conducted in Poland [21,23,33]. In other parts of Europe, the percentage of A. alata infected foxes differs depending on the investigation (and region) from very high [3,34], moderate, and low [1,8,12,18,19,35] to areas where these trematodes were not detected [17,36,37]. ...
The aim of the study was to analyze the distribution of the main groups of parasitic helminths within the small intestine of the red fox on the example of animals coming from eastern Poland. Two hundred and sixteen red foxes shot in eastern Poland were used in the investigation. Before examination, each small intestine was divided into three equal parts: anterior (A), middle (M), and posterior (P). Each part was examined separately with the sedimentation and counting technique. Six different types of intestinal parasites were detected: Alaria alata (78.7%), Mesocestoides spp. (78.2%), hookworms (72.7%), Taenia spp. (53.2%), Toxocara/Toxascaris (43.1%), and Echinococcus multilocularis (18.5%). Alaria alata was most often found in A and in the only-A variant. Taenia spp. and Toxocara/Toxascaris occurred often in A and were the second (after A. alata) parasites in terms of frequency occurring in the only-A variant. Mesocestoides spp. was most commonly located in M. Parasites with predilection sites located mainly in M and P were E. multilocularis and hookworms. In all parasite species, the variant covering the entire intestine (A + M + P) was found in samples with a higher intensity compared to variants limited to one or two fragments. Our investigation, as one of the few of its type, conducted a comprehensive analysis of the distribution of intestinal helminths in the small intestine of the red fox. It showed significant differences in the distribution of parasitic helminths in the small intestine of the red fox. Determining typical predilection sites for parasites in the intestine can be helpful in creating effective diagnostic methods.
