Bilharziella Polonica Research Articles

The species composition of the definitive hosts of the trematode <i>Bilharziella polonica</i> (Schistosomatidae) of Southern Karelia (Northwestern Russia)

We performed a parasitological survey of helminths of 398 waterfowl specimens from an ecologically unique territory of southern Karelia (North-West Russia). This is the first study of species composition and infection of birds that are definitive hosts of Bilharziella polonica have been obtained. The trematoda of Bilharziella polonica has been recorded only in seven species of birds — mallard, teal, garganey, goldeneye, tufted duck, shoveler, and red-necked grebe. The species of B. polonica has been recorded of red-necked grebe for the North-West of Russia for the first time. The role of infected birds of Bilharziella polonica in support of schistosomiasis, a disease that causes morbidity for causing human cercarial dermatitis or swimmer’s itch, were shown. We present data that life cycle of Bilharziella polonica is successfully implemented in the conditions of Karelia.

Diversity of transcripts of toll-like receptors in hemocytes of Planorbarius corneus mollusсs (Gastropoda, Pulmonata) uninfected and infected with Bilharziella polonica trematodes

Transcriptome of hemocytes from uninfected Planorbarius corneus snails and snails naturally infected with Bilharziella polonica (Schistosomatidae) was obtained and analyzed. Transcripts encoding all groups of immune factors previously described for other gastropods were found. Pathogen recognition molecules are the most diverse group of transcripts encoding immunity factors. Toll-like receptors of 11 types were identified. No differences in the set of toll-like receptors between infected and uninfected mollusсs were found. The data obtained expand our knowledge on immune reactions of snails to trematode invasion and make it possible to consider Planorbarius corneus as a new model for studying molluscs immune reactions.

The transcriptomic analysis of Planorbarius corneus hemocytes (Gastropoda) naturally infected with Bilharziella polonica (Schistosomatidae)

The study of molluscan innate immunity is essential for understanding the evolution of the immune system. An advance in the knowledge of their immune system can be achieved by increasing the number of model species. Our study focuses on the immunity of Planorbarius corneus, a pulmonate snail widely distributed in Eurasia. These snails are intermediate hosts of many trematodes, including Bilharziella polonica (Schistosomatidae). In this paper we obtained and analyzed transcriptomes of hemocytes of uninfected snails Planorbarius corneus and snails naturally infected with Bilharziella polonica. The transcriptomes were found to contain transcripts encoding all major groups of immune factors previously described for other gastropods. Pathogen-recognition molecules were the most diverse group of immune factors. Comparison of the transcriptomes of the infected and the uninfected molluscs showed that the expression of some genes changed during infection. Our results extend the knowledge of immune responses of pulmonate snails to trematode invasion and promote P. corneus as a new model for the study of molluscan defence reactions.

Threat of cercarial dermatitis in Hungary: A first report of Trichobilharzia franki from the mallard (Anas platyrhynchos) and European ear snail (Radix auricularia) using molecular methods.

Cercarial dermatitis in humans is a re-emerging zoonotic disease caused by infectious larvae of avian blood flukes within the Schistosomatidae family. Upon water contact, these avian schistosome larvae directly penetrate human skin and cause irritation. Between September 2018 and September 2020, carcasses of 94 mallards (Anas platyrhynchos), two green-winged teals (Anas crecca) along with one ferruginous duck (Aythya nyroca) were examined. Birds were collected within 12 regions of Hungary, representative of 9 different counties. Inspecting both morphological characters and molecular data, the cytochrome oxidase subunit I (COI) and large subunit ribosomal DNA (LSU rDNA) sequences, Bilharziella polonica and Dendritobilharzia pulverulenta were each identified. Most importantly, Trichobilharzia franki was found for the first time in Hungary and in 5 dispersed counties in conjunction with of 3 counties where other avian schistosomes were found. Of note, these avian blood flukes were predominately encountered in wild mallards (∼50%) and not in birds reared for hunting (∼1%). In total, 245 European ear snails (Radix auricularia), a known intermediate host of Trichobilharzia spp., were collected from an urban pond in Eger, Hungary. Five snails (∼2%) consistently shed numerous furcocercariae of T. franki that were confirmed by molecular methods. Our findings help to pinpoint a contemporary life cycle of this avian schistosome within an urban environment, a location regularly visited by various wild waterfowl and the possible species of avian schistosomes responsible for cercarial dermatitis in Hungary. Taken as a whole, we demonstrate the actual and potential risk zone for cercarial dermatitis, particularly with reference to R. auricularia distributions, within Hungary and across Central Europe.

Life cycle of Bilharziella polonica (Trematoda, Schistosomatidae) parasite of semi-aquatic birds in Uzbekistan

Schistosomatidae are an actively studied ecological group of trematodes. Their ability to cause various parasitic diseases in animals and humans makes them an interesting object of study for a number of research centres worldwide. One of the commonest species in this group is Bilharziella polonica (Kowalewsky, 1895), whose mature stages have been recorded in aquatic and semi-aquatic birds in Uzbekistan. Our research team established that the following birds were infected with mature trematodes B. polonica: Anas platyrhynchos (23%), A. crecca (18%), Podiceps ruficollis (11%), Ardea cinerea (14%) and one individual of Oxyura leucocephala. The highest infection rate was shown by the mallard A. platyrhynchos (23%) and common teal A. crecca (18%). The infection intensity ranged between 2 and 27 individuals. Research into various types of water bodies in Karakalpakstan identified 10 mollusc species – Lymnaeidae (4 species), Planorbidae (4 species) and Physidae (2 species). Cercariae morphologically similar to larvae of B. polonica were found in two species, Planorbis planorbis and P. tangitarensis. 6 chicks of domestic ducks were experimentally infected with those cercariae to track the life cycle of B. polonica in the organism of a definitive host. Helmintholological dissections showed that every duck was infected with B. polonica, which became mature 23–27 days after the infection. Eggs of B. polonica were recorded in the excrement of one of the birds 33–35 days after the infection. Based on field and experimental research, we identify the mollusc P. tangitarensis as a new intermediate host for B. polonica in Uzbekistan.

GEOGRAPHIC AND ECOLOGIC ASPECTS OF THE COMMUNITY STRUCTURE OF TREMATODES OF MALLARDS (ANAS PLATYRHYNCHOS) IN NORTHERN POLAND AND THE CZECH REPUBLIC.

Trematode infestation of Mallards (Anas platyrhynchos) varies between northern Poland and the Czech Republic. We determined the trematode fauna of juvenile and adult Mallards from Poland in 2010-16 (n=79 Mallards) and from the Czech Republic in 1964-2001 (n=296). Infracommunity diversity of trematodes from juvenile Mallards, defined by the Brillouin index and mean number of species, was significantly greater in Poland than it was in the Czech Republic. There were more species and greater biodiversity in the trematode communities of Mallards from Poland, where the environment is more natural and less altered by human activity than it is in the Czech Republic. In the trematode community of juvenile Mallards, the Simpson's index of biodiversity was higher in the Czech Republic than it was in Poland. The Berger-Parker dominance index was comparable in both countries. In terms of prevalence, the structure of the trematode fauna was hierarchic, and trematode species had different positions in this hierarchy in the two countries. Statistically significant differences in the epidemiologic indices between infection of juvenile Mallards from Poland and the Czech Republic were noted for Bilharziella polonica, Echinostoma miyagawai, Echinostoma revolutum, Prosthogonimus cuneatus, Prosthogonimus ovatus, Notocotylus attenuatus, Echinoparyphium recurvatum, Australapatemon minor, Apatemon gracilis, Cyathocotyle prussica, Hypoderaeum conoideum, Metorchis xanthosomus, Psilochasmus oxyurus, and Cotylurus cornutus.

Thermal preferences of bird schistosome snail hosts increase the risk of swimmer's itch

Ambient temperature strongly affects host parasite interactions, especially when both are ectothermic. Bird schistosomes, which cercariae are known as agents of swimmer's itch and their snail hosts can be a good example of this phenomenon. The snails of these parasites play the key role, as the source of harmful larvae. Cercarial dermatitis is noted even in areas when prevalence of parasites in snail populations is very low. The main question is what adaptation in snail-fluke association can lead to a sufficient number of cercariae causing swimmer's itch in lake water? The influence of ambient temperature on snail survival and cercarial production as well as the thermal preferences of two host species naturally infected with bird schistosomes were studied. The 24-h preferences of Lymnaea stagnalis infected with Trichobilharzia szidati, and Planorbarius corneus infected with Bilharziella polonica were recorded using an oblong thermal gradient set (OTGS). Both cercariae releasing hosts of bird schistosomes preferred a significantly lower temperature than non-infected snails. Additionally, at a higher temperature, the survival of snail hosts was shortened as a result of the increase in daily cercarial expulsion. An especially interesting result concerns the release of a significantly larger total cercariae number by L. stagnalis at lower than at higher temperatures. These data indicate that preferences of infected snails to low temperature microhabitats can increase host survival and parasite success, as well as affecting the increase in the number of invasive larvae in the environment increasing the risk of swimmer's itch.

System of suborder Schistosomatida (Platyhelminthes: Trematoda)

The purpose of the research: system retrofit of suborder Schistosomatidа in reliance on their morfo-biological distinctions. Materials and methods. Samples of adult and 5 species of larvas have been collected and tested: Schistosoma turkestanicum Skryabin, 1913, Bilharziella polonica (Kowalewsky, 1899), Trichobilharzia ocellata (La Valette, 1854), Dendritobilharzia loossi Skryabin, 1924 and Gigantobilharzia acotylea Odhner, 1910. Adult phases of trematode have been identified in accordance to common methods. Identification of cercaria larva produced by water living shell-fish (Lymnaeidae, Planorbidae, Physidae, Melanoididae) has been carried out according to indicators. Current system of trematode suborder Schistosomatidа - vertebrate animals and man parasites are analyzed. Results and discussion. New variant of system of trematode suborder Schistosomatidа order is proposed. Schistosomatida morfo-biological distinctions and biocycles are taken as a basis. Two families are distinguished in this suborder: Schistosomatidae and Bilharziellidae, which represent parasites of warm-blooded vertebrate animals. There are two families of Sanguinicolidae and Spirorchiidae in suborder Sanguinicolida, which consist of fish and reptile parasites respectively. For Schistosomatida order the new underclass Schistosomatidea is founded. Sanguinicolida order is left as the part of Digenea underclass consisting of androgynous fluke.

Having bird schistosomes in mind-the first detection of Bilharziella polonica (Kowalewski 1895) in the bird neural system.

Nasal bird schistosomes can cause bilharziosis in birds and have the potential to cause swimmer's itch in humans. We determined the prevalence of bird schistosomes in 106 mallards (Anas plathyrhynchos) from 11 water sources in Germany from 2014. Dissections were performed focusing on parasitic infections of the neural system. Infections with Trichobilharzia regenti (Horák et al. 1998) were found in 21% of the birds (n=22), whereas Bilharziella polonica (Kowalewski 1895) were found between the brain membranes (meninges) and the brain, in the spinal cord or in the intestine of 12% of the mallards (n=13). No significant influence of sex, age, and body condition between infected and non-infected animals was observed. Our study provides the first description of B. polonica from the neural system of birds and provides an epidemiological understanding of a parasite of human health concern.

Digenean communities in the tufted duck [Aythya fuligula (L., 1758)] and greater scaup [A. marila (L., 1761)] wintering in the north-west of Poland

A total of 124 specimens of the tufted duck, Aythya fuligula, and 63 greater scaup, A. marila, were examined for digenean parasites. Both duck species, which overwinter in a coastal lake connected with the southern Baltic (north-west Poland) were found to support Amblosoma exile, Cyathocotyle prussica, Paracoenogonimus ovatus, Australapatemon minor, Cotylurus cornutus, Echinoparyphium recurvatum, Echinostoma revolutum and Notocotylus attenuatus. In addition, the tufted duck hosted Hypoderaeum conoideum, Bilharziella polonica, Neoeucotyle zakharovi, Renicola mediovitellata, Psilochasmus oxyurus, Psilostomum brevicolle and Cryptocotyle concava; Echinostoma nordiana occurred in the greater scaup only. The two duck species differed significantly in the intensity and abundance of their digenean infection. Aythya marila harboured higher intensity levels and a wider assemblage of digeneans than A. fuligula, and this was likely to be due to differences in the pre-wintering exposure of the duck species to infective stages of these freshwater digeneans. Digenean communities in both duck species, strongly dominated by E. recurvatum, were relatively similar in their structure. No significant sex-dependent differences in digenean infections were revealed, except for the infection with N. attenuatus in A. fuligula. Similarly, there were no significant age-dependent differences (adult versus immature birds) in digenean infections, except for that with N. attenuatus in A. fuligula. The structural similarity between digenean communities in the two duck species is most likely an effect of overlapping diets based on freshwater molluscs, components of the digenean transmission pathway to definitive hosts.

The neuromuscular system in freshwater furcocercaria from Belarus. II Diplostomidae, Strigeidae, and Cyathocotylidae

The neuromuscular system (NMS) in cercariae of Diplostomum pseudospathaceum, Cotylurus szidati, Australapatemon burti, Holostephanus volgensis, and Paracoenogonimus ovatus was studied with immunocytochemical methods and confocal scanning laser microscopy. The patterns of F-actin in the musculature, 5-HT immunoreactive (-IR), FMRF-amide-IR neuronal elements, and α-tubulin-IR in sensory receptors were investigated. The NMS in the five species studied were compared with each other and with three species of Schistosomatidae studied earlier (Bilharziella polonica, Trichobilharzia szidati, and Trichobilharzia franki). No major structural differences in the musculature, the 5-HT-IR or FMRF-IR neuronal elements were noticed between the cercariae. The minor variations observed in the musculature were related to the size and organization of the muscle fibers. The checked pattern formed by the transverse muscle fibers in the tail stems of D. pseudospathaceum, C. szidati, A. burti, H. volgensis, and P. ovatus was not observed in B. polonica, T. szidati, and T. franki. A trend in the differentiation of the longitudinal muscle fibers in the furca from evenly distributed fibers in H. volgensis and P. ovatus to many bundles in D. pseudospathaceum and two well-organized lateral bundles in C. szidati, A. burti, and Trichobilharzia spp. was observed. The transverse muscle fibers in the furca follow the same trend. The number of 5-HT-IR neurons in the cercarial bodies varied between 10 and 16. In cercariae of H. volgensis and P. ovatus, the central nervous system (CNS) was less centralized compared to the CNS in the other species studied, with only two 5-HT-IR marker neurons in each brain ganglion and the other neurons distributed evenly along the main cords. In the tails of H. volgensis and P. ovatus, many transverse 5-HT-IR comissures were found. In the tails of higher strigeidid cercariae, only a few crosslinks were observed. The number and distribution of sensory receptors on the bodies and tails of the cercarial species differed from each other. A trend in the differentiation of the sensory receptors in the tails was discerned. A process of grouping and decrease in number of ciliated receptors in the stem and in the furca from H. volgensis and P. ovatus to Schistosomatid cercariae took place.

Molecular taxonomic identification of Schistosomatidae from Naroch Lake and Polonevichi Lake in Belarus

In Belarus, Naroch Lake is the only area with a high incidence of the human cercarial dermatitis (HCD). However, very little is known about the taxonomy of avian schistosomes, the causative agents of the disease, which are found in Naroch Lake and other lakes in Belarus. In this study, we used a molecular approach to investigate the systematic position and biodiversity of avian schistosomes from Naroch Lake and Polonevichi Lake. Based on the sequence analysis of the ITS genomic region, we were able to detect four different species of bird schistosomes in Naroch Lake ( Trichobilharzia szidati, Trichobilharzia franki, Bilharziella polonica and a novel Trichobilharzia species) and two species in Polonevichi Lake ( T. szidati and B. polonica). The data were used to reveal the phylogenetic position of HCD causative cercariae found in Belarusian water reservoirs and to establish their relationships within the group of avian schistosomes. We discuss the possibility of identifying species of Trichobilharzia using the fragment length polymorphism analysis of the ITS region. Possible epidemiological causes of HCD incidence in Belarus are also discussed.

Detection of European Trichobilharzia Schistosomes (T. franki, T. szidati, and T. regenti) Based on Novel Genome Sequences

The most frequent causative agents of cercarial dermatitis in Europe are the avian schistosomes of the genus Trichobilharzia . They preferably parasitize birds of the Anatidae. Trichobilharzia spp. schistosomes are also able to penetrate mammalian skin, posing a health risk to mammals, including humans. Currently several loci from nuclear and mitochondrial genomes are determined for European species of Trichobilharzia . Among them there is 1 genome sequence, ToSau3A, which is suitable for detection of Trichobilharzia spp. infection in aquatic systems. In the present paper, we used a PCR assay to obtain novel genome sequences from cercariae isolates of 3 European bird schistosome species ( Trichobilharzia franki , Trichobilharzia szidati , and Trichobilharzia regenti ) collected from freshwater ponds in Belorussia and Russia. We applied RAPD-fingerprinting using 1 random primer to differentiate 3 trichobilharzian species and subsequently cloned and sequenced putative species-specific RAPD fragments. One of them (410 bp in length), which was obtained for T. franki , revealed 64% homology with the repeat region of Schistosoma mansoni (GenBank FN357352) and turned out to be suitable for designing a specific primer pair (TR98F and TR98R) to detect 7 novel DNA sequences in the genome of 3 European Trichobilharzia species. The newly designed primer pair was found to be potentially suitable for PCR-based detection of trichobilharzian infection in snails. PCR primers TR98F and TR98R amplified only the DNA isolated from cercariae and sporocysts of 3 trichobilharzian species, but neither the DNA of 3 other digenean species ( Bilharziella polonica , Apatemon sp., and Diplostomum sp.) nor the DNA of uninfected host snails ( Lymnaea stagnalis , Radix auricularia , and Radix ovata ).

Avian schistosomes in French aquatic birds: a molecular approach

The prevalence of human cercarial dermatitis (HCD) caused by bird schistosomes appears to be increasing in France, in light of the impact of tourism combined with high densities of wild aquatic hosts in freshwater areas. The present work expands our knowledge of schistosome systematics by including samples of bird schistosomes collected from their natural hosts in France. Heads (318) and viscera (81) of aquatic birds belonging to 16 species from five orders, collecting during the hunting seasons or found dead, were autopsied for nasal and visceral schistosomes. Eggs and/or adults were analysed by molecular methods using the D2 domain and the second internal transcribed spacer (ITS-2) region of rDNA to determine species. Even if nasal eggs were polymorphic according to the host, all haplotypes were similar to that of Trichobilharzia regenti. Marked diversity of visceral species was observed. Final hosts under natural conditions were reported. For the first time, Trichobilharzia franki is reported in its natural bird hosts, Anas platyrhynchos, Anas crecca, Aythya fuligula and Cygnus olor. We also identified T. szidati in A. crecca and Anas clypeata. Bilharziella polonica was found in six species of aquatic birds, including Grus grus. This finding is the first record of bird schistosomes in this aquatic bird. Three new taxa of visceral schistosomes in Anser anser are strongly suspected according to their haplotypes. Futhermore, a new haplotype of visceral schistosomes isolated in Cygnus olor and similar to Allobilharzia visceralis was identified.

QUALITATIVE AND QUANTITATIVE BEHAVIORAL TRAITS IN A COMMUNITY OF FURCOCERCARIAE TREMATODES: TOOLS FOR SPECIES SEPARATION?

Many trematode cercariae show distinct behavioral features, which have commonly been used in species identification in combination with morphological characteristics. However, information regarding cercariae behavior has often not been quantified in detail, or it is scattered in the literature, which is why the appropriate level of precision in behavioral identity, particularly in groups of cercariae species showing considerable morphological overlap, has not been properly established. In this study, we investigated one such group, the furcocercariae trematodes, by studying their behavior in a community consisting of 8 species (Diplostomum pseudospathaceum, Ichthyocotylurus variegatus, Cotylurus brevis, Cercaria spinulosa, Australapatemom sp., Australapatemom burti, Sanguinicola sp., and Bilharziella polonica) in central Finland. Our aim was not to develop an identification formula on the basis of behavior but to investigate and propose characteristic measurements applicable in separation of cercariae species. We used a 2-level approach, first recording qualitative behavioral traits of the cercariae, including swimming type and resting position; and, second, more detailed quantitative behavioral characteristics, such as resting time, swimming time, and swimming speed. Essentially, species showing a 2-phase behavior were distinguishable according to qualitative traits (resting position), whereas with those showing continuous swimming behavior, a combination of qualitative and quantitative traits (swimming speed) was required. These results suggest that characteristics of cercariae behavior can not only be used in species identification but also in general life history comparisons investigating details of the cercariae transmission.

Bird schistosomes of wildfowl in the Czech Republic and Poland

In 2005, we dissected 102 wildfowl from the Czech Republic and 73 wildfowl from Poland including representatives of Anseriformes, Gruiformes and Gaviiformes. Schistosome infection was found in a total of 21 (29%) and 23 (23%) birds from Poland and the Czech Republic, respectively. All infected birds belonged to the order Anseriformes. The prevalences of nasal and visceral species were, respectively, 22% and 16% in Poland and 6% and 19% in the Czech Republic. Four species of schistosomes were found: Bilharziella polonica Kowalewski, 1895, Trichobilharzia regenti Horák, Koláfová et Dvorák, 1998, T. szidati Neuhaus, 1952, and an undetermined schistosome from the intestinal wall of Anas penelope L. The finding of T. szidati represents the first record of the parasite from natural final host since the species description.

Furcocercous cercariae (Trematoda) from freshwater snails in Central Finland

AbstractA total of eight species of furcocercous cercariae of four families (Strigeidae, Diplostomidae, Schistosomatidae and Sanguinicolidae), were found in 2005 in Lake Konnevesi in Central Finland in four snail species (Valvata macrostoma, Lymnaea stagnalis, Bathyomphalus contortus and Planorbarius corneus). Australapatemon burti (Miller, 1923), Australapatemon sp., Cotylurus brevis Dubois et Rausch, 1950, Cercaria spinulosa Ginetsinskaya, 1959 and Sanguinicola sp. are new species records for Finland. Ichthyocotylurus variegatus (Creplin, 1825) and Bilharziella polonica (Kowalewski, 1895) were first recorded as cercariae in Finland. The most common cercariae were A. burti (prevalence 13.3%) and Diplostomum pseudospathaceum Niewiadomska, 1984 (10.0%). Our study represents the first host record of Valvata macrostoma for larval stages of Australapatemon sp. and Sanguinicola sp.

Seasonal morphological variations in bird schistosomes

The present work is a contribution to the systematics of Bilhorziello and Dendritobilharzio. Wildfowl was killed in hunting seasons or found dead in Champagne-Ardenne region, France, and autopsied with focus on schistosomes. Seven Anas plotyrhynchos (mallards), one Ardeo cinerea (grey heron) and two Cygnus olor (mute swans) were parasitized by Bilharziella. One C. olor was parasitized by Dendritobilharzia. Depending on season and hosts, various morphological forms of Bilharziello suggesting several species were observed. The differences in male and female worms concerned the morphology of genital apparatus, the spination on suckers, the body size and proportions. However, the comparison of DNA sequences led to a conclusion that these forms belonged to one species, Bilharziella polonica (Kowalewski, 1895). The morphological features and the body sizes of our samples of Dendritobilharzia seemed to differ from the type species of D. pulverulenta (Braun, 1901). Nevertheless, molecular analysis confirmed identity. We hypothesize that the differences in Bilharziella and Dendritobilharzia might be linked to internal host factors (e.g. hormonal levels), and influenced by season, host, and worm age. The definition of the genera Bilharziello and Dendritobilharzio was amended.

Trematodes of the Eurasian coot (Fulica atra L) in the Belgrade area

A total of 118 Eurasian coots (Fulica atra L) from the Belgrade area were examined and 68.64% were found to be infected with trematodes. Nine species of trematodes were detected: Echinostoma sarcinum, Metorchis xanthosomus Hyptiasmus oculeus, Cyclocoelum mutabile, Cotylurus hebraicus, Notocotylus attenuatus, Notocotylus pacifera, Tanaisia longivitelata and Bilharziella polonica. These results showed the significant role of the Eurasian coot in the epizootiology of trematodosis in other birds, wild and domestic waterfowl, gallinacea and fish.

Is there a potential danger of "swimmer's itch in Poland?

Tests with cercariae of Trichobilharzia szidati (Neuhaus, 1952) and Bilharziella polonica (Kowalewski, 1895) from naturally parasitised host snails from lake Jeziorak in north Poland were carried out on human volunteers under laboratory conditions. Only T. szidati was capable of causing the symptoms of "swimmer's itch". In the experiment with B. polonica no symptoms of dermatitis were observed either after the first or second exposure.