Avian schistosomes in French aquatic birds: a molecular approach

Abstract

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.

Avian Schistosomes and Outbreaks of Cercarial Dermatitis

“…Current results based on all of the available sequence data in GenBank for the internal transcribed spacer (ITS) region indicate that there are about nine distinct lineages, only two of which are described: Gigantobilharzia and Dendritobilharzia (40,(64)(65)(66)(67)(68)(69). Most of the lineages in this part of clade D have one to a few species and have been seen in only a few cases, many related to dermatitis outbreaks (12) ( Table 1).…”

“…This propensity to migrate large distances distinguishes avian schistosomes from mammalian schistosomes in terms of distribution, diversification, and host use, perhaps with the exception of Schistosoma mansoni (in terms of long-distance migration only) (124). Yet the schistosome species found in a wide range of avian host orders (e.g., Bilharziella and Dendritobilharzia) ( Table 1) are not the ones recurrently responsible for outbreaks and are also species that are not genetically diverse compared to other species (69,125,126). Currently, D. pulverulenta might be the most widespread single species of avian schistosome, crossing both the Northern and Southern Hemispheres (117,125,127,128).…”

“…1). Allobilharzia, from swans, and Anserobilharzia, from geese, both have a circumpolar distribution (69,70,105,129,130 (10). The area was a eutrophic municipal lake/pond with a dense population of Gyraulus parvus snails and Canada geese.…”

“…Most of the effort has been conducted using three gene regions. To date, the nuclear ribosomal DNA D1-D2 regions of 28S, the internal transcribed spacer (ITS) region, and the mitochondrial cox1 gene have been tested as molecular markers for systematics (40,63,67,69,70,105,123,248,249,251), epidemiology (252), and diagnostics (121,253). Sequencing of gene regions such as the nuclear ITS region and the mitochondrial cox1 gene not only has linked life cycle stages but also has suggested that our recognition of the diversity of avian schistosomes continues to grow (10, 12, 40, 65-67, 69, 70, 105, 129, 133, 135).…”

Swimmer's Itch in Belgium: First Recorded Outbreaks, Molecular Identification of the Parasite Species and Intermediate Hosts

“…The sequences were amplified using a commercial kit Taq PCR Master Mix (Qiagen, Hilden, Germany) in a Peltier Thermal Cycler (MJ Research). A protocol previously described ( Jouet et al 2008( Jouet et al , 2009) was followed. The rDNA of furcocercariae was amplified using the primers previously described (Mollaret et al 1997): C2¢B (forward) (5¢-GAA AAGTACTTTGRARAGAGA-3¢) and D2 (reverse) (5¢-TCC GTGTTTCAAGACGGG-3¢).…”