Molecular characterization and distribution of Schistosoma cercariae collected from naturally infected bulinid snails in northern and central Côte d'Ivoire

Abstract

Background: Accurate identification of schistosome species infecting intermediate host snails is important for understanding parasite transmission, schistosomiasis control and elimination. Cercariae emerging from infected snails cannot be precisely identified morphologically to the species level. We used molecular tools to clarify the distribution of the Schistosoma haematobium group species infecting bulinid snails in a large part of Côte d'Ivoire and confirmed the presence of interspecific hybrid schistosomes.

Methods: Between June 2016 and March 2017, Bulinus snails were sampled in 164 human-water contact sites from 22 villages of the northern and central parts of Côte d'Ivoire. Multi-locus genetic analysis (mitochondrial cox1 and nuclear ITS) was performed on individual schistosome cercariae shed from snails, in the morning and in the afternoon, for species and hybrid identification.

Results: Overall, 1923 Bulinus truncatus, 255 Bulinus globosus and 1424 Bulinus forskalii were obtained. Among 2417 Bulinus screened, 25 specimens (18 B. truncatus and seven B. globosus) shed schistosomes, with up to 14% infection prevalence per site and time point. Globally, infection rates per time point ranged between 0.6 and 4%. Schistosoma bovis, S. haematobium and S. bovis × S. haematobium hybrids infected 0.5%, 0.2% and 0.4% of the snails screened, respectively. Schistosoma bovis and hybrids were more prevalent in B. truncatus, whereas S. haematobium and hybrid infections were more prevalent in B. globosus. Schistosoma bovis-infected Bulinus were predominantly found in northern sites, while S. haematobium and hybrid infected snails were mainly found in central parts of Côte d'Ivoire.

Conclusions: The data highlight the necessity of using molecular tools to identify and understand which schistosome species are transmitted by specific intermediate host snails. The study deepens our understanding of the epidemiology and transmission dynamics of S. haematobium and S. bovis in Côte d'Ivoire and provides the first conclusive evidence for the transmission of S. haematobium × S. bovis hybrids in this West African country. Trial registration ISRCTN, ISRCTN10926858. Registered 21 December 2016; retrospectively registered (see: http://www.isrctn.com/ISRCTN10926858 ).

Keywords: Bulinus forskalii; Bulinus globosus; Bulinus truncatus; Côte d’Ivoire; Molecular markers; Schistosoma bovis; Schistosoma haematobium; Schistosome hybrids.

Fig. 1

Map of Côte d’Ivoire showing the location of the 22 villages that were included in the study together with the distribution and proportions of the different Bulinus species found at the different survey sites where schistosome transmission was detected and the proportion of the different schistosomes being transmitted at the seven positive sites. The names of the villages are indicated in black font and names of regions are in grey. Data are merged for all three surveys conducted between June 2016-March 2017