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Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley.

ABSTRACT: BACKGROUND:Urogenital schistosomiasis, caused by infection with Schistosoma haematobium, is endemic in Niger but complicated by the presence of Schistosoma bovis, Schistosoma curassoni and S. haematobium group hybrids along with various Bulinus snail intermediate host species. Establishing the schistosomes and snails involved in transmission aids disease surveillance whilst providing insights into snail-schistosome interactions/compatibilities and biology. METHODS:Infected Bulinus spp. were collected from 16 villages north and south of the Niamey region, Niger, between 2011 and 2015. From each Bulinus spp., 20-52 cercariae shed were analysed using microsatellite markers and a subset identified using the mitochondrial (mt) cox1 and nuclear ITS1?+?2 and 18S DNA regions. Infected Bulinus spp. were identified using both morphological and molecular analysis (partial mt cox1 region). RESULTS:A total of 87 infected Bulinus from 24 sites were found, 29 were molecularly confirmed as B. truncatus, three as B. forskalii and four as B. globosus. The remaining samples were morphologically identified as B. truncatus (n?=?49) and B. forskalii (n?=?2). The microsatellite analysis of 1124 cercariae revealed 186 cercarial multilocus genotypes (MLGs). Identical cercarial genotypes were frequently (60%) identified from the same snail (clonal populations from a single miracidia); however, several (40%) of the snails had cercariae of different genotypes (2-10 MLG's) indicating multiple miracidial infections. Fifty-seven of the B. truncatus and all of the B. forskalii and B. globosus were shedding the Bovid schistosome S. bovis. The other B. truncatus were shedding the human schistosomes, S. haematobium (n?=?6) and the S. haematobium group hybrids (n?=?13). Two B. truncatus had co-infections with S. haematobium and S. haematobium group hybrids whilst no co-infections with S. bovis were observed. CONCLUSIONS:This study has advanced our understanding of human and bovid schistosomiasis transmission in the Niger River Valley region. Human Schistosoma species/forms (S. haematobium and S. haematobium hybrids) were found transmitted only in five villages whereas those causing veterinary schistosomiasis (S. bovis), were found in most villages. Bulinus truncatus was most abundant, transmitting all Schistosoma species, while the less abundant B. forskalii and B. globosus, only transmitted S. bovis. Our data suggest that species-specific biological traits may exist in relation to co-infections, snail-schistosome compatibility and intramolluscan schistosome development.

SUBMITTER: Pennance T

PROVIDER: S-EPMC7247258 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley.

Pennance Tom T Allan Fiona F Emery Aidan A Rabone Muriel M Cable Jo J Garba Amadou Djirmay AD Hamidou Amina Amadou AA Webster Joanne P JP Rollinson David D Webster Bonnie L BL

Parasites & vectors 20200524 1

<h4>Background</h4>Urogenital schistosomiasis, caused by infection with Schistosoma haematobium, is endemic in Niger but complicated by the presence of Schistosoma bovis, Schistosoma curassoni and S. haematobium group hybrids along with various Bulinus snail intermediate host species. Establishing the schistosomes and snails involved in transmission aids disease surveillance whilst providing insights into snail-schistosome interactions/compatibilities and biology.<h4>Methods</h4>Infected Bulinus ...[more]

PMID: 32448268

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Project description:BACKGROUND:Human schistosomiasis is the second most important tropical disease and occurs in two forms in Africa (intestinal and urogenital) caused by the digenetic trematodes Schistosoma mansoni and Schistosoma haematobium, respectively. A proposed recent shift of schistosomiasis above a previously established altitudinal threshold of 1400 m above sea level in western Ugandan crater lakes has triggered more research interest there. METHODS:Based on extensive field sampling in western Uganda and beyond and employing an approach using sequences of the mitochondrial barcoding gene cytochrome c oxidase subunit 1 (cox1) this study aims were: (i) identification and establishment of the phylogenetic affinities of Bulinus species as potential hosts for Schistosoma spp.; (ii) determining diversity, frequency and distribution patterns of Bulinus spp.; and (iii) establishing genetic variability and phylogeographical patterns using Bayesian inference and parsimony network analyses. RESULTS:Out of the 58 crater lakes surveyed, three species of Bulinus snails were found in 34 crater lakes. Bulinus tropicus was dominating, Bulinus forskalii was found in two lakes and Bulinus truncatus in one. The latter two species are unconfirmed potential hosts for S. haematobium in this region. However, Bulinus tropicus is an important species for schistosomiasis transmission in ruminants. Bulinus tropicus comprised 31 haplotypes while both B. forskalii and B. truncatus exhibited only a single haplotype in the crater lakes. All species clustered with most of the haplotypes from surrounding lake systems forming source regions for the colonization of the crater lakes. CONCLUSIONS:This first detailed malacological study of the crater lakes systems in western Uganda revealed presence of Bulinus species that are either not known or not regionally known to be hosts for S. haematobium, the causing agent of human urogenital schistosomiasis. Though this disease risk is almost negligible, the observed dominance of B. tropicus in the crater lakes shows that there is a likelihood of a high risk of infections with Schistosoma bovis. Thus, extra attention should be accorded to safeguard wild and domestic ruminants in this region as the population benefits from these animals.

Project description:BackgroundThe Zanzibar Archipelago (Pemba and Unguja islands) is targeted for the elimination of human urogenital schistosomiasis caused by infection with Schistosoma haematobium where the intermediate snail host is Bulinus globosus. Following multiple studies, it has remained unclear if B. nasutus (a snail species that occupies geographically distinct regions on the Archipelago) is involved in S. haematobium transmission on Zanzibar. Additionally, S. haematobium was thought to be the only Schistosoma species present on the Zanzibar Archipelago until the sympatric transmission of S. bovis, a parasite of ruminants, was recently identified. Here we re-assess the epidemiology of schistosomiasis on Pemba and Unguja together with the role and genetic diversity of the Bulinus spp. involved in transmission.Methodology/principal findingsMalacological and parasitological surveys were conducted between 2016 and 2019. In total, 11,116 Bulinus spp. snails were collected from 65 of 112 freshwater bodies surveyed. Bulinus species identification were determined using mitochondrial cox1 sequences for a representative subset of collected Bulinus (n = 504) and together with archived museum specimens (n = 6), 433 B. globosus and 77 B. nasutus were identified. Phylogenetic analysis of cox1 haplotypes revealed three distinct populations of B. globosus, two with an overlapping distribution on Pemba and one on Unguja. For B. nasutus, only a single clade with matching haplotypes was observed across the islands and included reference sequences from Kenya. Schistosoma haematobium cercariae (n = 158) were identified from 12 infected B. globosus and one B. nasutus collected between 2016 and 2019 in Pemba, and cercariae originating from 69 Bulinus spp. archived in museum collections. Schistosoma bovis cercariae (n = 21) were identified from seven additional B. globosus collected between 2016 and 2019 in Pemba. By analysing a partial mitochondrial cox1 region and the nuclear ITS (1-5.8S-2) rDNA region of Schistosoma cercariae, we identified 18 S. haematobium and three S. bovis haplotypes representing populations associated with mainland Africa and the Indian Ocean Islands (Zanzibar, Madagascar, Mauritius and Mafia).Conclusions/significanceThe individual B. nasutus on Pemba infected with S. haematobium demonstrates that B. nasutus could also play a role in the local transmission of S. haematobium. We provide preliminary evidence that intraspecific variability of S. haematobium on Pemba may increase the transmission potential of S. haematobium locally due to the expanded intermediate host range, and that the presence of S. bovis complicates the environmental surveillance of schistosome infections.

Project description:BACKGROUND:Sound knowledge of the abundance and distribution of intermediate host snails is key to understanding schistosomiasis transmission and to inform effective interventions in endemic areas. METHODS:A longitudinal field survey of freshwater snails of biomedical importance was undertaken in the Niger River Valley (NRV) between July 2011 and January 2016, targeting Bulinus spp. and Biomphalaria pfeifferi (intermediate hosts of Schistosoma spp.), and Radix natalensis (intermediate host of Fasciola spp.). Monthly snail collections were carried out in 92 sites, near 20 localities endemic for S. haematobium. All bulinids and Bi. pfeifferi were inspected for infection with Schistosoma spp., and R. natalensis for infection with Fasciola spp. RESULTS:Bulinus truncatus was the most abundant species found, followed by Bulinus forskalii, R. natalensis and Bi. pfeifferi. High abundance was associated with irrigation canals for all species with highest numbers of Bulinus spp. and R. natalensis. Seasonality in abundance was statistically significant in all species, with greater numbers associated with dry season months in the first half of the year. Both B. truncatus and R. natalensis showed a negative association with some wet season months, particularly August. Prevalences of Schistosoma spp. within snails across the entire study were as follows: Bi. pfeifferi: 3.45% (79/2290); B. truncatus: 0.8% (342/42,500); and B. forskalii: 0.2% (24/11,989). No R. natalensis (n?=?2530) were infected. Seasonality of infection was evident for B. truncatus, with highest proportions shedding in the middle of the dry season and lowest in the rainy season, and month being a significant predictor of infection. Bulinus spp. and Bi. pfeifferi showed a significant correlation of snail abundance with the number of snails shedding. In B. truncatus, both prevalence of Schistosoma spp. infection, and abundance of shedding snails were significantly higher in pond habitats than in irrigation canals. CONCLUSIONS:Evidence of seasonality in both overall snail abundance and infection with Schistosoma spp. in B. truncatus, the main intermediate host in the region, has significant implications for monitoring and interrupting transmission of Schistosoma spp. in the NRV. Monthly longitudinal surveys, representing intensive sampling effort have provided the resolution needed to ascertain both temporal and spatial trends in this study. These data can inform planning of interventions and treatment within the region.

Project description:BACKGROUND:The Lake Victoria basin is one of the most persistent hotspots of schistosomiasis in Africa, the intestinal form of the disease being studied more often than the urogenital form. Most schistosomiasis studies have been directed to Schistosoma mansoni and their corresponding intermediate snail hosts of the genus Biomphalaria, while neglecting S. haematobium and their intermediate snail hosts of the genus Bulinus. In the present study, we used DNA sequences from part of the cytochrome c oxidase subunit 1 (cox1) gene and the internal transcribed spacer 2 (ITS2) region to investigate Bulinus populations obtained from a longitudinal survey in Lake Victoria and neighbouring systems during 2010-2019. METHODS:Sequences were obtained to (i) determine specimen identities, diversity and phylogenetic positions, (ii) reconstruct phylogeographical affinities, and (iii) determine the population structure to discuss the results and their implications for the transmission and epidemiology of urogenital schistosomiasis in Lake Victoria. RESULTS:Phylogenies, species delimitation methods (SDMs) and statistical parsimony networks revealed the presence of two main groups of Bulinus species occurring in Lake Victoria; B. truncatus/B. tropicus complex with three species (B. truncatus, B. tropicus and Bulinus sp. 1), dominating the lake proper, and a B. africanus group, prevalent in banks and marshes. Although a total of 47 cox1 haplotypes, were detected within and outside Lake Victoria, there was limited haplotype sharing (only Haplotype 6 was shared between populations from Lake Victoria open waters and neighbouring aquatic systems) - an indication that haplotypes are specific to habitats. CONCLUSIONS:The Bulinus fauna of Lake Victoria consists of at least B. truncatus, B. tropicus, Bulinus sp. 1 (B. trigonus?) and B. ugandae. The occurrence and wide distribution of Bulinus species in Lake Victoria potentially implies the occurrence of urogenital schistosomiasis in communities living along the shores and on islands of the lake who depend solely on the lake for their livelihood. More in-depth studies are needed to obtain a better picture of the extent of the disease in the Lake Victoria basin.

Project description:BackgroundTemperature is an important factor that influences the biology and ecology of intermediate host (IH) snails and the schistosome parasites they transmit. Although temperature shifts due to climate change has been predicted to affect the life history traits of IH snails and parasite production, the mechanisms of how this may affect parasite abundance and disease risks are still not clear.Materials and methodsUsing data from laboratory and field experiments, we developed a deterministic compartmental simulation model based on difference equations using a weekly time step that represented the life cycle of Bulinus globosus. We simulated snail population dynamics and the associated production of cercariae assuming current environmental temperatures as well as projected temperature increases of 1 °C and 2 °C.ResultsThe model generated snail fecundity and survival rates similar to those observed in the laboratory and also produced reasonable snail population dynamics under seasonally varying temperatures representative of generally favorable environmental conditions. Simulated relative abundances of both snails and cercariae decreased with increasing environmental temperatures, with maximum snail abundances decreased by 14% and 27%, and maximum cercariae productions decreased by 8% and 17%, when temperatures were increased by 1 °C and 2 °C, respectively.ConclusionThe results indicate that future rise in temperature due to climate change may alter the abundance of B. globosus and impact on the prevalence of schistosomiasis. Furthermore, increased temperatures may not linearly influence the abundance of S. haematobium. These results may have important implications for schistosomiasis control programmes in view of temperature driven changes in the life history traits of B. globosus and S. haematobium. Our study recommends that the use of deterministic models incorporating the effects of temperature on the life history traits of IH snails would be vital in understanding the potential impact of climate change on schistosomiasis incidences and prevalence.

Project description:Only a fraction of the Biomphalaria and Bulinus snail community shows patent infection with schistosomes despite continuous exposure to the parasite, indicating that a substantial proportion of snails may resist infection. Accordingly, exterminating the schistosome intermediate snail hosts in transmission foci in habitats that may extend to kilometres is cost-prohibitive and damaging to the ecological equilibrium and quality of water and may be superfluous. It may be more cost effective with risk less ecological damage to focus on discovering the parameters governing snail susceptibility and resistance to schistosome infection. Therefore, laboratory bred Biomphalaria alexandrina and Bulinus truncatus snails were exposed to miracidia of laboratory-maintained Schistosoma mansoni and S. haematobium, respectively. Snails were examined for presence or lack of infection association with soft tissue and hemolymph content of proteins, cholesterol, and triglycerides, evaluated using standard biochemical techniques and palmitic, oleic, linoleic, and arachidonic acid, assayed by ultraperformance liquid chromatography-tandem mass spectrometry. Successful schistosome infection of B. alexandrina and B. truncatus consistently and reproducibly correlated with snails showing highly significant (up to P < 0.0001) decrease in soft tissue and hemolymph content of the monounsaturated fatty acid, oleic acid, and the polyunsaturated fatty acids, linoleic, and arachidonic acids as compared to naïve snails. Snails that resisted twice infection had soft tissue content of oleic, linoleic, and arachidonic acid similar to naïve counterparts. High levels of soft tissue and hemolymph oleic, linoleic, and arachidonic acid content appear to interfere with schistosome development in snails. Diet manipulation directed to eliciting excessive increase of polyunsaturated fatty acids in snails may protect them from infection and interrupt disease transmission in a simple and effective manner.

Project description:BackgroundSchistosomiasis is caused by Schistosoma mansoni and S. haematobium in Africa. These schistosome parasites use freshwater snail intermediate hosts to complete their lifecycle. Varied prevalence rates of these parasites in the snail intermediate hosts were reported from several African countries, but there were no summarized data for policymakers. Therefore, this study was aimed to systematically summarize the prevalence and geographical distribution of S. mansoni and S. haematobium among freshwater snails in Africa.MethodsLiterature search was carried out from PubMed, Science Direct, and Scopus which reported the prevalence of S. mansoni and S. haematobium among freshwater snails in Africa. The pooled prevalence was determined using a random-effect model, while heterogeneities between studies were evaluated by I 2 test. The meta-analyses were conducted using Stata software, metan command.ResultsA total of 273,643 snails were examined for the presence of S. mansoni and S. haematobium cercaria in the eligible studies. The pooled prevalence of schistosome cercaria among freshwater snails was 5.5% (95% CI: 4.9-6.1%). The pooled prevalence of S. mansoni and S. haematobium cercaria was 5.6% (95% CI: 4.9-6.3%) and 5.2% (95% CI: 4.6-5.7%), respectively. The highest pooled prevalence was observed from Nigeria (19.0%; 95% CI: 12.7-25.3%), while the lowest prevalence was reported from Chad (0.05%; 95% CI: 0.03-0.13). Higher prevalence of schistosome cercaria was observed from Bulinus globosus (12.3%; 95% CI: 6.2-18.3%) followed by Biomphalaria sudanica (6.7%; 95% CI: 4.5-9.0%) and Biomphalaria pfeifferi (5.1%; 95% CI: 4.1-6.2%). The pooled prevalence of schistosome cercaria obtained using PCR was 26.7% in contrast to 4.5% obtained by shedding cercariae.ConclusionThis study revealed that nearly 6% of freshwater snails in Africa were infected by either S. haematobium or S. mansoni. The high prevalence of schistosomes among freshwater snails highlights the importance of appropriate snail control strategies in Africa.

Dataset Information

Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley.

Publications

Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley.

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