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Hydrology and density feedbacks control the ecology of intermediate hosts of schistosomiasis across habitats in seasonal climates.

ABSTRACT: We report about field and theoretical studies on the ecology of the aquatic snails (Bulinus spp. and Biomphalaria pfeifferi) that serve as obligate intermediate hosts in the complex life cycle of the parasites causing human schistosomiasis. Snail abundance fosters disease transmission, and thus the dynamics of snail populations are critically important for schistosomiasis modeling and control. Here, we single out hydrological drivers and density dependence (or lack of it) of ecological growth rates of local snail populations by contrasting novel ecological and environmental data with various models of host demography. Specifically, we study various natural and man-made habitats across Burkina Faso's highly seasonal climatic zones. Demographic models are ranked through formal model comparison and structural risk minimization. The latter allows us to evaluate the suitability of population models while clarifying the relevant covariates that explain empirical observations of snail abundance under the actual climatic forcings experienced by the various field sites. Our results link quantitatively hydrological drivers to distinct population dynamics through specific density feedbacks, and show that statistical methods based on model averaging provide reliable snail abundance projections. The consistency of our ranking results suggests the use of ad hoc models of snail demography depending on habitat type (e.g., natural vs. man-made) and hydrological characteristics (e.g., ephemeral vs. permanent). Implications for risk mapping and space-time allocation of control measures in schistosomiasis-endemic contexts are discussed.

SUBMITTER: Perez-Saez J

PROVIDER: S-EPMC4988578 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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Hydrology and density feedbacks control the ecology of intermediate hosts of schistosomiasis across habitats in seasonal climates.

Perez-Saez Javier J Mande Theophile T Ceperley Natalie N Bertuzzo Enrico E Mari Lorenzo L Gatto Marino M Rinaldo Andrea A

Proceedings of the National Academy of Sciences of the United States of America 20160509 23

We report about field and theoretical studies on the ecology of the aquatic snails (Bulinus spp. and Biomphalaria pfeifferi) that serve as obligate intermediate hosts in the complex life cycle of the parasites causing human schistosomiasis. Snail abundance fosters disease transmission, and thus the dynamics of snail populations are critically important for schistosomiasis modeling and control. Here, we single out hydrological drivers and density dependence (or lack of it) of ecological growth ra ...[more]

PMID: 27162339

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Project description:BackgroundThe control of schistosomiasis is particularly difficult in sub-Saharan Africa, which currently harbours 95% of this disease. The target population for preventive chemotherapy (PC) is expanded to all age group at risk of infection, thus increasing the demands of praziquantel (PZQ) tablets according to the new released guideline by World Health Organization. Due to the gap between available PZQ for PC and requirements, alternative approaches to assess endemicity of schistosomiasis in a community, are urgently needed for more quick and precise methods. We aimed to find out to which degree the infection status of snails can be used to guide chemotherapy against schistosomiasis.MethodsWe searched literature published from January 1991 to December 2022, that reported on the prevalence rates of Schistosoma mansoni, S. haematobium in the intermediate snails Biomphalaria spp. and Bulinus spp., respectively, and in humans. A random effect model for meta-analyses was used to calculate the pooled prevalence estimate (PPE), with heterogeneity assessed using I-squared statistic (I2), with correlation and regression analysis for the exploration of the relationship between human S. mansoni and S. haematobium infections and that in their specific intermediate hosts.ResultsForty-seven publications comprising 59 field investigations were included. The pooled PPE of schistosomiasis, schistosomiasis mansoni and schistosomiasis haematobium in humans were 27.5% [95% confidence interval (CI): 24.0-31.1%], 25.6% (95% CI: 19.9-31.3%), and 28.8% (95% CI: 23.4-34.3%), respectively. The snails showed an overall infection rate of 8.6% (95% CI: 7.7-9.4%), with 12.1% (95% CI: 9.9-14.2%) in the Biomphalaria spp. snails and 6.9% (95% CI: 5.7-8.1%) in the Bulinus spp. snails. The correlation coefficient was 0.3 (95% CI: 0.01-0.5%, P < 0.05) indicating that the two variables, i.e. all intermediate host snails on the one hand and the human host on the other, were positively correlated.ConclusionsThe prevalence rate of S. mansoni and S. haematobium is still high in endemic areas. Given the significant, positive correlation between the prevalence of schistosomes in humans and the intermediate snail hosts, more attention should be paid to programme integration of snail surveillance in future.

Project description:BackgroundSchistosomiasis, also known as bilharzia, is the second important parasitic disease after malaria. The present study aimed to evaluate the molluscicidal effects of silver nanoparticles on Biomphalaria alexandrina, B. glabrata, Oncomelania hupensis, snail intermediate hosts of intestinal schistosomes (i.e. Schistosoma mansoni and S. japonicum), along with the changes their antioxidant enzymes.MethodsSilver (Ag) nano powder (Ag-NPs) was selected to test the molluscicidal effects on three species of freshwater snails. Exposure to Ag-NPs induced snail mortality and the LC50 and LC90 values of Ag-NPs for each snail species were calculated by probit analysis. Control snails were maintained under the same experimental conditions in dechlorinated water. Snail hemolymph was collected to measure the levels of antioxidant enzymes, such as total antioxidants capacity (TCA), glutathione (GSH), catalase (CAT) and nitric oxide (NO). In addition, the non-target organism, Daphnia magna, was exposed to a series of Ag-NPs concentration, similar to the group of experimental snails, in order to evaluate the LC50 and LC90 and compare these values to those obtained for the targeted snails.ResultsThe results indicated that Ag-NPs had a molluscicidal effect on tested snails with the variation in lethal concentration. The LC50 values of Ag-NPs for B. alexandrina snails exposed for 24, 48, 72 hrs and 7 days were 7.91, 5.69, 3.83 and 1.91 parts per million (ppm), respectively. The LC50 values for B. glabrata snails exposed for 24, 48, 72 hrs and 7 days were 16.55, 10.44, 6.91 and 4.13 ppm, respectively, while the LC50 values for O. hupensis snails exposed for 24, 48, 72 hrs and 7 days were 46.5, 29.85, 24.49 and 9.62 ppm, respectively. Moreover, there is no mortality detected on D. magna when exposed to more than double and half concentration (50 ppm) of Ag-NPs during a continuous period of 3 hrs, whereas the LC90 value for B. alexandrina snails was 18 ppm. The molluscicidal effect of the synthesized Ag-NPs seems to be linked to a potential reduction of the antioxidant activity in the snail's hemolymph.ConclusionsSynthesized Ag-NPs have a clear molluscicidal effect against various snail intermediate hosts of intestinal schistosome parasites and could potentially serve as next generation molluscicides.

Project description:BackgroundThe 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.MethodsSequences 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.ResultsPhylogenies, 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.ConclusionsThe 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:BackgroundDespite their importance for designing and evaluating schistosomiasis control trials, little attention in the literature has been dedicated to sampling protocols for the parasite's snail intermediate hosts since their first development. We propose a comparative analysis of time-based and quadrat sampling protocols to quantify the seasonal variations in the abundance of these aquatic snail species of medical importance.Methodology/principal findingsSnail populations were monitored during 42 consecutive months in three types of habitats (ephemeral pond, ephemeral river and permanent stream) in two sites covering different climatic zones in Burkina Faso. We employed both a widely used time-based protocol of 30min of systematic collection at a weekly interval, and a quadrat protocol of 8 replicates per sample at a monthly interval. The correspondence between the two protocols was evaluated using an ensemble of statistical models including linear and saturating-type functional forms as well as allowing for count zero-inflation. The quadrat protocol yielded on average a relative standard error of 40%, for a mean snail density of 16.7 snails/m2 and index of dispersion of 1.51. Both protocols yielded similar seasonal patterns in snail abundance, confirming the asynchrony between permanent and ephemeral habitats with respect to the country's seasonal rainfall patterns. Formal model comparison of the link between time vs. quadrat counts showed strong support of saturation for the latter and measurement zero-inflation, providing important evidence for the presence of density feedbacks in the snail's population dynamics, as well as for spatial clustering.Conclusions/significanceIn addition to the agreement with the time-based method, quadrat sampling provided insight into snail population dynamics and comparable density estimates across sites. The re-evaluation of these "traditional" sampling protocols, as well as the correspondence between their outputs, is of practical importance for the design and evaluation of schistosomiasis control trials.

Project description:The metabolic diversity present in microbial communities enables cooperation toward accomplishing more complex tasks than possible by a single organism. Members of a consortium communicate by exchanging metabolites or signals that allow them to coordinate their activity through division of labor. In contrast with monocultures, evidence suggests that microbial consortia self-organize to form spatial patterns, such as observed in biofilms or in soil aggregates, that enable them to respond to gradient, to improve resource interception and to exchange metabolites more effectively. Current biotechnological applications of microorganisms remain rudimentary, often relying on genetically engineered monocultures (e.g., pharmaceuticals) or mixed-cultures of partially known composition (e.g., wastewater treatment), yet the vast potential of "microbial ecological power" observed in most natural environments, remains largely underused. In line with the Unified Microbiome Initiative (UMI) which aims to "discover and advance tools to understand and harness the capabilities of Earth's microbial ecosystems," we propose in this concept paper to capitalize on ecological insights into the spatial and modular design of interlinked microbial consortia that would overcome limitations of natural systems and attempt to optimize the functionality of the members and the performance of the engineered consortium. The topology of the spatial connections linking the various members and the regulated fluxes of media between those modules, while representing a major engineering challenge, would allow the microbial species to interact. The modularity of such spatially linked microbial consortia (SLMC) could facilitate the design of scalable bioprocesses that can be incorporated as parts of a larger biochemical network. By reducing the need for a compatible growth environment for all species simultaneously, SLMC will dramatically expand the range of possible combinations of microorganisms and their potential applications. We briefly review existing tools to engineer such assemblies and optimize potential benefits resulting from the collective activity of their members. Prospective microbial consortia and proposed spatial configurations will be illustrated and preliminary calculations highlighting the advantages of SLMC over co-cultures will be presented, followed by a discussion of challenges and opportunities for moving forward with some designs.

Project description:BackgroundOpisthorchis viverrini (Ov) is a complex-life-cycle trematode affecting 10 million people in SEA (Southeast Asia). Human infection occurs when infected cyprinid fish are consumed raw or undercooked. Ov requires three hosts and presents two free-living parasitic stages. As a consequence Ov transmission and infection in intermediate and human hosts are strongly mediated by environmental factors and understanding how environmental variability influences intermediate host abundance is critical. The objectives of this study were 1) to document water parameters, intermediate hosts abundance and infection spatio-temporal variation, 2) to assess their causal relationships and identify windows of transmission risk.Methodology/principal findingsFish and snails were collected monthly for one year at 12 sites in Lawa Lake, an Ov-endemic region of Khon Kaen Province in Northeast Thailand. Physicochemical water parameters [pH, temperature (Tp), dissolved oxygen (DO), Salinity, electrical conductivity (EC), total dissolved solid (TDS), nitrite nitrogen (NO2-N), lead (Pb), total coliform bacteria (TCB) and fecal coliform bacteria (FCB)] were measured. Multivariate analyses, linear models and kriging were used to characterize water parameter variation and its influence on host abundance and infection prevalence. We found that sampling sites could be grouped in three clusters and discriminated along a nitrogen-salinity gradient where higher levels in the lake's southern region predicted higher Bithynia relative abundance (P<0.05) and lower snail and fish species diversity (P<0.05). Highest Bithynia abundance occurred during rainy season (P<0.001), independently of site influence. Cyprinids were the most abundant fish family and higher cyprinid relative abundance was found in areas with higher Bithynia relative abundance (P<0.05). Ov infection in snails was anecdotal while Ov infection in fish was higher in the southern region (P<0.001) at sites showing high FCB.Conclusions/significanceOur results indicate that water contamination and waterways configuration can influence freshwater communities' assemblages possibly creating ideal conditions for sustained transmission. Sustainable control may require a better appreciation of the system's ecology with wise governance and development planning particularly in the current context of SEA agricultural intensification and landscape modification.

Dataset Information

Hydrology and density feedbacks control the ecology of intermediate hosts of schistosomiasis across habitats in seasonal climates.

Publications

Hydrology and density feedbacks control the ecology of intermediate hosts of schistosomiasis across habitats in seasonal climates.

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