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Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts.

ABSTRACT: Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Increased prevalence and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife and a projected 2- to 5-fold increase in global agrochemical use by 2050. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat and decreasing densities of snail predators. Epidemiological models indicate that these agrochemical effects can increase transmission of schistosomes. Identifying agricultural practices or agrochemicals that minimize disease risk will be critical to meeting growing food demands while improving human wellbeing.

SUBMITTER: Halstead NT

PROVIDER: S-EPMC5826950 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts.

Halstead Neal T NT Hoover Christopher M CM Arakala Arathi A Civitello David J DJ De Leo Giulio A GA Gambhir Manoj M Johnson Steve A SA Jouanard Nicolas N Loerns Kristin A KA McMahon Taegan A TA Ndione Raphael A RA Nguyen Karena K Raffel Thomas R TR Remais Justin V JV Riveau Gilles G Sokolow Susanne H SH Rohr Jason R JR

Nature communications 20180226 1

Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Increased prevalence and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife a ...[more]

PMID: 29483531

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Project description:BACKGROUND:Schistosomiasis is responsible for the second highest burden of disease among neglected tropical diseases globally, with over 90 percent of cases occurring in African regions where drugs to treat the disease are only sporadically available. Additionally, human re-infection after treatment can be a problem where there are high numbers of infected snails in the environment. Recent experiments indicate that aquatic factors, including plants, nutrients, or predators, can influence snail abundance and parasite production within infected snails, both components of human risk. This study investigated how snail host abundance and release of cercariae (the free swimming stage infective to humans) varies at water access sites in an endemic region in Senegal, a setting where human schistosomiasis prevalence is among the highest globally. METHODS/PRINCIPAL FINDINGS:We collected snail intermediate hosts at 15 random points stratified by three habitat types at 36 water access sites, and counted cercarial production by each snail after transfer to the laboratory on the same day. We found that aquatic vegetation was positively associated with per-capita cercarial release by snails, probably because macrophytes harbor periphyton resources that snails feed upon, and well-fed snails tend to produce more parasites. In contrast, the abundance of aquatic macroinvertebrate snail predators was negatively associated with per-capita cercarial release by snails, probably because of several potential sublethal effects on snails or snail infection, despite a positive association between snail predators and total snail numbers at a site, possibly due to shared habitat usage or prey tracking by the predators. Thus, complex bottom-up and top-down ecological effects in this region plausibly influence the snail shedding rate and thus, total local density of schistosome cercariae. CONCLUSIONS/SIGNIFICANCE:Our study suggests that aquatic macrophytes and snail predators can influence per-capita cercarial production and total abundance of snails. Thus, snail control efforts might benefit by targeting specific snail habitats where parasite production is greatest. In conclusion, a better understanding of top-down and bottom-up ecological factors that regulate densities of cercarial release by snails, rather than solely snail densities or snail infection prevalence, might facilitate improved schistosomiasis control.

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:BackgroundSchistosomiasis is a chronic parasitic disease, that affects over 207 million people and causes over 200,000 deaths annually, mainly in sub-Saharan Africa. Although many health measures have been carried out to limit parasite transmission, significant numbers of non-human primates such as Chlorocebus aethiops (Ch. aethiops) (vervet) and Papio anubis (baboon) are infected with S. mansoni, notably in Ethiopia, where they are expected to have potentially significant implications for transmission and control efforts.ObjectiveThe objective of this study was to assess and compare the genetic diversity and population structure of S. mansoni isolates from human and non-human primates free-ranging in close proximity to villages in selected endemic areas of Ethiopia.MethodsA cross-sectional study was conducted in three transmission sites: Bochesa, Kime and Fincha. A total of 2,356 S. mansoni miracidia were directly isolated from fecal specimens of 104 hosts (i.e. 60 human hosts and 44 non-human primates). We performed DNA extraction and PCR amplification using fourteen microsatellite loci.ResultsAt population scale we showed strong genetic structure between the three sample sites. At the definitive host scale, we observed that host factors can shape the genetic composition of parasite infra-populations. First, in male patients, we observed a positive link between parasite genetic diversity and the age of the patients. Second, we observed a difference in genetic diversity which was high in human males, medium in human females and low in non-human primates (NHPs). Finally, whatever the transmission site no genetic structure was observed between human and non-human primates, however, there appears to be little barriers, if any, host specificity of the S. mansoni populations with cross-host infections.ConclusionOccurrence of infection of a single host with multiple S. mansoni strains and inter- and intra-host genetic variations was observed. Substantial genetic diversity and gene flow across the S. mansoni population occurred at each site and non-human primates likely play a role in local transmission and maintenance of infection. Therefore, public health and wildlife professionals should work together to improve disease control and elimination strategies.

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.

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Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts.

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Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts.

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