Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis.
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ABSTRACT:
SUBMITTER: Laidemitt MR
PROVIDER: S-EPMC6917487 | biostudies-literature | 2019 Dec
REPOSITORIES: biostudies-literature
Publications
Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis.
Laidemitt Martina R MR Anderson Larissa C LC Wearing Helen J HJ Mutuku Martin W MW Mkoji Gerald M GM Loker Eric S ES
eLife 20191217
Human disease agents exist within complex environments that have underappreciated effects on transmission, especially for parasites with multi-host life cycles. We examined the impact of multiple host and parasite species on transmission of the human parasite <i>Schistosoma mansoni</i> in Kenya. We show <i>S. mansoni</i> is impacted by cattle and wild vertebrates because of their role in supporting trematode parasites, the larvae of which have antagonistic interactions with <i>S. mansoni</i> in ...[more]
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Project description:Recently, the World Health Organization recognized that efforts to interrupt schistosomiasis transmission through mass drug administration have been ineffective in some regions; one of their new recommended strategies for global schistosomiasis control emphasizes targeting the freshwater snails that transmit schistosome parasites. We sought to identify robust indicators that would enable precision targeting of these snails. At the site of the world's largest recorded schistosomiasis epidemic-the Lower Senegal River Basin in Senegal-intensive sampling revealed positive relationships between intermediate host snails (abundance, density, and prevalence) and human urogenital schistosomiasis reinfection (prevalence and intensity in schoolchildren after drug administration). However, we also found that snail distributions were so patchy in space and time that obtaining useful data required effort that exceeds what is feasible in standard monitoring and control campaigns. Instead, we identified several environmental proxies that were more effective than snail variables for predicting human infection: the area covered by suitable snail habitat (i.e., floating, nonemergent vegetation), the percent cover by suitable snail habitat, and size of the water contact area. Unlike snail surveys, which require hundreds of person-hours per site to conduct, habitat coverage and site area can be quickly estimated with drone or satellite imagery. This, in turn, makes possible large-scale, high-resolution estimation of human urogenital schistosomiasis risk to support targeting of both mass drug administration and snail control efforts.
| S-EPMC6859407 | biostudies-literature
Project description:BackgroundSchistosomiasis is a neglected tropical disease endemic in 54 countries. A major Schistosoma species, Schistosoma mansoni, is sustained via a life cycle that includes both human and snail hosts. Mathematical models of S. mansoni transmission, used to elucidate the complexities of the transmission cycle and estimate the impact of intervention efforts, often focus primarily on the human host. However, S. mansoni incurs physiological costs in snails that vary with the age of the snail when first infected. Snail demography and the age of snail infection could thus affect the force of infection experienced by humans, which is frequently used to predict the impact of various control strategies.MethodsTo address how these snail host and parasite interactions influence model predictions, we developed deterministic models of schistosomiasis transmission that include varying complexity in the snail population age structure. Specifically, we examined how model outputs, such as schistosome prevalence in human and snail populations, respond to the inclusion of snail age structure.ResultsOur models suggest that snail population age structure modifies the force of infection experienced by humans and the relationship between snail infection prevalence and corresponding human infection prevalence. There are significant differences in estimated snail infection, cercarial density and mean worm burden between models without snail population dynamics and those with snail populations, and between models with a homogeneous snail population and those with age stratification. The variation between finely age-stratified snail populations and those grouped into only juvenile and adult life stages is, however, minimal.ConclusionsThese results indicate that including snails and snail age structure in a schistosomiasis transmission model alters the relationship between snail and human infection prevalence. This highlights the importance of accounting for a heterogeneous intermediate host population in models of schistosomiasis transmission where the impact of proposed control measures is being considered.
| S-EPMC7860629 | biostudies-literature
Project description:BackgroundCombating infectious diseases and halting biodiversity loss are intertwined challenges crucial to ensure global health. Biodiversity can constrain the spread of vector-borne pathogens circulation, necessitating a deeper understanding of ecological mechanisms underlying this pattern. Our study evaluates the relative importance of biodiversity and the abundance of Bulinus truncatus, a major intermediate host for the trematode Schistosoma haematobium on the circulation of this human pathogen at aquatic transmission sites.MethodsWe combined mathematical modelling and a molecular based empirical study to specifically assess the effect of co-infections between S. haematobium and other trematodes within their B. truncatus snail hosts; and B. truncatus abundance at transmission sites, on the production of S. haematobium infective cercariae stages released into the aquatic environment.ResultsOur modelling approach shows that more competitive trematode species exploiting B. truncatus as an intermediate host at the transmission site level leads to higher co-infection rates within snail hosts, subsequently reducing the production of S. haematobium cercariae. Conversely, an increase in B. truncatus abundance results in lower co-infection rates, and a higher proportion of S. haematobium cercariae released into the environment. Our empirical data from the field support these findings, indicating a significant negative effect of local trematode species richness (P-value = 0.029; AIC = 14.9) and co-infection rates (P-value = 0.02, AIC = 17.4) on the dominance of S. haematobium based on our GLMM models, while B. truncatus abundance positively influences S. haematobium dominance (P-value = 0.047, AIC = 20.1).ConclusionsOur study highlights the importance of biodiversity in influencing the transmission of S. haematobium through the effect of antagonistic interactions between trematodes within bulinid snail hosts. This effect intensifies when B. truncatus populations are low, promoting co-infections within snails. In line with the One Health concept, our results suggest that maintaining high level of freshwater biodiversity to sustain global trematode diversity at transmission sites can help reducing the circulation of Schistosoma species locally.
| S-EPMC11386086 | biostudies-literature
Project description:Effects of parasites on individual hosts can eventually translate to impacts on host communities. In particular, parasitism can differentially affect host fitness among sympatric and interacting host species. We examined whether the impact of shared parasites varied among host species within the same community. Specifically, we looked at the impacts of the acanthocephalan Acanthocephalus galaxii, the trematodes Coitocaecum parvum and Maritrema poulini, and the nematode Hedruris spinigera, on three host species: the amphipods, Paracalliope fluviatilis and Paracorophium excavatum, and the isopod, Austridotea annectens. We assessed parasite infection levels in the three host species and tested for effects on host survival, behavior, probability of pairing, and fecundity. Maritrema poulini and C. parvum were most abundant in P. excavatum but had no effect on its survival, whereas they negatively affected the survival of P. fluviatilis, the other amphipod. Female amphipods carrying young had higher M. poulini and C. parvum abundance than those without, yet the number of young carried was not linked to parasite abundance. Behavior of the isopod A. annectens was affected by M. poulini infection; more heavily infected individuals were more active. Paracorophium excavatum moved longer distances when abundance of C. parvum was lower, yet no relationship existed with respect to infection by both M. poulini and C. parvum. The differential effects of parasites on amphipods and isopods may lead to community-wide effects. Understanding the consequences of parasitic infection and differences among host species is key to gaining greater insight into the role of parasite mediation in ecosystem dynamics.
| S-EPMC5496554 | biostudies-other
Project description:Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.
| S-EPMC8833218 | biostudies-literature
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.
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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.
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Project description:Influenza viruses rapidly diversify within individual human infections. Several recent studies have deep-sequenced clinical influenza infections to identify viral variation within hosts, but it remains unclear how within-host mutations fare at the between-host scale. Here, we compare the genetic variation of H3N2 influenza within and between hosts to link viral evolutionary dynamics across scales. Synonymous sites evolve at similar rates at both scales, indicating that global evolution at these putatively neutral sites results from the accumulation of within-host variation. However, nonsynonymous mutations are depleted between hosts compared to within hosts, suggesting that selection purges many of the protein-altering changes that arise within hosts. The exception is at antigenic sites, where selection detectably favors nonsynonymous mutations at the global scale, but not within hosts. These results suggest that selection against deleterious mutations and selection for antigenic change are the main forces that act on within-host variants of influenza virus as they transmit and circulate between hosts.
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Project description:Eliminating human parasitic disease often requires interrupting complex transmission pathways. Even when drugs to treat people are available, disease control can be difficult if the parasite can persist in nonhuman hosts. Here, we show that restoration of a natural predator of a parasite's intermediate hosts may enhance drug-based schistosomiasis control. Our study site was the Senegal River Basin, where villagers suffered a massive outbreak and persistent epidemic after the 1986 completion of the Diama Dam. The dam blocked the annual migration of native river prawns (Macrobrachium vollenhoveni) that are voracious predators of the snail intermediate hosts for schistosomiasis. We tested schistosomiasis control by reintroduced river prawns in a before-after-control-impact field experiment that tracked parasitism in snails and people at two matched villages after prawns were stocked at one village's river access point. The abundance of infected snails was 80% lower at that village, presumably because prawn predation reduced the abundance and average life span of latently infected snails. As expected from a reduction in infected snails, human schistosomiasis prevalence was 18 ± 5% lower and egg burden was 50 ± 8% lower at the prawn-stocking village compared with the control village. In a mathematical model of the system, stocking prawns, coupled with infrequent mass drug treatment, eliminates schistosomiasis from high-transmission sites. We conclude that restoring river prawns could be a novel contribution to controlling, or eliminating, schistosomiasis.
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