Dataset Information

The impact of seasonality on the dynamics and control of Ascaris lumbricoides infections.

ABSTRACT: Intestinal nematode infections affect a huge proportion of the world's population. Increasingly these infections, particularly amongst the poorest communities, are controlled through mass drug treatment programs. Seasonal variations of climate and behaviour in these regions can be significant, but their impact on the dynamics of infection and implications for the effectiveness of any mass drug treatment program (a pulsed reduction in worm burden in hosts) is not clearly understood. Here the effect of seasonality on the dynamics of the soil-based helminth, Ascaris lumbricoides, is investigated using a reformulated version of the Anderson-May model for macro-parasitic infections. Explicit analytical expressions are obtained for the stable oscillatory solution over the annual cycle, which provides a means of relating times of peak numbers of eggs, larvae and mature worms to seasonal variations. Numerical and analytical techniques are then used to consider the impact of seasonality on the optimal timing of drug treatment. Our results show that there is a relatively large window for the timing of optimal treatment, and the impact of repeated annual mass drug treatments can be substantially improved if they are timed to coincide with the months when the number of eggs and larvae are at their lowest - minimising reinfection. In terms of a more measurable quantity, in our example this corresponds to the months when the seasonal temperature is highest. Multiple annual treatments at (or close to) the optimal time each year are predicted to achieve local elimination in the community, whereas treatment at other times has a more limited impact. A key finding is that even for pronounced seasonality, perturbations in mean worm burden, and hence seasonal variation in observed egg output, may be small, potentially explaining why seasonal effects have been overlooked. Taken together these results suggest that seasonality of soil-transmitted helminths requires further experimental, field and mathematical study if the impact for mass drug administration programs is to be exploited.

SUBMITTER: Cooper AJ

PROVIDER: S-EPMC6013298 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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The impact of seasonality on the dynamics and control of Ascaris lumbricoides infections.

Cooper A J AJ Hollingsworth T Déirdre TD

Journal of theoretical biology 20180522

Intestinal nematode infections affect a huge proportion of the world's population. Increasingly these infections, particularly amongst the poorest communities, are controlled through mass drug treatment programs. Seasonal variations of climate and behaviour in these regions can be significant, but their impact on the dynamics of infection and implications for the effectiveness of any mass drug treatment program (a pulsed reduction in worm burden in hosts) is not clearly understood. Here the effe ...[more]

PMID: 29800536

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Project description:BackgroundAscaris lumbricoides exhibits density-dependent egg production, a process which has a marked impact on both the transmission dynamics and the stability of the parasite population. Evidence suggests that the egg production of female Ascaris is also associated with the size of the worm. If worm size is mediated by density-dependent processes then the size of female worms may have a causal impact upon patterns of Ascaris egg production.ResultsWe analyse data collected from a cohort of human hosts, and demonstrate that the per host mean weight (a proxy for size) of female Ascaris is dependent on the number of infecting females (worm burden) following a pattern of initial facilitation followed by limitation. Applying a negative binomial (NB) generalized linear model (GLM) and a zero-inflated negative binomial (ZINB) model we confirm that the per host female mean weight is significantly associated with per host egg production. Despite these associations, the mean weight of female Ascaris has little causal impact on patterns of density-dependent egg output. The ZINB model is able to account for the disproportionately large number of zero egg counts within the data and is shown to be a consistently better fit than the NB model. The probability of observing a zero egg count is demonstrated as being negatively associated with both female worm burden and female mean weight.ConclusionThe mean weight of female Ascaris is statistically significantly associated with egg output, and follows a consistent pattern of facilitation preceding limitation with increasing female worm burden. Despite these relationships, incorporation of female Ascaris mean weight into models of egg output has little effect on patterns of density dependence. The ZINB model is a superior fit to the data than the NB model and provides additional information regarding the mechanisms that result in a zero egg count. The ZINB model is shown to be a useful tool for the analysis of individual-based egg output data.

Project description:BackgroundAscaris lumbricoides causes human ascariasis, the most prevalent helminth disease, infecting approximately 1 billion individuals globally. In 2019 the global disease burden was estimated to be 754,000 DALYs and resulted in 2090 deaths. In the absence of a vaccination strategy, treatment of ascariasis has relied on anthelminthic chemotherapy, but drug resistance is a concern. The propensity for reinfection is also a major challenge to disease control; female worms lay up to 200,000 eggs daily, which contaminate surrounding environments and remain viable for years, resulting in high transmission rates. Understanding the molecular mechanisms of reproductive processes, including control of egg production, spermatogenesis, oogenesis and embryogenesis, will drive the development of new drugs and/or vaccine targets for future ascariasis control.MethodsTranscriptome profiles of discrete reproductive and somatic tissue samples were generated from adult male and female worms using Illumina HiSeq with 2 × 150 bp paired-end sequencing. Male tissues included: testis germinal zone, testis part of vas deferens, seminal vesicle and somatic tissue. Female tissues included: ovary germinal zone, ovary part of the oviduct, uterus and somatic tissue. Differentially expressed genes (DEGs) were identified from the fragments per kilobases per million reads (FPKM) profiles. Hierarchical analysis was performed to identify tissue-specific genes. Furthermore, Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were employed to identify significant terms and pathways for the DEGs.ResultsDEGs involved in protein phosphorylation and adhesion molecules were indicated to play a crucial role in spermatogenesis and fertilization, respectively. Those genes associated with the G-protein-coupled receptor (GPCR) signaling pathway and small GTPase-mediated signal transduction pathway play an essential role in cytoskeleton organization during oogenesis. Additionally, DEGs associated with the SMA genes and TGF-β signaling pathway are crucial in adult female embryogenesis. Some genes associated with particular biological processes and pathways that were identified in this study have been linked to defects in germline development, embryogenesis and reproductive behavior. In the enriched KEGG pathway analysis, Hippo signaling, oxytocin signaling and tight junction pathways were identified to play a role in Ascaris male and female reproductive systems.ConclusionsThis study has provided comprehensive transcriptome profiles of discrete A. lumbricoides reproductive tissue samples, revealing the molecular basis of these functionally important tissues. The data generated from this study will provide fundamental knowledge on the reproductive biology of Ascaris and will inform future target identification for anti-ascariasis drugs and/or vaccines.

Dataset Information

The impact of seasonality on the dynamics and control of Ascaris lumbricoides infections.

Publications

The impact of seasonality on the dynamics and control of Ascaris lumbricoides infections.

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