Impact Of Environment, Host Microbiome, And Stress On Angiostrongylus Cantonensis (rat Lungworm) Transmission
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2023
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University of Hawaii at Manoa
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Abstract
Angiostrongylus cantonensis, commonly known as rat lungworm, is a nematode parasite widely distributed in tropical and subtropical regions, and is the causative agent of neuroangiostrongyliasis, a leading cause of eosinophilic meningitis globally. This parasite completes its life-cycle in various gastropod species (intermediate host) and rat species (definitive host). Humans are accidental hosts, becoming infected by ingesting infectious stage larvae, present in snails. Symptoms of neuroangiostrongyliasis can be severe, occasionally leading to death. Other mammals and birds also serve as accidental hosts. Although A. cantonensis was originally discovered in 1935, it wasn’t linked to human disease until 1961, when found in the brain of a deceased Hawaiʻi State Hospital patient. Since 1961, the parasite’s life-cycle and distribution have been discovered, but relatively little is known about A. cantonensis. Therefore, I developed three projects to explore the effects of the environment, stress, and host microbial communities on host-parasite dynamics and human transmission. The first project involved the collection of 16 snail species from 39 sites across Oʻahu, where A. cantonensis infection prevalence and intensity were determined using qPCR targeting the ITS1 region of DNA. Generalized linear mixed models (GLMMs) were constructed, incorporating environmental data to assess the influence of rainfall and temperature on these infection metrics. The analysis revealed higher infection prevalence and intensity in snails inhabiting wetter, cooler regions compared to snails in hotter, drier areas. In the second project, 196 snails (Parmarion martensi) were subjected to stress, leading to the release of infectious larvae in 13.3% of the stressed snails’ slime, while non-stressed snails did not release any larvae. Permutation tests and GLMMs demonstrated that stress significantly alters the parasite-host relationship, with snail infection intensity positively correlated with the presence of A. cantonensis larvae in their slime. These findings suggest that snail slime may serve as an alternative zoonotic transmission pathway. The third project involved a comparison of the effect of A. cantonensis infection on the microbial communities of snail guts (Parmarion martensi and Lissachatina fulica), rat feces and rat skin (Rattus rattus and R. norvegicus) using high-throughput sequencing of 16S ribosomal RNA. Analysis of microbial abundance with GLMMs revealed a significant interaction between infection status, host species, and individual bacteria. Shifts in individual bacterial abundances in response to A. cantonensis infection were most pronounced in the gut microbiota of infected snails, characterized by large log2FoldChange values. Changes in microbial abundance in rat feces were less pronounced, and relatively minor in rat skin. Notably, certain bacterial groups displayed remarkable increases in abundance in both taxa, suggesting potential protective symbiosis in response to A. cantonensis infection. Furthermore, differences in host susceptibility were observed to be associated with varying degrees of microbial disturbance. Parmarion martensi, a highly susceptible snail host, exhibited less microbial dysbiosis than L. fulica, a less susceptible host, suggesting the existence of unique adaptations and coadaptations in host-parasite interactions, potentially driven by the evolutionary history of the parasite and host. These projects contribute to the understanding of host-parasite relationships and provide valuable ecological insights for future research on A. cantonensis. The findings highlight the risk for human neuroangiostrongyliasis in different environments, the influence of stress in disease transmission, and the potential for microbial targets to be developed for therapeutic intervention and disease prevention. Furthermore, these discoveries have implications for ongoing efforts to mitigate human transmission and disease caused by A. cantonensis.
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Angiostrongylus cantonensis, Lungworms, Host-parasite relationships--Genetic aspects, Parasitic diseases--Transmission
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