Movement and sociodemographic predictors of zoonotic and human hookworm infection in rural Madagascar

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Abstract
Hookworms infect half a billion people worldwide, disproportionately impacting those living in poverty. Previous research has focused on sociodemographic predictors of infection, while less is known about how human land use influences infection. Moreover, recent molecular research has revealed that humans are frequently infected by multiple hookworm species that likely differ in their transmission patterns. In this study, we combined DNA metabarcoding of human and domesticated animal parasites with fine-scale GPS movement data to investigate how hookworm infection relates to people's land use and sociodemographic characteristics in three villages in rural Madagascar. We found high hookworm infection prevalence (52% in women and 69% in men; n = 881). Necator americanus predominated (53% prevalence), but the zoonotic hookworm Ancylostoma ceylanicum was also common (20% prevalence). Domesticated animals hosted several parasite species typically absent in humans. However, the zoonotic hookworm A. ceylanicum was highly prevalent in dogs (67-88% across villages). Consistent with previous findings, men had double the odds of Necator americanus infection than women, and prevalence was higher in those with lower material wealth (64% prevalence in the bottom quartile versus 47% prevalence in the top quartile). Zoonotic hookworm infections were more common in men than women (OR = 1.54), those with less formal education, and those reporting close contact with dogs (OR = 1.61). Regarding land use by people, we found that larger home ranges and greater use of vegetated areas outside villages was linked with increased N. americanus , but not A. ceylanicum, infection risk. Network analyses revealed that infected individuals were more strongly connected to each other than to uninfected individuals on networks of shared vegetated patches outside of the village. However, in one village with low levels of vegetation cover, we found significant spatial associations between people’s dwellings and human hookworm infections, illustrating the importance of ecological context for hookworm transmission. These findings underscore the importance of integrating fine-scale land use patterns with sociodemographic risk factors to better understand and mitigate human and zoonotic hookworm transmission.

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