Spatial heterogeneity, host movement and mosquito-borne disease transmission.

Miguel A Acevedo,Maia Martcheva,Craig W Osenberg,Kenneth Lopiano,Nick Ruktanonchai,Olivia Prosper,T Trevor Caughlin,David L Smith,James M Mccaw

doi:10.1371/journal.pone.0127552

Abstract

Mosquito-borne diseases are a global health priority disproportionately affecting low-income populations in tropical and sub-tropical countries. These pathogens live in mosquitoes and hosts that interact in spatially heterogeneous environments where hosts move between regions of varying transmission intensity. Although there is increasing interest in the implications of spatial processes for mosquito-borne disease dynamics, most of our understanding derives from models that assume spatially homogeneous transmission. Spatial variation in contact rates can influence transmission and the risk of epidemics, yet the interaction between spatial heterogeneity and movement of hosts remains relatively unexplored. Here we explore, analytically and through numerical simulations, how human mobility connects spatially heterogeneous mosquito populations, thereby influencing disease persistence (determined by the basic reproduction number R 0), prevalence and their relationship. We show that, when local transmission rates are highly heterogeneous, R 0 declines asymptotically as human mobility increases, but infection prevalence peaks at low to intermediate rates of movement and decreases asymptotically after this peak. Movement can reduce heterogeneity in exposure to mosquito biting. As a result, if biting intensity is high but uneven, infection prevalence increases with mobility despite reductions in R 0. This increase in prevalence decreases with further increase in mobility because individuals do not spend enough time in high transmission patches, hence decreasing the number of new infections and overall prevalence. These results provide a better basis for understanding the interplay between spatial transmission heterogeneity and human mobility, and their combined influence on prevalence and R 0.

Highlights

More than half of the world’s population is infected with some kind of vector-borne pathogen [1,2,3], resulting in an enormous burden on human health, life, and economies [4]
We have explored the way that disease prevalence and R0 — two important measures of mosquito-borne pathogen transmission — display a complex non-monotonic relationship as a result of spatial heterogeneity in mosquito density and human mobility
We showed that prevalence was maximized at low rates of movement, whereas R0 always decreased with increasing movement rates. These results suggest that the relationship between R0 and prevalence is intimately intertwined with the interaction between host movement and the degree of spatial heterogeneity in a region

Summary

Introduction

More than half of the world’s population is infected with some kind of vector-borne pathogen [1,2,3], resulting in an enormous burden on human health, life, and economies [4]. Mathematical models continue to play an important role in the scientific understanding of vector-borne disease dynamics and informing decisions regarding control [10,11,12,13,14] and elimination [15,16,17], owing to their ability to summarize complex spatio-temporal dynamics. There is increasing interest in the implications of spatial processes for vector-borne disease dynamics [18,19,20,21,22], most models that describe these dynamics assume spatially homogeneous transmission, and do not incorporate host movement [23,24,25]. Understanding the interaction between connectivity—defined by the rate of movement of hosts among patches—and spatial heterogeneity in transmission via mathematical models has the potential to better inform control and eradication strategies of mosquito-borne diseases in real-world settings [37, 40]

Methods

Results

Conclusion