Heterogeneity in Mosquito Biting Patterns: Epidemiological Consequences and Relevance for Malaria Control

Abstract

Malaria is a threat to global health and wellbeing and control remains a significant epidemiological challenge. The biting patterns of anopheline mosquitoes, which transmit falciparum malaria, are influenced by a variety of environmental, population dynamic, and behavioral factors. As a result, human exposure to malaria is significantly heterogeneous between individuals and over time. Heterogeneity in exposure increases disease persistence and amplifies transmission because those individuals most likely to be infected by infectious mosquitoes are also most likely to infect uninfected mosquitoes. Knowledge of the nature of heterogeneous transmission is essential to reducing or eliminating the global malaria burden.

Mosquito biting patterns are explored using mosquito catch data from three communities in Uganda between October 2011 and March 2013. Heterogeneity in exposure, as measured by the Pareto index, the coefficient of variation, and the dispersion parameter, k, decreases with mean biting intensity. Biting patterns are well described by a power law with a gradient greater than one, suggesting significant over-dispersion in the distribution of bites. Significant associations between seasonal and environmental variables and heterogeneity are also observed, but these may be confounded by seasonal and environmental differences in mean biting intensity.

The relevance of the observed mean-heterogeneity relationship to basic epidemiological parameters is explored. The force of infection saturates at high biting intensities, but not as quickly as predicted by models that assume constant levels of heterogeneity across the spectrum of biting intensity. Likewise, transmission efficiency declines less rapidly than fixed-heterogeneity models predict. The basic reproduction number increases with biting intensity and the coefficient of variation, and a global minimum value exists such that at certain points, decreases in mean biting intensity lead to increases in the basic reproduction number. As a result, elimination may be more difficult than originally thought and may require new control strategies. From these findings it is apparent that a precise understanding of the dynamics and drivers of heterogeneity are essential to successful malaria control.