Coupled Heterogeneities and Their Impact on Parasite Transmission and Control

Abstract

Most host-parasite systems exhibit remarkable heterogeneity in the contribution to transmission of certain individuals, locations, host infectious states, or parasite strains. While significant advancements have been made in the understanding of the impact of transmission heterogeneity in epidemic dynamics and parasite persistence and evolution, the knowledge base of the factors contributing to transmission heterogeneity is limited. We argue that research efforts should move beyond considering the impact of single sources of heterogeneity and account for complex couplings between conditions with potential synergistic impacts on parasite transmission. Using theoretical approaches and empirical evidence from various host-parasite systems, we investigate the ecological and epidemiological significance of couplings between heterogeneities and discuss their potential role in transmission dynamics and the impact of control.

Keywords: dengue; risk heterogeneity; superspreader; transmission heterogeneity; vector-borne pathogen; within-host dynamics.

Figure I. System properties responsible for dengue virus transmission

Colored boxes identify specific traits known to vary in space (yellow), time or among individual people (blue), mosquitoes (red), or viruses (green). Black bold text identify functional heterogeneities known to have a direct impact in virus pathogen transmission and propagation.

Figure I. Epidemiologic impact of coupling contact rates and infectiousness

(A) The proportion of the population assigned to each of four types (i.e., low-low, low-high, high-low, high-high) under different scenarios about coupling. (B) Effects of positive (blue), negative (red), or no (black) coupling on R₀ given different levels of heterogeneity in contact when sick and infectiousness. The extent of heterogeneity in contact and infectiousness are assumed to be equal under a given scenario (i.e., at a given point on the x-axis in (B)). The overall extent of heterogeneity—i.e., how low is low and how high is high—is increased from left to right on the x-axis in (B).

Figure 1. Coupled heterogeneities in dengue virus transmission

(A) The contribution of each individual in a population to dengue virus (DENV) transmission (expressed as the individual-level R₀, R_0,i, defined as the espected number of secondary infections produced by each individual in a fully susceptible population) may differ between endemic and epidemic settings due to the levels of virus circulation and the proportion of individuals that are immune to the circulating serotype(s). With endemic transmission, the distribution of R_0,i is significantly biased towards zero (due to the high proportion of immune individuals) whereas during epidemics a much larger proportion of the population contributes to transmission. Despite this difference, the expected distribution of R_0,i allows grouping the individual contribution of individuals to transmission as poor (blue box), intermediate (yellow box) and high (red box). (B) Multiple functional heterogeneities can lead to this uneven distribution of R_0,i. As an extreme example, individuals with high out of home mobility, high infectiousness to mosquitoes, and high mosquito attractiveness will infect more mosquitoes and contribute more to transmission compared to individuals in the low end of the spectrum for these characteristics. Such heterogeneities are not independent from each other. For instance, disease manifestations (severity of dengue infection) may be correlated with multiple conditions, positively (green lines) or negatively (orange lines). (C) Diagram outlining what is known about the correlation structure among various sources of heterogeneity in DENV transmission.