From superspreaders to disease hotspots: linking transmission across hosts and space

Abstract

Since the identification and imprisonment of "Typhoid Mary," a woman who infected at least 47 people with typhoid in the early 1900s, epidemiologists have recognized that 'superspreading' hosts play a key role in disease epidemics. Such variability in transmission also exists among species within a community (amplification hosts) and among habitat patches across a landscape (disease 'hotspots'), underscoring the need for an integrative framework for studying transmission heterogeneity. Here, we synthesize literature on human, plant, and animal diseases to evaluate the relative contributions of host, pathogen, and environmental factors in driving transmission heterogeneity across hosts and space. We show that host and spatial heterogeneity are closely linked and that quantitatively assessing the contribution of infectious individuals, species, or environmental patches to overall transmission can aid management strategies. We conclude by posing hypotheses regarding how pathogen natural history influences transmission heterogeneity and highlight emerging frontiers in the study of transmission heterogeneity.

Keywords: competent species; contact network; disease management; reservoir potential; transmission focus.

Figure 1

Aggregated distributions of factors influencing transmission potential across hosts and space. (a) A few yellow‐necked mouse (Apodemus flavicollis) individuals released most of the total eggs of the nematode Heligmosomoides polygyrus (modified with permission from Ferrari et al. 2004). (b) American robins (Turdus migratorius) infected a much greater percentage of mosquitoes with West Nile virus than did other bird species, and more than would be expected from their relative abundance (data from Kilpatrick et al. 2006). (c) A few ponds have very high percentages of snails infected with the trematode Ribeiroia ondatrae (Johnson unpublished data).

Figure 2

Conceptual diagram illustrating causes (purple boxes) and consequences (blue box) of transmission heterogeneity (green boxes), as well as connections across hosts and space (large blue arrows). Here, “contact rate” refers to contacts between either two host species or a host and vector; “dispersal” refers to the movement of a pathogen from one environmental patch to another; and “host community” refers to the density of hosts and their collective reservoir potential. Many of the consequences of, and linkages between, heterogeneity at multiple scales remain to be discovered (Panel 2).

Figure 3

Hypothetical contact network showing potential super‐spreaders (red circles) with higher than average connections to the rest of the network. The human, robin, and farm icons represent some of the possible identities of these potential super‐spreaders. Blue circles represent nodes (eg individuals, species, or locations) with lower than average connections (red lines) to the rest of the network.