Who acquires infection from whom and how? Disentangling multi-host and multi-mode transmission dynamics in the 'elimination' era

Abstract

Multi-host infectious agents challenge our abilities to understand, predict and manage disease dynamics. Within this, many infectious agents are also able to use, simultaneously or sequentially, multiple modes of transmission. Furthermore, the relative importance of different host species and modes can itself be dynamic, with potential for switches and shifts in host range and/or transmission mode in response to changing selective pressures, such as those imposed by disease control interventions. The epidemiology of such multi-host, multi-mode infectious agents thereby can involve a multi-faceted community of definitive and intermediate/secondary hosts or vectors, often together with infectious stages in the environment, all of which may represent potential targets, as well as specific challenges, particularly where disease elimination is proposed. Here, we explore, focusing on examples from both human and animal pathogen systems, why and how we should aim to disentangle and quantify the relative importance of multi-host multi-mode infectious agent transmission dynamics under contrasting conditions, and ultimately, how this can be used to help achieve efficient and effective disease control.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.

Keywords: control; dynamics; multi-host; multi-mode; pathogen; transmission.

Figure 1.

Classification of pathogens by life cycle complexity, number of hosts and number of transmission modes. (Online version in colour.)

Figure 2.

Multiplicity of pathogen transmission pathways and control opportunities. Examples include, infected infectious hosts can be targeted by: test and slaughter of livestock and domestic animals, e.g. FMDV, brucellosis; prophylactic drug treatment to reduce infectious stages transmission to environment, e.g. human MDA for Schistsosoma spp., or to offspring, e.g. targeted use of anti-retroviral drugs to reduce the likelihood of vertical transmission of HIV; human use of condoms to prevent sexually transmitted infections, e.g. syphilis, HIV. Indirect environmental and vector-borne transmission can be targeted by: improved health education and sanitation programmes to minimize environmental transmission, e.g. cholera, Guinea worm; improved burial practices to reduce the risk of transmission from people who have died due to, e.g. Ebola; vector and intermediate host control, e.g. malaria, schistosomiasis, dengue. Uninfected hosts can be targeted by: vaccination of uninfected humans to prevent human-to-human direct transmission, e.g. measles, or of livestock or domestic animals to prevent human transmission, e.g. domestic dogs to reduce human cases of rabies due to dog bites, or sheep and cattle to prevent brucellosis transmission to humans; health education.

Figure 3.

Schematics of simplified models for systems with multiple host species (a) and multiple transmission modes (b). Model compartments and parameters are defined in table 2. Block arrows represent the flow of individuals between compartments; dashed and dotted arrows represent transmission within and between species, respectively; line arrows show release and decay of indirectly transmitted infective stages. The model in (a) depicts a system with two host species, with the force of infection λ_i(t) in each host species i at time t defined as the sum of the forces of infection that can be attributed to transmission from each infected host species j. The model in (b) shows a single-host system with three modes of transmission, two of which are direct and one of which is indirect via a ‘pool’ of infective stages E, which could represent infective stages in the environment, a vector or an intermediate host. In this multi-mode system, the total force of infection is defined as the sum of the forces of infection that can be attributed to each transmission mode, k.