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’.

Genetic diversity of primate strongylid nematodes: Do sympatric nonhuman primates and humans share their strongylid worms?

“…Understanding the epidemiology of multihost pathogens is considered a major challenge in infectious disease research (Bowden & Drake, 2013;Webster, Borlase, & Rudge, 2017;Woolhouse, Taylor, & Haydon, 2001). In recent decades the global and local impacts of multihost diseases, particularly emerging zoonotic diseases, on human health and economy have resulted in attempts to unravel transmission patterns among all host-species involved (Bird & Mazet, 2018;Morens & Fauci, 2013;Wang & Crameri, 2014).…”

Lost in transmission…?

“…Several authors highlighted recent advances, both in technologies that allow extensive data on the spatial and temporal dynamics of parasite genotypes to be generated, and in statistical techniques (e.g. hierarchical Bayesian modelling) that can allow deeper insight into transmission pathways and rates than previously possible [2,6,14]. In addition, there were suggestions that transmission might not always be as complicated as feared.…”

Quantifying direct and indirect contacts for the potential transmission of infection between species using a multilayer contact network

“…However, while this may be somewhat limiting, there are numerous other examples where such peaks in environmental transmission might occur from shared refuge use (Godfrey et al, 2009;Leu et al, 2010) through to resource patches such as watering holes (Paull et al, 2012;Barasona et al, 2014) or anthropogenic food sources (Becker et al, 2015). In addition, the importance of indirect transmission will depend on other aspects of the system, such as the ability of the pathogen to persist in the environment and the relative likelihood of transmission occurring via different routes (Webster et al, 2017). However, if this additional information is available then it could be incorporated into a multilayer network model of infection within multi-host systems.…”

“…Between-species transmission of infection in multi-host disease systems remains poorly understood, despite representing a potentially important opportunity for disease control (Plowright et al, 2017;Webster et al, 2017). The behaviours that might result in transmission of infections between species are often rare (Viana et al, 2014), with successful transfer and establishment of the pathogen in a new host being rarer still (Woolhouse et al, 2001).…”

“…This distinction can be particularly important when direct interactions among potential hosts are rare, which is likely to be the case for between-species transmission (Viana et al, 2014). Identifying the relative importance of direct and indirect transmission, and the behaviours involved, are therefore likely to be important prerequisites to the development of effective disease management strategies (Plowright et al, 2017;Webster et al, 2017).…”