Date Published: June 19, 2014
Publisher: Public Library of Science
Author(s): Christian Gortazar, Leslie A. Reperant, Thijs Kuiken, José de la Fuente, Mariana Boadella, Beatriz Martínez-Lopez, Francisco Ruiz-Fons, Agustin Estrada-Peña, Christian Drosten, Graham Medley, Richard Ostfeld, Townsend Peterson, Kurt C. VerCauteren, Christian Menge, Marc Artois, Constance Schultsz, Richard Delahay, Jordi Serra-Cobo, Robert Poulin, Frederic Keck, Alonso A. Aguirre, Heikki Henttonen, Andrew P. Dobson, Susan Kutz, Juan Lubroth, Atle Mysterud, Vincent Racaniello.
The number of pathogens known to infect humans is ever increasing. Whether such increase reflects improved surveillance and detection or actual emergence of novel pathogens is unclear. Nonetheless, infectious diseases are the second leading cause of human mortality and disability-adjusted life years lost worldwide , . On average, three to four new pathogen species are detected in the human population every year . Most of these emerging pathogens originate from nonhuman animal species.
The suitability of any species to act as a host to a particular pathogen varies due to both host species– and pathogen-dependent factors, which define the species barriers. The species barriers separating nonhuman animal species from humans and thus of concern for zoonotic pathogens are the focus of this paper. However, the proposed conceptual framework is applicable to any host-pathogen system.
The emergence of zoonotic pathogens in humans is dependent on interactions between humans and infected animal reservoir and/or vector hosts or their environment (Figure 1, center). The extent of such interactions is influenced by the prevalence of zoonotic pathogens in the animal reservoir or vector populations, which is in turn influenced by these populations’ health and immune status. In addition, the population dynamics of humans, animal reservoirs, and vectors drive ecological processes that govern pathogen abundance and spread, both within and among species . Increased exposure of humans to animal pathogens can result from changes in the dynamics of any of these populations (Figure 1, inner circle). These changes can be divided into three categories: first, increased interspecies contact between humans and the animal reservoir and/or vector; second, population growth or aggregation of humans, animal reservoir, and/or vector; and third, their geographic range expansion, at least where this expansion involves overlapping ranges. Changes in one aspect of human, animal reservoir, or vector population dynamics may affect another; for example, population growth may accompany range expansion.
The proposed framework helps identify essential gaps in our understanding of the chain of emergence of zoonotic pathogens in humans and, in particular, of ecological processes underlying crossing of the interspecies barrier. Major gaps include characterization of the relationships between environmental conditions, especially climate and weather, and host and/or vector population dynamics, as well as exploration of pathogen survival and propagation in the environment. Recent studies have aimed at addressing such issues using novel approaches  and are essential in order to detect and predict associations between drivers such as climate change or weather variability and pathogen emergence , . The current focus in ecology addresses primarily single host-pathogen systems and needs to be expanded to a multihost, multipathogen perspective. Interactions between host, vector, and pathogenic and nonpathogenic infectious agents likely play important roles in the dynamics of zoonotic pathogens at the human-animal interface . Lastly, systematic assessment of actual human exposure to zoonotic pathogens, e.g., by serology, is lacking, calling for a more holistic approach to understanding the complete chain of emergence. Most evidence for the role of anthropogenic changes, e.g., encroachment into natural habitats, on zoonotic pathogen emergence is anecdotal or indirect and generally biased towards developed countries.
The identification of a limited number of mutually exclusive drivers of zoonotic pathogen emergence and of current knowledge gaps is essential to improve risk assessment and prevention measures. The links between pathogen emergence in humans and their underlying factors are typically speculative and associative and usually only account for a short section of the chain of emergence. Overall, knowledge of causal relationships between changes in population dynamics or interspecies contact, on the one hand, and pathogen emergence in humans, on the other, is fragmentary and incomplete at best. Existing studies in this area generally are limited in scope and typically lack quantitative assessment of human exposure to zoonotic pathogens at the human-animal interface.