Pathways to zoonotic spillover

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Abstract

Zoonotic diseases present a substantial global health burden. In this Opinion article, Plowright et al. present an integrative conceptual and quantitative model that reveals that all zoonotic pathogens must overcome a hierarchical series of barriers to cause spillover infections in humans.

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The online version of this article (doi:10.1038/nrmicro.2017.45) contains supplementary material, which is available to authorized users.

Abstract

Zoonotic spillover, which is the transmission of a pathogen from a vertebrate animal to a human, presents a global public health burden but is a poorly understood phenomenon. Zoonotic spillover requires several factors to align, including the ecological, epidemiological and behavioural determinants of pathogen exposure, and the within-human factors that affect susceptibility to infection. In this Opinion article, we propose a synthetic framework for animal-to-human transmission that integrates the relevant mechanisms. This framework reveals that all zoonotic pathogens must overcome a hierarchical series of barriers to cause spillover infections in humans. Understanding how these barriers are functionally and quantitatively linked, and how they interact in space and time, will substantially improve our ability to predict or prevent spillover events. This work provides a foundation for transdisciplinary investigation of spillover and synthetic theory on zoonotic transmission.

Supplementary information

The online version of this article (doi:10.1038/nrmicro.2017.45) contains supplementary material, which is available to authorized users.

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Author and article information

Contributors

Raina K. Plowright: raina.plowright@montana.edu

Bio :

Raina K. Plowright is Assistant Professor of Epidemiology at Montana State University, Bozeman, USA. She received her veterinary degree from the University of Sydney, Australia, and then travelled to the USA as an Australian Fulbright and Centennial Scholar to do her Ph.D. in ecology and M.Sc. in epidemiology at the University of California, Davis, USA. She was a David H. Smith Conservation Research Fellow at the Center for Infectious Disease Dynamics at Pennsylvania State University, USA. Her group at Montana State University studies pathogens that spill over from animals to people, the dynamics of zoonotic pathogens in wildlife populations, and pathogens that threaten wildlife conservation.

Colin R. Parrish:

Bio :

Colin R. Parrish is the John M. Olin Professor of Virology in the Baker Institute for Animal Health at the College of Veterinary Medicine, Cornell University, Ithaca, New York, USA. His research focuses on the study of viruses, virus structures and the evolution of new viral host ranges. His studies also examine the general basis of viral emergence, in particular the risk factors that are associated with the origins of new viruses in humans or other animals. For example, he studies canine parvovirus and canine influenza viruses emerging to cause epidemics in dogs.

Hamish McCallum:

Bio :

Hamish McCallum is a professor in the Griffith School of Environment and Environmental Futures Institute at Griffith University, Queensland, Australia. After his B.Sc. at Monash University, Melbourne, Victoria, Australia, he completed his Ph.D. under the supervision of Roy Anderson at Imperial College London, UK. His research primarily focuses on the ecology of infectious diseases in wildlife using quantitative approaches. The systems he works on include Tasmanian devil facial tumour disease, the amphibian chytrid fungus, Hendra virus in pteropid bats and chlamydial disease in koalas.

Peter J. Hudson:

Bio :

Peter J. Hudson is the Willaman Professor of Biology and Director of The Huck Institutes of Life Sciences at Pennsylvania State University, USA. He investigates the dynamics of infections in free-living animal populations, spillover between host species, and patterns of invasion and consequences for wildlife populations. He received his doctorate from the University of Oxford, UK, and he was elected a fellow of the Royal Society in 2008.

Albert I. Ko:

Bio :

Albert I. Ko is Professor of Epidemiology and Department Chair of Epidemiology of Microbial Diseases at the Yale School of Public Health, New Haven, Connecticut, USA. His research centres on the health problems that have emerged as a consequence of rapid urbanization and social inequity. He coordinates a research and training programme on urban slum health in Brazil and is conducting prospective community-based studies on rat-borne leptospirosis, dengue, meningitis and respiratory infections. More recently, his team has mobilized the public health research capacity at their site in the city of Salvador, Brazil to investigate the ongoing outbreak of Zika virus and resulting microcephaly.

Andrea L. Graham:

Bio :

Andrea L. Graham is Associate Professor of Ecology and Evolutionary Biology at Princeton University, New Jersey, USA. She earned her A.B. in biology and sculpture from Mount Holyoke College, South Hadley, Massachusetts, USA, and her Ph.D. in ecology and evolutionary biology from Cornell University, Ithaca, New York, USA, before completing her postdoctoral training at the University of Edinburgh, UK. She then held 2 independent research fellowships at Edinburgh and moved to Princeton University in 2011. Her research interests centre on the causes and consequences of immunological heterogeneity.

James O. Lloyd-Smith:

Bio :

James O. Lloyd-Smith is Professor in the Departments of Ecology and Evolutionary Biology, and Biomathematics at University of California, Los Angeles, USA. His research programme explores the ecological and evolutionary dynamics of infectious diseases in animal and human populations, with emphasis on the emergence of zoonotic pathogens and drug-resistant strains. His group combines mathematical models, statistical analysis, and laboratory, clinical and field studies to learn about diseases such as monkeypox, leptospirosis and influenza. He received his Ph.D. from the University of California, Berkeley, USA, where he studied heterogeneity in disease transmission dynamics, and he carried out his postdoctoral studies at Pennsylvania State University, USA.

Journal

Journal ID (nlm-ta): Nat Rev Microbiol

Journal ID (iso-abbrev): Nat. Rev. Microbiol

Title: Nature Reviews. Microbiology

Publisher: Nature Publishing Group UK (London )

ISSN (Print): 1740-1526

ISSN (Electronic): 1740-1534

Publication date (Electronic): 30 May 2017

Publication date (Print): 2017

Volume: 15

Issue: 8

Pages: 502-510

Affiliations

[1 ]GRID grid.41891.35, ISNI 0000 0001 2156 6108, Department of Microbiology and Immunology, , Montana State University, ; Bozeman, 59717 Montana USA

[2 ]GRID grid.5386.8, ISNI 000000041936877X, Colin R. Parrish is at the Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853, USA., ; ,

[3 ]GRID grid.1022.1, ISNI 0000 0004 0437 5432, Griffith School of Environment, Griffith University, ; Brisbane, 4111 Queensland Australia

[4 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Peter J. Hudson is at the Center for Infectious Disease Dynamics, Pennsylvania State University, State College, Pennsylvania 16802, USA., ; ,

[5 ]GRID grid.47100.32, ISNI 0000000419368710, Department of Epidemiology of Microbial Diseases, , Yale School of Public Health, ; New Haven, 06520–8034 Connecticut USA

[6 ]GRID grid.16750.35, ISNI 0000 0001 2097 5006, Department of Ecology & Evolutionary Biology, , Princeton University, Princeton, ; 08544 New Jersey USA

[7 ]GRID grid.19006.3e, ISNI 0000 0000 9632 6718, Department of Ecology & Evolutionary Biology, , University of California, Los Angeles, Los Angeles, California 90095-7239, USA, ; ,

[8 ]GRID grid.453035.4, ISNI 0000 0004 0533 8254, and at Fogarty International Center, National Institutes of Health, Bethesda, Maryland 20892–2220, USA., ; ,

Article

Publisher ID: BFnrmicro201745

DOI: 10.1038/nrmicro.2017.45

PMC ID: 5791534

PubMed ID: 28555073

SO-VID: 0ffaf675-7bd1-476b-936e-3bd314420dde

License:

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