J E Childs J S Mackenzie J A Richt (Eds.) The Biology, Circumstances and Consequences of Cross-Species Transmission 315 Current Topics in Microbiology and Immunology Editors R.W Compans, Atlanta/Georgia M.D Cooper, Birmingham/Alabama T Honjo, Kyoto · H Koprowski, Philadelphia/Pennsylvania F Melchers, Basel · M.B.A Oldstone, La Jolla/California S Olsnes, Oslo · P.K Vogt, La Jolla/California James E Childs John S Mackenzie Jürgen A Richt (Eds.) Wildlife and Emerging Zoonotic Diseases: The Biology, Circumstances and Consequences of Cross-Species Transmission With 49 Figures and 21 Tables James E Childs, ScD Senior Research Scientist Department of Epidemiology and Public Health and Center for Eco-Epidemiology Yale University School of Medicine 60 College St., P.O Box 208034 New Haven, CT 06520-8034 USA e-mail: Jamesechilds@comcast.net John S Mackenzie, Ph.D Premier’s Fellow and Professor of Tropical Infectious Diseases, and Deputy CEO Australian Biosecurity Cooperative Research Centre for Emerging Infectious Diseases Curtin University of Technology GPO Box U1987 Perth, WA Australia 6845 e-mail: J.Mackenzie@curtin.edu.au Jürgen A Richt, DVM, Ph.D Veterinary Medical Officer, Lead Scientist Virus and Prion Diseases of Livestock Research Unit National Animal Disease Center USDA, ARS 2300 Dayton Ave Ames, IA 50010 USA e-mail: juergen.richt@ars.usda.gov Library of Congress Catalog Number 72-152360 ISSN 0070-217X ISBN 978-3-540-70961-9 Springer Berlin Heidelberg New York This work is subject to copyright All rights reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September, 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag Violations are liable for prosecution under the German Copyright Law Springer is a part of Springer Science+Business Media springeronline.com © Springer-Verlag Berlin Heidelberg 2007 The use of general descriptive names, registered names, trademarks, etc in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use Product liability: The publisher cannot guarantee the accuracy of any information about dosage and application contained in this book In every individual case the user must check such information by consulting the relevant literature Editor: Simon Rallison, Guildford Desk editor: Anne Clauss, Heidelberg Cover design: WMX Design, Heidelberg Typesetting and Production: SPi, India Printed on acid-free paper SPIN 11330721 27/3150/YL – List of Contents Introduction: Conceptualizing and Partitioning the Emergence Process of Zoonotic Viruses from Wildlife to Humans J E Childs, J A Richt and J S Mackenzie Infectious Disease Modeling and the Dynamics of Transmission L A Real and R Biek 33 The Evolutionary Genetics of Viral Emergence E C Holmes and A J Drummond 51 Influenza Viruses in Animal Wildlife Populations R J Webby, R G Webster and J A Richt 67 Overviews of Pathogen Emergence: Which Pathogens Emerge, When and Why? S Cleaveland, D T Haydon and L Taylor 85 Infection and Disease in Reservoir and Spillover Hosts: Determinants of Pathogen Emergence 113 P W Daniels, K Halpin, A Hyatt and D Middleton Henipaviruses: Emerging Paramyxoviruses Associated with Fruit Bats 133 H E Field, J S Mackenzie and P Daszak Emergence of Lyssaviruses in the Old World: The Case of Africa 161 L H Nel and C E Rupprecht Tuberculosis: A Reemerging Disease at the Interface of Domestic Animals and Wildlife 195 M V Palmer Emergence and Persistence of Hantaviruses 217 S L Klein and C H Calisher vi List of Contents Arenaviruses 253 J P Gonzalez, S Emonet, X de Lamballerie and R Charrel Ecological Havoc, the Rise of White-Tailed Deer, and the Emergence of Amblyomma americanum-Associated Zoonoses in the United States 289 C D Paddock and M J Yabsley Bats, Civets and the Emergence of SARS 325 L.-F Wang and B T Eaton Poxviruses and the Passive Quest for Novel Hosts 345 R L Regnery Ebolavirus and Other Filoviruses 363 J P Gonzalez, X Pourrut and E Leroy Pre-spillover Prevention of Emerging Zoonotic Diseases: What Are the Targets and What Are the Tools? 389 J E Childs Impediments to Wildlife Disease Surveillance, Research, and Diagnostics 445 D E Stallknecht Collaborative Research Approaches to the Role of Wildlife in Zoonotic Disease Emergence 463 P Daszak, J H Epstein, A M Kilpatrick, A A Aguirre, W B Karesh and A A Cunningham Surveillance and Response to Disease Emergence 477 Angela Merianos Index 511 List of Contributors (Addresses stated at the beginning of respective chapters) Aguirre, A.A 463 Angela Merianos 477 Biek, R Karesh, W.B 463 Kilpatrick, A.M 463 Klein, S.L 217 33 Leroy, E Calisher, C.H 217 Charrel, R 253 Childs, J.E 389 Cleaveland, S 85 Cunningham, A.A 463 Daniels, P.W 113 Daszak, P 133 de Lamballerie, X 253 Drummond, A.J 51 Eaton, B.T Emonet, S Epstein, J.H 325 253 463 Field, H.E 133 Gonzalez, J.-P 253 Halpin, K Haydon, D.T Holmes, E.C Hyatt, A 113 85 51 113 363 Mackenzie, J.S 1, 133 Middleton, D 113 Nel, L.H 161 Paddock, C.D 289 Palmer, M.V 195 Pourrut, X 363 Real, L.A 33 Regnery, R.L 345 Richt, J.A Rupprecht, C E 161 Stallknecht, D.E Taylor, L 85 Wang, L.-F Webby, R.J Webster, R.G 325 67 67 Yabsley, M.J 289 445 CTMI (2007) 315:1–31 © Springer-Verlag Berlin Heidelberg 2007 Introduction: Conceptualizing and Partitioning the Emergence Process of Zoonotic Viruses from Wildlife to Humans J E Childs1 · J A Richt2 · J S Mackenzie3(* ü) Department of Epidemiology and Public Health, Yale School of Medicine, 60 College St., P.O Box 208034 New Haven, CT 06520-8034, USA Veterinary Medical Officer, National Animal Disease Center, 2300 Dayton Ave, Ames, IA 50010, USA Premier’s Research Fellow, Australian Biosecurity CRC, Curtin University of Technology, GPO Box U1987 Perth, WA, Australia 6845 J.Mackenzie@curtin.edu.au 1.1 1.2 Introduction Cross-Species Transmission (Spillover) Pathogenesis in the Reservoir Host and Secondary Host The Comparative Ecology of Zoonosis Emergence and Species Invasion Four Transition Stages to Emergence: The First Two Are Prerequisite Two Transition Stages Are Required for Pandemic Emergence The Basic Reproductive Potential R0 as a Measure of Viral Relative Fitness 2.1 2.2 2.3 3.1 3.2 3.3 3.4 3 4 3.4.2 3.4.3 3.4.4 3.4.5 Modifying Factors in the Emergence Process Abiotic Factors in Emergence Evolutionary and Intrinsic Biotic Factors in Emergence Extrinsic Biotic Interactions in Emergence Anthropogenic Influences as a Special Class of Extrinsic Factors in Emergence Habitat Modification, Human Encroachment, and Modern Agricultural Practices Domestic Animals Provide a Bounty of Novel Niches Human Population Demographics and Urbanization The Miracle of Modern Transport The Miracle of Modern Medicine 4.1 4.2 Invasion Biology as a Paradigm for Disease Emergence 16 Termination Points and Pitfalls on the Route to Emergence or Invasion 16 Human Invaded or Human Invader? 17 3.4.1 8 10 10 11 11 12 13 13 5.1 5.2 5.3 5.4 J E Childs et al Qualities of Zoonotic Viruses Emerging by Different Transition Routes Emergence Via Reiterative Processes of Contact and Spillover Spillover Subsequently Sustained by Human-to-Human Transmission The Road to Human Adaptation: A Still-Life with SARS CoV? Adaptation of Zoonotic Viruses to the Human HR and Pandemic Emergence 18 18 18 20 21 References 22 Abstract This introduction provides a telegraphic overview of the processes of zoonotic viral emergence, the intricacies of host–virus interactions, and the distinct role of biological transitions and modifying factors The process of emergence is conceptualized as two transition stages which are common and required for all disease emergence, (1) human contact with the infectious agent and (2) cross-species transmission of the agent, and two transition stages which are not required for emergence and appear unavailable to many zoonotic pathogens, (3) sustained human-to-human transmission and (4) genetic adaptation to the human host The latter two transitions are presumably prerequisites for the pandemic emergence of a pathogen The themes introduced herein are amplified and explored in detail by the contributors to this volume Each author explores the mechanisms and unique circumstances by which evolution, biology, history, and current context have contrived to drive the emergence of different zoonotic agents by a series of related events; although recognizable similarities exist among the events leading to emergence the details and circumstances are never repetitive Introduction The process of zoonotic disease emergence can be understood by coupling knowledge of how zoonotic viruses have evolved and are maintained among their wildlife hosts, transmitted across a species barrier to cause productive infection in a taxonomically distinct secondary host, initiate a pathologic process causing disease, and, by repetitive infection within the secondary host species, result in incident morbidity or mortality of sufficient magnitude to be detected and characterized as a novel health concern of local, regional, or global significance (see the chapter by Childs, this volume) Obviously, we possess no such knowledge for any zoonotic virus or zoonotic disease, but casting the emergence process in this context underscores how disciplinary boundaries are blurred; advances require approaches spanning the spectrum of biological inquiry, and solutions to imminent threats require approaches unbounded by the notion of specific scientific discipline The emergence process involves ecological interactions at the individual, species, community, and global scale The dynamic circumstances and relative Introduction importance of the participants reflect the evolutionary context in which zoonotic agents have become accommodated to, and been accommodated by, their reservoir hosts (HRs) (see the chapters by Cleaveland et al and by Holmes and Drummond, this volume), the diversity of reservoir species involved, their geographic ranges and the local dispersion of host and pathogen populations In turn, historical factors have modified and blurred traditional patterns of species distribution, abundance, and diversity, and are continually transforming the landscape of opportunity on which zoonotic viruses with their HRs mingle with novel, potentially susceptible secondary host species (HS)s (see the chapters by Daszak et al., Field et al., Regnery, and Wang and Eaton, this volume) The current historical circumstances are unprecedented in their efficiency for continually shuffling an expanding repertoire of zoonotic viruses and hosts, introducing them in novel ecologic circumstances to a wealth of previously unavailable and unexplored niches Within the last decade, the accelerated pace of rapid translocations of infected HRs or HSs have heralded a sea change in how we view the public health threat posed by zoonotic viruses (Childs 2004), as testified by the emergence of SARs coronavirus (SARS CoV) (Drosten et al 2003; see the chapter by Wang and Eaton, this volume), influenza A subtype H5N1 (Peiris et al 2004; see chapter by Webby et al., this volume), West Nile virus (WNV) (Lanciotti et al 1999), Nipah virus (NiV) (Chua et al 1999; see the chapter by Field et al., this volume), and Monkeypox virus (Anderson et al 2003; see the chapter by Regnery, this volume) 1.1 Cross-Species Transmission (Spillover) Inherent in the term “cross-species transmission” (or spillover) is the ability for a foreign virus, once introduced into an individual of a H S population, to complete the virus infectious cycle: (1) adsorption, penetration, and uncoating, or separation of the viral nucleic acid from the capsid; (2) transcription, translation, and replication, and; (3) assembly and release (Nayak 2000) Binding and entry into permissive HS cells is mediated by common or related cellular receptors Additional bouts of infection following virus release from infected cells lead to the dissemination of virus throughout the host’s tissue(s), precipitating, as a byproduct, pathologic alterations in the individual HS identifiable as symptomatic disease 1.2 Pathogenesis in the Reservoir Host and Secondary Host The pathogenic course of infection and disease within the secondary host (HS) may bear little correspondence to the infectious process and outcome within the ... Mackenzie Jürgen A Richt (Eds.) Wildlife and Emerging Zoonotic Diseases: The Biology, Circumstances and Consequences of Cross-Species Transmission With 49 Figures and 21 Tables James E Childs,... overview of the processes of zoonotic viral emergence, the intricacies of host–virus interactions, and the distinct role of biological transitions and modifying factors The process of emergence... and P Daszak Emergence of Lyssaviruses in the Old World: The Case of Africa 161 L H Nel and C E Rupprecht Tuberculosis: A Reemerging Disease at the Interface of Domestic Animals and Wildlife