Globalization, Land Use, Global Warming, and the Invasion of West Nile Virus
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1 Globalization, Land Use, Global Warming, and the Invasion of West Nile Virus A. Marm Kilpatrick 1, Laura D. Kramer 2, Peter Daszak 3 1 Department of Ecology and Evolutionary Biology, University of California, Santa Cruz 2 Wadsworth Center, NY State Dept. Health 3 EcoHealth Alliance
2 Kilpatrick 2011 Science Evolution
3 Drivers of Emergence for Vector- Borne Pathogens Defining an EID: (8): e69951
4 Drivers of Emergence for Vector- Borne Pathogens Globalization Pathogen introduction Vector introduction Host introduction Land use change Agriculture and urbanization Community ecology and transmission dynamics Climate and climate change Evolution Pathogens, vectors, hosts
5 Kilpatrick 2011 Science The Invasion of West Nile virus
6 Are there fewer WNV cases in Latin America? Guatemala case study Mosquito Ent. Risk & chicken seroconversion similar to MD (2004); Coachel. Cty, CA (2004) Human incidence: 0.3-3/100K 2012 WNV Cases for Guatemala (15.5M): Dengue: 11,860 Also cross-protection? Kilpatrick 2011 Science (Morales-Betoulle, Komar, Kilpatrick et al 2013 AJTMH)
7 WNV: Lessons learned, Outstanding questions Lessons learned (to enable control): How do vector-borne diseases move between regions? Who are the important vectors and hosts? What are the disease dynamics of an invading vectorborne pathogen? What factors influence the intensity of epidemics? Outstanding questions: Will there be additional big years for WNV like 2002, 2003 and 2012?
8 WNV: Lessons learned, Outstanding questions Lessons learned (to enable control): How do vector-borne diseases move between regions? Who are the important vectors and hosts? What are the disease dynamics of an invading vectorborne pathogen? What factors influence the intensity of epidemics? Outstanding questions: Will there be additional big years for WNV like 2002, 2003 and 2012?
9 Pathways of introduction for a zoonotic vector-borne disease 1. Human 2. Wind transported mosquito 3. Human transported mosquito (boats, planes) 4. Human transported non-human host 5. Migratory host: Highest probability pathways for West Nile virus introduction Hawaii, Galapagos: Mosquitoes on airplanes (Kilpatrick et al 2004; 2006) Caribbean: Migratory birds (Douglas et al 2007)
10 WNV: Lessons learned, Outstanding questions Lessons learned (to enable control): How do vector-borne diseases move between regions? Who are the important vectors and hosts? Need to do vector control What are the disease dynamics of an invading vectorborne pathogen? What factors influence the intensity of epidemics? Outstanding questions: Will there be additional big years for WNV like 2002, 2003 and 2012?
11 Which mosquitoes will be the dominant vectors for an invading pathogen? >170 species of mosquitoes in North America What should we measure, and how should we determine the relative importance of each factor? Qualitative: + to ++++ (Turell et al 2002) Host preference Field isolations of virus Vector competence Quantitative approach: (Kilpatrick et al 2005)
12 Identifying the vector(s) of WNV Force of infection correlated with human cases 1-3 weeks in advance (Kilpatrick et al 2006 PLoS Biology; 2013 Am J Epid.) Density of infected mosquitoes feeding on: Birds (enzootic vector); Humans (bridge vector) FOI a i APC v a i = fraction of feedings on host i A = mosquito abundance P = mosquito infection prevalence C v = Partial vector competence; fraction of infected mosquitoes that transmit Kilpatrick et al 2005 EID
13 100 % of WNV transmission % of WNV transmission/foi Cx. erythrothorax Humans (Bridge) Transmission to birds Transmission to Human Birds (enzootic) Cx. pipiens Cx. restuans Cx. species Cx. tarsalis Colorado; Kilpatrick & Pape 2013 Am. J Epidem. 0.1% 0.2% 0.1% WNV Vectors: Just 1-2, not 60! Maryland, DC, Virginia Kilpatrick unpub. data Ae aegypti Ae. albopictus Ae. canadensis Ae. triseriatus Ae. vexans Cx. erraticus Cx. pipiens Cx. restuans Cx. salinarius Other Aedes Total Anopheles % of WNV transmission Bridge vector Enzootic vector New York Kilpatrick et al 2005 EID 0 Aedes vexans Coq. perturbans Cx. pipiens+ restuans Culex salinarius Culiseta melanura Ae. canadensis Ae. japonicus Ae. solicitans Ae. trivittatus
14 WNV: Lessons learned, Outstanding questions Lessons learned: How do vector-borne diseases move between regions? Who are the important vectors and hosts? Need for wildlife vaccination or culling or predicting hotspots, or predicting temporal variation What are the disease dynamics of an invading vectorborne pathogen? What factors influence the intensity of epidemics? Outstanding questions: Will there be additional big years for WNV like 2002, 2003 and 2012?
15
16 Which host(s) will be important for an invading pathogen? What should we measure, and how should we determine the relative importance of each factor? Assessments based on 1-2 factors: Abundance: H. sparrows (Komar et al 2001) Competence/infectiousness: H. sparrows, grackles, blue jays, crows (Komar et al 2003) Dead infected birds, seroprevalence: Crows, jays, house sparrows (Marfin et al 2001; Bernard et al 2001; Komar et al 2001) A Quantitative Approach
17 The contribution of a host to pathogen amplification General expression for a multi-host, multi-vector pathogen The contribution of each host species is: Kilpatrick 2011 Science
18 WNV Amplification (who is infecting the mosquitoes?) Host i amplification = a 2 i C i ( S i / N i ) / N i a i = fraction of Cx. pipiens bloodmeals from host i c i = competence of host i (viremia duration, magnitude) S i /N j = Fraction of host species i seronegative (=1 for HY birds) N i = Density of host i Note: this is a point estimate for a species contribution to R e Kilpatrick 2011 Science
19 Amplification Potential (fraction of WNV-infectious mosquitoes) 100% 80% 60% 40% 20% 0% DC, Maryland; Kilpatrick et al 2006; In Review Baltimore Foggy Bottom Bethesda Takoma Park Reservoir Hosts: Just a few, not 100s A. robin E. starling R. pigeon M. dove G. catbird N. mockingbird H. sparrow Crows S. sparrow N. cardinal Finches Wrens Other birds Colorado; Kent et al 2009 JME 100% Contribution to amplification 80% 60% 40% 20% 0% June July August Chicago, Illinois Hamer et al 2009 AJTMH Raptor Passerines House sparrows A. robin Doves
20 Our Job: Distilling Complexity WNV is transmitted among birds and from birds to humans primarily by a single vector One or at most a few (3-5) hosts are responsible for infecting 75-95% of mosquitoes
21 The wildcard: Pathogen Evolution Following Introduction
22 Evolution: Adaptation to vectors Culex pipiens mosquitoes Kilpatrick et al 2008 PLoS Pathogens
23 A What factors influence spatial variation in WNV transmission?
24 Drivers of spatial variation in WNV Land use Agriculture (Bowden et al 2011 AJMTH; Crowder et al 2013 PLoS One) Urbanization (Bowden et al 2011 AJMTH; Andreadis et al 2004 VBZD; Gomez et al 2008 EID; Bradley et al 2008) What are the mechanism(s) for these patterns?
25 Overall Conclusions Despite potential complexity, actually relatively tractable with rigorous research Few important mosquitoes Few important hosts Future epidemics are actually predictable in some locations Uncertainties to watch out for Evolution of pathogen, vector, hosts Changes in human behavior
26 Acknowledgements Collaborators Peter Marra, Smithsonian Graduate students, Post Docs, Field and Lab Technicians Matt Jones, NYSDOH Ryan Peters, UCSC/George Mason Heidi Brightman, Jessica Norton, Scott Laeser, Alex Arp, and 27 others Neighborhood Nestwatch residents: Mutryns, Goughs, Marras, Hunters, & Browns Funding: NSF, NIH, NIAID
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