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01-03-2019 | Original Contribution

Linking Bird and Mosquito Data to Assess Spatiotemporal West Nile Virus Risk in Humans

Authors: Benoit Talbot, Merlin Caron-Lévesque, Mark Ardis, Roman Kryuchkov, Manisha A. Kulkarni

Published in: EcoHealth | Issue 1/2019

Abstract

West Nile virus (WNV; family Flaviviridae) causes a disease in humans that may develop into a deadly neuroinvasive disease. In North America, several peridomestic bird species can develop sufficient viremia to infect blood-feeding mosquito vectors without succumbing to the virus. Mosquito species from the genus Culex, Aedes and Ochlerotatus display variable host preferences, ranging between birds and mammals, including humans, and may bridge transmission among avian hosts and contribute to spill-over transmission to humans. In this study, we aimed to test the effect of density of three mosquito species and two avian species on WNV mosquito infection rates and investigated the link between spatiotemporal clusters of high mosquito infection rates and clusters of human WNV cases. We based our study around the city of Ottawa, Canada, between the year 2007 and 2014. We found a large effect size of density of two mosquito species on mosquito infection rates. We also found spatiotemporal overlap between a cluster of high mosquito infection rates and a cluster of human WNV cases. Our study is innovative because it suggests a role of avian and mosquito densities on mosquito infection rates and, in turn, on hotspots of human WNV cases.

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Andreadis TG (2012) The contribution of Culex pipiens complex mosquitoes to transmission and persistence of West Nile Virus in North America. Journal of the American Mosquito Control Association 28:137–151. https://doi.org/10.2987/8756-971x-28.4s.137 CrossRefPubMed

Apperson CS, Hassan HK, Harrison BA, Savage HM, Aspen SE, Farajollahi A, Crans W, Daniels TJ, Falco RC, Benedict M, Anderson M, McMillen L, Unnasch TR (2004) Host feeding patterns of established and potential mosquito vectors of West Nile Virus in the eastern United States. Vector-Borne Zoonotic Diseases 4:71–82. https://doi.org/10.1089/153036604773083013 CrossRefPubMed

Artsob H, Lindsay R, Drebot M (2006) Biodiversity-related aspects of West Nile Virus and its cycle in nature. Biodiversity 7:18–23. https://doi.org/10.1080/14888386.2006.9712790 CrossRef

Barton K (2013) MuMIn: Multi-Model Inference. Krakow: Institute of Nature Conservation

Burkett-Cadena ND, Graham SP, Hassan HK, Guyer C, Eubanks MD, Katholi CR, Unnasch TR (2008) Blood feeding patterns of potential arbovirus vectors of the genus Culex targeting ectothermic hosts. American Society of Tropical Medicine and Hygiene 79:809–815CrossRef

Chancey C, Grinev A, Volkova E, Rios M (2015) The global ecology and epidemiology of West Nile Virus. BioMed Research International 2015:1–20. https://doi.org/10.1155/2015/376230 CrossRef

Chaves A, Sotomayor-Bonilla J, Monge O, Ramírez A, Galindo F, Sarmiento-Silva RE, Gutiérrez-Espeleta GA, Suzán G (2016) West Nile Virus in resident birds from Yucatan, Mexico. Journal of Wildlife Diseases 52:159–163. https://doi.org/10.7589/2015-02-046 CrossRefPubMed

Darsie R, Ward R (2005) Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico, 2nd ed., Gainsville: University Press of Florida

Diaz LA, Quaglia AI, Konigheim BS, Boris AS, Aguilar JJ, Komar N, Contigiani MS (2016) Activity patterns of St. Louis Encephalitis and West Nile Viruses in free ranging birds during a human encephalitis outbreak in Argentina. PLOS ONE 11:e0161871. https://doi.org/10.1371/journal.pone.0161871

Drebot MA, Lindsay R, Barker IK, Buck PA, Fearon M, Hunter F, Sockett P, Artsob H (2003) West Nile virus surveillance and diagnostics: a Canadian perspective. Canadian Journal of Infectious Diseases and Medical Microbiology 14:105–114CrossRef

Eisen RJ, Eisen L (2008) Spatial modeling of human risk of exposure to vector-borne pathogens based on epidemiological versus arthropod vector data. Journal of Medical Entomology 45:181–192. https://doi.org/10.1603/0022-2585(2008)45%5b181:smohro%5d2.0.co;2 CrossRefPubMed

Environment and Natural Resources Canada (2018) Past Weather and Climate, Historical Data. Ottawa, ON, Canada

Epstein PR, Defilippo C (2001) West Nile Virus and drought. Global Change Human Health 2:105–107. https://doi.org/10.1023/A:1015089901425 CrossRef

Farajollahi A, Fonseca DM, Kramer LD, Marm Kilpatrick A (2011) “Bird biting” mosquitoes and human disease: A review of the role of Culex pipiens complex mosquitoes in epidemiology. Infection, Genetics and Evolution 11:1577–1585. https://doi.org/10.1016/j.meegid.2011.08.013 CrossRefPubMedCentralPubMed

Foppa IM, Beard RH, Mendenhall IH (2011) The impact of West Nile virus on the abundance of selected North American birds. BMC Veterinary Research 7:43. https://doi.org/10.1186/1746-6148-7-43 CrossRefPubMedCentralPubMed

Ganser C, Wisely SM (2013) Patterns of spatio-temporal distribution, abundance, and diversity in a mosquito community from the eastern Smoky Hills of Kansas. Journal of Vector Ecology 38:229–236. https://doi.org/10.1111/j.1948-7134.2013.12035.x CrossRefPubMed

Giordano BV, Kaur S, Hunter FF (2017) West Nile Virus in Ontario, Canada: a twelve-year analysis of human case prevalence, mosquito surveillance, and climate data. PLOS ONE 12:e0183568. https://doi.org/10.1371/journal.pone.0183568 CrossRefPubMedCentralPubMed

Greenberg JA, Lujan DA, DiMenna MA, Wearing HJ, Hofkin BV (2013) Identification of blood meal sources in Aedes vexans and Culex quinquefasciatus in Bernalillo County, New Mexico. Journal of Insect Science 13:1–12. https://doi.org/10.1673/031.013.7501 CrossRef

Gubler DJ (2007) The continuing spread of West Nile Virus in the western hemisphere. Clinical Infectious Diseases 45:1039–1046. https://doi.org/10.1086/521911 CrossRefPubMed

Hamer GL, Kitron UD, Brawn JD, Loss SR, Ruiz MO, Goldberg TL, Walker ED (2008) Culex pipiens (Diptera: Culicidae): a bridge vector of West Nile Virus to humans. Journal of Medical Entomology 45:125–128. https://doi.org/10.1093/jmedent/45.1.125 CrossRefPubMed

Hamer GL, Kitron UD, Goldberg TL, Brawn JD, Loss SR, Ruiz MO, Hayes DB, Walker ED (2009) Host selection by Culex pipiens mosquitoes and West Nile Virus amplification. American Society of Tropical Medicine and Hygiene 80:268–278CrossRef

Hughes TP, Paul JH, Smithburn KC, Burke AW (1940) A neurotropic virus isolated from the blood of a native of Uganda. American Society of Tropical Medicine and Hygiene s1-20:471–492. https://doi.org/10.4269/ajtmh.1940.s1-20.471

Johnson PCD (2014) Extension of Nakagawa & Schielzeth’s R _GLMM ² to random slopes models. Methods in Ecology and Evolution 5:944–946. https://doi.org/10.1111/2041-210x.12225 CrossRefPubMedCentralPubMed

Kaufman MG, Fonseca DM (2014) Invasion biology of Aedes japonicus japonicus (Diptera: Culicidae). Annual Review of Entomology 59:31–49. https://doi.org/10.1146/annurev-ento-011613-162012 CrossRefPubMedCentralPubMed

Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD (2006) Host heterogeneity dominates West Nile Virus transmission. Proceedings of Royal Society B: Biological Sciences 273:2327–2333. https://doi.org/10.1098/rspb.2006.3575 CrossRef

Kilpatrick AM, LaDeau SL, Marra PP (2007) Ecology of West Nile Virus transmission and its impact on bird in the western hemisphere. The Auk 124:1121. https://doi.org/10.1642/0004-8038(2007)124%5b1121:eownvt%5d2.0.co;2 CrossRef

Komar O, Robbins MB, Klenk K, Blitvich BJ, Marlenee NL, Burkhalter KL, Gubler DJ, Gonzálvez G, Peña CJ, Peterson AT, Komar N (2003) West Nile Virus transmission in resident birds, Dominican Republic. Emerging Infectious Diseases Dis 9:1299–1302. https://doi.org/10.3201/eid0910.030222 CrossRefPubMedCentralPubMed

Kulldorff M (1997) A spatial scan statistic. Communications in Statistics Theory and Methods 26:1481–1496. https://doi.org/10.1080/03610929708831995 CrossRef

Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE, Davis BS, Roehrig JT (2000) Rapid detection of West Nile Virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcriptase-PCR assay. Journal of Clinical Microbiology 38:4066–4071PubMed

Levi ME (2013) West Nile Virus Infection in the Immunocompromised Patient. Current Infectious Disease Reports 15:478–485. https://doi.org/10.1007/s11908-013-0367-8 CrossRef

Levine RS, Hedeen DL, Hedeen MW, Hamer GL, Mead DG, Kitron UD (2017) Avian species diversity and transmission of West Nile Virus in Atlanta, Georgia. Parasit Vectors 10. https://doi.org/10.1186/s13071-017-1999-6

Mallya S, Sander B, Roy-Gagnon M-H, Taljaard M, Jolly A, Kulkarni MA (2018) Factors associated with human West Nile virus infection in Ontario: a generalized linear mixed modelling approach. BMC Infectious Diseases 18:1–9. https://doi.org/10.1186/s12879-018-3052-6 CrossRef

Marini G, Rosá R, Pugliese A, Heesterbeek H (2017) Exploring vector-borne infection ecology in multi-host communities: a case study of West Nile virus. Journal of Theoretical Biology 415:58–69. https://doi.org/10.1016/j.jtbi.2016.12.009 CrossRefPubMed

Molaei G, Andreadis TG (2006) Identification of avian- and mammalian-derived bloodmeals in Aedes vexans and Culiseta melanura (Diptera: Culicidae) and its implication for West Nile Virus transmission in Connecticut, USA. Journal of Medical Entomology 43:1088–1093. https://doi.org/10.1603/0022-2585(2006)43%5b1088:ioaamb%5d2.0.co;2 CrossRefPubMed

Morales-Betoulle ME, Komar N, Panella NA, Alvarez D, López MR, Betoulle J-L, Sosa SM, Müller ML, Kilpatrick AM, Lanciotti RS, Johnson BW, Powers AM, Cordón-Rosales C, Arbovirus Ecology Work Group (2013) West Nile virus ecology in a tropical ecosystem in Guatemala. American Society of Tropical Medicine and Hygiene 88:116–126. https://doi.org/10.4269/ajtmh.2012.12-0276 CrossRef

Ontario Ministry of Health and Long-Term Care (2017) Infectious disease protocol, Appendix B: provincial case definitions for reportable diseases: West Nile Virus illness. Toronto, ON, Canada

Ozdenerol E, Taff G, Akkus C (2013) Exploring the spatio-temporal dynamics of reservoir hosts, vectors, and human hosts of West Nile Virus: a review of the recent literature. International Journal of Environmental Research and Public Health 10:5399–5432. https://doi.org/10.3390/ijerph10115399 CrossRefPubMedCentralPubMed

Public Health Ontario (2013) Guide for Public Health Units: Considerations for Adult Mosquito Control. Toronto: Queen’s Printer for Ontario

Public Health Ontario (2012) Vector-Borne Diseases: 2012 Summary Report. Toronto: Queen’s Printer for Ontario

Reisen WK (2013) Ecology of West Nile Virus in North America. Viruses 5:2079–2105. https://doi.org/10.3390/v5092079 CrossRefPubMedCentralPubMed

Reisen WK, Fang Y, Martinez VM (2006) Effects of temperature on the transmission of West Nile Virus by Culex tarsalis (Diptera: Culicidae). Journal of Medical Entomology 43:309–317. https://doi.org/10.1093/jmedent/43.2.309 CrossRefPubMed

Reisen WK, Padgett K, Fang Y, Woods L, Foss L, Anderson J, Kramer V (2013) Chronic infections of West Nile Virus detected in California dead birds. Vector-Borne Zoonotic Diseases 13:401–405. https://doi.org/10.1089/vbz.2012.1097 CrossRefPubMed

Ruiz MO, Tedesco C, McTighe TJ, Austin C, Kitron U (2004) Environmental and social determinants of human risk during a West Nile Virus outbreak in the greater Chicago area, 2002. International Journal of Health Geographic 3:8. https://doi.org/10.1186/1476-072x-3-8 CrossRef

Shepard JJ, Andreadis TG, Thomas MC, Molaei G (2016) Host associations of mosquitoes at Eastern Equine Encephalitis Virus foci in Connecticut, USA. Parasit Vectors 9. https://doi.org/10.1186/s13071-016-1765-1

Smith KA, Campbell GD, Pearl DL, Jardine CM, Salgado-Bierman F, Nemeth NM (2018) A retrospective summary of raptor mortality in Ontario, Canada (1991–2014), including the effects of West Nile Virus. Journal of Wildlife Diseases 54:261–271. https://doi.org/10.7589/2017-07-157 CrossRefPubMed

Statistics Canada (2016) Health Profile. Ottawa, ON, Canada

Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s Information Criterion. Behavioral Ecology and Sociobiology 65:13–21. https://doi.org/10.1007/s00265-010-1037-6 CrossRef

Thielman A, Hunter F (2007) A photographic key to the adult female mosquitoes (Diptera: Culicidae) of Canada. Canadian Journal of Arthropod Identification 4:1–116. https://doi.org/10.3752/cjai.2007.04 CrossRef

Trawinski PR, MacKay DS (2008) Meteorologically conditioned time-series predictions of West Nile Virus vector mosquitoes. Vector-Borne Zoonotic Diseases 8:505–522. https://doi.org/10.1089/vbz.2007.0202 CrossRefPubMed

TSentr gigieny i ėpidemiologii v Respublike Tatarstan (2013) Likhoradka Zapadnogo Nila. Kazanskiĭ gosudarstvennyĭ meditsinskiĭ, Kazan, Russia

van der Meulen KM, Pensaert MB, Nauwynck HJ (2005) West Nile Virus in the vertebrate world. Archives of Virology 150:637–657. https://doi.org/10.1007/s00705-004-0463-z CrossRefPubMed

VanDalen KK, Hall JS, Clark L, McLean RG, Smeraski C (2013) West Nile Virus infection in American robins: new insights on dose response. PLoS ONE 8:e68537. https://doi.org/10.1371/journal.pone.0068537 CrossRefPubMedCentralPubMed

Winters AM, Bolling BG, Beaty BJ, Blair CD, Eisen RJ, Meyer AM, Pape WJ, Moore CG, Eisen L (2008) Combining mosquito vector and human disease data for improved assessment of spatial West Nile Virus disease risk. American Society of Tropical Medicine and Hygiene 78:654–665CrossRef

Wood DM, Dang PT, Ellis RA (1979) The mosquitoes of Canada: Diptera, Culicidae. Hull, QC, Canada: Agriculture Canada

Yoo E-H, Chen D, Diao C, Russell C (2016) The effects of weather and environmental factors on West Nile Virus mosquito abundance in Greater Toronto Area. Earth Interaction 20:1–22. https://doi.org/10.1175/ei-d-15-0003.1 CrossRef

Title: Linking Bird and Mosquito Data to Assess Spatiotemporal West Nile Virus Risk in Humans
Authors: Benoit Talbot
Merlin Caron-Lévesque
Mark Ardis
Roman Kryuchkov
Manisha A. Kulkarni
Publication date: 01-03-2019
Publisher: Springer US
Published in: EcoHealth / Issue 1/2019
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI: https://doi.org/10.1007/s10393-019-01393-8

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Linking Bird and Mosquito Data to Assess Spatiotemporal West Nile Virus Risk in Humans

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