Volume 86, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Temperature has played a critical role in the spatiotemporal dynamics of West Nile virus transmission throughout California from its introduction in 2003 through establishment by 2009. We compared two novel mechanistic measures of transmission risk, the temperature-dependent ratio of virus extrinsic incubation period to the mosquito gonotrophic period (BT), and the fundamental reproductive ratio (R) based on a mathematical model, to analyze spatiotemporal patterns of receptivity to viral amplification. Maps of BT and R were created at 20-km scale and compared throughout California to seroconversions in sentinel chicken flocks at half-month intervals. Overall, estimates of BT and R agreed with intensity of transmission measured by the frequency of sentinel chicken seroconversions. Mechanistic measures such as these are important for understanding how temperature affects the spatiotemporal dynamics of West Nile virus transmission and for delineating risk estimates useful to inform vector control agency intervention decisions and communicate outbreak potential.


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  1. Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, Steele K, Crise B, Volpe KE, Crabtree MB, Scherret JH, Hall RA, Mackenzie JS, Cropp CB, Panigrahy B, Ostlund E, Schmitt B, Malkinson M, Banet C, Weissman J, Komar N, Savage HM, Stone W, McNamara T, Gubler DJ, , 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286: 23332337.[Crossref] [Google Scholar]
  2. Reisen W, Lothrop H, Chiles R, Madon M, Cossen C, Woods L, Husted S, Kramer V, Edman J, , 2004. West Nile virus in California. Emerg Infect Dis 10: 13691378.[Crossref] [Google Scholar]
  3. Hom A, Marcus L, Kramer VL, Cahoon BE, Glaser C, Cossen C, Baylis E, Jean C, Tu EH, Eldridge BF, Carney R, Padgett K, Sun B, Reisen WK, Woods L, Husted S, , 2005. Surveillance for mosquito-borne encephalitis virus activity and human disease, including West Nile virus in California, 2004. Proc Mosq Vector Control Assoc Calif 73: 6677. [Google Scholar]
  4. Wheeler SS, Barker CM, Fang Y, Armijos MV, Carroll BD, Husted S, Johnson WO, Reisen WK, , 2009. Differential impacts of West Nile virus on California birds. Condor 111: 120.[Crossref] [Google Scholar]
  5. California Department of Public Health, 2010. California West Nile Virus. Available at: http://westnile.ca.gov. Accessed March 24, 2011. [Google Scholar]
  6. Reisen WK, Fang Y, Martinez VM, , 2006. Effects of temperature on the transmission of West Nile virus by Culex tarsalis (Diptera: Culicidae). J Med Entomol 43: 309317.[Crossref] [Google Scholar]
  7. Liu A, Lee V, Galusha D, Slade MD, Diuk-Wasser M, Andreadis T, Scotch M, Rabinowitz PM, , 2009. Risk factors for human infection with West Nile virus in Connecticut: a multi-year analysis. Int J Hlth Geograph 8: 67.[Crossref] [Google Scholar]
  8. Ruiz MO, Chaves LF, Hamer GL, Sun T, Brown WM, Walker ED, Haramis L, Goldberg TL, Kitron UD, , 2010. Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA. Parasites and Vectors 19: 19.[Crossref] [Google Scholar]
  9. Soverow JE, Wellenius GA, Fisman DN, Mittleman MA, , 2009. Infectious disease in a warming world: how weather influenced West Nile virus in the United States (2001–2005). Environ Health Perspect 117: 10491052.[Crossref] [Google Scholar]
  10. Reisen WK, Milby MM, Presser SB, Hardy JL, , 1992. Ecology of mosquitoes and St. Louis encephalitis virus in the Los Angeles Basin of California, 1987–1990. J Med Entomol 29: 582598.[Crossref] [Google Scholar]
  11. Kilpatrick AM, Meola MA, Moudy RM, Kramer LD, , 2008. Temperature, viral genetics, and the transmission of West Nile virus by Culex pipiens mosquitoes. PLoS Pathogens 27 e1000092. [Google Scholar]
  12. Bowman C, Gumel AB, van den Driessche P, Wu J, Zhu H, , 2005. A mathematical model for assessing control strategies against West Nile virus. Bull Math Biol 67: 11071133.[Crossref] [Google Scholar]
  13. Blayneh KW, Gumel AB, Lenhart S, Clayton T, , 2010. Backward bifurcation and optimal control in transmission dynamics of West Nile virus. Bull Math Biol 72: 10061028.[Crossref] [Google Scholar]
  14. Liu RS, Shuai JP, Wu JH, Zhu HP, , 2006. Modeling spatial spread of West Nile virus and impact of directional dispersal of birds. Math Biosci Eng 3: 145160. [Google Scholar]
  15. Cruz-Pacheco G, Esteva L, Montano-Hirose JA, Vargas C, , 2005. Modeling the dynamics of West Nile virus. Bull Math Biol 67: 11571172.[Crossref] [Google Scholar]
  16. Hartemink NA, Davis SA, Reiter P, Hubalek Z, Heesterbeek JAP, , 2007. Importance of bird-to-bird transmission for the establishment of West Nile virus. Vector Borne Zoonotic Dis 7: 575584.[Crossref] [Google Scholar]
  17. Jiang JF, Qiu ZP, , 2009. The complete classification for dynamics in a nine-dimensional West Nile virus model. SIAM J Appl Math 69: 12051227.[Crossref] [Google Scholar]
  18. Jiang JF, Qiu ZP, Wu JH, Zhu HP, , 2009. Threshold conditions for West Nile virus outbreaks. Bull Math Biol 71: 627647.[Crossref] [Google Scholar]
  19. Kenkre VM, Parmenter RR, Peixoto LD, Sadasiv L, , 2005. A theoretical framework for the analysis of the West Nile virus epidemic. Math Comput Model 42: 313324.[Crossref] [Google Scholar]
  20. Lewis M, Renclawowicz J, Van den Driessche P, , 2006. Traveling waves and spread rates for a West Nile virus model. Bull Math Biol 68: 323.[Crossref] [Google Scholar]
  21. Lewis MA, Renclawowicz J, van den Driessche P, Wonham M, , 2006. A comparison of continuous and discrete-time West Nile virus models. Bull Math Biol 68: 491509.[Crossref] [Google Scholar]
  22. Lord CC, Day JF, , 2001. Simulation studies of St. Louis encephalitis and West Nile viruses: the impact of bird mortality. Vector Borne Zoonotic Dis 1: 317329.[Crossref] [Google Scholar]
  23. Rappole JH, Compton BW, Leimgruber P, Robertson J, King DI, Renner SC, , 2006. Modeling movement of West Nile virus in the western hemisphere. Vector Borne Zoonotic Dis 6: 128139.[Crossref] [Google Scholar]
  24. Thomas DM, Urena B, , 2001. A model describing the evolution of West Nile-like encephalitis in New York City. Math Comput Model 34: 771781.[Crossref] [Google Scholar]
  25. Wan H, Zhu HP, , 2010. The backward bifurcation in compartmental models for West Nile virus. Math Biosci 227: 2028.[Crossref] [Google Scholar]
  26. Wonham MJ, Camino-Beck T, Lewis MA, , 2004. An epidemiological model for West Nile virus: invasion analysis and control applications. Proc R Soc Lond B Biol Sci 271: 501507.[Crossref] [Google Scholar]
  27. Wonham MJ, Lewis MA, Brauer F, van den Driessche P, Wu J, , 2008. A comparative analysis of models for West Nile virus. , eds. Mathematical Epidemiology. Berlin: Springer-Verlag, 365390.[Crossref] [Google Scholar]
  28. Wonham MJ, Lewis MA, Renclawowicz J, Van den Driessche P, , 2006. Transmission assumptions generate conflicting predictions in host-vector disease models: a case study in West Nile virus. Ecol Lett 9: 706725.[Crossref] [Google Scholar]
  29. California Department of Public Health, 2011. Mosquito and Vector Control Association of California, University of California. California Mosquito-Borne Virus Surveillance and Response Plan. Available at: http://westnile.ca.gov/downloads.php?download_id=820&filename=2008_CA_Mosq_Surv.pdf. Accessed March 3, 2012. [Google Scholar]
  30. Barker CM, Kramer VL, Reisen WK, , 2010. Decision Support System for Mosquito and Arbovirus Control in California. Earthzine: an IEEE Publication. Available at: http://www.earthzine.org/2010/09/24/decision-support-system-for-mosquito-and-arbovirus-control-in-california/. Accessed January 14, 2012. [Google Scholar]
  31. Nemani R, Votava P, Michaelis A, White M, Melton F, Milesi C, Pierce L, Golden K, Hashimoto H, Ichii K, Johnson L, Jolly M, Myneni R, Tague C, Coughlan J, Running S, Aswathanarayana U, , 2007. Remote sensing methodologies for ecosystem management. , ed. Food and Water Security. Oxford, UK: Taylor & Francis, 119. [Google Scholar]
  32. Newhouse VF, Chamberlain RW, Johnston JG, Jr Sudia WD, , 1966. Use of dry ice to increase mosquito catches of the CDC miniature light trap. Mosq News 26: 3035. [Google Scholar]
  33. Reisen WK, Presser SB, Lin J, Enge B, Hardy JL, Emmons RW, , 1994. Viremia and serological responses in adult chickens infected with western equine encephalomyelitis and St. Louis encephalitis viruses. J Am Mosq Control Assoc 10: 549555. [Google Scholar]
  34. Patiris PJ, Oceguera LF, 3rd Peck GW, Chiles RE, Reisen WK, Hanson CV, , 2008. Serologic diagnosis of West Nile and St. Louis encephalitis virus infections in domestic chickens. Am J Trop Med Hyg 78: 434441. [Google Scholar]
  35. Development Core Team R, , 2009. R: A Language and Environment for Statistical Computing. Vienna, Austria: Foundation for Statistical Computing. [Google Scholar]
  36. Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M, , 2003. Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9: 311322.[Crossref] [Google Scholar]
  37. Reisen WK, Fang Y, Martinez VM, , 2005. Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. J Med Entomol 42: 367375.[Crossref] [Google Scholar]
  38. Nemeth NM, Oesterle PT, Bowen RA, , 2009. Humoral immunity to West Nile virus is long-lasting and protective in the house sparrow (Passer domesticus). Am J Trop Med Hyg 80: 864869. [Google Scholar]
  39. Reisen WK, Chiles RE, Green EN, Fang Y, Mahmood F, , 2003. Previous infection protects finches from re-infection with St. Louis encephalitis virus. J Med Entomol 40: 300305.[Crossref] [Google Scholar]
  40. Goddard LB, Roth AE, Reisen WK, Scott TW, , 2003. Vertical transmission of West Nile virus by three California Culex (Diptera: Culicidae) species. J Med Entomol 40: 743746.[Crossref] [Google Scholar]
  41. Reisen WK, Fang Y, Lothrop HD, Martinez VM, Wilson J, O'Connor P, Carney R, Cahoon-Young B, Shafii M, Brault AC, , 2006. Overwintering of West Nile virus in southern California. J Med Entomol 43: 344355.[Crossref] [Google Scholar]
  42. Dawson JR, Stone WB, Ebel GD, Young DS, Galinski DS, Pensabene JP, Franke MA, Eidson M, Kramer LD, , 2007. Crow deaths caused by West Nile virus during winter. Emerg Infect Dis 13: 19121914.[Crossref] [Google Scholar]
  43. Garmendia AE, Van Kruiningen HJ, French RA, Anderson JF, Andreadis TG, Kumar A, West AB, , 2000. Recovery and identification of West Nile virus from a hawk in winter. J Clin Microbiol 38: 31103111. [Google Scholar]
  44. Thiemann TC, , 2011. Bloodfeeding patterns of Culex tarsalis and the Culex pipiens complex in California. Entomology. Davis, CA: University of California, 110. [Google Scholar]
  45. Chaves LF, Harrington LC, Keogh CL, Nguyen AM, Kitron UD, , 2010. Blood feeding patterns of mosquitoes: random or structured? Front Zool 7: 3.[Crossref] [Google Scholar]
  46. Goddard L, Roth A, Reisen WK, Scott TW, , 2003. Extrinsic incubation period of West Nile virus in four California Culex (Diptera: Culicidae) species. Proc Mosq Vector Control Assoc Calif 71: 7075. [Google Scholar]
  47. van den Driessche P, Watmough J, , 2002. Reproduction numbers and sub-threshold endemic equilibria for compartmental models of disease transmission. Math Biosci 180: 2948.[Crossref] [Google Scholar]
  48. Anderson RM, May RM, , 1991. Infectious Diseases of Humans: Dynamics and Control. Oxford, UK: Oxford University Press. [Google Scholar]
  49. Heffernan JM, Smith RJ, Wahl LM, , 2005. Perspectives on the basic reproductive ratio. J R Soc Interface 2: 281293.[Crossref] [Google Scholar]
  50. Massad E, Coutinho FAB, Burattini MN, Amaku M, , 2010. Estimation of R0 from the initial phase of an outbreak of a vector-borne infection. Trop MedInternational Hlth 15: 120126. [Google Scholar]
  51. Dushoff J, Huang WZ, Castillo-Chavez C, , 1998. Backwards bifurcations and catastrophe in simple models of fatal diseases. J Math Biol 36: 227248.[Crossref] [Google Scholar]
  52. Lipsitch M, Nowak MA, Ebert D, May RM, , 1995. The population dynamics of vertically and horizontally transmitted parasites. Proc Biol Sci 260: 321327.[Crossref] [Google Scholar]
  53. Gaff H, Hartley D, Leahy N, , 2007. An epidemiological model of Rift Valley fever. Electron J Diff Eqn 2007: 112. [Google Scholar]
  54. Fraser C, Riley S, Anderson RM, Ferguson NM, , 2004. Factors that make an infectious disease outbreak controllable. Proc Natl Acad Sci USA 101: 61466151.[Crossref] [Google Scholar]
  55. Meyer RP, Hardy JL, Reisen WK, , 1990. Diel changes in adult mosquito microhabitat temperatures and their relationship to the extrinsic incubation of arboviruses in mosquitoes in Kern County, California, USA. J Med Entomol 27: 607614.[Crossref] [Google Scholar]
  56. Reisen WK, Lothrop HD, Meyer RP, , 1997. Time of host-seeking by Culex tarsalis (Diptera: Culicidae) in California. J Med Entomol 34: 430437.[Crossref] [Google Scholar]
  57. Matala A, , 2008. Sample Size Requirement for Monte Carlo–Simulations Using Latin Hypercube Sampling. Helsinki University of Technology, Department of Engineering Physics and Mathematics, Systems Analysis Laboratory. Available at: www.sal.tkk.fi/publications/pdf-files/emat08.pdf. Accessed January 14, 2012. [Google Scholar]
  58. Garrett-Jones C, Shidrawi GR, , 1969. Malaria vectorial capacity of a population of Anopheles gambiae: an exercise in epidemiological entomology. Bull World Health Organ 40: 531545. [Google Scholar]
  59. Mitchell CJ, Millian KY, Jr, 1981. Continued host seeking by partially engorged Culex tarsalis (Diptera: Culicidae) collected in nature. J Med Entomol 18: 249250.[Crossref] [Google Scholar]
  60. Reisen WK, , 1995. Effect of temperature on Culex tarsalis (Diptera: Culicidae) from the Coachella and San Joaquin Valleys of California. J Med Entomol 32: 636645.[Crossref] [Google Scholar]
  61. Wekesa JW, Yuval B, Washino RK, , 1997. Multiple blood feeding by Anopheles freeborni and Culex tarsalis (Diptera:Culicidae): spatial and temporal variation. J Med Entomol 34: 219225.[Crossref] [Google Scholar]
  62. Reeves WC, Hardy JL, Reisen WK, Milby MM, , 1994. Potential effect of global warming on mosquito-borne arboviruses. J Med Entomol 31: 323332.[Crossref] [Google Scholar]
  63. Lambrechts L, Paaijmans KP, Fansiri T, Carrington LB, Kramer LD, Thomas MB, Scott TW, , 2011. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti . Proc Natl Acad Sci USA 108: 74607465.[Crossref] [Google Scholar]
  64. Reisen WK, Wheeler SS, Garcia S, Fang Y, , 2010. Migratory birds and the dispersal of arboviruses in California. Am J Trop Med Hyg 83: 808815.[Crossref] [Google Scholar]
  65. Kwan JL, Kluh S, Madon MB, Nguyen DV, Barker CM, Reisen WK, , 2010. Sentinel chicken seroconversions track tangential transmission of West Nile virus to humans in the greater Los Angeles area of California. Am J Trop Med Hyg 83: 11371145.[Crossref] [Google Scholar]
  66. Reisen WK, Lothrop HD, Wheeler SS, Kennsington M, Gutierrez A, Fang Y, Garcia S, Lothrop B, , 2008. Persistent West Nile virus transmission and the apparent displacement St. Louis encephalitis virus in southeastern California, 2003–2006. J Med Entomol 45: 494508.[Crossref] [Google Scholar]
  67. Reisen WK, Carroll BD, Takahashi R, Fang Y, Garcia S, Martinez VM, Quiring R, , 2009. Repeated West Nile virus epidemic transmission in Kern County, California, 2004–2007. J Med Entomol 46: 139157.[Crossref] [Google Scholar]
  68. Reisen WK, Milby MM, Reeves WC, Meyer RP, Bock ME, , 1983. Population ecology of Culex tarsalis (Diptera: Culicidae) in a foothill environment of Kern County, California: temporal changes in female relative abundance, reproductive status, and survivorship. Ann Entomol Soc Am 76: 800808.[Crossref] [Google Scholar]
  69. Reisen WK, Lothrop HD, Hardy JL, , 1995. Bionomics of Culex tarsalis (Diptera: Culicidae) in relation to arbovirus transmission in southeastern California. J Med Entomol 32: 316327.[Crossref] [Google Scholar]
  70. Cornell Laboratory of Ornithology, 2011. The Birds of North America. Available at: http://bna.birds.cornell.edu/bna/. Accessed May 9, 2011. [Google Scholar]
  71. Dohm DJ, O'Guinn M, Turell MJ, , 2002. Effect of environmental temperature on the ability of Culex pipiens (Diptera: Culicidae) to transmit West Nile virus. J Med Entomol 39: 221225.[Crossref] [Google Scholar]
  72. Kilpatrick AM, LaDeau SL, Marra PP, , 2007. Ecology of West Nile virus transmission and its impact on birds in the Western Hemisphere. Auk 124: 11211136.[Crossref] [Google Scholar]

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  • Received : 31 May 2011
  • Accepted : 04 Feb 2012
  • Published online : 01 May 2012

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