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Title: Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts

Abstract

The effect of global climate change on infectious disease remains hotly debated because multiple extrinsic and intrinsic drivers interact to influence transmission dynamics in nonlinear ways. The dominant drivers of widespread pathogens, like West Nile virus, can be challenging to identify due to regional variability in vector and host ecology, with past studies producing disparate findings. Here, we used analyses at national and state scales to examine a suite of climatic and intrinsic drivers of continental-scale West Nile virus epidemics, including an empirically derived mechanistic relationship between temperature and transmission potential that accounts for spatial variability in vectors. We found that drought was the primary climatic driver of increased West Nile virus epidemics, rather than within-season or winter temperatures, or precipitation independently. Local-scale data from one region suggested drought increased epidemics via changes in mosquito infection prevalence rather than mosquito abundance. In addition, human acquired immunity following regional epidemics limited subsequent transmission in many states. We show that over the next 30 years, increased drought severity from climate change could triple West Nile virus cases, but only in regions with low human immunity. Lastly, these results illustrate how changes in drought severity can alter the transmission dynamics of vector-borne diseases.

Authors:
ORCiD logo [1];  [2];  [3];  [3];  [4];  [5]; ORCiD logo [6]
  1. Univ. of California, Santa Cruz, CA (United States); National Center for Atmospheric Research, Boulder, CO (United States)
  2. Northwestern Univ., Evanston, IL (United States); Stanford Univ., Stanford, CA (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. New York State Dept. of Health, Slingerlands, NY (United States); SUNY, Albany, NY (United States)
  5. Stanford Univ., Stanford, CA (United States)
  6. Univ. of California, Santa Cruz, CA (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1344995
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Additional Journal Information:
Journal Volume: 284; Journal Issue: 1848; Journal ID: ISSN 0962-8452
Publisher:
The Royal Society Publishing
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; vector-borne disease; nonlinear temperature–disease relationship; Culex; disease ecology; global warming

Citation Formats

Paull, Sara H., Horton, Daniel E., Ashfaq, Moetasim, Rastogi, Deeksha, Kramer, Laura D., Diffenbaugh, Noah S., and Kilpatrick, A. Marm. Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts. United States: N. p., 2017. Web. doi:10.1098/rspb.2016.2078.
Paull, Sara H., Horton, Daniel E., Ashfaq, Moetasim, Rastogi, Deeksha, Kramer, Laura D., Diffenbaugh, Noah S., & Kilpatrick, A. Marm. Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts. United States. doi:10.1098/rspb.2016.2078.
Paull, Sara H., Horton, Daniel E., Ashfaq, Moetasim, Rastogi, Deeksha, Kramer, Laura D., Diffenbaugh, Noah S., and Kilpatrick, A. Marm. Wed . "Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts". United States. doi:10.1098/rspb.2016.2078. https://www.osti.gov/servlets/purl/1344995.
@article{osti_1344995,
title = {Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts},
author = {Paull, Sara H. and Horton, Daniel E. and Ashfaq, Moetasim and Rastogi, Deeksha and Kramer, Laura D. and Diffenbaugh, Noah S. and Kilpatrick, A. Marm},
abstractNote = {The effect of global climate change on infectious disease remains hotly debated because multiple extrinsic and intrinsic drivers interact to influence transmission dynamics in nonlinear ways. The dominant drivers of widespread pathogens, like West Nile virus, can be challenging to identify due to regional variability in vector and host ecology, with past studies producing disparate findings. Here, we used analyses at national and state scales to examine a suite of climatic and intrinsic drivers of continental-scale West Nile virus epidemics, including an empirically derived mechanistic relationship between temperature and transmission potential that accounts for spatial variability in vectors. We found that drought was the primary climatic driver of increased West Nile virus epidemics, rather than within-season or winter temperatures, or precipitation independently. Local-scale data from one region suggested drought increased epidemics via changes in mosquito infection prevalence rather than mosquito abundance. In addition, human acquired immunity following regional epidemics limited subsequent transmission in many states. We show that over the next 30 years, increased drought severity from climate change could triple West Nile virus cases, but only in regions with low human immunity. Lastly, these results illustrate how changes in drought severity can alter the transmission dynamics of vector-borne diseases.},
doi = {10.1098/rspb.2016.2078},
journal = {Proceedings of the Royal Society B: Biological Sciences},
number = 1848,
volume = 284,
place = {United States},
year = {2017},
month = {2}
}

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Cited by: 1 work
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Figures / Tables:

Figure 1 Figure 1: Mechanisms influencing WNV transmission. (a) Variables (blue/white) that influence human WNND cases (red/dark grey) either positively (green/whitearrows) or negatively (black arrows), either directly, or via effects on mosquito populations (purple/light grey). Note that it is the product of mosquito abundance and prevalence that determine risk to humans. Themore » fitted relationships for the temperature-dependent: (b) biting rate [15], (c) mortality rate [16,17], (d) and the inverse of the extrinsic incubation period [18,19] (L.D. Kramer and A.M.K., unpublished data) were used to generate (e) the resulting estimated relationships between temperature and partial-R0 for West Nile virus for C. tarsalis (triangles, dashed lines), C. pipiens (circles, solid lines) and C. quinquefasciatus (cross-hatches,dotted lines; see Material and methods). (Online version in colour.)« less

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    dataset, January 2017


    Supplementary material from "Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts"
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    • Paull, Sara H.; Horton, Daniel E.; Ashfaq, Moetasim
    • Figshare-Supplementary information for journal article at DOI: 10.1098/rspb.2016.2078, 1 docx file (5.38 MB)
    • DOI: 10.6084/m9.figshare.c.3677074

    Supplementary material from "Drought and immunity determine the intensity of West Nile virus epidemics and climate change impacts"
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    • DOI: 10.1038/nature02759

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    • DOI: 10.1038/nclimate1783

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    Inter-Annual Associations Between Precipitation and Human Incidence of West Nile Virus in the United States
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    • Vector-Borne and Zoonotic Diseases, Vol. 7, Issue 3
    • DOI: 10.1089/vbz.2006.0590

    Rapid Amplification of West Nile Virus: The Role of Hatch-Year Birds
    journal, February 2008

    • Hamer, Gabriel L.; Walker, Edward D.; Brawn, Jeffrey D.
    • Vector-Borne and Zoonotic Diseases, Vol. 8, Issue 1
    • DOI: 10.1089/vbz.2007.0123

    National and Regional Associations Between Human West Nile Virus Incidence and Demographic, Landscape, and Land Use Conditions in the Coterminous United States
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    • DeGroote, John P.; Sugumaran, Ramanathan
    • Vector-Borne and Zoonotic Diseases, Vol. 12, Issue 8
    • DOI: 10.1089/vbz.2011.0786

    Predicting Human West Nile Virus Infections With Mosquito Surveillance Data
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    • Kilpatrick, A. Marm; Pape, W. John
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    • DOI: 10.1093/aje/kwt046

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    Drought-Induced Amplification and Epidemic Transmission of West Nile Virus in Southern Florida
    journal, March 2005

    • Shaman, Jeffrey; Day, Jonathan F.; Stieglitz, Marc
    • Journal of Medical Entomology, Vol. 42, Issue 2
    • DOI: 10.1093/jmedent/42.2.134

    Effects of Temperature on the Transmission of West Nile Virus by Culex tarsalis (Diptera: Culicidae)
    journal, March 2006

    • Reisen, William K.; Fang, Ying; Martinez, Vincent M.
    • Journal of Medical Entomology, Vol. 43, Issue 2
    • DOI: 10.1093/jmedent/43.2.309

    Flushing Effect of Rain on Container-Inhabiting Mosquitoes Aedes aegypti and Culex pipiens (Diptera: Culicidae)
    journal, January 2008

    • Koenraadt, C. J. M.; Harrington, L. C.
    • Journal of Medical Entomology, Vol. 45, Issue 1
    • DOI: 10.1093/jmedent/45.1.28

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    • Kermack, W. O.; McKendrick, A. G.
    • Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 115, Issue 772
    • DOI: 10.1098/rspa.1927.0118

    Host stress hormones alter vector feeding preferences, success, and productivity
    journal, August 2016

    • Gervasi, Stephanie S.; Burkett-Cadena, Nathan; Burgan, Sarah C.
    • Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1836
    • DOI: 10.1098/rspb.2016.1278

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    Globalization, Land Use, and the Invasion of West Nile Virus
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    Monitoring EU Emerging Infectious Disease Risk Due to Climate Change
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    Modeling the average population of La Crosse vectors in Knox County, Tennessee
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    A quantitative comparison of West Nile virus incidence from 2013 to 2018 in Emilia-Romagna, Italy
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    Key Factors Influencing the Incidence of West Nile Virus in Burleigh County, North Dakota
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    Biological Adaptations Associated with Dehydration in Mosquitoes
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      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.