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Temperature determines Zika, dengue and chikungunya transmission potential in the Americas

Erin A. Mordecai, Jeremy M. Cohen, Michelle V. Evans, Prithvi Gudapati, Leah R. Johnson, Kerri Miazgowicz, Courtney C. Murdock, Jason R. Rohr, Sadie J. Ryan, Van Savage, Marta Shocket, Anna Stewart Ibarra, Matthew B. Thomas, Daniel P. Weikel
doi: https://doi.org/10.1101/063735
Erin A. Mordecai
aBiology Department, Stanford University, 371 Serra Mall, Stanford, CA 94305
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  • For correspondence: emordeca@stanford.edu
Jeremy M. Cohen
bDepartment of Integrative Biology, University of South Florida, 4202 East Fowler Ave, SCA110 Tampa, FL33620
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Michelle V. Evans
cOdum School of Ecology, University of Georgia, 140 E. Green St., Athens, GA 30602
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Prithvi Gudapati
aBiology Department, Stanford University, 371 Serra Mall, Stanford, CA 94305
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Leah R. Johnson
bDepartment of Integrative Biology, University of South Florida, 4202 East Fowler Ave, SCA110 Tampa, FL33620
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Kerri Miazgowicz
dCenter for Tropical and Emerging Global Disease, Department of Infectious Diseases, University of Georgia College of Veterinary Medicine, 501 D.W. Brooks Drive, Athens, GA 30602
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Courtney C. Murdock
cOdum School of Ecology, University of Georgia, 140 E. Green St., Athens, GA 30602
dCenter for Tropical and Emerging Global Disease, Department of Infectious Diseases, University of Georgia College of Veterinary Medicine, 501 D.W. Brooks Drive, Athens, GA 30602
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Jason R. Rohr
bDepartment of Integrative Biology, University of South Florida, 4202 East Fowler Ave, SCA110 Tampa, FL33620
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Sadie J. Ryan
eDepartment of Geography, University of Florida, PO Box 117315, Turlington Hall, Gainesville, FL32611
fEmerging Pathogens Institute, University of Florida, P.O. Box 100009, 2055 Mowry Road Gainesville, FL32610
gCenter for Global Health and Translational Science, Department of Microbiology and Immunology, Weiskotten Hall, SUNY Upstate Medical University, Syracuse, NY 13210
hSchool of Life Sciences, College of Agriculture, Engineering, and Science, University of KwaZulu Natal, Private Bag X01, Scottsville, 3209, KwaZulu Natal, South Africa
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Van Savage
iDepartment of Ecology and Evolutionary Biology, University of California Los Angeles and Department of Biomathematics, University of California Los Angeles, Los Angeles, CA 90095
jSanta Fe Institute, 1399 Hyde Park Rd, Santa Fe, NM 87501
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Marta Shocket
kDepartment of Biology, Indiana University, 1001 E. 3rd St., Jordan Hall 142, Bloomington, IN 47405
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Anna Stewart Ibarra
lCenter for Global Health and Translational Sciences, SUNY Upstate Medical University, Syracuse, NY 13210
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Matthew B. Thomas
mDepartment of Entomology and Center for Infectious Disease Dynamics, Penn State University, 112 Merkle Lab, University Park, PA 16802
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Daniel P. Weikel
nDepartment of Biostatistics, University of Michigan, 1415 Washington Heights, Ann Arbor, MI 48109
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Abstract

Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand virus transmission ecology for Aedes aegypti and Ae. albopictus mosquitoes. An estimated 3.9 billion people in 120 countries are at risk for these diseases. Temperature defines the fundamental potential for vector-borne disease transmission, yet the potential for transmission in sub-tropical and temperate regions remains uncertain. Using mechanistic transmission models fit to mosquito and virus physiology data and validated with human case data, we show that mean temperature accurately bounds transmission risk for Zika, chikungunya, and dengue in the Americas. Transmission occurs between 18-34°C and peaks at 29°C for Ae. aegypti (between 11-28°C with a peak at 26°C for Ae. albopictus). As predicted, high relative incidence of Zika, dengue, and chikungunya in humans occurs between 23-32°C, peaks at 27-29°C, and is very low outside the predicted range. As a proxy for infrastructure and vector control effort, economic reliance on tourism explains some departures from areas otherwise suitable for high rates of transmission. Nonetheless, the temperature-based models alone provide fundamental eco-physiological measures of transmission potential. Tropical and subtropical regions are suitable for extended seasonal or year-round transmission by Ae. aegypti and Ae. albopictus. By contrast, potential transmission in temperate areas is constrained to at most three months per year even if vectors are present (which is currently not the case for large parts of the US). Such brief transmission windows limit the likelihood and potential extent of epidemics following disease introduction in temperate zones.

Significance statement Viruses transmitted by Aedes aegypti and Ae. albopictus mosquitoes, including Zika, dengue, and chikungunya, present one of the most rapidly growing infectious disease threats, putting an estimated 3.9 billion people in 120 countries at risk. Understanding the relationship between transmission and climate, particularly temperature, is critical for predicting and responding to potential spread into sub-tropical and temperate areas. Using models informed by laboratory experiments and tested against actual human infection data, we show that transmission potential of these three viruses is substantial between 23-32°C and peaks at 27-29°C. This implies that while year-round transmission is likely in tropical and sub-tropical areas, temperate areas are at risk for at most seasonal transmission, given that the necessary mosquito species are present.

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Posted July 15, 2016.
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Temperature determines Zika, dengue and chikungunya transmission potential in the Americas
Erin A. Mordecai, Jeremy M. Cohen, Michelle V. Evans, Prithvi Gudapati, Leah R. Johnson, Kerri Miazgowicz, Courtney C. Murdock, Jason R. Rohr, Sadie J. Ryan, Van Savage, Marta Shocket, Anna Stewart Ibarra, Matthew B. Thomas, Daniel P. Weikel
bioRxiv 063735; doi: https://doi.org/10.1101/063735
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Temperature determines Zika, dengue and chikungunya transmission potential in the Americas
Erin A. Mordecai, Jeremy M. Cohen, Michelle V. Evans, Prithvi Gudapati, Leah R. Johnson, Kerri Miazgowicz, Courtney C. Murdock, Jason R. Rohr, Sadie J. Ryan, Van Savage, Marta Shocket, Anna Stewart Ibarra, Matthew B. Thomas, Daniel P. Weikel
bioRxiv 063735; doi: https://doi.org/10.1101/063735

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