Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models
Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae. albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmissio...
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Published in | PLoS neglected tropical diseases Vol. 11; no. 4; p. e0005568 |
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Main Authors | , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
27.04.2017
Public Library of Science (PLoS) |
Subjects | |
Online Access | Get full text |
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Abstract | Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae. albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmission for Zika, chikungunya, and dengue change with mean temperature, and we show that these predictions are well matched by human case data. Across all three viruses, models and human case data both show that transmission occurs between 18-34°C with maximal transmission occurring in a range from 26-29°C. Controlling for population size and two socioeconomic factors, temperature-dependent transmission based on our mechanistic model is an important predictor of human transmission occurrence and incidence. Risk maps indicate that tropical and subtropical regions are suitable for extended seasonal or year-round transmission, but transmission in temperate areas is limited to at most three months per year even if vectors are present. Such brief transmission windows limit the likelihood of major epidemics following disease introduction in temperate zones. |
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AbstractList | Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae. albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmission for Zika, chikungunya, and dengue change with mean temperature, and we show that these predictions are well matched by human case data. Across all three viruses, models and human case data both show that transmission occurs between 18-34°C with maximal transmission occurring in a range from 26-29°C. Controlling for population size and two socioeconomic factors, temperature-dependent transmission based on our mechanistic model is an important predictor of human transmission occurrence and incidence. Risk maps indicate that tropical and subtropical regions are suitable for extended seasonal or year-round transmission, but transmission in temperate areas is limited to at most three months per year even if vectors are present. Such brief transmission windows limit the likelihood of major epidemics following disease introduction in temperate zones. Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae . albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmission for Zika, chikungunya, and dengue change with mean temperature, and we show that these predictions are well matched by human case data. Across all three viruses, models and human case data both show that transmission occurs between 18–34°C with maximal transmission occurring in a range from 26–29°C. Controlling for population size and two socioeconomic factors, temperature-dependent transmission based on our mechanistic model is an important predictor of human transmission occurrence and incidence. Risk maps indicate that tropical and subtropical regions are suitable for extended seasonal or year-round transmission, but transmission in temperate areas is limited to at most three months per year even if vectors are present. Such brief transmission windows limit the likelihood of major epidemics following disease introduction in temperate zones. Understanding the drivers of recent Zika, dengue, and chikungunya epidemics is a major public health priority. Temperature may play an important role because it affects virus transmission by mosquitoes, through its effects on mosquito development, survival, reproduction, and biting rates as well as the rate at which mosquitoes acquire and transmit viruses. Here, we measure the impact of temperature on transmission by two of the most common mosquito vector species for these viruses, Aedes aegypti and Ae . albopictus . We integrate data from several laboratory experiments into a mathematical model of temperature-dependent transmission, and find that transmission peaks at 26–29°C and can occur between 18–34°C. Statistically comparing model predictions with recent observed human cases of dengue, chikungunya, and Zika across the Americas suggests an important role for temperature, and supports model predictions. Using the model, we predict that most of the tropics and subtropics are suitable for transmission in many or all months of the year, but that temperate areas like most of the United States are only suitable for transmission for a few months during the summer (even if the mosquito vector is present). |
Audience | Academic |
Author | Lippi, Catherine A Gudapati, Prithvi Johnson, Leah R Thomas, Matthew B Miazgowicz, Kerri Shocket, Marta S Weikel, Daniel P Cohen, Jeremy M Murdock, Courtney C Mordecai, Erin A Evans, Michelle V Rohr, Jason R Savage, Van Stewart Ibarra, Anna Ryan, Sadie J |
AuthorAffiliation | 1 Biology Department, Stanford University, 371 Serra Mall, Stanford, CA, United States of America 2 Department of Integrative Biology, University of South Florida, 4202 East Fowler Ave, SCA110 Tampa, FL, United States of America 6 Center for Tropical and Emerging Global Disease, Department of Infectious Diseases, University of Georgia College of Veterinary Medicine, 501 D.W. Brooks Drive, Athens, GA, United States of America 11 Santa Fe Institute, Santa Fe, NM, United States of America 10 Department of Ecology and Evolutionary Biology, University of California Los Angeles and Department of Biomathematics, University of California Los Angeles, Los Angeles, CA, United States of America 13 Center for Global Health and Translational Sciences, SUNY Upstate Medical University, Syracuse, NY, United States of America 12 Department of Biology, Indiana University, Jordan Hall 142, Bloomington, IN, United States of America 5 Department of Geography, University of Florida, Turlington Hall, Gainesville, F |
AuthorAffiliation_xml | – name: 15 Department of Biostatistics, University of Michigan, 1415 Washington Heights, Ann Arbor, MI, United States of America – name: 7 Emerging Pathogens Institute, University of Florida, Gainesville, FL, United States of America – name: 3 Odum School of Ecology, University of Georgia, Athens, GA, United States of America – name: 4 Department of Statistics, Virginia Polytechnic and State University, 250 Drillfield Drive Blacksburg, VA, United States of America – name: Institute for Disease Modeling, UNITED STATES – name: 8 Center for Global Health and Translational Science, Department of Microbiology and Immunology, Weiskotten Hall, SUNY Upstate Medical University, Syracuse, NY, United States of America – name: 10 Department of Ecology and Evolutionary Biology, University of California Los Angeles and Department of Biomathematics, University of California Los Angeles, Los Angeles, CA, United States of America – name: 13 Center for Global Health and Translational Sciences, SUNY Upstate Medical University, Syracuse, NY, United States of America – name: 6 Center for Tropical and Emerging Global Disease, Department of Infectious Diseases, University of Georgia College of Veterinary Medicine, 501 D.W. Brooks Drive, Athens, GA, United States of America – name: 9 School of Life Sciences, College of Agriculture, Engineering, and Science, University of KwaZulu Natal, Private Bag X01, Scottsville, KwaZulu Natal, South Africa – name: 1 Biology Department, Stanford University, 371 Serra Mall, Stanford, CA, United States of America – name: 11 Santa Fe Institute, Santa Fe, NM, United States of America – name: 14 Department of Entomology and Center for Infectious Disease Dynamics, Penn State University, 112 Merkle Lab, University Park, PA, United States of America – name: 12 Department of Biology, Indiana University, Jordan Hall 142, Bloomington, IN, United States of America – name: 2 Department of Integrative Biology, University of South Florida, 4202 East Fowler Ave, SCA110 Tampa, FL, United States of America – name: 5 Department of Geography, University of Florida, Turlington Hall, Gainesville, FL, United States of America |
Author_xml | – sequence: 1 givenname: Erin A orcidid: 0000-0002-4402-5547 surname: Mordecai fullname: Mordecai, Erin A organization: Biology Department, Stanford University, 371 Serra Mall, Stanford, CA, United States of America – sequence: 2 givenname: Jeremy M surname: Cohen fullname: Cohen, Jeremy M organization: Department of Integrative Biology, University of South Florida, 4202 East Fowler Ave, SCA110 Tampa, FL, United States of America – sequence: 3 givenname: Michelle V surname: Evans fullname: Evans, Michelle V organization: Odum School of Ecology, University of Georgia, Athens, GA, United States of America – sequence: 4 givenname: Prithvi surname: Gudapati fullname: Gudapati, Prithvi organization: Biology Department, Stanford University, 371 Serra Mall, Stanford, CA, United States of America – sequence: 5 givenname: Leah R surname: Johnson fullname: Johnson, Leah R organization: Department of Statistics, Virginia Polytechnic and State University, 250 Drillfield Drive Blacksburg, VA, United States of America – sequence: 6 givenname: Catherine A surname: Lippi fullname: Lippi, Catherine A organization: Department of Geography, University of Florida, Turlington Hall, Gainesville, FL, United States of America – sequence: 7 givenname: Kerri surname: Miazgowicz fullname: Miazgowicz, Kerri organization: Center for Tropical and Emerging Global Disease, Department of Infectious Diseases, University of Georgia College of Veterinary Medicine, 501 D.W. Brooks Drive, Athens, GA, United States of America – sequence: 8 givenname: Courtney C surname: Murdock fullname: Murdock, Courtney C organization: Center for Tropical and Emerging Global Disease, Department of Infectious Diseases, University of Georgia College of Veterinary Medicine, 501 D.W. Brooks Drive, Athens, GA, United States of America – sequence: 9 givenname: Jason R surname: Rohr fullname: Rohr, Jason R organization: Department of Integrative Biology, University of South Florida, 4202 East Fowler Ave, SCA110 Tampa, FL, United States of America – sequence: 10 givenname: Sadie J surname: Ryan fullname: Ryan, Sadie J organization: School of Life Sciences, College of Agriculture, Engineering, and Science, University of KwaZulu Natal, Private Bag X01, Scottsville, KwaZulu Natal, South Africa – sequence: 11 givenname: Van surname: Savage fullname: Savage, Van organization: Santa Fe Institute, Santa Fe, NM, United States of America – sequence: 12 givenname: Marta S surname: Shocket fullname: Shocket, Marta S organization: Department of Biology, Indiana University, Jordan Hall 142, Bloomington, IN, United States of America – sequence: 13 givenname: Anna surname: Stewart Ibarra fullname: Stewart Ibarra, Anna organization: Center for Global Health and Translational Sciences, SUNY Upstate Medical University, Syracuse, NY, United States of America – sequence: 14 givenname: Matthew B surname: Thomas fullname: Thomas, Matthew B organization: Department of Entomology and Center for Infectious Disease Dynamics, Penn State University, 112 Merkle Lab, University Park, PA, United States of America – sequence: 15 givenname: Daniel P surname: Weikel fullname: Weikel, Daniel P organization: Department of Biostatistics, University of Michigan, 1415 Washington Heights, Ann Arbor, MI, United States of America |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28448507$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2017 Public Library of Science 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mordecai EA, Cohen JM, Evans MV, Gudapati P, Johnson LR, Lippi CA, et al. (2017) Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models. PLoS Negl Trop Dis 11(4): e0005568. https://doi.org/10.1371/journal.pntd.0005568 2017 Mordecai et al 2017 Mordecai et al 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Mordecai EA, Cohen JM, Evans MV, Gudapati P, Johnson LR, Lippi CA, et al. (2017) Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models. PLoS Negl Trop Dis 11(4): e0005568. https://doi.org/10.1371/journal.pntd.0005568 |
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Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. Conceptualization: EAM MBT VS SJR LRJ ASI JRR.Data curation: JMC MVE PG KM CCM MS DPW EAM CAL.Formal analysis: EAM MVE PG KM MSS DPW LRJ CAL.Funding acquisition: EAM JRR SJR MBT ASI LRJ VS CCM.Investigation: JMC MVE PG KM CCM MS DPW CAL EAM.Methodology: EAM LRJ SJR MSS.Project administration: EAM.Software: LRJ EAM MSS MVE DPW.Supervision: EAM MBT JRR VS LRJ SJR ASI CCM.Validation: LRJ EAM.Visualization: JMC SJR LRJ EAM.Writing – original draft: EAM.Writing – review & editing: EAM JMC MVE PG LRJ CAL KM CCM JRR SJR VS MSS ASI MBT DPW. |
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SubjectTerms | Aedes - growth & development Aedes aegypti Aedes albopictus Alphavirus Analysis Animals Aquatic insects Biology and life sciences Blood Chikungunya fever Chikungunya Fever - epidemiology Chikungunya Fever - transmission Chikungunya virus Computer viruses Dengue Dengue - epidemiology Dengue - transmission Dengue fever Dengue virus Disease control Disease transmission Disease Transmission, Infectious Epidemics Epidemiology Female Flaviviridae Flavivirus Humans Infectious diseases Influence Medicine and Health Sciences Models, Statistical Mosquito Vectors - growth & development Mosquitoes Physical Sciences Population number Public health Research and Analysis Methods Seasonal comparisons Seasons Social factors Socioeconomic data Socioeconomic factors Socioeconomics Temperate zones Temperature Temperature dependence Togaviridae Topography, Medical Transmission Tropical diseases Vector-borne diseases Viral diseases Viral infections Zika virus Zika virus infection Zika Virus Infection - epidemiology Zika Virus Infection - transmission |
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Title | Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models |
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