Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus

Abstract During the recent yellow fever (YF) epidemics in Brazil, human cases were attributed to spillover infections via sylvatic mosquito transmission. Despite YF virus (YFV) transmission in major urban centers with insufficient vaccination coverage and abundant populations of the domestic vector,...

Full description

Saved in:
Bibliographic Details
Main Authors: Divya P. Shinde, Jessica A. Plante, Dionna Scharton, Brooke Mitchell, Jordyn Walker, Sasha R. Azar, Rafael K. Campos, Lívia Sacchetto, Betânia P. Drumond, Nikos Vasilakis, Kenneth S. Plante, Scott C. Weaver
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54146-9
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846171825670717440
author Divya P. Shinde
Jessica A. Plante
Dionna Scharton
Brooke Mitchell
Jordyn Walker
Sasha R. Azar
Rafael K. Campos
Lívia Sacchetto
Betânia P. Drumond
Nikos Vasilakis
Kenneth S. Plante
Scott C. Weaver
author_facet Divya P. Shinde
Jessica A. Plante
Dionna Scharton
Brooke Mitchell
Jordyn Walker
Sasha R. Azar
Rafael K. Campos
Lívia Sacchetto
Betânia P. Drumond
Nikos Vasilakis
Kenneth S. Plante
Scott C. Weaver
author_sort Divya P. Shinde
collection DOAJ
description Abstract During the recent yellow fever (YF) epidemics in Brazil, human cases were attributed to spillover infections via sylvatic mosquito transmission. Despite YF virus (YFV) transmission in major urban centers with insufficient vaccination coverage and abundant populations of the domestic vector, Aedes aegypti, there was no evidence of human-amplified transmission. Furthermore, the historic absence of YF in Asia, despite abundant Ae. aegypti and an immunologically naive human population, is unexplained. We tested the hypothesis that pre-existing, heterologous flavivirus immunity, specifically from dengue (DENV) and Zika (ZIKV) viruses, limits YFV viremia and transmission by Ae. aegypti. We infected cynomolgus macaques with DENV or ZIKV, then challenged them 6–9 months later with YFV. We then measured viremia and disease and allowed Ae. aegypti mosquitoes to feed during peak macaque viremia. Although prior heterologous immunity had variable effects on disease, DENV and ZIKV immunity consistently suppressed YFV viremia. Despite no statistical difference due to a small sample size, the suppression in viremia led to a significant reduction in Ae. aegypti infection and a lack of transmission potential. These results support the hypothesis that, in DENV- and ZIKV-endemic regions such as South America and Asia, human flavivirus immunity suppresses YFV human amplification potential, reducing the risk of urban outbreaks.
format Article
id doaj-art-8cadf7cb3c2a4f769d8677035a9297bc
institution Kabale University
issn 2041-1723
language English
publishDate 2024-11-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-8cadf7cb3c2a4f769d8677035a9297bc2024-11-10T12:32:37ZengNature PortfolioNature Communications2041-17232024-11-0115111110.1038/s41467-024-54146-9Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virusDivya P. Shinde0Jessica A. Plante1Dionna Scharton2Brooke Mitchell3Jordyn Walker4Sasha R. Azar5Rafael K. Campos6Lívia Sacchetto7Betânia P. Drumond8Nikos Vasilakis9Kenneth S. Plante10Scott C. Weaver11Department of Microbiology and Immunology, University of Texas Medical BranchDepartment of Microbiology and Immunology, University of Texas Medical BranchDepartment of Microbiology and Immunology, University of Texas Medical BranchDepartment of Microbiology and Immunology, University of Texas Medical BranchDepartment of Microbiology and Immunology, University of Texas Medical BranchDepartment of Pathology, University of Texas Medical BranchDepartment of Microbiology and Immunology, University of Texas Medical BranchLaboratório de Pesquisas em Virologia, Departamento de Doenças Dermatológicas, Infecciosas e Parasitárias, Faculdade de Medicina de São José do Rio Preto, São José do Rio PretoDeparment of Microbiology—Institute of Biological Sciences, Universidade Federal de Minas GeraisWorld Reference Center for Emerging Viruses and Arboviruses, University of Texas Medical BranchDepartment of Microbiology and Immunology, University of Texas Medical BranchDepartment of Microbiology and Immunology, University of Texas Medical BranchAbstract During the recent yellow fever (YF) epidemics in Brazil, human cases were attributed to spillover infections via sylvatic mosquito transmission. Despite YF virus (YFV) transmission in major urban centers with insufficient vaccination coverage and abundant populations of the domestic vector, Aedes aegypti, there was no evidence of human-amplified transmission. Furthermore, the historic absence of YF in Asia, despite abundant Ae. aegypti and an immunologically naive human population, is unexplained. We tested the hypothesis that pre-existing, heterologous flavivirus immunity, specifically from dengue (DENV) and Zika (ZIKV) viruses, limits YFV viremia and transmission by Ae. aegypti. We infected cynomolgus macaques with DENV or ZIKV, then challenged them 6–9 months later with YFV. We then measured viremia and disease and allowed Ae. aegypti mosquitoes to feed during peak macaque viremia. Although prior heterologous immunity had variable effects on disease, DENV and ZIKV immunity consistently suppressed YFV viremia. Despite no statistical difference due to a small sample size, the suppression in viremia led to a significant reduction in Ae. aegypti infection and a lack of transmission potential. These results support the hypothesis that, in DENV- and ZIKV-endemic regions such as South America and Asia, human flavivirus immunity suppresses YFV human amplification potential, reducing the risk of urban outbreaks.https://doi.org/10.1038/s41467-024-54146-9
spellingShingle Divya P. Shinde
Jessica A. Plante
Dionna Scharton
Brooke Mitchell
Jordyn Walker
Sasha R. Azar
Rafael K. Campos
Lívia Sacchetto
Betânia P. Drumond
Nikos Vasilakis
Kenneth S. Plante
Scott C. Weaver
Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus
Nature Communications
title Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus
title_full Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus
title_fullStr Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus
title_full_unstemmed Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus
title_short Potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus
title_sort potential role of heterologous flavivirus immunity in preventing urban transmission of yellow fever virus
url https://doi.org/10.1038/s41467-024-54146-9
work_keys_str_mv AT divyapshinde potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT jessicaaplante potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT dionnascharton potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT brookemitchell potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT jordynwalker potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT sasharazar potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT rafaelkcampos potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT liviasacchetto potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT betaniapdrumond potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT nikosvasilakis potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT kennethsplante potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus
AT scottcweaver potentialroleofheterologousflavivirusimmunityinpreventingurbantransmissionofyellowfevervirus