Mechanical transmission of dengue virus by Aedes aegypti may influence disease transmission dynamics during outbreaks.

Aedes aegypti mosquito Animal models of dengue virus Dengue transmission Mathematical modelling of disease outbreak

Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Aug 2023
Historique:
received: 30 03 2023
revised: 02 07 2023
accepted: 06 07 2023
medline: 14 8 2023
pubmed: 25 7 2023
entrez: 24 7 2023
Statut: ppublish

Résumé

Dengue virus outbreaks are increasing in number and severity worldwide. Viral transmission is assumed to require a minimum time period of viral replication within the mosquito midgut. It is unknown if alternative transmission periods not requiring replication are possible. We used a mouse model of dengue virus transmission to investigate the potential of mechanical transmission of dengue virus. We investigated minimal viral titres necessary for development of symptoms in bitten mice and used resulting parameters to inform a new model of dengue virus transmission within a susceptible population. Naïve mice bitten by mosquitoes immediately after they took partial blood meals from dengue infected mice showed symptoms of dengue virus, followed by mortality. Incorporation of mechanical transmission into mathematical models of dengue virus transmission suggest that this supplemental transmission route could result in larger outbreaks which peak sooner. The potential of dengue transmission routes independent of midgut viral replication has implications for vector control strategies that target mosquito lifespan and suggest the possibility of similar mechanical transmission routes in other disease-carrying mosquitoes. This study was funded by grants from the National Health Research Institutes, Taiwan (04D2-MMMOST02), the Human Frontier Science Program (RGP0033/2021), the National Institutes of Health (1R01AI143698-01A1, R01AI151004 and DP2AI152071) and the Ministry of Science and Technology, Taiwan (MOST104-2321-B-400-016).

Sections du résumé

BACKGROUND BACKGROUND
Dengue virus outbreaks are increasing in number and severity worldwide. Viral transmission is assumed to require a minimum time period of viral replication within the mosquito midgut. It is unknown if alternative transmission periods not requiring replication are possible.
METHODS METHODS
We used a mouse model of dengue virus transmission to investigate the potential of mechanical transmission of dengue virus. We investigated minimal viral titres necessary for development of symptoms in bitten mice and used resulting parameters to inform a new model of dengue virus transmission within a susceptible population.
FINDINGS RESULTS
Naïve mice bitten by mosquitoes immediately after they took partial blood meals from dengue infected mice showed symptoms of dengue virus, followed by mortality. Incorporation of mechanical transmission into mathematical models of dengue virus transmission suggest that this supplemental transmission route could result in larger outbreaks which peak sooner.
INTERPRETATION CONCLUSIONS
The potential of dengue transmission routes independent of midgut viral replication has implications for vector control strategies that target mosquito lifespan and suggest the possibility of similar mechanical transmission routes in other disease-carrying mosquitoes.
FUNDING BACKGROUND
This study was funded by grants from the National Health Research Institutes, Taiwan (04D2-MMMOST02), the Human Frontier Science Program (RGP0033/2021), the National Institutes of Health (1R01AI143698-01A1, R01AI151004 and DP2AI152071) and the Ministry of Science and Technology, Taiwan (MOST104-2321-B-400-016).

Identifiants

pubmed: 37487418
pii: S2352-3964(23)00288-8
doi: 10.1016/j.ebiom.2023.104723
pmc: PMC10382859
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104723

Subventions

Organisme : NIAID NIH HHS
ID : DP2 AI152071
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI143698
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI151004
Pays : United States

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests OSA. is a founder of Agragene, Inc. with equity interest and a founder of Synvect with equity interest. The terms of this arrangement have been reviewed and approved by the University of California, San Diego in accordance with its conflict of interest policies. All remaining authors declare no competing interests.

Auteurs

Hsing-Han Li (HH)

National Mosquito-Borne Disease Control Research Center, NHRI, Miaoli, 350401, Taiwan; National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan; Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA, 92093, USA.

Matthew P Su (MP)

Graduate School of Science, Nagoya University, Nagoya, 464-8602, Japan; Institute for Advanced Research, Nagoya University, Nagoya, 464-8601, Japan.

Shih-Cheng Wu (SC)

National Mosquito-Borne Disease Control Research Center, NHRI, Miaoli, 350401, Taiwan; National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan; Department of Clinical Laboratory Sciences and Medical Biotechnology, College of Medicine, National Taiwan University, Taipei, 10048, Taiwan; Department of Laboratory Medicine, National Taiwan University Hospital, College of Medicine, National Taiwan University, Taipei, 10021, Taiwan.

Hsiao-Hui Tsou (HH)

Institute of Population Health Sciences, National Health Research Institutes, Zhunan, Miaoli, 350401, Taiwan; Graduate Institute of Biostatistics, College of Public Health, China Medical University, Taichung, 40402, Taiwan.

Meng-Chun Chang (MC)

Department of Life Science & Institute of Bioinformatics and Structural Biology, National Tsing Hua University, Hsinchu, Taiwan.

Yu-Chieh Cheng (YC)

Institute of Population Health Sciences, National Health Research Institutes, Zhunan, Miaoli, 350401, Taiwan.

Kuen-Nan Tsai (KN)

Institute of Molecular and Genomic Medicine, NHRI, Miaoli, 350401, Taiwan.

Hsin-Wei Wang (HW)

National Mosquito-Borne Disease Control Research Center, NHRI, Miaoli, 350401, Taiwan; National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan.

Guan-Hua Chen (GH)

National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan; Department of Biological Science and Technology, National Yang Ming Chiao Tung University, Hsinchu, 300, Taiwan.

Cheng-Kang Tang (CK)

National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan; Program of Plant Protection and Health, Academy of Circular Economy, National Chung Hsing University, Taichung, 402202, Taiwan.

Pei-Jung Chung (PJ)

National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan.

Wan-Ting Tsai (WT)

National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan.

Li-Rung Huang (LR)

Institute of Molecular and Genomic Medicine, NHRI, Miaoli, 350401, Taiwan.

Yueh Andrew Yueh (YA)

Institute of Biotechnology and Pharmaceutical Research, NHRI, Miaoli, 350401, Taiwan.

Hsin-Wei Chen (HW)

National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan.

Chao-Ying Pan (CY)

Department of Health, Kaohsiung City Government, Kaohsiung, 800852, Taiwan.

Omar S Akbari (OS)

Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA, 92093, USA.

Hsiao-Han Chang (HH)

Department of Life Science & Institute of Bioinformatics and Structural Biology, National Tsing Hua University, Hsinchu, Taiwan.

Guann-Yi Yu (GY)

National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan.

John M Marshall (JM)

Divisions of Biostatistics and Epidemiology, School of Public Health, University of California, Berkeley, CA, 94720, USA.

Chun-Hong Chen (CH)

National Mosquito-Borne Disease Control Research Center, NHRI, Miaoli, 350401, Taiwan; National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan. Electronic address: chunhong@gmail.com.

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