Mechanical transmission of dengue virus by Aedes aegypti may influence disease transmission dynamics during outbreaksResearch in context

Hsing-Han Li; Matthew P. Su; Shih-Cheng Wu; Hsiao-Hui Tsou; Meng-Chun Chang; Yu-Chieh Cheng; Kuen-Nan Tsai; Hsin-Wei Wang; Guan-Hua Chen; Cheng-Kang Tang; Pei-Jung Chung; Wan-Ting Tsai; Li-Rung Huang; Yueh Andrew Yueh; Hsin-Wei Chen; Chao-Ying Pan; Omar S. Akbari; Hsiao-Han Chang; Guann-Yi Yu; John M. Marshall; Chun-Hong Chen

EBioMedicine (Aug 2023)

Mechanical transmission of dengue virus by Aedes aegypti may influence disease transmission dynamics during outbreaksResearch in context

Hsing-Han Li,
Matthew P. Su,
Shih-Cheng Wu,
Hsiao-Hui Tsou,
Meng-Chun Chang,
Yu-Chieh Cheng,
Kuen-Nan Tsai,
Hsin-Wei Wang,
Guan-Hua Chen,
Cheng-Kang Tang,
Pei-Jung Chung,
Wan-Ting Tsai,
Li-Rung Huang,
Yueh Andrew Yueh,
Hsin-Wei Chen,
Chao-Ying Pan,
Omar S. Akbari,
Hsiao-Han Chang,
Guann-Yi Yu,
John M. Marshall,
Chun-Hong Chen

Affiliations

Hsing-Han Li: 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: Graduate School of Science, Nagoya University, Nagoya, 464-8602, Japan; Institute for Advanced Research, Nagoya University, Nagoya, 464-8601, Japan
Shih-Cheng Wu: 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: 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: Department of Life Science & Institute of Bioinformatics and Structural Biology, National Tsing Hua University, Hsinchu, Taiwan
Yu-Chieh Cheng: Institute of Population Health Sciences, National Health Research Institutes, Zhunan, Miaoli, 350401, Taiwan
Kuen-Nan Tsai: Institute of Molecular and Genomic Medicine, NHRI, Miaoli, 350401, Taiwan
Hsin-Wei Wang: 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: 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: 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: National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan
Wan-Ting Tsai: National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan
Li-Rung Huang: Institute of Molecular and Genomic Medicine, NHRI, Miaoli, 350401, Taiwan
Yueh Andrew Yueh: Institute of Biotechnology and Pharmaceutical Research, NHRI, Miaoli, 350401, Taiwan
Hsin-Wei Chen: National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan
Chao-Ying Pan: Department of Health, Kaohsiung City Government, Kaohsiung, 800852, Taiwan
Omar S. Akbari: Division of Biological Sciences, Section of Cell and Developmental Biology, University of California, San Diego, La Jolla, CA, 92093, USA
Hsiao-Han Chang: Department of Life Science & Institute of Bioinformatics and Structural Biology, National Tsing Hua University, Hsinchu, Taiwan
Guann-Yi Yu: National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan
John M. Marshall: Divisions of Biostatistics and Epidemiology, School of Public Health, University of California, Berkeley, CA, 94720, USA
Chun-Hong Chen: National Mosquito-Borne Disease Control Research Center, NHRI, Miaoli, 350401, Taiwan; National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan; Corresponding author. National Institute of Infectious Diseases and Vaccinology, NHRI, Miaoli, 350401, Taiwan.

Journal volume & issue: Vol. 94
p. 104723

Abstract

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Summary: 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: 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: 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: 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: 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).

Published in EBioMedicine

ISSN: 2352-3964 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General)
Website: http://www.journals.elsevier.com/ebiomedicine/

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