Dataset Information

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

ABSTRACT:

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).

SUBMITTER: Li HH

PROVIDER: S-EPMC10382859 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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Publications

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

Li Hsing-Han HH Su Matthew P MP Wu Shih-Cheng SC Tsou Hsiao-Hui HH Chang Meng-Chun MC Cheng Yu-Chieh YC Tsai Kuen-Nan KN Wang Hsin-Wei HW Chen Guan-Hua GH Tang Cheng-Kang CK Chung Pei-Jung PJ Tsai Wan-Ting WT Huang Li-Rung LR Yueh Yueh Andrew YA Chen Hsin-Wei HW Pan Chao-Ying CY Akbari Omar S OS Chang Hsiao-Han HH Yu Guann-Yi GY Marshall John M JM Chen Chun-Hong CH

EBioMedicine 20230722

<h4>Background</h4>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.<h4>Methods</h4>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 sy ...[more]

PMID: 37487418

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Project description:BackgroundMosquito-borne arboviruses are expanding their territory and elevating their infection prevalence due to the rapid climate change, urbanization, and increased international travel and global trade. Various significant arboviruses, including the dengue virus, Zika virus, Chikungunya virus, and yellow fever virus, are all reliant on the same primary vector, Aedes aegypti. Consequently, the occurrence of arbovirus coinfection in mosquitoes is anticipated. Arbovirus coinfection in mosquitoes has two patterns: simultaneous and sequential. Numerous studies have demonstrated that simultaneous coinfection of arboviruses in mosquitoes is unlikely to exert mutual developmental influence on these viruses. However, the viruses' interplay within a mosquito after the sequential coinfection seems intricated and not well understood.Methodology/principal findingsWe conducted experiments aimed at examining the phenomenon of arbovirus sequential coinfection in both mosquito cell line (C6/36) and A. aegypti, specifically focusing on dengue virus (DENV, serotype 2) and Zika virus (ZIKV). We firstly observed that DENV and ZIKV can sequentially infect mosquito C6/36 cell line, but the replication level of the subsequently infected ZIKV was significantly suppressed. Similarly, A. aegypti mosquitoes can be sequentially coinfected by these two arboviruses, regardless of the order of virus exposure. However, the replication, dissemination, and the transmission potential of the secondary virus were significantly inhibited. We preliminarily explored the underlying mechanisms, revealing that arbovirus-infected mosquitoes exhibited activated innate immunity, disrupted lipid metabolism, and enhanced RNAi pathway, leading to reduced susceptibility to the secondary arbovirus infections.Conclusions/significanceOur findings suggest that, in contrast to simultaneous arbovirus coinfection in mosquitoes that can promote the transmission and co-circulation of these viruses, sequential coinfection appears to have limited influence on arbovirus transmission dynamics. However, it is important to note that more experimental investigations are needed to refine and expand upon this conclusion.

Project description:Dengue virus serotype 4 (DENV-4) circulated in Aedes aegypti in 2016 and 2017 in Florida in the absence of human index cases, compelling a full assessment of local mosquito vector competence and DENV-4 risk. To better understand DENV-4 transmission risk in Florida, we used an expanded suite of tests to measure and compare the vector competencies of both an established colony of A. aegypti (Orlando strain [ORL]) and a field-derived colony from Collier County, FL, in 2018 (COL) for a Haitian DENV-4 human field isolate and a DENV-4 laboratory strain (Philippines H241). We immediately noted that ORL saliva positivity was higher for the field than for laboratory DENV-4 strains. In a subsequent comparison with the recent COL mosquito colony, we also observed significantly higher midgut infection of COL and ORL by the Haitian DENV-4 field strain and a significantly higher saliva positivity rate for COL, although overall saliva virus titers were similar between the two. These data point to a potential midgut infection barrier for the DENV-4 laboratory strain for both mosquito colonies and indicate that the marked differences in transmission potential estimates hinge on virus-vector combinations. Our study highlights the importance of leveraging an expanded suite of testing methods with emphasis on utilizing local mosquito populations and field-relevant dengue virus serotypes and strains to accurately estimate transmission risk in a given setting. IMPORTANCE DENV-4 was found circulating in Florida (FL) A. aegypti mosquitoes in the absence of human index cases in the state (2016 to 2017). How DENV-4 was maintained locally is unclear, presenting a major gap in our understanding of DENV-4 public health risk. We determined the baseline arbovirus transmission potential of laboratory and field colonies of A. aegypti for both laboratory and field isolates of DENV-4. We observed a high transmission potential of field populations of A. aegypti and evidence of higher vertical transmission of the DENV-4 field isolate, providing clues to the possible mechanism of undetected DENV-4 maintenance in the state. Our findings also move the field forward in the development of best practices for evaluating arbovirus vector competence, with evidence that transmission potential estimates vary depending on the mosquito-virus combinations. These data emphasize the poor suitability of laboratory-established virus strains and the high relevance of field-derived mosquito populations in estimating transmission risk.

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Dataset Information

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

Background

Methods

Findings

Interpretation

Funding

Publications

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

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