Successive Bloodmeals Enhance Virus Dissemination within Mosquitoes and Increase Transmission Potential

Armstrong, Philip M.; Ehrlich, Hanna Y.; Magalhaes, Tereza; Miller, Megan R.; Conway, Patrick J.; Bransfield, Angela; Misencik, Michael J.; Gloria-Soria, Andrea; Warren, Joshua L.; Andreadis, Theodore G.; Shepard, John J.; Foy, Brian D.; Pitzer, Virginia E.; Brackney, Doug E.

doi:10.1038/s41564-019-0619-y

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Successive Bloodmeals Enhance Virus Dissemination within Mosquitoes and Increase Transmission Potential

2 2020
By Armstrong, Philip M. ; Ehrlich, Hanna Y. ; Magalhaes, Tereza ; ...
http://dx.doi.org/10.1038/s41564-019-0619-y
Source: Nat Microbiol. 5(2):239-247

[PDF-2.57 MB]

English

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Details:

Alternative Title:

Nat Microbiol
Personal Author:

Armstrong, Philip M. ; Ehrlich, Hanna Y. ; Magalhaes, Tereza ; Miller, Megan R. ; Conway, Patrick J. ; ... More +

Armstrong, Philip M. ; Ehrlich, Hanna Y. ; Magalhaes, Tereza ; Miller, Megan R. ; Conway, Patrick J. ; Bransfield, Angela ; Misencik, Michael J. ; Gloria-Soria, Andrea ; Warren, Joshua L. ; Andreadis, Theodore G. ; Shepard, John J. ; Foy, Brian D. ; Pitzer, Virginia E. ; Brackney, Doug E. Less -
Description:

The recent Zika virus (ZIKV) and chikungunya virus epidemics highlight the explosive nature of arthropod-borne viruses (arboviruses) transmitted by Aedes spp. mosquitoes|. Vector competence and the extrinsic incubation period (EIP) are two key entomological parameters used to assess the public health risk posed by arboviruses|. These are typically measured empirically by offering mosquitoes an infectious blood meal and temporally sampling mosquitoes to determine the infection and transmission status. This approach has been used for the better part of a century; however, it does not accurately capture the biology and behaviour of many mosquito vectors that refeed frequently (every 2-3 d)|. Here, we demonstrate that acquisition of a second non-infectious blood meal significantly shortens the EIP of ZIKV-infected Aedes aegypti by enhancing virus dissemination from the mosquito midgut. Similarly, a second blood meal increases the competence of this species for dengue virus and chikungunya virus as well as Aedes albopictus for ZIKV, suggesting that this phenomenon may be common among other virus-vector pairings and that A. albopictus might be a more important vector than once thought. Blood-meal-induced microperforations in the virus-impenetrable basal lamina that surrounds the midgut provide a mechanism for enhanced virus escape. Modelling of these findings reveals that a shortened EIP would result in a significant increase in the basic reproductive number, R|, estimated from experimental data. This helps to explain how A. aegypti can sustain explosive epidemics such as ZIKV despite relatively poor vector competence in single-feed laboratory trials. Together, these data demonstrate a direct and unrecognized link between mosquito feeding behaviour, EIP and vector competence.
Keywords:

[+]

Aedes Animals Arbovirus Infections Basic Reproduction Number Chikungunya Fever Dengue Digestive System Female Host Microbial Interactions Humans Male Mice Microscopy, Electron, Scanning Models, Biological Mosquito Vectors Zika Virus Infection
Source:

Nat Microbiol. 5(2):239-247
Pubmed ID:

31819213
Pubmed Central ID:

PMC7199921
Document Type:

Journal Article
Funding:

UL1 TR001863/TR/NCATS NIH HHSUnited States/ ; R01 AI112970/AI/NIAID NIH HHSUnited States/ ; R21 AI129464/AI/NIAID NIH HHSUnited States/ ; KL2 TR001862/TR/NCATS NIH HHSUnited States/ ; U01 CK000509/CK/NCEZID CDC HHSUnited States/

UL1 TR001863/TR/NCATS NIH HHSUnited States/ ; R01 AI112970/AI/NIAID NIH HHSUnited States/ ; R21 AI129464/AI/NIAID NIH HHSUnited States/ ; KL2 TR001862/TR/NCATS NIH HHSUnited States/ ; U01 CK000509/CK/NCEZID CDC HHSUnited States/ Less -
Collection(s):

CDC Public Access
Main Document Checksum:

[+]

urn:sha256:d3d68609d77f429838492dd41f771f4263b1cd4790792539bec6d7277d80aebc
Download URL:

https://stacks.cdc.gov/view/cdc/87622/cdc_87622_DS1.pdf
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