Format

Send to

Choose Destination
Nat Microbiol. 2019 Dec 9. doi: 10.1038/s41564-019-0619-y. [Epub ahead of print]

Successive blood meals enhance virus dissemination within mosquitoes and increase transmission potential.

Author information

1
Center for Vector-Borne and Zoonotic Diseases, Department of Environmental Sciences, The Connecticut Agricultural Experiment Station, New Haven, CT, USA. philip.armstrong@ct.gov.
2
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT, USA. philip.armstrong@ct.gov.
3
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT, USA.
4
Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO, USA.
5
Center for Vector-Borne and Zoonotic Diseases, Department of Environmental Sciences, The Connecticut Agricultural Experiment Station, New Haven, CT, USA.
6
Department of Biomedical Sciences, Quinnipiac University, Hamden, CT, USA.
7
Department of Biostatistics, Yale School of Public Health, Yale University, New Haven, CT, USA.
8
Center for Vector-Borne and Zoonotic Diseases, Department of Environmental Sciences, The Connecticut Agricultural Experiment Station, New Haven, CT, USA. doug.brackney@ct.gov.
9
Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT, USA. doug.brackney@ct.gov.

Abstract

The recent Zika virus (ZIKV) and chikungunya virus epidemics highlight the explosive nature of arthropod-borne viruses (arboviruses) transmitted by Aedes spp. mosquitoes1,2. Vector competence and the extrinsic incubation period (EIP) are two key entomological parameters used to assess the public health risk posed by arboviruses3. 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)4. 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, R0, 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.

PMID:
31819213
DOI:
10.1038/s41564-019-0619-y

Supplemental Content

Full text links

Icon for Nature Publishing Group
Loading ...
Support Center