Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors

Russell, Tanya L., Beebe, Nigel W., Bugoro, Hugo, Apairamo, Allan, Chow, Weng K., Cooper, Robert D., Collins, Frank H., Lobo, Neil F., and Burkot, Thomas R. (2016) Frequent blood feeding enables insecticide-treated nets to reduce transmission by mosquitoes that bite predominately outdoors. Malaria Journal, 15. 156. pp. 1-9.

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Abstract

Background: The effectiveness of vector control on malaria transmission by long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) depends on the vectors entering houses to blood feed and rest when people are inside houses. In the Solomon Islands, significant reductions in malaria have been achieved in the past 20 years with insecticide-treated bed nets, IRS, improved diagnosis and treatment with artemisinin combination therapies; despite the preference of the primary vector, Anopheles farauti, to feed outdoors and early in the evening and thereby avoid potential exposure to insecticides. Rational development of tools to complement LLINs and IRS by attacking vectors outdoor requires detailed knowledge of the biology and behaviours of the target species.

Methods: Malaria transmission in Central Province, Solomon Islands was estimated by measuring the components comprising the entomological inoculation rate (EIR) as well as the vectorial capacity of An. farauti. In addition, the daily and seasonal biting behaviour of An. farauti, was examined and the duration of the feeding cycle was estimated with a mark-release-recapture experiment.

Results: Anopheles farauti was highly exophagic with 72 % captured by human landing catches (HLC) outside of houses. Three-quarters (76 %) of blood feeding on humans was estimated to occur before 21.00 h. When the hourly location of humans was considered, the proportion of exposure to mosquito bites on humans occurring indoors (πⁱ) was only 0.130 ± 0.129. Peak densities of host seeking An. farauti occurred between October and January. The annual EIR was estimated to be 2.5 for 2012 and 33.2 for 2013. The length of the feeding cycle was 2.1 days.

Conclusions: The short duration of the feeding cycle by this species offers an explanation for the substantial control of malaria that has been achieved in the Solomon Islands by LLINs and IRS. Anopheles farauti is primarily exophagic and early biting, with 13 % of mosquitoes entering houses to feed late at night during each feeding cycle. The two-day feeding cycle of An. farauti requires females to take 5–6 blood meals before the extrinsic incubation period (EIP) is completed; and this could translate into substantial population-level mortality by LLINs or IRS before females would be infectious to humans with Plasmodium falciparum and Plasmodium vivax. Although An. farauti is primarily exophagic, the indoor vector control tools recommended by the World Health Organization (LLINs and IRS) can still provide an important level of control. Nonetheless, elimination will likely require vector control tools that target other bionomic vulnerabilities to suppress transmission outdoors and that complement the control provided by LLINs and IRS.

Item ID: 43471
Item Type: Article (Research - C1)
ISSN: 1475-2875
Keywords: Anopheles farauti, Solomon Islands, bionomics, mark-release-recapture, feeding cycle, seasonality, biting profile
Additional Information:

© 2016 Russell et al.

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Funders: Bill and Melinda Gates Foundation (BMGF), National Institute of Allergy and Infectious Diseases (NIAID) of the National Institutes of Health for the International Center of Excellence in Malaria Research (NIH-ICEMR) Southwest Pacific
Projects and Grants: BMGF Grant No. 45114, NIAID U19AI08986
Research Data: http://dx.doi.org/10.4225/28/56C671268CF73
Date Deposited: 22 Jul 2016 03:54
FoR Codes: 31 BIOLOGICAL SCIENCES > 3109 Zoology > 310913 Invertebrate biology @ 50%
32 BIOMEDICAL AND CLINICAL SCIENCES > 3207 Medical microbiology > 320704 Medical parasitology @ 25%
42 HEALTH SCIENCES > 4203 Health services and systems > 420315 One health @ 25%
SEO Codes: 92 HEALTH > 9201 Clinical Health (Organs, Diseases and Abnormal Conditions) > 920109 Infectious Diseases @ 100%
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