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

Abstract

BackgroundThe 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.MethodsMalaria 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.ResultsAnopheles 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.ConclusionsThe 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.

Increasingly inbred and fragmented populations ofPlasmodium vivaxwith declining transmission

“…These village "neighbourhoods" of parasite lineages appear to emanate from within-household co-transmission of highly related parasites. This radius of high genetic relatedness is consistent with the mosquito flight path (Charlwood, et al 1988;Russell, et al 2016). Thus, the fine scale patterns of population structure detected are likely to be driven by mosquito movement, rather than that of the human host.…”

“…Despite the principal vector in Solomon Islands, Anopheles farauti, feeding outdoors (Russell, et al 2016), much of the exposure to infective bites remains highly clustered around homes. This vector behaviour is considered to be a major challenge for elimination, but our data suggests that interventions focused on index households (e.g.…”

The diversity of Anopheles blood feeding patterns suggests different malaria protection strategies in different localities

“…In conclusion, this study suggests four important findings for public health control: (1) API may be significantly lower at the provincial level compared to the sub-district level and varied accordingly, suggesting that malaria foci may be maintained in a locality from a provincial level, especially in areas of low to moderate endemicity; (2) the importance of mosquito abundance information may reflect malaria incidence rate in a location 42,43 ;…”

“…It has been shown that the distribution of ITNs is responsible for a reduction of 68% in malaria burden in sub-Saharan Africa 1 . This control method has been widely distributed and a dramatic increase in use has resulted in the mass utilization of ITNs in many countries 2,3 . Additionally, personal protection has been found to be effective against mosquito bites and its use has led to a reduction in malaria infection 4-6 .…”

Modelling the impact of the long-term use of insecticide-treated bed nets on Anopheles mosquito biting time

“…It should, therefore, have been expected that endophilic malaria vectors, such as A. gambiae and A. funestus would gradually change their feeding and resting behaviour as a reaction against the current strategies of indoor spreading of insecticides and the distribution of ITNs. In fact, evidence of changes in biting and resting behaviour of malaria vectors, have been mounting up in recent years [ 9 – 13 ]. The presence of outdoor-activity, early-biting malaria vectors have been reported in many countries in Africa, such as Benin [ 14 ], Tanzania [ 15 ], Kenya [ 16 – 18 ], Nigeria [ 19 ], Uganda [ 20 ], Gambia [ 21 ], Ghana [ 22 ] and Rwanda [ 23 ], amongst others.…”