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Going Beyond Personal Protection Against Mosquito Bites to Eliminate Analysis BMJ Glob Health: first published as 10.1136/bmjgh-2016-000198 on 26 April 2017. Downloaded from Going beyond personal protection against mosquito bites to eliminate malaria transmission: population suppression of malaria vectors that exploit both human and animal blood Gerry F Killeen,1,2 Samson S Kiware,1 Fredros O Okumu,1,3 Marianne E Sinka,4 Catherine L Moyes,5 N Claire Massey,4 Peter W Gething,5 John M Marshall,6 Carlos J Chaccour,7,8 Lucy S Tusting5 To cite: Killeen GF, ABSTRACT Key questions Kiware SS, Okumu FO, et al. Protecting individuals and households against Going beyond personal mosquito bites with long-lasting insecticidal nets protection against mosquito What is already known about this topic? (LLINs) or indoor residual spraying (IRS) can suppress bites to eliminate malaria ▸ The only significant infectious reservoirs for the transmission: population entire populations of unusually efficient malaria vector two most common human malaria parasites are suppression of malaria species that predominantly feed indoors on humans. other humans, so most of the world’s infection vectors that exploit both Mosquitoes which usually feed on animals are less burden is mediated by a small number of highly human and animal blood. reliant on human blood, so they are far less vulnerable efficient vector mosquitoes that predominantly feed BMJ Global Health 2017;2: to population suppression effects of such human- on humans. e000198. doi:10.1136/ targeted insecticidal measures. Fortunately, the dozens ▸ Fortunately, these extraordinarily efficient malaria bmjgh-2016-000198 of mosquito species which primarily feed on animals vectors are also highly vulnerable to attack with are also relatively inefficient vectors of malaria, so insecticidal personal protection measures for personal protection against mosquito bites may be humans, such as long-lasting insecticidal nets Received 26 September 2016 sufficient to eliminate transmission. However, a handful (LLINs) and indoor residual spraying (IRS), which Revised 9 November 2016 of mosquito species are particularly problematic can suppress or even eliminate entire populations Accepted 13 November 2016 vectors of residual malaria transmission, because they of such human-dependent mosquitoes. http://gh.bmj.com/ feed readily on both humans and animals. These ▸ A larger number of malaria vector species strongly unusual vectors feed often enough on humans to be prefer feeding on animals, so they are far less vul- potent malaria vectors, but also often enough on nerable to population suppression with LLINs, IRS animals to evade population control with LLINs, IRS or or any other insecticidal personal protection any other insecticidal personal protection measure measure. However, they are also far less efficient targeted only to humans. Anopheles arabiensis and vectors, so personal protection alone may be suffi- on September 28, 2021 by guest. Protected copyright. A. coluzzii in Africa, A. darlingi in South America and cient to eliminate the transmission they mediate. A. farauti in Oceania, as well as A. culicifacies species E, A. fluviatilis species S, A. lesteri and A. minimus in What are the new findings? Asia, all feed readily on either humans or animals and ▸ If malaria is ever to be eliminated, the one of the collectively mediate residual malaria transmission greatest vector control challenges ahead is pre- across most of the tropics. Eliminating malaria sented by a small number of vector species which transmission by vectors exhibiting such dual host feed readily on both humans and animals. preferences will require aggressive mosquito Mosquitoes with such flexible, dual feeding prefer- population abatement, rather than just personal ences can feed frequently enough on humans to protection of humans. Population suppression of even mediate intense residual malaria transmission, but these particularly troublesome vectors is achievable often enough on animals to evade mass population with a variety of existing vector control technologies suppression with LLINs, IRS or any other insecti- that remain underdeveloped or underexploited. cidal personal protection measures for humans. ▸ Anopheles arabiensis and A. coluzzii in Africa, A. For numbered affiliations see darlingi in South America and A. farauti in Oceania, end of article. as well as Anopheles culicifacies species E, A. flu- INTRODUCTION viatilis species S, A. lesteri and A. minimus in Asia, The global distribution of malaria is over- all feed readily on either humans or animals. Correspondence to Collectively, these eight species dominate residual Gerry Killeen; whelmingly determined by environmental malaria transmission across most of the tropics. [email protected] factors, particularly climate and the Killeen GF, et al. BMJ Glob Health 2017;2:e000198. doi:10.1136/bmjgh-2016-000198 1 BMJ Global Health BMJ Glob Health: first published as 10.1136/bmjgh-2016-000198 on 26 April 2017. Downloaded from their preferred blood source.2411Figure 1 illustrates Key questions how A. funestus and A. gambiae consistently feed predom- Recommendations for policy inantly on human blood throughout their range. This, together with the fact that these two vector species tend ▸ Eliminating malaria transmission by these eight exceptionally to bite humans while they are sleeping indoors in the important vectors will require aggressive mosquito abatement, middle of the night,12 means that IRS and LLIN cam- to kill entire vector populations en masse, rather than just per- paigns can have dramatic effects on both these sonal or household protection of humans. species.2411Indeed both species have been eliminated ▸ A number of existing and emerging vector control technolo- or almost eliminated from a range of African settings gies are available, which target mosquitoes when they feed on 24 fi animals or during other life cycle stages, and could achieve with LLINs or IRS. In the Paci c, Anopheles punctula- population abatement of even these particularly troublesome tus, as well as its sibling species A. koliensis and A. farauti, vectors. can readily feed on pigs, but such alternative hosts are ▸ Development and evaluation of these underexploited alterna- scarce across much of their range, so they also often rely tives to LLINs and IRS is urgently needed, and requires imme- predominantly on humans for blood (figure 1). An. diate strategic investment if the long-term goal of malaria farauti can persist despite high coverage with LLINs and eradication is ever to be achieved. IRS, even where pigs are scarce, by feeding on humans outdoors in the early evening.413However, 12 A. punctulatus and A. koliensis that feed at night when behavioural characteristics of local mosquito vectors. humans are indoors can be very vulnerable to these The two most important species of human malaria para- measures, and have even been eliminated from some of sites (Plasmodium falciparum and P. vivax) are both strict the Solomon Islands.4 fi anthroponoses with no signi cant animal reservoir, so the It has long been noted that feeding in the middle of more a mosquito species feeds on humans, the more effi- 1–3 the night, when most people are usually asleep indoors, cient it will be as a vector of malaria. The vast bulk of appears to be a behavioural specialisation of mosquitoes ’ the world s malaria burden therefore occurs in the which regularly feed on humans.214Indeed it is the late- poorest, least-developed countries of Africa and Oceania, night foraging activity peaks of African vectors, rather where a small number of unusually efficient malaria 12 than any particular preference for feeding indoors, that vectors have evolved to specialise in feeding on humans. cause most of their encounters with humans to occur Fortunately, this exceptional propensity to attack people indoors so LLINs and IRS are highly effective.12 While also makes them vulnerable to attack with insecticidal mea- 24 these preferred nocturnal feeding times ensure that sures for protecting humans against bites. protection measures like LLINs and IRS effectively target most of the times and locations when exposure Population suppression of human-dependent vectors would otherwise occur, it is the associated strong pre- through insecticidal personal protection ference for humans that ensures that protection for http://gh.bmj.com/ Malaria vector control with long-lasting insecticidal nets the human user reduces vector survival at population – – (LLINs) and/or indoor residual spraying (IRS) accounts level.2 41517 for most of the malaria cases and malaria-related deaths In fact, the vulnerability to IRS and LLINs of A. funestus averted over recent years.56These strategies can provide and A. gambiae in Africa, as well as An. punctulatus and far more than just personal protection, by suppressing A. koliensis in the Pacific, is so striking that it has been the densities and survival rates of entire vector popula- suggested that Allee effects may occur in mosquito on September 28, 2021 by guest. Protected copyright. – tions.7 9 This mosquito population suppression function populations.4 Allee effects are widespread among a is often referred to as mosquito population abatement diversity of animals, plants and microbes, and arise when and causes an epidemiological mass effect on malaria the fitness of individuals depends on overall population transmission across entire communities. While the mos- size or density.18 19 Consequently, a population can quito population abatement function of LLINs and IRS rapidly collapse once
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