Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island

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Abstract

Background Vector control through indoor residual spraying (IRS) has been employed on Bioko Island, Equatorial Guinea, under the Bioko Island Malaria Control Project (BIMCP) since 2004. This study analyses the change in mosquito abundance, species composition and outdoor host-seeking proportions from 2009 to 2014, after 11 years of vector control on Bioko Island. Methods All-night indoor and outdoor human landing catches were performed monthly in the Bioko Island villages of Mongola, Arena Blanca, Biabia and Balboa from 2009 to 2014. Collected mosquitoes were morphologically identified and a subset of Anopheles gambiae sensu lato (s.l.) were later identified molecularly to their sibling species. Mosquito collection rates, species composition and indoor/outdoor host-seeking sites were analysed using generalized linear mixed models to assess changes in mosquito abundance and behaviour. Results The overall mosquito collection rate declined in each of the four Bioko Island villages. Anopheles coluzzii and Anopheles melas comprised the An. gambiae s.l. mosquito vector population, with a range of species proportions across the four villages. The proportion of outdoor host-seeking An. gambiae s.l. mosquitoes increased significantly in all four villages with an average increase of 58.8 % [57.9, 59.64 %] in 2009 to 70.0 % [67.8, 72.0 %] in 2014. Outdoor host-seeking rates did not increase in the month after an IRS spray round compared to the month before, suggesting that insecticide repellency has little impact on host-seeking behaviour. Conclusion While vector control on Bioko Island has succeeded in substantial reduction in overall vector biting rates, populations of An. coluzzii and An. melas persist. Host-seeking behaviour has changed in these An. gambiae s.l. populations, with a shift towards outdoor host-seeking. During this study period, the proportion of host-seeking An. gambiae s.l. caught outdoors observed on Bioko Island increased to high levels, exceeding 80 % in some locations. It is possible that there may be a genetic basis underlying this large shift in host-seeking behaviour, in which case outdoor feeding could pose a serious threat to current vector control programmes. Currently, the BIMCP is preparing for this potential challenge by testing source reduction as a complementary control effort that also targets outdoor transmission. Electronic supplementary material The online version of this article (doi:10.1186/s12936-016-1286-6) contains supplementary material, which is available to authorized users.

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Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania

Tanya Russell, Nicodem Govella, Salum Azizi … (2011)

Background Insecticide-treated nets (ITNs) and indoor residual spraying (IRS) represent the front-line tools for malaria vector control globally, but are optimally effective where the majority of baseline transmission occurs indoors. In the surveyed area of rural southern Tanzania, bed net use steadily increased over the last decade, reducing malaria transmission intensity by 94%. Methods Starting before bed nets were introduced (1997), and then after two milestones of net use had been reached-75% community-wide use of untreated nets (2004) and then 47% use of ITNs (2009)-hourly biting rates of malaria vectors from the Anopheles gambiae complex and Anopheles funestus group were surveyed. Results In 1997, An. gambiae s.l. and An. funestus mosquitoes exhibited a tendency to bite humans inside houses late at night. For An. gambiae s.l., by 2009, nocturnal activity was less (p = 0.0018). At this time, the sibling species composition of the complex had shifted from predominantly An. gambiae s.s. to predominantly An. arabiensis. For An. funestus, by 2009, nocturnal activity was less (p = 0.0054) as well as the proportion biting indoors (p < 0.0001). At this time, An. funestus s.s. remained the predominant species within this group. As a consequence of these altered feeding patterns, the proportion (mean ± standard error) of human contact with mosquitoes (bites per person per night) occurring indoors dropped from 0.99 ± 0.002 in 1997 to 0.82 ± 0.008 in 2009 for the An. gambiae complex (p = 0.0143) and from 1.00 ± <0.001 to only 0.50 ± 0.048 for the An. funestus complex (p = 0.0004) over the same time period. Conclusions High usage of ITNs can dramatically alter African vector populations so that intense, predominantly indoor transmission is replaced by greatly lowered residual transmission, a greater proportion of which occurs outdoors. Regardless of the underlying mechanism, the residual, self-sustaining transmission will respond poorly to further insecticidal measures within houses. Additional vector control tools which target outdoor biting mosquitoes at the adult or immature stages are required to complement ITNs and IRS.

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The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis

Marianne Sinka, Michael J Bangs, Sylvie Manguin … (2011)

Background This is the second in a series of three articles documenting the geographical distribution of 41 dominant vector species (DVS) of human malaria. The first paper addressed the DVS of the Americas and the third will consider those of the Asian Pacific Region. Here, the DVS of Africa, Europe and the Middle East are discussed. The continent of Africa experiences the bulk of the global malaria burden due in part to the presence of the An. gambiae complex. Anopheles gambiae is one of four DVS within the An. gambiae complex, the others being An. arabiensis and the coastal An. merus and An. melas. There are a further three, highly anthropophilic DVS in Africa, An. funestus, An. moucheti and An. nili. Conversely, across Europe and the Middle East, malaria transmission is low and frequently absent, despite the presence of six DVS. To help control malaria in Africa and the Middle East, or to identify the risk of its re-emergence in Europe, the contemporary distribution and bionomics of the relevant DVS are needed. Results A contemporary database of occurrence data, compiled from the formal literature and other relevant resources, resulted in the collation of information for seven DVS from 44 countries in Africa containing 4234 geo-referenced, independent sites. In Europe and the Middle East, six DVS were identified from 2784 geo-referenced sites across 49 countries. These occurrence data were combined with expert opinion ranges and a suite of environmental and climatic variables of relevance to anopheline ecology to produce predictive distribution maps using the Boosted Regression Tree (BRT) method. Conclusions The predicted geographic extent for the following DVS (or species/suspected species complex*) is provided for Africa: Anopheles (Cellia) arabiensis, An. (Cel.) funestus*, An. (Cel.) gambiae, An. (Cel.) melas, An. (Cel.) merus, An. (Cel.) moucheti and An. (Cel.) nili*, and in the European and Middle Eastern Region: An. (Anopheles) atroparvus, An. (Ano.) labranchiae, An. (Ano.) messeae, An. (Ano.) sacharovi, An. (Cel.) sergentii and An. (Cel.) superpictus*. These maps are presented alongside a bionomics summary for each species relevant to its control.

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Characterizing, controlling and eliminating residual malaria transmission

Gerry F. Killeen (2014)

Long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) interventions can reduce malaria transmission by targeting mosquitoes when they feed upon sleeping humans and/or rest inside houses, livestock shelters or other man-made structures. However, many malaria vector species can maintain robust transmission, despite high coverage of LLINs/IRS containing insecticides to which they are physiologically fully susceptible, because they exhibit one or more behaviours that define the biological limits of achievable impact with these interventions: (1) Natural or insecticide-induced avoidance of contact with treated surfaces within houses and early exit from them, thus minimizing exposure hazard of vectors which feed indoors upon humans; (2) Feeding upon humans when they are active and unprotected outdoors, thereby attenuating personal protection and any consequent community-wide suppression of transmission; (3) Feeding upon animals, thus minimizing contact with insecticides targeted at humans or houses; (4) Resting outdoors, away from insecticide-treated surfaces of nets, walls and roofs. Residual malaria transmission is, therefore, defined as all forms of transmission that can persist after achieving full universal coverage with effective LLINs and/or IRS containing active ingredients to which local vector populations are fully susceptible. Residual transmission is sufficiently intense across most of the tropics to render malaria elimination infeasible without new or improved vector control methods. Many novel or improved vector control strategies to address residual transmission are emerging that either: (1) Enhance control of adult vectors that enter houses to feed and/or rest by killing, repelling or excluding them; (2) Kill or repel adult mosquitoes when they attack people outdoors; (3) Kill adult mosquitoes when they attack livestock; (4) Kill adult mosquitoes when they feed upon sugar or; (5) Kill immature mosquitoes in aquatic habitats. To date, none of these options has sufficient supporting evidence to justify full-scale programmatic implementation. Concerted investment in their rigorous selection, development and evaluation is required over the coming decade to enable control and, ultimately, elimination of residual malaria transmission. In the meantime, national programmes may assess options for addressing residual transmission under programmatic conditions through pilot studies with strong monitoring, evaluation and operational research components, similar to the Onchocerciasis Control Programme.

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Author and article information

Contributors

Jacob I. Meyers: jacob.i.meyers@gmail.com

Sharmila Pathikonda: sharmilapathikonda@yahoo.com

Zachary R. Popkin-Hall: zachary.popkin@gmail.com

Matthew C. Medeiros: matthewcimedeiros@tamu.edu

Godwin Fuseini: gfuseini@mcd.org

Abrahan Matias: amatias@mcd.org

Guillermo Garcia: guillermo.garcia-contreras1@student.lshtm.ac.uk

Hans J. Overgaard: hans.overgaard@umb.no

Vani Kulkarni: vaninova@gmail.com

Vamsi P. Reddy: vamsi.rio@gmail.com

Christopher Schwabe: cschwabe@mcd.org

Jo Lines: jo.lines@lshtm.ac.uk

Immo Kleinschmidt: immo.kleinschmidt@lshtm.ac.uk

Michel A. Slotman: maslotman@tamu.edu

Journal

Journal ID (nlm-ta): Malar J

Journal ID (iso-abbrev): Malar. J

Title: Malaria Journal

Publisher: BioMed Central (London )

ISSN (Electronic): 1475-2875

Publication date (Electronic): 26 April 2016

Publication date PMC-release: 26 April 2016

Publication date Collection: 2016

Volume: 15

Electronic Location Identifier: 239

Affiliations

[ ]Department of Entomology, Texas A&M University, College Station, TX USA

[ ]Medical Care Development International, Malabo, Equatorial Guinea

[ ]Department of Mathematical Sciences and Technology, Norwegian University of Life Sciences, Ås, Norway

[ ]Institut de Recherche Pour Le Développement (IRD), MIVEGEC, Montpellier, France

[ ]Department of Entomology, Faculty of Agriculture, Kasetsart University, Bangkok, Thailand

[ ]Medical Care Development International, Silver Spring, MD USA

[ ]MRC Tropical Epidemiology Group, London School of Hygiene and Tropical Medicine, London, UK

[ ]School of Pathology, Faculty of Health Sciences, University of Witwatersrand, Johannesburg, South Africa

Article

Publisher ID: 1286

DOI: 10.1186/s12936-016-1286-6

PMC ID: 4845310

PubMed ID: 27113244

SO-VID: 7c3159f0-4e3d-4fa8-8711-768b4e0f2503

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Open AccessThis 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.

History

Date received : 6 January 2016

Date accepted : 13 April 2016

Funding

Funded by: Bioko Island Malaria Control Project

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ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: outdoor host-seeking,anopheles gambiae,anopheles coluzzii,anopheles melas,bioko island,equatorial guinea,bioko island malaria control project,indoor residual spraying,vector control

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ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: outdoor host-seeking, anopheles gambiae, anopheles coluzzii, anopheles melas, bioko island, equatorial guinea, bioko island malaria control project, indoor residual spraying, vector control

Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island

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Most cited references 26

Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania

The dominant Anopheles vectors of human malaria in Africa, Europe and the Middle East: occurrence data, distribution maps and bionomic précis

Characterizing, controlling and eliminating residual malaria transmission

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