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      Evaluating putative repellent ‘push’ and attractive ‘pull’ components for manipulating the odour orientation of host-seeking malaria vectors in the peri-domestic space

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          Abstract

          Background

          Novel malaria vector control approaches aim to combine tools for maximum protection. This study aimed to evaluate novel and re-evaluate existing putative repellent ‘push’ and attractive ‘pull’ components for manipulating the odour orientation of malaria vectors in the peri-domestic space.

          Methods

          Anopheles arabiensis outdoor human landing catches and trap comparisons were implemented in large semi-field systems to (i) test the efficacy of Citriodiol ® or transfluthrin-treated fabric strips positioned in house eave gaps as push components for preventing bites; (ii) understand the efficacy of MB5-baited Suna-traps in attracting vectors in the presence of a human being; (iii) assess 2-butanone as a CO 2 replacement for trapping; (iv) determine the protection provided by a full push-pull set up. The air concentrations of the chemical constituents of the push–pull set-up were quantified.

          Results

          Microencapsulated Citriodiol ® eave strips did not provide outdoor protection against host-seeking An. arabiensis. Transfluthrin-treated strips reduced the odds of a mosquito landing on the human volunteer (OR 0.17; 95% CI 0.12–0.23). This impact was lower (OR 0.59; 95% CI 0.52–0.66) during the push-pull experiment, which was associated with low nighttime temperatures likely affecting the transfluthrin vaporisation. The MB5-baited Suna trap supplemented with CO 2 attracted only a third of the released mosquitoes in the absence of a human being; however, with a human volunteer in the same system, the trap caught < 1% of all released mosquitoes. The volunteer consistently attracted over two-thirds of all mosquitoes released. This was the case in the absence (‘pull’ only) and in the presence of a spatial repellent (‘push-pull’), indicating that in its current configuration the tested ‘pull’ does not provide a valuable addition to a spatial repellent. The chemical 2-butanone was ineffective in replacing CO 2. Transfluthrin was detectable in the air space but with a strong linear reduction in concentrations over 5 m from release. The MB5 constituent chemicals were only irregularly detected, potentially suggesting insufficient release and concentration in the air for attraction.

          Conclusion

          This step-by-step evaluation of the selected ‘push’ and ‘pull’ components led to a better understanding of their ability to affect host-seeking behaviours of the malaria vector An. arabiensis in the peri-domestic space and helps to gauge the impact such tools would have when used in the field for monitoring or control.

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          The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015

          Since the year 2000, a concerted campaign against malaria has led to unprecedented levels of intervention coverage across sub-Saharan Africa. Understanding the effect of this control effort is vital to inform future control planning. However, the effect of malaria interventions across the varied epidemiological settings of Africa remains poorly understood owing to the absence of reliable surveillance data and the simplistic approaches underlying current disease estimates. Here we link a large database of malaria field surveys with detailed reconstructions of changing intervention coverage to directly evaluate trends from 2000 to 2015 and quantify the attributable effect of malaria disease control efforts. We found that Plasmodium falciparum infection prevalence in endemic Africa halved and the incidence of clinical disease fell by 40% between 2000 and 2015. We estimate that interventions have averted 663 (542–753 credible interval) million clinical cases since 2000. Insecticide-treated nets, the most widespread intervention, were by far the largest contributor (68% of cases averted). Although still below target levels, current malaria interventions have substantially reduced malaria disease incidence across the continent. Increasing access to these interventions, and maintaining their effectiveness in the face of insecticide and drug resistance, should form a cornerstone of post-2015 control strategies.
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            The use of push-pull strategies in integrated pest management.

            Push-pull strategies involve the behavioral manipulation of insect pests and their natural enemies via the integration of stimuli that act to make the protected resource unattractive or unsuitable to the pests (push) while luring them toward an attractive source (pull) from where the pests are subsequently removed. The push and pull components are generally nontoxic. Therefore, the strategies are usually integrated with methods for population reduction, preferably biological control. Push-pull strategies maximize efficacy of behavior-manipulating stimuli through the additive and synergistic effects of integrating their use. By orchestrating a predictable distribution of pests, efficiency of population-reducing components can also be increased. The strategy is a useful tool for integrated pest management programs reducing pesticide input. We describe the principles of the strategy, list the potential components, and present case studies reviewing work on the development and use of push-pull strategies in each of the major areas of pest control.
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              Characterizing, controlling and eliminating residual malaria transmission

              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
                mnjoroge@icipe.org
                ufillinger@icipe.org
                adamsaddler.as@gmail.com
                smoore@ihi.or.tz
                willem.takken@wur.nl
                joop.vanloon@wur.nl
                Alexandra.Hiscox@lshtm.ac.uk
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                11 January 2021
                11 January 2021
                2021
                : 14
                : 42
                Affiliations
                [1 ]GRID grid.419326.b, ISNI 0000 0004 1794 5158, International Centre of Insect Physiology and Ecology (icipe), ; Human Health Theme, Nairobi, 00100 Kenya
                [2 ]GRID grid.4818.5, ISNI 0000 0001 0791 5666, Laboratory of Entomology, , Wageningen University and Research, ; P.O. Box 16, 6700 AA Wageningen, The Netherlands
                [3 ]GRID grid.416786.a, ISNI 0000 0004 0587 0574, Department of Epidemiology and Public Health, , Swiss Tropical and Public Health Institute, ; Socinstrasse 57, 4051 833 Basel, Switzerland
                [4 ]GRID grid.6612.3, ISNI 0000 0004 1937 0642, University of Basel, ; Petersplatz 1, Basel, Switzerland
                [5 ]GRID grid.414543.3, ISNI 0000 0000 9144 642X, Department of Environmental Health and Ecological Sciences, , Ifakara Health Institute, ; P.O. Box 74, Bagamoyo, Tanzania
                [6 ]GRID grid.8991.9, ISNI 0000 0004 0425 469X, London School of Hygiene and Tropical Medicine, , ARCTEC, ; Keppel Street, London, WC1E 7HT UK
                Author information
                http://orcid.org/0000-0002-4037-431X
                Article
                4556
                10.1186/s13071-020-04556-7
                7802213
                33430963
                a0f66a61-2586-4988-aba8-b5e3a31e1ac4
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

                History
                : 14 September 2020
                : 16 December 2020
                Funding
                Funded by: Innovative Vector Control Consortium (IVCC)
                Funded by: UK’s Foreign, Commonwealth & Development Office (FCDO)
                Funded by: Swedish International Development Cooperation Agency (Sida)
                Funded by: Federal Democratic Republic of Ethiopia
                Funded by: Swiss Agency for Development and Cooperation (SDC)
                Funded by: Government of the Republic of Kenya
                Categories
                Research
                Custom metadata
                © The Author(s) 2021

                Parasitology
                malaria,vector control,outdoor-biting,spatial repellent,pmd,citriodiol,transfluthrin,gc-fid,semi-field study

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