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      Mosquito odour-baited mass trapping reduced malaria transmission intensity: a result from a controlled before-and-after intervention study

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          Abstract

          Background

          Conventional vector control strategies have significantly reduced the malaria burden. The sustainability of these methods is currently challenged. Odour-based traps are emerging technologies that can complement the existing tools. Implementation of odour-based traps for mass trapping is limited due to the restricted range of vectors caught with available carbon dioxide-dependent lures, and the lack of comprehensive field studies. The objective of this study was to assess the impact of odour-mediated mass trapping targeting outdoor vectors, using a synthetic cattle urine lure that attracts a wide range of vector species in a variety of physiological states, on malaria prevalence and entomological parameters to determine malaria transmission intensities.

          Methods

          A controlled before-and-after study was conducted in two rural communities in southern Ethiopia. Baseline monthly entomological and seasonal cross-sectional malaria prevalence surveys were conducted in both communities for a year. Then, mass trapping of mosquitoes was conducted in one of the villages, while the monthly entomological surveillance and seasonal malaria prevalence surveys continued in both villages. Generalised linear mixed models were constructed and tested to determine which factors were significantly affected by the intervention.

          Results

          Mass trapping contributed to the reduction of the population of the principal malaria vector, Anopheles arabiensis, and the associated entomological indicators, the human bite rate (HBR) and the entomological inoculation rate (EIR), in the intervention village compared to the control village. The intervention village had an average HBR by An. arabiensis of 3.0 (95% CI 1.4–4.6) during the peak malaria transmission season, compared to 10.5 (95% CI − 0.5–21.5; P < 0.0001) in the control village. The intervention village (mean 0.02, 95% CI − 0.05–0.4.8) had a daily EIR eight times lower than the control village (mean 0.17, 95% CI), which likely contributed to the reduced malaria prevalence in the intervention community following its introduction by ca. 60% (95% CI 55–63).

          Conclusions

          The combined use of odour-based mass trapping and conventional control strategies coincided with a reduction of human-vector contact and malaria prevalence, providing support for odour-baited technologies as a viable option for next-generation vector control tools. Further cluster-randomised control studies are recommended in different eco-epidemiological settings with varying malaria transmission intensities.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12916-024-03255-9.

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          Most cited references28

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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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            Mosquito feeding behavior and how it influences residual malaria transmission across Africa

            Significance Malaria transmission persists even when mosquito control is used effectively. This “residual transmission” measures all forms of transmission that are beyond the reach of standard insecticidal nets and indoor residual spraying of insecticides when used optimally. The epidemiological importance of the time of day mosquitoes bite and how much this contributes to residual transmission is unclear. The scale of the problem must be understood to demonstrate the need for outdoor vector control tools. An additional 10.6 million clinical cases of malaria are predicted annually given the 10% higher level of outdoor biting observed here. Mosquito species and behavior data together with people’s resting and sleeping patterns are needed to fully measure indoor intervention efficacy and accurately quantify residual transmission.
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              Species Shifts in the Anopheles gambiae Complex: Do LLINs Successfully Control Anopheles arabiensis?

              Introduction High coverage of conventional and long-lasting insecticide treated nets (ITNs and LLINs) in parts of E Africa are associated with reductions in local malaria burdens. Shifts in malaria vector species ratio have coincided with the scale-up suggesting that some species are being controlled by ITNs/LLINs better than others. Methods Between 2005–2006 six experimental hut trials of ITNs and LLINs were conducted in parallel at two field stations in northeastern Tanzania; the first station was in Lower Moshi Rice Irrigation Zone, an area where An. arabiensis predominates, and the second was in coastal Muheza, where An. gambiae and An. funestus predominate. Five pyrethroids and one carbamate insecticide were evaluated on nets in terms of insecticide-induced mortality, blood-feeding inhibition and exiting rates. Results In the experimental hut trials mortality of An. arabiensis was consistently lower than that of An. gambiae and An. funestus. The mortality rates in trials with pyrethroid-treated nets ranged from 25–52% for An. arabiensis, 63–88% for An. gambiae s.s. and 53–78% for An. funestus. All pyrethroid-treated nets provided considerable protection for the occupants, despite being deliberately holed, with blood-feeding inhibition (percentage reduction in biting rates) being consistent between species. Veranda exiting rates did not differ between species. Percentage mortality of mosquitoes tested in cone bioassays on netting was similar for An. gambiae and An. arabiensis. Conclusions LLINs and ITNs treated with pyrethroids were more effective at killing An. gambiae and An. funestus than An. arabiensis. This could be a major contributing factor to the species shifts observed in East Africa following scale up of LLINs. With continued expansion of LLIN coverage in Africa An. arabiensis is likely to remain responsible for residual malaria transmission, and species shifts might be reported over larger areas. Supplementary control measures to LLINs may be necessary to control this vector species.
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                Author and article information

                Contributors
                rickard.ignell@slu.se
                Journal
                BMC Med
                BMC Med
                BMC Medicine
                BioMed Central (London )
                1741-7015
                29 January 2024
                29 January 2024
                2024
                : 22
                : 41
                Affiliations
                [1 ]Department of Zoological Sciences, Addis Ababa University, ( https://ror.org/038b8e254) Addis Ababa, Ethiopia
                [2 ]Public Health Entomology Research Team, Ethiopian Public Health Institute, ( https://ror.org/00xytbp33) Addis Ababa, Ethiopia
                [3 ]Aklilu Lemma Institute of Pathobiology, Addis Ababa University, ( https://ror.org/038b8e254) Addis Ababa, Ethiopia
                [4 ]GRID grid.36316.31, ISNI 0000 0001 0806 5472, Natural Resources Institute, , University of Greenwich, ; London, UK
                [5 ]Disease Vector Group, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, ( https://ror.org/02yy8x990) Alnarp, Sweden
                Article
                3255
                10.1186/s12916-024-03255-9
                10823605
                38281908
                d6001188-c73d-46c1-9681-8fb1a20da513
                © The Author(s) 2024

                Open Access This 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
                : 1 June 2023
                : 11 January 2024
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;
                Award ID: e033101
                Award Recipient :
                Funded by: Swedish University of Agricultural Sciences
                Categories
                Research Article
                Custom metadata
                © BioMed Central Ltd., part of Springer Nature 2024

                Medicine
                anopheles,malaria vectors,chemical ecology,malaria prevalence
                Medicine
                anopheles, malaria vectors, chemical ecology, malaria prevalence

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