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      Effects of indoor residual spraying and outdoor larval control on Anopheles coluzzii from São Tomé and Príncipe, two islands with pre-eliminated malaria

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          Abstract

          Background

          Vector control is a key component of malaria prevention. Two major vector control strategies have been implemented in São Tomé and Príncipe (STP), indoor residual spraying (IRS) and outdoor larval control using Bacillus thuringiensis israelensis ( Bti). This study evaluated post-intervention effects of control strategies on vector population density, composition, and knockdown resistance mutation, and their implications for malaria epidemiology in STP.

          Methods

          Mosquitoes were collected by indoor and outdoor human landing catches and mosquito light traps in seven districts. Mosquito density was calculated by numbers of captured adult mosquitoes/house/working hour. Mitochondrial cytochrome c oxidase subunit I ( COI) was PCR amplified and sequenced to understand the spatial–temporal population composition of malaria vector in STP. Knockdown resistance L1014F mutation was detected using allele-specific PCR. To estimate the malaria transmission risks in STP, a negative binomial regression model was constructed. The response variable was monthly incidence, and the explanatory variables were area, rainfall, entomological inoculation rate (EIR), and kdr mutation frequency.

          Results

          Malaria vector in STP is exophilic Anopheles coluzzii with significant population differentiation between Príncipe and São Tomé (mean F ST = 0.16, p < 0.001). Both vector genetic diversity and knockdown resistance mutation were relatively low in Príncipe (mean of kdr frequency = 15.82%) compared to São Tomé (mean of kdr frequency = 44.77%). Annual malaria incidence rate in STP had been rapidly controlled from 37 to 2.1% by three rounds of country-wide IRS from 2004 to 2007. Long-term application of Bti since 2007 kept the mosquito density under 10 mosquitoes/house/hr/month, and malaria incidence rate under 5% after 2008, except for a rising that occurred in 2012 (incidence rate = 6.9%). Risk factors of area (São Tomé compared to Príncipe), rainfall, outdoor EIR, and kdr mutation frequency could significantly increase malaria incidence by 9.33–11.50, 1.25, 1.07, and 1.06 fold, respectively.

          Conclusions

          Indoor residual spraying could rapidly decrease Anopheles density and malaria incidence in STP. Outdoor larval control using Bti is a sustainable approach for controlling local vector with exophilic feature and insecticide resistance problem. Vector control interventions should be intensified especially at the north-eastern part of São Tomé to minimize impacts of outbreaks.

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          Most cited references52

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          Gene flow and the geographic structure of natural populations

          M Slatkin (1987)
          There is abundant geographic variation in both morphology and gene frequency in most species. The extent of geographic variation results from a balance of forces tending to produce local genetic differentiation and forces tending to produce genetic homogeneity. Mutation, genetic drift due to finite population size, and natural selection favoring adaptations to local environmental conditions will all lead to the genetic differentiation of local populations, and the movement of gametes, individuals, and even entire populations--collectively called gene flow--will oppose that differentiation. Gene flow may either constrain evolution by preventing adaptation to local conditions or promote evolution by spreading new genes and combinations of genes throughout a species' range. Several methods are available for estimating the amount of gene flow. Direct methods monitor ongoing gene flow, and indirect methods use spatial distributions of gene frequencies to infer past gene flow. Applications of these methods show that species differ widely in the gene flow that they experience. Of particular interest are those species for which direct methods indicate little current gene flow but indirect methods indicate much higher levels of gene flow in the recent past. Such species probably have undergone large-scale demographic changes relatively frequently.
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            Urbanization, malaria transmission and disease burden in Africa.

            Many attempts have been made to quantify Africa's malaria burden but none has addressed how urbanization will affect disease transmission and outcome, and therefore mortality and morbidity estimates. In 2003, 39% of Africa's 850 million people lived in urban settings; by 2030, 54% of Africans are expected to do so. We present the results of a series of entomological, parasitological and behavioural meta-analyses of studies that have investigated the effect of urbanization on malaria in Africa. We describe the effect of urbanization on both the impact of malaria transmission and the concomitant improvements in access to preventative and curative measures. Using these data, we have recalculated estimates of populations at risk of malaria and the resulting mortality. We find there were 1,068,505 malaria deaths in Africa in 2000 - a modest 6.7% reduction over previous iterations. The public-health implications of these findings and revised estimates are discussed.
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              The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors.

              High insecticide resistance resulting from insensitive acetylcholinesterase (AChE) has emerged in mosquitoes. A single mutation (G119S of the ace-1 gene) explains this high resistance in Culex pipiens and in Anopheles gambiae. In order to provide better documentation of the ace-1 gene and the effect of the G119S mutation, we present a three-dimension structure model of AChE, showing that this unique substitution is localized in the oxyanion hole, explaining the insecticide insensitivity and its interference with the enzyme catalytic functions. As the G119S creates a restriction site, a simple PCR test was devised to detect its presence in both A. gambiae and C. pipiens, two mosquito species belonging to different subfamilies (Culicinae and Anophelinae). It is possibile that this mutation also explains the high resistance found in other mosquitoes, and the present results indicate that the PCR test detects the G119S mutation in the malaria vector A. albimanus. The G119S has thus occurred independently at least four times in mosquitoes and this PCR test is probably of broad applicability within the Culicidae family.
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                Author and article information

                Contributors
                f03844002@ntu.edu.tw
                jclien1217@gmail.com
                titinatseng@gmail.com
                again1118@gmail.com
                linwy@ntu.edu.tw
                hurngyi@ntu.edu.tw
                kunhtsai@ntu.edu.tw
                Journal
                Malar J
                Malar. J
                Malaria Journal
                BioMed Central (London )
                1475-2875
                5 December 2019
                5 December 2019
                2019
                : 18
                : 405
                Affiliations
                [1 ]ISNI 0000 0004 0546 0241, GRID grid.19188.39, Institute of Environmental and Occupational Health Sciences, College of Public Health, , National Taiwan University, ; Taipei, Taiwan
                [2 ]Taiwan Anti-Malaria Advisory Mission, São Tomé, São Tomé and Príncipe
                [3 ]ISNI 0000 0004 0546 0241, GRID grid.19188.39, Institute of Epidemiology and Preventive Medicine, College of Public Health, , National Taiwan University, ; Taipei, Taiwan
                [4 ]ISNI 0000 0004 0546 0241, GRID grid.19188.39, Department of Public Health, College of Public Health, , National Taiwan University, ; Taipei, Taiwan
                [5 ]ISNI 0000 0004 0546 0241, GRID grid.19188.39, Graduate Institute of Clinical Medicine, College of Medicine, , National Taiwan University, ; Taipei, Taiwan
                Author information
                http://orcid.org/0000-0002-6154-113X
                Article
                3037
                10.1186/s12936-019-3037-y
                6896513
                31806029
                a7b43dee-05d9-456f-b18a-e2ea5e32e1df
                © The Author(s) 2019

                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
                : 30 July 2019
                : 26 November 2019
                Funding
                Funded by: Ministry of Foreign Affairs, Taiwan
                Funded by: FundRef http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: 103-2314-B-002-036-MY2
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Infectious disease & Microbiology
                são tomé and príncipe,anopheles coluzzii,indoor residual spraying,bacillus thuringiensis israelensis,vector density,cytochrome c oxidase subunit i,knockdown resistance mutation

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