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      Dramatic decreases of malaria transmission intensities in Ifakara, south-eastern Tanzania since early 2000s

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          Abstract

          Background

          Ongoing epidemiological transitions across Africa are particularly evident in fast-growing towns, such as Ifakara in the Kilombero valley, south-eastern Tanzania. This town and its environs (population ~ 70,000) historically experienced moderate to high malaria transmission, mediated mostly by Anopheles gambiae and Anopheles funestus. In early 2000s, malaria transmission [ Plasmodium falciparum entomological inoculation rate (P fEIR)] was estimated at ~ 30 infectious bites/person/year (ib/p/yr). This study assessed the P fEIR after 15 years, during which there had been rapid urbanization and expanded use of insecticide-treated nets (ITNs).

          Methods

          Randomly-selected 110 households were sampled across Ifakara town and four adjacent wards. Mosquitoes were trapped nightly or monthly (June.2015–May.2016) using CDC-light-traps indoors, Suna ® traps outdoors and human landing catches (HLC) indoors and outdoors. All Anopheles mosquitoes were morphologically identified and analysed by ELISA for Plasmodium circumsporozoite proteins. Mosquito blood meals were identified using ELISA, and sub-samples of An. gambiae and An. funestus examined by PCR to distinguish morphologically-similar siblings. Insecticide resistance was assessed using WHO-susceptibility assays, and some Anopheles were dissected to examine ovariole tracheoles for parity.

          Results

          After 3572 trap-nights, one Plasmodium-infected Anopheles was found (an An. funestus caught outdoors in Katindiuka-ward by HLC), resulting in overall P fEIR of 0.102 ib/p/yr. Nearly 80% of malaria vectors were from Katindiuka and Mlabani wards. Anopheles gambiae densities were higher outdoors (64%) than indoors (36%), but no such difference was observed for An. funestus. All An. funestus and 75% of An. gambiae dissected were parous. Anopheles gambiae complex consisted entirely of Anopheles arabiensis, while An. funestus included 84.2% An. funestus s.s., 4.5% Anopheles rivulorum, 1.4% Anopheles leesoni and 9.9% with unamplified-DNA. Anopheles gambiae were susceptible to bendiocarb and malathion, but resistant to pyrethroids, DDT and pirimiphos-methyl. Most houses had brick walls and/or iron roofs (> 90%), and 52% had screened windows.

          Conclusion

          Malaria transmission in Ifakara has decreased by > 99% since early-2000s, reaching levels nearly undetectable with current entomological methods. These declines are likely associated with ITNs use, urbanization and improved housing. Remaining risk is now mostly in peri-urban wards, but concerted efforts could further decrease local transmission. Parasitological surveys are required to assess actual prevalence, incidence and importation rates.

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          Most cited references44

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          The Analysis of Spatial Association by Use of Distance Statistics

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            Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction.

            A ribosomal DNA-polymerase chain reaction (PCR) method has been developed for species identification of individuals of the five most widespread members of the Anopheles gambiae complex, a group of morphologically indistinguishable sibling mosquito species that includes the major vectors of malaria in Africa. The method, which is based on species-specific nucleotide sequences in the ribosomal DNA intergenic spacers, may be used to identify both species and interspecies hybrids, regardless of life stage, using either extracted DNA or fragments of a specimen. Intact portions of a mosquito as small as an egg or the segment of one leg may be placed directly into the PCR mixture for amplification and analysis. The method uses a cocktail of five 20-base oligonucleotides to identify An. gambiae, An. arabiensis, An. quadriannnulatus, and either An. melas in western Africa or An. melas in eastern and southern Africa.
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              Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania

              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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                Author and article information

                Contributors
                lfinda@ihi.or.tz
                Journal
                Malar J
                Malar. J
                Malaria Journal
                BioMed Central (London )
                1475-2875
                16 October 2018
                16 October 2018
                2018
                : 17
                : 362
                Affiliations
                [1 ]ISNI 0000 0000 9144 642X, GRID grid.414543.3, Environmental Health and Ecological Science Department, , Ifakara Health Institute, ; P. O. Box 53, Ifakara, Tanzania
                [2 ]ISNI 0000 0004 1937 1135, GRID grid.11951.3d, School of Public Health, Faculty of Health Sciences, , University of the Witwatersrand, ; Johannesburg, South Africa
                [3 ]ISNI 0000 0004 1937 0642, GRID grid.6612.3, University of Basel, ; Basel, Switzerland
                [4 ]ISNI 0000 0004 0587 0574, GRID grid.416786.a, Swiss Tropical and Public Health Institute, ; Basel, Switzerland
                [5 ]ISNI 0000 0001 2193 314X, GRID grid.8756.c, Institute of Biodiversity, Animal Health and Comparative Medicine, , University of Glasgow, ; Glasgow, G12 8QQ UK
                Article
                2511
                10.1186/s12936-018-2511-2
                6192315
                30326881
                dbb70daf-2c97-446e-a8be-a4416dad2aba
                © The Author(s) 2018

                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
                : 5 July 2018
                : 8 October 2018
                Funding
                Funded by: Wellcome Trust
                Award ID: WT102350/Z/13
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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