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      Spatial-temporal heterogeneity in malaria receptivity is best estimated by vector biting rates in areas nearing elimination

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          Abstract

          Background

          Decisions on when vector control can be withdrawn after malaria is eliminated depend on the receptivity or potential of an area to support vector populations. To guide malaria control and elimination programmes, the potential of biting rates, sporozoite rates, entomological inoculation rates and parity rates to estimate malaria receptivity and transmission were compared within and among geographically localised villages of active transmission in the Western Province of the Solomon Islands.

          Results

          Malaria transmission and transmission potential was heterogeneous in both time and space both among and within villages as defined by anopheline species composition and biting densities. Biting rates during the peak biting period (from 18:00 to 00:00 h) of the primary vector, Anopheles farauti, ranged from less than 0.3 bites per person per half night in low receptivity villages to 26 bites per person in highly receptive villages. Within villages, sites with high anopheline biting rates were significantly clustered. Sporozoite rates provided evidence for continued transmission of Plasmodium falciparum, P. vivax and P. ovale by An. farauti and for incriminating An. hinesorum, as a minor vector, but were unreliable as indicators of transmission intensity.

          Conclusions

          In the low transmission area studied, sporozoite, entomological inoculation and parity rates could not be measured with the precision required to provide guidance to malaria programmes. Receptivity and potential transmission risk may be most reliably estimated by the vector biting rate. These results support the meaningful design of operational research programmes to ensure that resources are focused on providing information that can be utilised by malaria control programmes to best understand both transmission, transmission risk and receptivity across different areas.

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          Most cited references27

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          Malaria resurgence: a systematic review and assessment of its causes

          Background Considerable declines in malaria have accompanied increased funding for control since the year 2000, but historical failures to maintain gains against the disease underscore the fragility of these successes. Although malaria transmission can be suppressed by effective control measures, in the absence of active intervention malaria will return to an intrinsic equilibrium determined by factors related to ecology, efficiency of mosquito vectors, and socioeconomic characteristics. Understanding where and why resurgence has occurred historically can help current and future malaria control programmes avoid the mistakes of the past. Methods A systematic review of the literature was conducted to identify historical malaria resurgence events. All suggested causes of these events were categorized according to whether they were related to weakened malaria control programmes, increased potential for malaria transmission, or technical obstacles like resistance. Results The review identified 75 resurgence events in 61 countries, occurring from the 1930s through the 2000s. Almost all resurgence events (68/75 = 91%) were attributed at least in part to the weakening of malaria control programmes for a variety of reasons, of which resource constraints were the most common (39/68 = 57%). Over half of the events (44/75 = 59%) were attributed in part to increases in the intrinsic potential for malaria transmission, while only 24/75 (32%) were attributed to vector or drug resistance. Conclusions Given that most malaria resurgences have been linked to weakening of control programmes, there is an urgent need to develop practical solutions to the financial and operational threats to effectively sustaining today’s successful malaria control programmes.
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            The entomological inoculation rate and Plasmodium falciparum infection in African children.

            Malaria is an important cause of global morbidity and mortality. The fact that some people are bitten more often than others has a large effect on the relationship between risk factors and prevalence of vector-borne diseases. Here we develop a mathematical framework that allows us to estimate the heterogeneity of infection rates from the relationship between rates of infectious bites and community prevalence. We apply this framework to a large, published data set that combines malaria measurements from more than 90 communities. We find strong evidence that heterogeneous biting or heterogeneous susceptibility to infection are important and pervasive factors determining the prevalence of infection: 20% of people receive 80% of all infections. We also find that individual infections last about six months on average, per infectious bite, and children who clear infections are not immune to new infections. The results have important implications for public health interventions: the success of malaria control will depend heavily on whether efforts are targeted at those who are most at risk of infection.
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              Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa.

              Epidemiologic patterns of malaria infection are governed by environmental parameters that regulate vector populations of Anopheles mosquitoes. The intensity of malaria parasite transmission is normally expressed as the entomologic inoculation rate (EIR), the product of the vector biting rate times the proportion of mosquitoes infected with sporozoite-stage malaria parasites. Malaria transmission intensity in Africa is highly variable with annual EIRs ranging from 1,000 infective bites per person per year. Malaria control programs often seek to reduce morbidity and mortality due to malaria by reducing or eliminating malaria parasite transmission by mosquitoes. This report evaluates data from 31 sites throughout Africa to establish fundamental relationships between annual EIRs and the prevalence of Plasmodium falciparum malaria infection. The majority of sites fitted a linear relationship (r2 = 0.71) between malaria prevalence and the logarithm of the annual EIR. Some sites with EIRs 80%. The basic relationship between EIR and P. falciparum prevalence, which likely holds in east and west Africa, and across different ecologic zones, shows convincingly that substantial reductions in malaria prevalence are likely to be achieved only when EIRs are reduced to levels less than 1 infective bite per person per year. The analysis also highlights that the EIR is a more direct measure of transmission intensity than traditional measures of malaria prevalence or hospital-based measures of infection or disease incidence. As such, malaria field programs need to consider both entomologic and clinical assessments of the efficacy of transmission control measures.
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                Author and article information

                Contributors
                tom.burkot@jcu.edu.au
                hugo.bugoro@sinu.edu.sb
                apairamo@gmail.com
                Bob.Cooper@defence.gov.au
                decheve1@nd.edu
                danyal_odabasi@hotmail.com
                n.beebe@uq.edu.au
                Victoria.Makuru.1@nd.edu
                honglinx@yahoo.com
                jdavids2@nd.edu
                nicholas.deason@nih.gov
                hedrick2010@gmail.com
                jxk14@case.edu
                frank@nd.edu
                nlobo@nd.edu
                tanya.russell@jcu.edu.au
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                27 November 2018
                27 November 2018
                2018
                : 11
                : 606
                Affiliations
                [1 ]ISNI 0000 0004 0474 1797, GRID grid.1011.1, James Cook University, Australian Institute of Tropical Health and Medicine, ; Cairns, QLD 4870 Australia
                [2 ]National Vector Borne Disease Control Programme, Ministry of Health and Medical Services, Honiara, Solomon Islands
                [3 ]Research Department, Solomon Islands National University, Honiara, Solomon Islands
                [4 ]GRID grid.237081.f, Australian Army Malaria Institute, ; Gallipoli Barracks, Enoggera, 4052 Australia
                [5 ]ISNI 0000 0001 2168 0066, GRID grid.131063.6, Department of Biological Sciences, , Eck Institute for Global Health, University of Notre Dame, ; Notre Dame, IN 46556 USA
                [6 ]ISNI 0000 0004 0587 0574, GRID grid.416786.a, Swiss Tropical and Public Health Institute, ; Basel, Switzerland
                [7 ]ISNI 0000 0004 1937 0642, GRID grid.6612.3, University of Basel, ; Basel, Switzerland
                [8 ]ISNI 0000 0000 9320 7537, GRID grid.1003.2, University of Queensland, School of Biological Sciences, ; QLD, St. Lucia, 4068 Australia
                [9 ]GRID grid.1016.6, CSIRO, ; Dutton Park, Brisbane, QLD 4102 Australia
                [10 ]Western Province Malaria Control, Gizo, Western Province Solomon Islands
                [11 ]ISNI 0000 0001 2164 3847, GRID grid.67105.35, Center for Global Health & Diseases, Case Western Reserve University School of Medicine, ; Cleveland, Ohio 44106–4983 USA
                Article
                3201
                10.1186/s13071-018-3201-1
                6260740
                30482239
                2da17b55-2534-4613-937d-057d5bfd1e3d
                © 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
                : 20 September 2018
                : 14 November 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award ID: 45114
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000060, National Institute of Allergy and Infectious Diseases;
                Award ID: U19AI08986
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Parasitology
                anopheles farauti,anopheles hinesorum,malaria,receptivity,elimination,solomon islands
                Parasitology
                anopheles farauti, anopheles hinesorum, malaria, receptivity, elimination, solomon islands

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