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      Seasonal and Spatial Dynamics of the Primary Vector of Plasmodium knowlesi within a Major Transmission Focus in Sabah, Malaysia

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          Abstract

          Background

          The simian malaria parasite Plasmodium knowlesi is emerging as a public health problem in Southeast Asia, particularly in Malaysian Borneo where it now accounts for the greatest burden of malaria cases and deaths. Control is hindered by limited understanding of the ecology of potential vector species.

          Methodology/Principal Findings

          We conducted a one year longitudinal study of P. knowlesi vectors in three sites within an endemic area of Sabah, Malaysia. All mosquitoes were captured using human landing catch. Anopheles mosquitoes were dissected to determine, oocyst, sporozoites and parous rate. Anopheles balabacensis is confirmed as the primary vector of. P. knowlesi (using nested PCR) in Sabah for the first time. Vector densities were significantly higher and more seasonally variable in the village than forest or small scale farming site. However An. balabacensis survival and P. knowlesi infection rates were highest in forest and small scale farm sites. Anopheles balabacensis mostly bites humans outdoors in the early evening between 1800 to 2000hrs.

          Conclusions/Significance

          This study indicates transmission is unlikely to be prevented by bednets. This combined with its high vectorial capacity poses a threat to malaria elimination programmes within the region.

          Author Summary

          The first natural infection of Plasmodium knowlesi was reported 40 years ago. At that time it was perceived that the infection would not affect humans. However, now P. knowlesi is the predominant malaria species (38% of the cases) infecting people in Malaysia and is a notable obstacle to malaria elimination in the country. Plasmodium knowlesi has also been reported from all countries in Southeast Asia with the exception of Lao PDR and Timor Leste. In Sabah, Malaysian Borneo cases of human P. knowlesi are increasing. Thus, a comprehensive understanding of the bionomics of the vectors is required so as to enable proper control strategies. Here, we conducted a longitudinal study in Kudat district, Sabah, to determine and characterize the vectors of P. knowlesi within this transmission foci. Anopheles balabacensis was the predominant mosquito in all study sites and is confirmed as vector for P. knowlesi and other simian malaria parasites. The peak biting time was in the early part of the evening between1800 to 2000. Thus, breaking the chain of transmission is an extremely challenging task for the malaria elimination programme.

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          Most cited references30

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          A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT).

          The absolute necessity for rational therapy in the face of rampant drug resistance places increasing importance on the accuracy of malaria diagnosis. Giemsa microscopy and rapid diagnostic tests (RDTs) represent the two diagnostics most likely to have the largest impact on malaria control today. These two methods, each with characteristic strengths and limitations, together represent the best hope for accurate diagnosis as a key component of successful malaria control. This review addresses the quality issues with current malaria diagnostics and presents data from recent rapid diagnostic test trials. Reduction of malaria morbidity and drug resistance intensity plus the associated economic loss of these two factors require urgent scaling up of the quality of parasite-based diagnostic methods. An investment in anti-malarial drug development or malaria vaccine development should be accompanied by a parallel commitment to improve diagnostic tools and their availability to people living in malarious areas.
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            A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies.

            A nested polymerase chain reaction (PCR) assay that uses Plasmodium genus-specific primers for the initial PCR (nest 1) amplification and either genus- or species-specific primers for the nest 2 amplifications was tested on laboratory and field samples. With in vitro cultured Plasmodium falciparum-infected blood samples, it was capable of detecting six parasites/microl of blood using DNA prepared from 25-microl blood spots on filter paper. The assay was evaluated on fingerprick blood samples collected on filter paper from 129 individuals living in a malaria-endemic area in Malaysia. Malaria prevalence by genus-specific nested PCR was 35.6% (46 of 129) compared with 28.7% (37 of 129) by microscopy. The nested PCR detected seven more malaria samples than microscopy in the first round of microscopic examination, malaria in three microscopically negative samples, six double infections identified as single infections by microscopy and one triple infection identified as a double infection by microscopy. The nested PCR assay described is a sensitive technique for collecting accurate malaria epidemiologic data. When coupled with simple blood spot sampling, it is particularly useful for screening communities in remote regions of the world.
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              Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology.

              To clarify mechanisms linking deforestation, anopheline ecology, and malaria epidemiology, this study draws together 60 examples of changes in anopheline ecology and malaria incidence as a consequence of deforestation and agricultural development. The deforestation projects were classified based on subsequent land use and were reviewed in terms of their impact on anopheline density and malaria incidence. To further examine different anopheline responses to land transformation, two major ecological characteristics of 31 anopheline species were tested for their associations with changes in their densities and malaria incidence. Although niche width of anopheline species was not associated with density changes, sun preference was significantly associated with an increase in density. This study suggests the possibility of predicting potential impacts of future deforestation on vector density by using information on types of planned agricultural development and the ecology of local anopheline species.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                8 October 2015
                October 2015
                : 9
                : 10
                : e0004135
                Affiliations
                [1 ]Parasitology Department, Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
                [2 ]Department of Pathobiology and Medical Diagnostics, Faculty of Medicine and Health Sciences, Universiti Sabah Malaysia, Kota Kinabalu, Sabah, Malaysia
                [3 ]Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
                [4 ]Jesselton Medical Centre, Kota Kinabalu, Sabah, Malaysia
                [5 ]Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Scotland, United Kingdom
                Liverpool School of Tropical Medicine, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: IV CD HMF THC TW. Performed the experiments: IV MLW THC CSL LTK KF WYWS. Analyzed the data: MLW THC HMF IV. Contributed reagents/materials/analysis tools: TW. Wrote the paper: IV HMF THC MLW KF CD.

                Article
                PNTD-D-15-01138
                10.1371/journal.pntd.0004135
                4598189
                26448052
                72d3f3d0-cab2-4b43-9c8d-fe2c7f9b29e7
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 29 June 2015
                : 10 September 2015
                Page count
                Figures: 5, Tables: 4, Pages: 15
                Funding
                This study was supported by: University of Malaya High Impact Research Grant UM.C/625/1/HIR/099 J-20011-73822; University of Malaya student Grant IPP 105-2014A, Medical Research Council, Natural Environment Research Council, Economic and Social Research Council, and Biotechnology and Biosciences Research Council for the funding received for this project through the Environmental & Social Ecology of Human Infectious Diseases Initiative (ESEI), MRC Grant Number: G1100796. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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