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Ecology: A Prerequisite for Malaria Elimination and Eradication

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      Abstract

      Gerry Killeen and colleagues argue that malaria eradication efforts will not be successful until a better understanding of the ecology and evolution of the mosquito vectors is gained.

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      Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya

      Summary Background As efforts to control malaria are expanded across the world, understanding the role of transmission intensity in determining the burden of clinical malaria is crucial to the prediction and measurement of the effectiveness of interventions to reduce transmission. Furthermore, studies comparing several endemic sites led to speculation that as transmission decreases morbidity and mortality caused by severe malaria might increase. We aimed to assess the epidemiological characteristics of malaria in Kilifi, Kenya, during a period of decreasing transmission intensity. Methods We analyse 18 years (1990–2007) of surveillance data from a paediatric ward in a malaria-endemic region of Kenya. The hospital has a catchment area of 250 000 people. Clinical data and blood-film results for more than 61 000 admissions are reported. Findings Hospital admissions for malaria decreased from 18·43 per 1000 children in 2003 to 3·42 in 2007. Over 18 years of surveillance, the incidence of cerebral malaria initially increased; however, malaria mortality decreased overall because of a decrease in incidence of severe malarial anaemia since 1997 (4·75 to 0·37 per 1000 children) and improved survival among children admitted with non-severe malaria. Parasite prevalence, the mean age of children admitted with malaria, and the proportion of children with cerebral malaria began to change 10 years before hospitalisation for malaria started to fall. Interpretation Sustained reduction in exposure to infection leads to changes in mean age and presentation of disease similar to those described in multisite studies. Changes in transmission might not lead to immediate reductions in incidence of clinical disease. However, longitudinal data do not indicate that reductions in transmission intensity lead to transient increases in morbidity and mortality. Funding Wellcome Trust, Kenya Medical Research Institute.
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        Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis

        Summary Background Malaria is a major cause of morbidity and mortality in Africa. International effort and funding for control has been stepped up, with substantial increases from 2003 in the delivery of malaria interventions to pregnant women and children younger than 5 years in The Gambia. We investigated the changes in malaria indices in this country, and the causes and public-health significance of these changes. Methods We undertook a retrospective analysis of original records to establish numbers and proportions of malaria inpatients, deaths, and blood-slide examinations at one hospital over 9 years (January, 1999–December, 2007), and at four health facilities in three different administrative regions over 7 years (January, 2001–December, 2007). We obtained additional data from single sites for haemoglobin concentrations in paediatric admissions and for age distribution of malaria admissions. Findings From 2003 to 2007, at four sites with complete slide examination records, the proportions of malaria-positive slides decreased by 82% (3397/10861 in 2003 to 337/6142 in 2007), 85% (137/1259 to 6/368), 73% (3664/16932 to 666/11333), and 50% (1206/3304 to 336/1853). At three sites with complete admission records, the proportions of malaria admissions fell by 74% (435/2530 to 69/1531), 69% (797/2824 to 89/1032), and 27% (2204/4056 to 496/1251). Proportions of deaths attributed to malaria in two hospitals decreased by 100% (seven of 115 in 2003 to none of 117 in 2007) and 90% (22/122 in 2003 to one of 58 in 2007). Since 2004, mean haemoglobin concentrations for all-cause admissions increased by 12 g/L (85 g/L in 2000–04 to 97 g/L in 2005–07), and mean age of paediatric malaria admissions increased from 3·9 years (95% CI 3·7–4·0) to 5·6 years (5·0–6·2). Interpretation A large proportion of the malaria burden has been alleviated in The Gambia. Our results encourage consideration of a policy to eliminate malaria as a public-health problem, while emphasising the importance of accurate and continuous surveillance. Funding UK Medical Research Council.
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          Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya

          Background High coverage of insecticide-treated bed nets in Asembo and low coverage in Seme, two adjacent communities in western Nyanza Province, Kenya; followed by expanded coverage of bed nets in Seme, as the Kenya national malaria programme rolled out; provided a natural experiment for quantification of changes in relative abundance of two primary malaria vectors in this holoendemic region. Both belong to the Anopheles gambiae sensu lato (s.l.) species complex, namely A. gambiae sensu stricto (s.s.) and Anopheles arabiensis. Historically, the former species was proportionately dominant in indoor resting collections of females. Methods Data of the relative abundance of adult A. gambiae s.s. and A. arabiensis sampled from inside houses were obtained from the literature from 1970 to 2002 for sites west of Kisumu, Kenya, to the region of Asembo ca. 50 km from the city. A sampling transect was established from Asembo (where bed net use was high due to presence of a managed bed net distribution programme) eastward to Seme, where no bed net programme was in place. Adults of A. gambiae s.l. were sampled from inside houses along the transect from 2003 to 2009, as were larvae from nearby aquatic habitats, providing data over a nearly 40 year period of the relative abundance of the two species. Relative proportions of A. gambiae s.s. and A. arabiensis were determined for each stage by identifying species by the polymerase chain reaction method. Household bed net ownership was measured with surveys during mosquito collections. Data of blood host choice, parity rate, and infection rate for Plasmodium falciparum in A. gambiae s.s. and A. arabiensis were obtained for a sample from Asembo and Seme from 2005. Results Anopheles gambiae s.s. adult females from indoor collections predominated from 1970 to 1998 (ca. 85%). Beginning in 1999, A. gambiae s.s decreased proportionately relative to A. arabiensis, then precipitously declined to rarity coincident with increased bed net ownership as national bed net distribution programmes commenced in 2004 and 2006. By 2009, A. gambiae s.s. comprised proportionately ca. 1% of indoor collections and A. arabiensis 99%. In Seme compared to Asembo in 2003, proportionately more larvae were A. gambiae s.s., larval density was higher, and more larval habitats were occupied. As bed net use rose in Seme, the proportion of A. gambiae larvae declined as well. These trends continued to 2009. Parity and malaria infection rates were lower in both species in Asembo (high bed net use) compared to Seme (low bed net use), but host choice did not vary within species in both communities (predominantly cattle for A. arabiensis, humans for A. gambiae s.s.). Conclusions A marked decline of the A. gambiae s.s. population occurred as household ownership of bed nets rose in a region of western Kenya over a 10 year period. The increased bed net coverage likely caused a mass effect on the composition of the A. gambiae s.l. species complex, resulting in the observed proportionate increase in A. arabiensis compared to its closely related sibling species, A. gambiae s.s. These observations are important in evaluating the process of regional malaria elimination, which requires sustained vector control as a primary intervention.
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            Author and article information

            Affiliations
            [1 ]Biomedical and Environmental Thematic Group, Ifakara Health Institute, Dar es Salaam, United Republic of Tanzania
            [2 ]Faculty of Biomedical and Life Sciences, University of Glasgow, Glasgow, United Kingdom
            [3 ]Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America
            [4 ]International Development Research Centre, Ottawa, Ontario, Canada
            [5 ]International Centre for Insect Physiology and Ecology, Nairobi, Kenya
            [6 ]Foundation of the National Institutes of Health, Bethesda, Maryland, United States of America
            [7 ]University of California, Riverside, California, United States of America
            [8 ]Division of Parasitic Diseases, Centers for Disease Control and Prevention, Chamblee, Georgia, United States of America
            [9 ]Division of Epidemiology of Microbial Diseases, School of Public Health, Yale University, New Haven, Connecticut, United States of America
            [10 ]Vector Group, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
            Author notes

            ICMJE criteria for authorship read and met: HMF AD AB CB MG MM JG DF GFK. Agree with the manuscript's results and conclusions: HMF AD AB CB MG MM JG DF GFK. Wrote the first draft of the paper: GFK. Contributed to the writing of the paper: HMF AD AB CB MG MM JG DF. Participated in initial conception of the manuscript: JEG. HMF and GFK drafted the manuscript in consultation with all the other authors, all of whom contributed to the editing and finalization of the submitted draft.

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            Journal
            PLoS Med
            PLoS
            plosmed
            PLoS Medicine
            Public Library of Science (San Francisco, USA )
            1549-1277
            1549-1676
            August 2010
            August 2010
            3 August 2010
            : 7
            : 8
            2914634
            20689800
            09-PLME-PF-3586R2
            10.1371/journal.pmed.1000303
            This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
            Counts
            Pages: 7
            Categories
            Policy Forum
            Public Health and Epidemiology/Environmental Health
            Public Health and Epidemiology/Epidemiology
            Public Health and Epidemiology/Health Policy
            Public Health and Epidemiology/Infectious Diseases

            Medicine

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