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      Why is malaria associated with poverty? Findings from a cohort study in rural Uganda

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          Abstract

          Background

          Malaria control and sustainable development are linked, but implementation of ‘multisectoral’ intervention is restricted by a limited understanding of the causal pathways between poverty and malaria. We investigated the relationships between socioeconomic position (SEP), potential determinants of SEP, and malaria in Nagongera, rural Uganda.

          Methods

          Socioeconomic information was collected for 318 children aged six months to 10 years living in 100 households, who were followed for up to 36 months. Mosquito density was recorded using monthly light trap collections. Parasite prevalence was measured routinely every three months and malaria incidence determined by passive case detection. First, we evaluated the association between success in smallholder agriculture (the primary livelihood source) and SEP. Second, we explored socioeconomic risk factors for human biting rate (HBR), parasite prevalence and incidence of clinical malaria, and spatial clustering of socioeconomic variables. Third, we investigated the role of selected factors in mediating the association between SEP and malaria.

          Results

          Relative agricultural success was associated with higher SEP. In turn, high SEP was associated with lower HBR (highest versus lowest wealth index tertile: Incidence Rate Ratio 0.71, 95 % confidence intervals ( CI) 0.54–0.93, P = 0.01) and lower odds of malaria infection in children (highest versus lowest wealth index tertile: adjusted Odds Ratio 0.52, 95 % CI 0.35–0.78, P = 0.001), but SEP was not associated with clinical malaria incidence. Mediation analysis suggested that part of the total effect of SEP on malaria infection risk was explained by house type (24.9 %, 95 % CI 15.8–58.6 %) and food security (18.6 %, 95 % CI 11.6–48.3 %); however, the assumptions of the mediation analysis may not have been fully met.

          Conclusion

          Housing improvements and agricultural development interventions to reduce poverty merit further investigation as multisectoral interventions against malaria. Further interdisplinary research is needed to understand fully the complex pathways between poverty and malaria and to develop strategies for sustainable malaria control.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s40249-016-0164-3) contains supplementary material, which is available to authorized users.

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          Most cited references27

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          Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial.

          Anaemia caused by iron deficiency is common in children younger than age 5 years in eastern Africa. However, there is concern that universal supplementation of children with iron and folic acid in areas of high malaria transmission might be harmful. We did a randomised, placebo-controlled trial, of children aged 1-35 months and living in Pemba, Zanzibar. We assigned children to daily oral supplementation with: iron (12.5 mg) and folic acid (50 mug; n=7950), iron, folic acid, and zinc (n=8120), or placebo (n=8006); children aged 1-11 months received half the dose. Our primary endpoints were all-cause mortality and admission to hospital. Analyses were by intention to treat. This study is registered as an International Standard Randomised Controlled Trial, number ISRCTN59549825. The iron and folic acid-containing groups of the trial were stopped early on Aug 19, 2003, on the recommendation of the data and safety monitoring board. To this date, 24 076 children contributed a follow-up of 25,524 child-years. Those who received iron and folic acid with or without zinc were 12% (95% CI 2-23, p=0.02) more likely to die or need treatment in hospital for an adverse event and 11% (1-23%, p=0.03) more likely to be admitted to hospital; there were also 15% (-7 to 41, p=0.19) more deaths in these groups. Routine supplementation with iron and folic acid in preschool children in a population with high rates of malaria can result in an increased risk of severe illness and death. In the presence of an active programme to detect and treat malaria and other infections, iron-deficient and anaemic children can benefit from supplementation. However, supplementation of those who are not iron deficient might be harmful. As such, current guidelines for universal supplementation with iron and folic acid should be revised.
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            The evidence for improving housing to reduce malaria: a systematic review and meta-analysis

            Background The global malaria burden has fallen since 2000, sometimes before large-scale vector control programmes were initiated. While long-lasting insecticide-treated nets and indoor residual spraying are highly effective interventions, this study tests the hypothesis that improved housing can reduce malaria by decreasing house entry by malaria mosquitoes. Methods A systematic review and meta-analysis was conducted to assess whether modern housing is associated with a lower risk of malaria than traditional housing, across all age groups and malaria-endemic settings. Six electronic databases were searched to identify intervention and observational studies published from 1 January, 1900 to 13 December, 2013, measuring the association between house design and malaria. The primary outcome measures were parasite prevalence and incidence of clinical malaria. Crude and adjusted effects were combined in fixed- and random-effects meta-analyses, with sub-group analyses for: overall house type (traditional versus modern housing); screening; main wall, roof and floor materials; eave type; ceilings and elevation. Results Of 15,526 studies screened, 90 were included in a qualitative synthesis and 53 reported epidemiological outcomes, included in a meta-analysis. Of these, 39 (74 %) showed trends towards a lower risk of epidemiological outcomes associated with improved house features. Of studies assessing the relationship between modern housing and malaria infection (n = 11) and clinical malaria (n = 5), all were observational, with very low to low quality evidence. Residents of modern houses had 47 % lower odds of malaria infection compared to traditional houses (adjusted odds ratio (OR) 0°53, 95 % confidence intervals (CI) 0°42–0°67, p < 0°001, five studies) and a 45–65 % lower odds of clinical malaria (case–control studies: adjusted OR 0°35, 95 % CI 0°20–0°62, p <0°001, one study; cohort studies: adjusted rate ratio 0°55, 95 % CI 0°36–0°84, p = 0°005, three studies). Evidence of a high risk of bias was found within studies. Conclusions Despite low quality evidence, the direction and consistency of effects indicate that housing is an important risk factor for malaria. Future research should evaluate the protective effect of specific house features and incremental housing improvements associated with socio-economic development. Electronic supplementary material The online version of this article (doi:10.1186/s12936-015-0724-1) contains supplementary material, which is available to authorized users.
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              Malaria transmission, infection, and disease at three sites with varied transmission intensity in Uganda: implications for malaria control.

              The intensification of control interventions has led to marked reductions in malaria burden in some settings, but not others. To provide a comprehensive description of malaria epidemiology in Uganda, we conducted surveillance studies over 24 months in 100 houses randomly selected from each of three subcounties: Walukuba (peri-urban), Kihihi (rural), and Nagongera (rural). Annual entomological inoculation rate (aEIR) was estimated from monthly Centers for Disease Control and Prevention (CDC) light trap mosquito collections. Children aged 0.5-10 years were provided long-lasting insecticidal nets (LLINs) and followed for measures of parasite prevalence, anemia and malaria incidence. Estimates of aEIR were 2.8, 32.0, and 310 infectious bites per year, and estimates of parasite prevalence 7.4%, 9.3%, and 28.7% for Walukuba, Kihihi, and Nagongera, respectively. Over the 2-year study, malaria incidence per person-years decreased in Walukuba (0.51 versus 0.31, P = 0.001) and increased in Kihihi (0.97 versus 1.93, P < 0.001) and Nagongera (2.33 versus 3.30, P < 0.001). Of 2,582 episodes of malaria, only 8 (0.3%) met criteria for severe disease. The prevalence of anemia was low and not associated with transmission intensity. In our cohorts, where LLINs and prompt effective treatment were provided, the risk of complicated malaria and anemia was extremely low. However, malaria incidence was high and increased over time at the two rural sites, suggesting improved community-wide coverage of LLIN and additional malaria control interventions are needed in Uganda.
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                Author and article information

                Contributors
                lucy.tusting@lshtm.ac.uk
                jrek@idrc-uganda.org
                emmy3md@yahoo.com
                Sarah.staedke@lshtm.ac.uk
                mkamya@infocom.co.ug
                Jorge.Cano@lshtm.ac.uk
                Christian.bottomley@lshtm.ac.uk
                Dj3@soas.ac.uk
                gdorsey@medsfgh.ucsf.edu
                s.w.lindsay@durham.ac.uk
                jo.lines@lshtm.ac.uk
                Journal
                Infect Dis Poverty
                Infect Dis Poverty
                Infectious Diseases of Poverty
                BioMed Central (London )
                2049-9957
                4 August 2016
                4 August 2016
                2016
                : 5
                : 78
                Affiliations
                [1 ]Department of Disease Control, London School of Hygiene & Tropical Medicine, London, UK
                [2 ]Big Data Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK
                [3 ]Infectious Diseases Research Collaboration, Kampala, Uganda
                [4 ]Department of Clinical Research, London School of Hygiene and Tropical Medicine, London, UK
                [5 ]School of Medicine, Makerere University College of Health Sciences, Kampala, Uganda
                [6 ]MRC Tropical Epidemiology Group, London School of Hygiene and Tropical Medicine, London, UK
                [7 ]Department of Economics, SOAS, University of London, London, UK
                [8 ]Department of Medicine, University of California, San Francisco, USA
                [9 ]School of Biological and Biomedical Sciences, Durham University, Durham, UK
                Article
                164
                10.1186/s40249-016-0164-3
                4972958
                27488674
                2e001b95-403c-44a7-ad3d-fb1dd602abfa
                © The Author(s). 2016

                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
                : 18 February 2016
                : 24 June 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: U19AI089674
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award ID: OPP1053338
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                malaria,socioeconomic,poverty,development,housing,wealth index,uganda

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