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      Malaria prevention practices and associated environmental risk factors in a rural community in Wakiso district, Uganda

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          Abstract

          Background

          Besides use of insecticide-treated mosquito nets (ITNs) and indoor residual spraying (IRS), other complimentary measures including suitable housing structures, and environmental management that reduce breeding of malaria vectors, can be implemented at households to prevent the disease. However, most studies on malaria prevention have focused mainly on ITNs and IRS. The aim of this study was therefore to assess malaria prevention practices beyond ITNs and IRS, and associated environmental risk factors including housing structure in rural Wakiso district, Uganda.

          Methods

          A clustered cross-sectional survey was conducted among 727 households in Wakiso district. Data were collected using an interviewer-administered questionnaire and observational checklist. The questionnaire assessed participants’ household practices on malaria prevention, whereas the checklist recorded environmental risk factors for malaria transmission, and structural condition of houses. Poisson regression modeling was used to identify factors associated with use of mosquito nets by households.

          Results

          Of the 727 households, 471 (64.8%) owned at least one mosquito net. Use of mosquito nets by households was higher with increasing education level of participants—primary (aPR = 1.27 [95% CI: 1.00–1.60]), secondary (ordinary level) (aPR = 1.47 [95% CI: 1.16–1.85]) and advanced level / tertiary (aPR = 1.55 [95% CI: 1.19–2.01]), and higher household income (aPR = 1.09 [95% CI: 1.00–1.20]). Additionally, participants who were not employed were less likely to have mosquito nets used in their households (aPR = 0.83 [95% CI: 0.70–0.98]). Houses that had undergone IRS in the previous 12 months were 42 (5.8%), while 220 (43.2%) households closed their windows before 6.00 pm. Environmental risk factors found at households included presence of vessels that could potentially hold water for mosquito breeding 414 (56.9%), and stagnant water in compounds 144 (19.8%). Several structural deficiencies on houses that could promote entry of mosquitoes were found such as lack of screening in ventilators 645 (94.7%), and external doors not fitting perfectly into walls hence potential for mosquito entry 305 (42.0%).

          Conclusion

          There is need to increase coverage and utilisation of ITNs and IRS for malaria prevention in Wakiso district, Uganda. In addition, other malaria prevention strategies such as environmental management, and improving structural condition of houses are required to strengthen existing malaria prevention approaches.

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          Most cited references36

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          Insecticide-treated bed nets and curtains for preventing malaria.

          C Lengeler (2004)
          Malaria is an important cause of illness and death in many parts of the world, especially in sub-Saharan Africa. There has been a renewed emphasis on preventive measures at community and individual levels. Insecticide-treated nets (ITNs) are the most prominent malaria preventive measure for large-scale deployment in highly endemic areas. To assess the impact of insecticide-treated bed nets or curtains on mortality, malarial illness (life-threatening and mild), malaria parasitaemia, anaemia, and spleen rates. I searched the Cochrane Infectious Diseases Group trials register (January 2003), CENTRAL (The Cochrane Library, Issue 1, 2003), MEDLINE (1966 to October 2003), EMBASE (1974 to November 2002), LILACS (1982 to January 2003), and reference lists of reviews, books, and trials. I handsearched journals, contacted researchers, funding agencies, and net and insecticide manufacturers. Individual and cluster randomized controlled trials of insecticide-treated bed nets or curtains compared to nets without insecticide or no nets. Trials including only pregnant women were excluded. The reviewer and two independent assessors reviewed trials for inclusion. The reviewer assessed trial methodological quality and extracted and analysed data. Fourteen cluster randomized and eight individually randomized controlled trials met the inclusion criteria. Five trials measured child mortality: ITNs provided 17% protective efficacy (PE) compared to no nets (relative rate 0.83, 95% confidence interval (CI) 0.76 to 0.90), and 23% PE compared to untreated nets (relative rate 0.77, 95% CI 0.63 to 0.95). About 5.5 lives (95% CI 3.39 to 7.67) can be saved each year for every 1000 children protected with ITNs. In areas with stable malaria, ITNs reduced the incidence of uncomplicated malarial episodes in areas of stable malaria by 50% compared to no nets, and 39% compared to untreated nets; and in areas of unstable malaria: by 62% for compared to no nets and 43% compared to untreated nets for Plasmodium falciparum episodes, and by 52% compared to no nets and 11% compared to untreated nets for P. vivax episodes. When compared to no nets and in areas of stable malaria, ITNs also had an impact on severe malaria (45% PE, 95% CI 20 to 63), parasite prevalence (13% PE), high parasitaemia (29% PE), splenomegaly (30% PE), and their use improved the average haemoglobin level in children by 1.7% packed cell volume. ITNs are highly effective in reducing childhood mortality and morbidity from malaria. Widespread access to ITNs is currently being advocated by Roll Back Malaria, but universal deployment will require major financial, technical, and operational inputs.
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            Mosquito behavior and vector control.

            Effective indoor residual spraying against malaria vectors depends on whether mosquitoes rest indoors (i.e., endophilic behavior). This varies among species and is affected by insecticidal irritancy. Exophilic behavior has evolved in certain populations exposed to prolonged spraying programs. Optimum effectiveness of insecticide-treated nets presumably depends on vectors biting at hours when most people are in bed. Time of biting varies among different malaria vector species, but so far there is inconclusive evidence for these evolving so as to avoid bednets. Use of an untreated net diverts extra biting to someone in the same room who is without a net. Understanding choice of oviposition sites and dispersal behavior is important for the design of successful larval control programs including those using predatory mosquito larvae. Prospects for genetic control by sterile males or genes rendering mosquitoes harmless to humans will depend on competitive mating behavior. These methods are hampered by the immigration of monogamous, already-mated females.
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              Indoor residual spraying for preventing malaria.

              Primary malaria prevention on a large scale depends on two vector control interventions: indoor residual spraying (IRS) and insecticide-treated mosquito nets (ITNs). Historically, IRS has reduced malaria transmission in many settings in the world, but the health effects of IRS have never been properly quantified. This is important, and will help compare IRS with other vector control interventions. To quantify the impact of IRS alone, and to compare the relative impacts of IRS and ITNs, on key malariological parameters. We searched the Cochrane Infectious Diseases Group Specialized Register (September 2009), CENTRAL (The Cochrane Library 2009, Issue 3), MEDLINE (1966 to September 2009), EMBASE (1974 to September 2009), LILACS (1982 to September 2009), mRCT (September 2009), reference lists, and conference abstracts. We also contacted researchers in the field, organizations, and manufacturers of insecticides (June 2007). Cluster randomized controlled trials (RCTs), controlled before-and-after studies (CBA) and interrupted time series (ITS) of IRS compared to no IRS or ITNs. Studies examining the impact of IRS on special groups not representative of the general population, or using insecticides and dosages not recommended by the World Health Organization (WHO) were excluded. Two authors independently reviewed trials for inclusion. Two authors extracted data, assessed risk of bias and analysed the data. Where possible, we adjusted confidence intervals (CIs) for clustering. Studies were grouped into those comparing IRS with no IRS, and IRS compared with ITNs, and then stratified by malaria endemicity. IRS versus no IRSStable malaria (entomological inoculation rate (EIR) > 1): In one RCT in Tanzania IRS reduced re-infection with malaria parasites detected by active surveillance in children following treatment; protective efficacy (PE) 54%. In the same setting, malaria case incidence assessed by passive surveillance was marginally reduced in children aged one to five years; PE 14%, but not in children older than five years (PE -2%). In the IRS group, malaria prevalence was slightly lower but this was not significant (PE 6%), but mean haemoglobin was higher (mean difference 0.85 g/dL).In one CBA trial in Nigeria, IRS showed protection against malaria prevalence during the wet season (PE 26%; 95% CI 20 to 32%) but not in the dry season (PE 6%; 95% CI -4 to 15%). In one ITS in Mozambique, the prevalence was reduced substantially over a period of 7 years (from 60 to 65% prevalence to 4 to 8% prevalence; the weighted PE before-after was 74% (95% CI 72 to 76%).Unstable malaria (EIR 1): Only one RCT was done in an area of stable transmission (in Tanzania). When comparing parasitological re-infection by active surveillance after treatment in short-term cohorts, ITNs appeared better, but it was likely not to be significant as the unadjusted CIs approached 1 (risk ratio IRS:ITN = 1.22). When the incidence of malaria episodes was measured by passive case detection, no difference was found in children aged one to five years (risk ratio = 0.88, direction in favour of IRS). No difference was found for malaria prevalence or haemoglobin.Unstable malaria (EIR < 1): Two studies; for incidence and prevalence, the malaria rates were higher in the IRS group compared to the ITN group in one study. Malaria incidence was higher in the IRS arm in India (risk ratio IRS:ITN = 1.48) and in South Africa (risk ratio 1.34 but the cluster unadjusted CIs included 1). For malaria prevalence, ITNs appeared to give better protection against any infection compared to IRS in India (risk ratio IRS:ITN = 1.70) and also for both P. falciparum (risk ratio IRS:ITN = 1.78) and P. vivax (risk ratio IRS:ITN = 1.37). Historical and programme documentation has clearly established the impact of IRS. However, the number of high-quality trials are too few to quantify the size of effect in different transmission settings. The evidence from randomized comparisons of IRS versus no IRS confirms that IRS reduces malaria incidence in unstable malaria settings, but randomized trial data from stable malaria settings is very limited. Some limited data suggest that ITN give better protection than IRS in unstable areas, but more trials are needed to compare the effects of ITNs with IRS, as well as to quantify their combined effects.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 October 2018
                2018
                : 13
                : 10
                : e0205210
                Affiliations
                [1 ] Department of Disease Control and Environmental Health, School of Public Health, Makerere University College of Health Sciences, Kampala, Uganda
                [2 ] Uganda Virus Research Institute, Entebbe, Uganda
                [3 ] Cardiff School of Health Sciences, Cardiff Metropolitan University, Cardiff, Wales, United Kingdom
                [4 ] Department of Epidemiology and Biostatistics, School of Public Health, Makerere University College of Health Sciences, Kampala, Uganda
                [5 ] Medical Research Council, Uganda Virus Research Institute, Entebbe, Uganda
                [6 ] School of Sciences, Nkumba University, Entebbe, Uganda
                Instituto Rene Rachou, BRAZIL
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-3262-3918
                Article
                PONE-D-18-19844
                10.1371/journal.pone.0205210
                6177175
                30300396
                a2042c06-cf97-4ba5-95bc-fa97ddee83c0
                © 2018 Musoke et al

                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
                : 4 July 2018
                : 20 September 2018
                Page count
                Figures: 0, Tables: 4, Pages: 13
                Funding
                Funded by: Training Health Researchers into Vocational Excellence
                Award ID: 087540
                Award Recipient :
                The work was supported by Training Health Researchers into Vocational Excellence (THRiVE) in East Africa, grant number 087540, funded by Wellcome Trust. This investigation also received financial support from TDR, the Special Programme for Research and Training in Tropical Diseases, co-sponsored by UNICEF, UNDP, the World Bank and WHO. DM received support from the Africa Research Excellence Fund (AREF) grant number MUSOKEMRF-157-0013-F-MUSOK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Parasitic Diseases
                Malaria
                Medicine and Health Sciences
                Tropical Diseases
                Malaria
                Biology and Life Sciences
                Agriculture
                Agrochemicals
                Insecticides
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Ecology and Environmental Sciences
                Environmental Impacts
                Engineering and Technology
                Equipment
                Laboratory Equipment
                Ventilators
                People and Places
                Geographical Locations
                Africa
                Uganda
                Medicine and Health Sciences
                Women's Health
                Maternal Health
                Pregnancy
                Medicine and Health Sciences
                Women's Health
                Obstetrics and Gynecology
                Pregnancy
                Ecology and Environmental Sciences
                Environmental Management
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                All relevant data are within the paper and its Supporting Information files.

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