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Significant decline in lymphatic filariasis associated with nationwide scale-up of insecticide-treated nets in Zambia.

ABSTRACT: Lymphatic filariasis (LF) is a mosquito-borne disease, broadly endemic in Zambia, and is targeted for elimination by mass drug administration (MDA) of albendazole and diethylcarbamazine citrate (DEC) to at-risk populations. Anopheline mosquitoes are primary vectors of LF in Africa, and it is possible that the significant scale-up of malaria vector control over the past decade may have also impacted LF transmission, and contributed to a decrease in prevalence in Zambia. We therefore aimed to examine the putative association between decreasing LF prevalence and increasing coverage of insecticide-treated mosquito nets (ITNs) for malaria vector control, by comparing LF mapping data collected between 2003-2005 and 2009-2011 to LF sentinel site prevalence data collected between 2012 and 2014, before any anti-LF MDA was started. The coverage of ITNs for malaria was quantified and compared for each site in relation to the dynamics of LF. We found a significant decrease in LF prevalence from the years 2003-2005 (11.5% CI95 6.6; 16.4) to 2012-2014 (0.6% CI95 0.03; 1.1); at the same time, there was a significant scale-up of ITNs across the country from 0.2% (CI95 0.0; 0.3) to 76.1% (CI95 71.4; 80.7) respectively. The creation and comparison of two linear models demonstrated that the geographical and temporal variation in ITN coverage was a better predictor of LF prevalence than year alone. Whilst a causal relationship between LF prevalence and ITN coverage cannot be proved, we propose that the scale-up of ITNs has helped to control Anopheles mosquito populations, which have in turn impacted on LF transmission significantly before the scale-up of MDA. This putative synergy with vector control has helped to put Zambia on track to meet national and global goals of LF elimination by 2020.

SUBMITTER: Nsakashalo-Senkwe M

PROVIDER: S-EPMC5952671 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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Significant decline in lymphatic filariasis associated with nationwide scale-up of insecticide-treated nets in Zambia.

Nsakashalo-Senkwe M M Mwase E E Chizema-Kawesha E E Mukonka V V Songolo P P Masaninga F F Rebollo M P MP Thomas B B Bockarie M J MJ Betts H H Stothard J R JR Kelly-Hope L A LA

Parasite epidemiology and control 20170908 4

Lymphatic filariasis (LF) is a mosquito-borne disease, broadly endemic in Zambia, and is targeted for elimination by mass drug administration (MDA) of albendazole and diethylcarbamazine citrate (DEC) to at-risk populations. Anopheline mosquitoes are primary vectors of LF in Africa, and it is possible that the significant scale-up of malaria vector control over the past decade may have also impacted LF transmission, and contributed to a decrease in prevalence in Zambia. We therefore aimed to exam ...[more]

PMID: 29774291

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Project description:BackgroundInsecticide-treated nets (ITNs) and indoor residual spraying (IRS) of houses provide effective malaria transmission control. There is conflicting evidence about whether it is more beneficial to provide both interventions in combination. A cluster randomised controlled trial was conducted to investigate whether the combination provides added protection compared to ITNs alone.Methods and findingsIn northwest Tanzania, 50 clusters (village areas) were randomly allocated to ITNs only or ITNs and IRS. Dwellings in the ITN+IRS arm were sprayed with two rounds of bendiocarb in 2012. Plasmodium falciparum prevalence rate (PfPR) in children 0.5-14 y old (primary outcome) and anaemia in children <5 y old (secondary outcome) were compared between study arms using three cross-sectional household surveys in 2012. Entomological inoculation rate (secondary outcome) was compared between study arms. IRS coverage was approximately 90%. ITN use ranged from 36% to 50%. In intention-to-treat analysis, mean PfPR was 13% in the ITN+IRS arm and 26% in the ITN only arm, odds ratio = 0.43 (95% CI 0.19-0.97, n = 13,146). The strongest effect was observed in the peak transmission season, 6 mo after the first IRS. Subgroup analysis showed that ITN users were additionally protected if their houses were sprayed. Mean monthly entomological inoculation rate was non-significantly lower in the ITN+IRS arm than in the ITN only arm, rate ratio = 0.17 (95% CI 0.03-1.08).ConclusionsThis is the first randomised trial to our knowledge that reports significant added protection from combining IRS and ITNs compared to ITNs alone. The effect is likely to be attributable to IRS providing added protection to ITN users as well as compensating for inadequate ITN use. Policy makers should consider deploying IRS in combination with ITNs to control transmission if local ITN strategies on their own are insufficiently effective. Given the uncertain generalisability of these findings, it would be prudent for malaria control programmes to evaluate the cost-effectiveness of deploying the combination.Trial registrationwww.ClinicalTrials.gov NCT01697852 Please see later in the article for the Editors' Summary.

Project description: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.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.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.).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.

Project description:BackgroundEfforts to improve the impact of long-lasting insecticidal nets (LLINs) should be informed by understanding of the causes of decay in effect. Holes in LLINs have been estimated to account for 7-11% of loss in effect on vectorial capacity for Plasmodium falciparum malaria in an analysis of repeated cross-sectional surveys of LLINs in Kenya. This does not account for the effect of holes as a cause of net attrition or non-use, which cannot be measured using only cross-sectional data. There is a need for estimates of how much these indirect effects of physical damage on use and attrition contribute to decay in effectiveness of LLINs.MethodsUse, physical integrity, and survival were assessed in a cohort of 4514 LLINs followed for up to 4 years in Kenya. Flow diagrams were used to illustrate how the status of nets, in terms of categories of use, physical integrity, and attrition, changed between surveys carried out at 6-month intervals. A compartment model defined in terms of ordinary differential equations (ODEs) was used to estimate the transition rates between the categories. Effects of physical damage to LLINs on use and attrition were quantified by simulating counterfactuals in which there was no damage.ResultsAllowing for the direct effect of holes, the effect on use, and the effect on attrition, 18% of the impact on vectorial capacity was estimated to be lost because of damage. The estimated median lifetime of the LLINs was 2.9 years, but this was extended to 5.7 years in the counterfactual without physical damage. Nets that were in use were more likely to be in a damaged state than unused nets but use made little direct difference to LLIN lifetimes. Damage was reported as the reason for attrition for almost half of attrited nets, but the model estimated that almost all attrited nets had suffered some damage before attrition.ConclusionsFull quantification of the effects of damage will require measurement of the supply of new nets and of household stocks of unused nets, and also of their impacts on both net use and retention. The timing of mass distribution campaigns is less important than ensuring sufficient supply. In the Kenyan setting, nets acquired damage rapidly once use began and the damage led to rapid attrition. Increasing the robustness of nets could substantially increase their lifetime and impact but the impact of LLIN programmes on malaria transmission is ultimately limited by levels of use. Longitudinal analyses of net integrity data from different settings are needed to determine the importance of physical damage to nets as a driver of attrition and non-use, and the importance of frequent use as a cause of physical damage in different contexts.

Dataset Information

Significant decline in lymphatic filariasis associated with nationwide scale-up of insecticide-treated nets in Zambia.

Publications

Significant decline in lymphatic filariasis associated with nationwide scale-up of insecticide-treated nets in Zambia.

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