Indoor residual spraying (IRS) and long-lasting insecticide-treated bednets (LLINs) are common tools for reducing malaria transmission. We studied a cohort in Uganda with universal access to LLINs after 5 years of sustained IRS to explore LLIN adherence when malaria transmission has been greatly reduced. Eighty households and 526 individuals in Nagongera, Uganda were followed from October 2017 -October 2019. Every two weeks, mosquitoes were collected from sleeping rooms and LLIN adherence the prior night assessed. Episodes of malaria were diagnosed using passive surveillance. Risk factors for LLIN non-adherence were evaluated using multi-level mixed logistic regression. An age-matched case-control design was used to measure the association between LLIN non-adherence and malaria. Across all time periods, and particularly in the last 6 months, non-adherence was higher among both children <5 years (OR 3.31, 95% CI: 2.30-4.75; p<0.001) and school-aged children 5-17 years (OR 6.88, 95% CI: 5.01-9.45; p<0.001) compared to adults. In the first 18 months, collection of fewer mosquitoes was associated with non-adherence (OR 3.25, 95% CI: 2.92-3.63; p<0.001), and, in the last 6 months, residents of poorer households were less adherent (OR 5.1, 95% CI: 1.17-22.2; p = 0.03). Any reported non-adherence over the prior two months was associated with a 15-fold increase in the odds of having malaria (OR 15.0, 95% CI: 1.95 to 114.9; p = 0.009). Knowledge about LLIN use was high, and the most frequently reported barriers to use included heat and low perceived risk of malaria. Children, particularly school-aged, participants exposed to fewer mosquitoes, and those from poorer households, were less likely to use LLINs. Non-adherence to LLINs was associated with an increased risk of malaria. Strategies, such as behavior change communications, should be prioritized to ensure consistent LLIN use even when malaria transmission has been greatly reduced.

Background

Long lasting insecticide-treated bednets (LLINs) are the most widely used tool for preventing malaria. There has been a plateau in progress in the highest burden African countries since 2015, leading to questions about the effectiveness of LLINs. In this study, remote LLIN use monitors were deployed in a cohort in Eastern Uganda to explore how LLIN use interacts with mosquito exposure.

Methods

The SmartNet study included 20 households from May to October 2019. SmartNet devices recorded, every 15 min, whether an LLIN was unfurled or folded up. Unannounced visits were used to assess SmartNet accuracy. Risk factors associated with poor LLIN use were assessed using generalized linear equations. Female Anopheles exposure was estimated by combining hourly probabilities of exposure from human landing catches and measures of density from biweekly CDC light traps in participants rooms. Mosquito exposure averted by LLINs was quantified using SmartNet measurements and age-related differences were estimated using generalized linear equations, adjusting for relevant covariates and household clustering.

Results

96 individuals contributed 5,640 SmartNet observation nights. In 126 unannounced visits, SmartNet had an area under the curve of 0.869 in classifying whether the LLIN was up or down. The rate of non-use was 13.5% of nights (95% CI: 12.6-14.3%). Compared to children under 5, non-use was 1.8 times higher (95% CI: 1.6-2.1; p < 0.001) in children 5-15 years and 2.6 times higher (95% CI: 2.2-3.1; p < 0.001) in participants aged 15-<30years. There was no difference between children under 5 years and adults > 30 years. LLIN use averted 50.3% of female Anopheles mosquito exposure (95% CI: 40.0-60.0%), with decreasing point estimates of efficacy across age groups: from 61.7% (95% CI: 42.6-80.7%) in children under 5 years to 48.0% (95% CI: 29.1-66.8%) in adults over 30.

Conclusions

Objective monitors are accurate and can feasibly be deployed to obtain data about LLIN use. LLINs provided protection from only 50% of female Anopheles mosquito exposure in this cohort and protection was dependent upon age. In assessing the role of LLINs in malaria prevention it is crucial to consider the dynamics between mosquito exposure and LLIN use behaviors.