Measures of Malaria Burden after Long-Lasting Insecticidal Net Distribution and Indoor Residual Spraying at Three Sites in Uganda: A Prospective Observational Study

Abstract

BackgroundLong-lasting insecticidal nets (LLINs) and indoor residual spraying of insecticide (IRS) are the primary vector control interventions used to prevent malaria in Africa. Although both interventions are effective in some settings, high-quality evidence is rarely available to evaluate their effectiveness following deployment by a national malaria control program. In Uganda, we measured changes in key malaria indicators following universal LLIN distribution in three sites, with the addition of IRS at one of these sites.Methods and FindingsComprehensive malaria surveillance was conducted from October 1, 2011, to March 31, 2016, in three sub-counties with relatively low (Walukuba), moderate (Kihihi), and high transmission (Nagongera). Between 2013 and 2014, universal LLIN distribution campaigns were conducted in all sites, and in December 2014, IRS with the carbamate bendiocarb was initiated in Nagongera. High-quality surveillance evaluated malaria metrics and mosquito exposure before and after interventions through (a) enhanced health-facility-based surveillance to estimate malaria test positivity rate (TPR), expressed as the number testing positive for malaria/number tested for malaria (number of children tested for malaria: Walukuba = 42,833, Kihihi = 28,790, and Nagongera = 38,690); (b) cohort studies to estimate the incidence of malaria, expressed as the number of episodes per person-year [PPY] at risk (number of children observed: Walukuba = 340, Kihihi = 380, and Nagongera = 361); and (c) entomology surveys to estimate household-level human biting rate (HBR), expressed as the number of female Anopheles mosquitoes collected per house-night of collection (number of households observed: Walukuba = 117, Kihihi = 107, and Nagongera = 107). The LLIN distribution campaign substantially increased LLIN coverage levels at the three sites to between 65.0% and 95.5% of households with at least one LLIN. In Walukuba, over the 28-mo post-intervention period, universal LLIN distribution was associated with no change in the incidence of malaria (0.39 episodes PPY pre-intervention versus 0.20 post-intervention; adjusted rate ratio [aRR] = 1.02, 95% CI 0.36–2.91, p = 0.97) and non-significant reductions in the TPR (26.5% pre-intervention versus 26.2% post-intervention; aRR = 0.70, 95% CI 0.46–1.06, p = 0.09) and HBR (1.07 mosquitoes per house-night pre-intervention versus 0.71 post-intervention; aRR = 0.41, 95% CI 0.14–1.18, p = 0.10). In Kihihi, over the 21-mo post-intervention period, universal LLIN distribution was associated with a reduction in the incidence of malaria (1.77 pre-intervention versus 1.89 post-intervention; aRR = 0.65, 95% CI 0.43–0.98, p = 0.04) but no significant change in the TPR (49.3% pre-intervention versus 45.9% post-intervention; aRR = 0.83, 95% 0.58–1.18, p = 0.30) or HBR (4.06 pre-intervention versus 2.44 post-intervention; aRR = 0.71, 95% CI 0.30–1.64, p = 0.40). In Nagongera, over the 12-mo post-intervention period, universal LLIN distribution was associated with a reduction in the TPR (45...

Geostatistical modelling of malaria indicator survey data to assess the effects of interventions on the geographical distribution of malaria prevalence in children less than 5 years in Uganda

“…This finding contradicts findings from other studies that have reported ITN efficacy [32,34,35] and effectiveness [2,16,36,37]. However, these results are consistent to recent findings for Burkina Faso [12], Nigeria [11], Tanzania [9], and Senegal [10].…”

“…Uganda has the fourth highest number of Plasmodium falciparum infections [1] and some of the highest reported malaria transmission rates in the world [2]. Ninety five percent of the country has stable malaria transmission, with the rest having low and unstable transmission with potential for epidemics.…”

Marked variation in prevalence of malaria-protective human genetic polymorphisms across Uganda

“…The sites differed markedly, with very high transmission intensity, parasite prevalence, and malaria incidence in Tororo District, lower levels of all of these parameters in Kanungu District, and the lowest levels in Jinja District. Of note, malaria transmission was considerably greater in earlier surveys of Jinja District, and transmission has since decreased greatly in Tororo District after a campaign of indoor residual spraying of insecticide that was launched in 2014 (Katureebe et al, 2016). Historically, it appears that malaria transmission intensity followed the rank order Tororo > Jinja > Kanungu (Yeka et al, 2012).…”

“…The three Ugandan study sites differed greatly in recent malaria transmission intensity (Kamya et al, 2015; Katureebe et al, 2016). Tororo District has had very high transmission intensity recorded, with entomologic inoculation rates >300 infectious bites per year, although very recently transmission intensity has decreased due to an intensive IRS campaign.…”

Transcriptomic analysis of insecticide resistance in the lymphatic filariasis vectorCulex quinquefasciatus

“…This is a much lower frequency than observed in other vector mosquitoes where carbamates are routinely used in vector control 58 . Whilst insecticides linked to selection of A ce- 1 resistant alleles have not been officially applied for vector control in the studied area for over one decade 59,60 indoor residual spraying (IRS) using bendiocarb was conducted in Tororo from December 2014 - February 2015 61,62 , after the period of collection of these samples, and hence this allele frequency is higher than expected. Nevertheless, an indirect source of insecticide exposure due to agricultural activities could also be shaping the insecticide resistance as described for C. quinquefasciatus populations from Iran 63 .…”