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Review 3: "Dramatic Resurgence of Malaria after 7 Years of Intensive Vector Control Interventions in Eastern Uganda"

The study was highly rated for demonstrating that changes in the insecticides used in indoor residual spraying are linked to a resurgence of malaria in Eastern Uganda.

Published onMay 16, 2024
Review 3: "Dramatic Resurgence of Malaria after 7 Years of Intensive Vector Control Interventions in Eastern Uganda"
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key-enterThis Pub is a Review of
Dramatic resurgence of malaria after 7 years of intensive vector control interventions in Eastern Uganda
Dramatic resurgence of malaria after 7 years of intensive vector control interventions in Eastern Uganda
Description

Abstract Background Tororo District, Uganda experienced a dramatic decrease in malaria burden from 2015-19 following 5 years of indoor residual spraying (IRS) with carbamate (Bendiocarb) and then organophosphate (Actellic) insecticides. However, a marked resurgence occurred in 2020, which coincided with a change to a clothianidin-based IRS formulations (Fludora Fusion/SumiShield). To quantify the magnitude of the resurgence, investigate causes, and evaluate the impact of a shift back to IRS with Actellic in 2023, we assessed changes in malaria metrics in regions within and near Tororo District.Methods Malaria surveillance data from Nagongera Health Center, Tororo District was included from 2011-2023. In addition, a cohort of 667 residents from 84 houses was followed from August 2020 through September 2023 from an area bordering Tororo and neighboring Busia District, where IRS has never been implemented. Cohort participants underwent passive surveillance for clinical malaria and active surveillance for parasitemia every 28 days. Mosquitoes were collected in cohort households every 2 weeks using CDC light traps. Female Anopheles were speciated and tested for sporozoites and phenotypic insecticide resistance. Temporal comparisons of malaria metrics were stratified by geographic regions.Findings At Nagongera Health Center average monthly malaria cases varied from 419 prior to implementation of IRS; to 56 after 5 years of IRS with Bendiocarb and Actellic; to 1591 after the change in IRS to Fludora Fusion/SumiShield; to 155 after a change back to Actellic. Among cohort participants living away from the border in Tororo, malaria incidence increased over 8-fold (0.36 vs. 2.97 episodes per person year, p<0.0001) and parasite prevalence increased over 4-fold (17% vs. 70%, p<0.0001) from 2021 to 2022 when Fludora Fusion/SumiShield was used. Incidence decreased almost 5-fold (2.97 vs. 0.70, p<0.0001) and prevalence decreased by 39% (70% vs. 43%, p<0.0001) after shifting back to Actellic. There was a similar pattern among those living near the border in Tororo, with increased incidence between 2021 and 2022 (0.93 vs. 2.40, p<0.0001) followed by a decrease after the change to Actellic (2.40 vs. 1.33, p<0.001). Among residents of Busia, malaria incidence did not change significantly over the 3 years of observation. Malaria resurgence in Tororo was temporally correlated with the replacement of An. gambiae s.s. by An. funestus as the primary vector, with a marked decrease in the density of An. funestus following the shift back to IRS with Actellic. In Busia, An. gambiae s.s. remained the primary vector throughout the observation period. Sporozoite rates were approximately 50% higher among An. funestus compared to the other common malaria vectors. Insecticide resistance phenotyping of An. funestus revealed high tolerance to clothianidin, but full susceptibility to Actellic.Conclusions A dramatic resurgence of malaria in Tororo was temporally associated with a change to clothianidin-based IRS formulations and emergence of An. funestus as the predominant vector. Malaria decreased after a shift back to IRS with Actellic. This study highlights the ability of malaria vectors to rapidly circumvent control efforts and the importance of high-quality surveillance systems to assess the impact of malaria control interventions and generate timely, actionable data.

RR:C19 Evidence Scale rating by reviewer:

  • Reliable. The main study claims are generally justified by its methods and data. The results and conclusions are likely to be similar to the hypothetical ideal study. There are some minor caveats or limitations, but they would/do not change the major claims of the study. The study provides sufficient strength of evidence on its own that its main claims should be considered actionable, with some room for future revision.

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Review: This is a clear and informative study, well written and comprehensive. Kamya et al describe an observational study to confirm the causal influences for a resurgence of malaria in a district where IRS has been in place for nearly a decade. Combining epidemiological and entomological data, the authors conclude that the change in IRS insecticide  allowed an increase in density of resistant An. funestus  replacing the less effective vector An. arabiensis. Where no IRS had been implemented, the vector species composition was not altered and thus, although remaining high, malaria incidence and prevalence did not show the same pattern of resurgence and decrease after the potentially ineffective insecticide was replaced.

General typo note: many end of sentence references are listed after the full stop.

  • L81 – Uganda has universal distribution of LLINs – any info on usage?

  • L83 -  ‘one of the largest IRS programmes…’  - in relation to?  Is there a reference?

  • L87 – ‘our group’ replace with name of institute

  • L100 – [comment] – did the authors suspect the cause of the resurgence was to do with the change in IRS insecticide when the investigation was started? Was the reversion back to the organophosphate IRS a consequence of the study – or is this a retrospective study done more as an observation of how the different formulations may have had an impact?

  • L123 – why was the IRS compound changed to Actellic in 2016? Part of a considered rotations scheme? (same question for the change to clothianidin 2020)

  • L127 – the decision to revert to Actellic was made due to this study?

  • L133 – did the use of PBO nets from 2020 have an impact on malaria in Busia?

  • L139 – how many sites are regularly assessed/surveyed and how often? (for spatial and temporal trends) or are these based on cases presented at the health centre?

  • L222 - italicise  ‘Anopheles

  • L227 – why was IR assessed in mosquitoes from neighbouring district and not the district where the study was conducted?

  • L511 – other contributing factors could also be explored relating to the vector biology and ecology – the study indicates that it was a lack of control of An. funestus that may have caused much of the resurgence – and An. funestus has quite different behaviour from An. gambiae and An. arabiensis. For example, larval sites can be permanent or semi-permanent compared to the more transient larval sites of An. gambiae and An. funestus can replace An. arabiensis  in a process of temporal succession as the species prefers sites with more emergent vegetation compared to a more open larval sites of An. arabiensis, so some consideration of the surrounding environment (agriculture, swamps etc) would be useful for context – as well as other factors thar may influence the vectors – was rainfall lower over the study period? – potentially reducing An. gambiae but having little impact on An. funestus…

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