Outdoor Residual Insecticide Spraying (ODRS), a New Approach for the Control of the Exophilic Vectors of Human Visceral Leishmaniasis: Phlebotomus orientalis in East Africa

Abstract

Visceral Leishmaniasis (VL) due to Leishmania donovani is a neglected protozoan parasitic disease in humans, which is usually fatal if untreated. Phlebotomus orientalis, the predominant VL vector in East Africa, is a highly exophilic/exophagic species that poses a major challenge to current Integrated Vector Management (IVM). Here we report results of pilot studies conducted in rural villages in Gedarif state, Sudan, to evaluate outdoor residual spraying of 20mg active ingredient (a.i.) /m2 deltamethrin insecticide applied to the characteristic household compound boundary reed fence and to the outside of household buildings (Outdoor Residual Insecticide Spraying, ODRS), and as an alternative, spraying restricted to the boundary fence only (Restricted Outdoor Residual Insecticide Spraying, RODRS). Four to six clusters of 20 households were assigned to insecticide treatments or control in three experiments. Changes in sand fly numbers were monitored over 2,033 trap-nights over 43-76 days follow-up in four sentinel houses per cluster relative to unsprayed control clusters. Sand fly numbers were monitored by sticky traps placed on the ground on the inside ("outdoor") and the outside ("peridomestic") of the boundary fence, and by CDC light traps suspended outdoors in the household compound. The effects of ODRS on sand fly numbers inside sleeping huts were monitored by insecticide knockdown. After a single application, ODRS reduced P. orientalis abundance by 83%-99% in outdoor and peridomestic trap locations. ODRS also reduced numbers of P. orientalis found resting inside sleeping huts. RODRS reduced outdoor and peridomestic P. orientalis by 60%-88%. By direct comparison, RODRS was 58%-100% as effective as ODRS depending on the trapping method. These impacts were immediate on intervention and persisted during follow-up, representing a large fraction of the P. orientalis activity season. Relative costs of ODRS and RODRS delivery were $5.76 and $3.48 per household, respectively. The study demonstrates the feasibility and high entomological efficacy of ODRS and RODRS, and the expected low costs relative to current IVM practises. These methods represent novel sand fly vector control tools against predominantly exophilic/exophagic sand fly vectors, aimed to lower VL burdens in Sudan, with potential application in other endemic regions in East Africa.

Fig 1. Map of Gedarif state, Sudan, showing location of Jebel-Algana and Umsalala study villages in relation to Tabarakallah and Umelkher kala azar treatment centers.

Fig 2. Images of typical household layout in VL endemic villages in Gedarif state, eastern Sudan (this example in Jebel-Algana study village).

Each house consists of 2–4 thatched grass huts surrounded by a tall thatched reed fence that provides privacy. (A) Acacia and Balanites trees, associated with P. orientalis vectors, are commonly present within the property boundary, and (B) in the narrow earthen streets that separate household blocks. During the VL transmission season people sleep outside in within the household yard.

Fig 3. Variations in the natural numbers of P. orientalis at households in Jebel-Algana and Umslala villages, Gedarif state, Sudan. Sand flies were captured by CDC light traps and sticky traps at untreated households before (pre-intervention) and after treatment (post-intervention).

Houses labelled by their post-intervention subsequent assignment to full (ODRS) or restricted (RODRS) outdoor residual insecticide spraying, or as untreated controls (C). Data are aggregated for the three independent experiments: Exp. 1 conducted in Jebel-Alagna, 9th-16th June 2016; Exp. 2 conducted in Umsalala village, 2nd May-16th June 2017; and Exp. 3 conducted in Jebel-Algana, 31st March-20th June 2017. Error bars represent the interquartile range.

Fig 4. Effects of outdoor residual spraying of insecticide (ODRS) on the numbers of P. orientalis sand flies in Jebel-Algana village, Gedarif state, Sudan.

Sand flies were captured by sticky traps (ST) set at outdoor sites (A), and at peridomestic sites (B) during 1–4 days pre-intervention and 1–4 days post-intervention. Each bar represents the median numbers of P. orientalis from 32 trap nights (i.e. 4 trap nights at 4 houses in two clusters each). Error bars represent the interquartile range. Sand fly trapping was conducted between 9th -16th June 2016.

Fig 5

Effects of outdoor residual spraying of insecticides (ODRS) on the numbers of P. orientalis in Umsalala village, Gedarif state, Sudan. Sand flies were captured by sticky traps set at outdoor sites (A) and peridomestic sites (B), and by CDC light traps set at outdoor sites (C). Each point represents the median numbers of P. orientalis from 10–14 trap nights (A & B), or 15–16 trap nights with exception of 23–24 trap nights on day 43 (C). Error bars represent the interquartile range. Note differences in the Y-axis range. Sand fly trapping was conducted between 2nd May-16th June 2017.

Fig 6. Effects of full (ODRS) and restricted (RODRS) outdoor residual spraying of insecticide on the numbers of P. orientalis in Jebel-Algana village, Gedarif state, Sudan.

Sandflies were captured by sticky traps set at outdoor sites (A) and peridomestic sites (B) and by CDC light traps set at outdoor sites (C). Each point represents the median numbers of P. orientalis from 16 trap nights, except 32 trap nights on days -4 and +4, and 19–21 trap nights on day 76 in (C). Error bars represent the interquartile range. Note differences in the Y-axis range. Sand fly trapping was conducted between 31st March-20th June 2017.