Malaria vector species composition and entomological indices following indoor residual spraying in regions bordering Lake Victoria, Tanzania

Abstract

Background: Vector control through long-lasting insecticidal nets (LLINs) and focal indoor residual spraying (IRS) is a major component of the Tanzania national malaria control strategy. In mainland Tanzania, IRS has been conducted annually around Lake Victoria basin since 2007. Due to pyrethroid resistance in malaria vectors, use of pyrethroids for IRS was phased out and from 2014 to 2017 pirimiphos-methyl (Actellic® 300CS) was sprayed in regions of Kagera, Geita, Mwanza, and Mara. Entomological surveillance was conducted in 10 sprayed and 4 unsprayed sites to determine the impact of IRS on entomological indices related to malaria transmission risk.

Methods: WHO cone bioassays were conducted monthly on interior house walls to determine residual efficacy of pirimiphos-methyl CS. Indoor CDC light traps with or without bottle rotator were hung next to protected sleepers indoors and also set outdoors (unbaited) as a proxy measure for indoor and outdoor biting rate and time of biting. Prokopack aspirators were used indoors to capture resting malaria vectors. A sub-sample of Anopheles was tested by PCR to determine species identity and ELISA for sporozoite rate.

Results: Annual IRS with Actellic® 300CS from 2015 to 2017 was effective on sprayed walls for a mean of 7 months in cone bioassay. PCR of 2016 and 2017 samples showed vector populations were predominantly Anopheles arabiensis (58.1%, n = 4,403 IRS sites, 58%, n = 2,441 unsprayed sites). There was a greater proportion of Anopheles funestus sensu stricto in unsprayed sites (20.4%, n = 858) than in sprayed sites (7.9%, n = 595) and fewer Anopheles parensis (2%, n = 85 unsprayed, 7.8%, n = 591 sprayed). Biting peaks of Anopheles gambiae sensu lato (s.l.) followed periods of rainfall occurring between October and April, but were generally lower in sprayed sites than unsprayed. In most sprayed sites, An. gambiae s.l. indoor densities increased between January and February, i.e., 10-12 months after IRS. The predominant species An. arabiensis had a sporozoite rate in 2017 of 2.0% (95% CI 1.4-2.9) in unsprayed sites compared to 0.8% (95% CI 0.5-1.3) in sprayed sites (p = 0.003). Sporozoite rates were also lower for An. funestus collected in sprayed sites.

Conclusion: This study contributes to the understanding of malaria vector species composition, behaviour and transmission risk following IRS around Lake Victoria and can be used to guide malaria vector control strategies in Tanzania.

Keywords: Anopheles arabiensis; Anopheles funestus; Anopheles gambiae; Indoor residual spraying; Malaria vectors; Pirimiphos-methyl; Seasonality; Species composition; Tanzania.

Fig. 1

Study sites. Map of entomological surveillance sites in districts surrounding Lake Victoria, NW Tanzania. Showing all sites from entomological monitoring surveys conducted between 2015 and 2017

Fig. 2

Mean monthly percentage mortality (24 h) of Anopheles gambiae (Kisumu). Mean represents 24 h mortality after 30 min cone bioassay on mud, cement, painted, white wash, and burnt brick walls that were sprayed with Actellic® 300CS in 2015, 2016 and 2017. The red dotted line shows the WHO standard cut-off (80% mortality)

Fig. 3

Mean nightly indoor catch of Anopheles gambiae s.l. and Anopheles funestus s.l. Indoor density of An. gambiae s.l. and An. funestus s.l. collected from CDC light traps for sampling period 2016–2017 (except for Nyang’hwale (sprayed, 2017) and Tarime (unsprayed, 2017) where data were collected in 2017 only). a Kagera region with Biharamulo as control site. b Mwanza region with Busega (a close by site, in Simiyu region, as a control site. c Mara region with Tarime as control site. d Geita region with Bukombe as control sites. Arrows indicate time when IRS was conducted

Fig. 4

Biting rate for Anopheles gambiae s.l. Mean biting time of An. gambiae s.l. from CBR conducted indoors and outdoors. Mean hourly biting rate is indicated from 18:00 to 06:00 in sprayed and unsprayed areas

Fig. 5

Mosquito species composition. Species composition expressed as a proportion of Anopheles species tested by PCR in respective years a 2016 b 2017. In 2016, 8 of 10 sites were sprayed with Actellic® 300CS; in 2017, 9 of 13 sites were sprayed with Actellic® 300CS

Fig. 6

Indoor resting density for Anopheles gambiae s.l. a Kagera region with Biharamulo as control. b Geita, and Mwanza region with Bukombe and Busega as controls, respectively. c Mara region with Tarime as control. Arrows indicate time when IRS was conducted. Analysis of variance indicate significantly higher (p < 0.05) indoor resting densities across regions (i.e., Kagera, Geita, Mwanza, Mara)