Human and vector behaviors determine exposure to Anopheles in Namibia

Abstract

Background: Although the Republic of Namibia has significantly reduced malaria transmission, regular outbreaks and persistent transmission impede progress towards elimination. Towards an understanding of the protective efficacy, as well as gaps in protection, associated with long-lasting insecticidal nets (LLINs), human and Anopheles behaviors were evaluated in parallel in three malaria endemic regions, Kavango East, Ohangwena and Zambezi, using the Entomological Surveillance Planning Tool to answer the question: where and when are humans being exposed to bites of Anopheles mosquitoes?

Methods: Surveillance activities were conducted during the malaria transmission season in March 2018 for eight consecutive nights. Four sentinel structures per site were selected, and human landing catches and human behavior observations were consented to for a total of 32 collection nights per site. The selected structures were representative of local constructions (with respect to building materials and size) and were at least 100 m from each other. For each house where human landing catches were undertaken, a two-person team collected mosquitoes from 1800 to 0600 hours.

Results: Surveillance revealed the presence of the primary vectors Anopheles arabiensis, Anopheles gambiae sensu stricto (s.s.) and Anopheles funestus s.s., along with secondary vectors (Anopheles coustani sensu lato and Anopheles squamosus), with both indoor and outdoor biting behaviors based on the site. Site-specific human behaviors considerably increased human exposure to vector biting. The interaction between local human behaviors (spatial and temporal presence alongside LLIN use) and vector behaviors (spatial and temporal host seeking), and also species composition, dictated where and when exposure to infectious bites occurred, and showed that exposure was primarily indoors in Kavango East (78.6%) and outdoors in Ohangwena (66.7%) and Zambezi (81.4%). Human behavior-adjusted exposure was significantly different from raw vector biting rate.

Conclusions: Increased LLIN use may significantly increase protection and reduce exposure to malaria, but may not be enough to eliminate the disease, as gaps in protection will remain both indoors (when people are awake and not using LLINs) and outdoors. Alternative interventions are required to address these exposure gaps. Focused and question-based operational entomological surveillance together with human behavioral observations may considerably improve our understanding of transmission dynamics as well as intervention efficacy and gaps in protection.

Keywords: Anopheles biting behavior; Human behavior; Long-lasting insecticidal net use; Namibia.

Fig. 1

A map of the Republic of Namibia with sentinel site locations and administrative regions included in this study highlighted. 1 Okanghudi village (Ohangwena region), 2 Shadikongoro village (Kavango East region), and 3 Sibbinda village (Zambezi region)

Fig. 2

Overall Anopheles landing rates over the night (lines) and parallel human behaviors (bars) directly measured indoors and outdoors for Kavango East, Ohangwena and Zambezi regions

Fig. 3

Human behavior-adjusted biting rates for all Anopheles along with long-lasting insecticidal net (LLIN)-based protection across the night for Kavango East, Ohangwena, Zambezi. Insets (pie charts) indicate proportions of exposure to Anopheles bites in each of the primary exposure spaces—outdoors, indoors while awake, and indoors while asleep and not protected by an LLIN. Most exposure was outdoors for Ohangwena and Zambezi, with primarily indoor exposure for Kavango East

Fig. 4

Species-specific human behavior-adjusted biting rates and LLIN-based protection in Kavango East over the course of a night. Insets (pie charts) depict human behavior-adjusted spatial exposure. Both temporal and spatial exposure to different vectors was based on vector behaviors. Though spatial exposure to Anopheles arabiensis, Anopheles funestus sensu stricto (s.s.) and other Anopheles was similar, temporal exposure varied by each species. Exposure to Anopheles gambiae s.s. was primarily outdoors. The proportion of bites occurring indoors for an unprotected individual awhile awake, occurring while asleep for an unprotected individual, prevented by using an LLIN, occurring indoors for a protected user of an LLIN, and occurring outdoors for each site are presented in Table 2