Research Article: Linking human behaviours and malaria vector biting risk in south-eastern Tanzania

Date Published: June 3, 2019

Publisher: Public Library of Science

Author(s): Marceline F. Finda, Irene R. Moshi, April Monroe, Alex J. Limwagu, Anna P. Nyoni, Johnson K. Swai, Halfan S. Ngowo, Elihaika G. Minja, Lea P. Toe, Emmanuel W. Kaindoa, Maureen Coetzee, Lenore Manderson, Fredros O. Okumu, Luzia Helena Carvalho.


To accelerate malaria elimination in areas where core interventions such as insecticide-treated nets (ITNs) are already widely used, it is crucial to consider additional factors associated with persistent transmission. Qualitative data on human behaviours and perceptions regarding malaria risk was triangulated with quantitative data on Anopheles mosquito bites occurring indoors and outdoors in south-eastern Tanzania communities where ITNS are already used but lower level malaria transmission persists. Each night (18:00h-07:00h), trained residents recorded human activities indoors, in peri-domestic outdoor areas, and in communal gatherings. Host-seeking mosquitoes were repeatedly collected indoors and outdoors hourly, using miniaturized exposure-free double net traps (DN-Mini) occupied by volunteers. In-depth interviews were conducted with household representatives to explore perceptions on persistent malaria and its control. Higher proportions of people stayed outdoors than indoors in early-evening and early-morning hours, resulting in higher exposures outdoors than indoors during these times. However, exposure during late-night hours (22:00h–05:00h) occurred mostly indoors. Some of the popular activities that kept people outdoors included cooking, eating, relaxing and playing. All households had at least one bed net, and 83.9% of people had access to ITNs. Average ITN use was 96.3%, preventing most indoor exposure. Participants recorgnized the importance of ITNs but also noted that the nets were not perfect. No complementary interventions were reported being used widely. Most people believed transmission happens after midnight. We conclude that insecticide-treated nets, where properly used, can still prevent most indoor exposures, but significant risk continues unabated before bedtime, outdoors and at communal gatherings. Such exposure is greatest for rural and low-income households. There is therefore an urgent need for complementary interventions, particularly those targeting outdoor-biting and are applicable for all people including the marginalised populations such as migratory farmers and fishermen. Besides, the differences in community understanding of ongoing transmission, and feedback on imperfections of ITNs should be considered when updating malaria-related communication and interventions.

Partial Text

Malaria transmission in rural south-eastern Tanzania has significantly decreased over the past three decades [1,2], although the area is still classified as meso- or hyper-endemic based on the most recent surveys of malaria prevalence in school children [3]. Various factors have contributed to these declines, including improved case management and effective vector control measures, particularly wide-spread use of insecticide-treated nets (ITNs) [4–6]. Other factors such as urbanization and improved livelihood may have also played a role [7], although the exact measure of their contribution is not known. Factors associated with the persisting transmission include resistance to pyrethroids commonly used on insecticide-treated nets (the most common vector control intervention) [8], increased proportion of malaria mosquitoes biting people outdoors [8–10] and occupational factors such as migratory farming activities [11]. Indeed, interventions like ITNs offer protection mainly when people are sleeping indoors, leaving them mostly vulnerable outdoors [9,12,13]. To deploy effective complimentary interventions and to accelerate elimination efforts, it is therefore crucial to also investigate these additional factors and to identify potential opportunities for improvement.

Malaria transmission is influenced by biting patterns and infectiousness of different vector species, but also by human activities and behaviours [37]. Indeed, quantitative assessments of malaria transmission risk illustrate that it requires both the hazard (host-seeking, sporozoite-positive Anopheles) and exposure (susceptible humans at the right place and time coincident with the biting Anopheles) to be present [38]. This study assessed multiple human activities indoors and outdoors, as well as opinions and perceptions of the people, and also examined the biting behaviours of two major malaria vectors, An. arabienssis and An. funestus in rural and urban south eastern Tanzania villages. The main objectives were to identify major drivers of persistent malaria transmission exposure and to identify gaps and new opportunities for accelerating vector control beyond the current best tool, i.e. insecticide-treated nets. Overall, because of human behaviour and vector behaviors, human exposure to both An. arabiensis and An. funestus was higher indoors than outdoors regardless of the observed feeding preferences of these mosquito species. A majority of people moved indoors after 21:00h, from which point onwards till 05:00h, exposure was prevented by the relatively high bed net use in the area. On the other hand, outdoor exposure was higher than indoor exposure between 18:00h and 21:00h, and again between 05:00h and 07:00h because majority of the household members were mostly outdoors during these hours. Common activities, including cooking, eating and relaxing were conducted outdoors. These activities involved people sitting in one place for extended periods, hence more vulnerable to mosquito bites.

ITNs, where properly used, can still prevent most indoor exposures. However, significant risk continues unabated before bedtime, outdoors in peridomestic spaces, at communal gatherings, and during occupations such as farming and fishing. This remaining risk is greater in rural than urban areas and in low-income than high income households. These require scalable approaches to complement ITNs, particularly targeting outdoor-biting. The socio-ecenomic linkages with this persistent exposure also suggests that the complementary interventions, particularly those targeting outdoor exposure should prioritize low-income families. Second, the discordance in community understanding of persistent transmission and its control, and the feedback on imperfections of current approaches should be considered to update malaria-related communication, and improve future interventions.




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