Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania

Abstract

Background: African malaria vectors bite predominantly indoors at night so sleeping under an Insecticide-Treated Net (ITN) can greatly reduce malaria risk. Behavioural adaptation by mosquitoes to increasing ITN coverage could allow vector mosquitoes to bite outside of peak sleeping hours and undermine efficacy of this key malaria prevention measure.

Methods: High coverage with largely untreated nets has been achieved in the Kilombero Valley, southern Tanzania through social marketing programmes. Direct surveys of nightly biting activity by An. gambiae Giles were conducted in the area before (1997) and after (2004) implementation of ITN promotion. A novel analytical model was applied to estimate the effective protection provided by an ITN, based on published experimental hut trials combined with questionnaire surveys of human sleeping behaviour and recorded mosquito biting patterns.

Results: An. gambiae was predominantly endophagic and nocturnal in both surveys: Approximately 90% and 80% of exposure occurred indoors and during peak sleeping hours, respectively. ITNs consistently conferred >70% protection against exposure to malaria transmission for users relative to non-users.

Conclusion: As ITN coverage increases, behavioural adaptation by mosquitoes remains a future possibility. The approach described allows comparison of mosquito biting patterns and ITN efficacy at multiple study sites and times. Initial results indicate ITNs remain highly effective and should remain a top-priority intervention. Combined with recently developed transmission models, this approach allows rapid, informative and cost-effective preliminary comparison of diverse control strategies in terms of protection against exposure before more costly and intensive clinical trials.

Figure 1

Mean indoor and outdoor biting densities of An. gambiae at two sites in the Kilombero Valley in 1997 and 2004. Grey background shading represents the proportion of the human population in bed. Note these estimates reflect the biting rate experienced by a human landing catcher sampling exclusively indoors or outdoors, rather than the calculated biting rates experienced by a typical resident that are presented in figures 2 to 4 [see Additional file 1].

Figure 2

Proportion of all An. gambiae caught indoors and during peak sleeping hours (9 pm to 5 am) at two sites in the Kilombero Valley in 1997 and 2004. Standard errors are not plotted as they are consistently < 0.001 for all estimates, n = 674 and 5,931 in 1997 and 2004, respectively [see Additional file 1].

Figure 3

Estimated patterns of exposure to biting An. gambiae for ITN users and non-users at two sites in the Kilombero Valley in 1997 and 2004. Grey background shading represents the proportion of the human population in bed [see Additional file 1].

Figure 4

Estimated proportions of exposure to biting An. gambiae occurring indoors (π_i ; equation 7) and during peak sleeping hours (π_s ; equation 6)for non-users of ITNs as well as the estimated true protective efficacy of ITNs (P*; equation 5), for ITN users at two sites in the Kilombero Valley in 1997 and 2004 [see Additional file 1].

Figure 5

Predicted protection against exposure resulting from increasing coverage of either human populations with ITNs or aquatic stage vector populations with larvicides. Grey shading represents the level of protection recently reported for systematic application of microbial larvicides in rural Kenya [34]. The model [19] and input parameters are available for examination in the excel spreadsheet used to generate this figure [see Additional file 1].