Insecticide-Treated Nets Can Reduce Malaria Transmission by Mosquitoes Which Feed Outdoors

Nicodem J. Govella 0 1 2 Fredros O. Okumu 0 1 2 Gerry F. Killeen 0 1 2 0 Ifakara Health Institute , PO Box 78373, Kiko Avenue, Mikocheni, Dar es Salaam, Tanzania 1 Biomedical and Environmental Thematic Group , Coordination Office, Ifakara Health Institute , Dar es Salaam, Tanzania ; Disease Control and Vector Biology Unit, London School of Hygiene and Tropical Medicine , London, United Kingdom ; Vector Group, Liverpool School of Tropical Medicine , Liverpool, United Kingdom 2 Authors' addresses: Nicodem J. Govella and Gerry F. Killeen, Coordination Office, Ifakara Health Institute , Mikocheni, Dar es Salaam, Tanzania , and Vector Group, Liverpool School of Tropical Medicine , Pembroke Place, Liverpool, United Kingdom Insecticide treated nets (ITNs) represent a powerful means for controlling malaria in Africa because the mosquito vectors feed primarily indoors at night. The proportion of human exposure that occurs indoors, when people are asleep and can conveniently use ITNs, is therefore very high. Recent evidence suggests behavioral changes by malaria mosquito populations to avoid contact with ITNs by feeding outdoors in the early evening. We adapt an established mathematical model of mosquito behavior and malaria transmission to illustrate how ITNs can achieve communal suppression of malaria transmission exposure, even where mosquito evade them and personal protection is modest. We also review recent reports from Tanzania to show that conventional mosquito behavior measures can underestimate the potential of ITNs because they ignore the importance of human movements. - Insecticide-treated nets (ITNs) represent a powerful means for controlling malaria in Africa.1 This usefulness is due to the fact that the principal malaria vectors, from the Giles Anopheles gambiae and An. funestus species complexes,24 primarily feed indoors at night.2,5,6 Thus, the proportion of human exposure that occurs indoors (i), when persons are asleep and can conveniently use them, is very high (Figure 1AD). Such estimates of i, which take into consideration the movement patterns of persons are obtained in the field by weighting the observed indoor and outdoor biting rates at each period of the night by the proportion of humans that are typically in these two compartments at that time.6,7 When reasonable levels of community-wide coverage are achieved, with approximately half of the population using them each night,8,9 ITNs not only confer personal protection against infectious bites but can also reduce the survival, feeding frequency, feeding success, and density of vector mosquito populations.8,10 This finding means that ITNs not only prevent malaria in protected persons, but can also reduce the exposure of unprotected persons by suppressing transmission across entire communities.9,1115 Recent evidence suggests behavioral changes by malaria mosquito populations to avoid contact with ITNs by either feeding predominantly outdoors or in the early part of the evening.5,7,1618 Such changes can drastically reduce the level of personal protection conferred by ITNs for obvious reasons.5,7 These behavioral changes might have resulted from the selection of genetically inherited traits or, more directly, from plastic phenotypic adaptation in response to increased coverage of ITNs or indoor residual spraying.5,16,17 Such intervention pressure may even be strong enough to cause changes in species composition of vector populations by selectively eliminating the most susceptible species and leaving those that are less vulnerable.2,1923 For instance, An. arabiensis Patton, which is typically more exophilic, zoophagic, and exophagic than its sibling species An. gambiae sensu stricto, already dominates malaria transmission in parts of western Kenya where widespread use of ITNs has progressively diminished the importance of An. gambiae s.s as the main malaria vector.20 Although it is commonly perceived that ITNs are ineffective against outdoor-biting mosquitoes based on conventional measures of mosquito behavior,5,18,24 we adapt an established mathematical model of mosquito behavior and malaria transmission8,10 to examine the possibility that ITNs can achieve communal suppression of malaria transmission exposure, even where mosquito evade them and personal protection is modest. We adapt an existing model8 that was previously used to establish population-wide coverage thresholds levels of ITNs at which community-level protection is equivalent to or greater than personal protection.8 Specifically, we modify the model slightly to deal more realistically with vector populations that vary in terms of their feeding behaviors. The probability of mosquitoes surviving their eventual host attack (P) is adjusted to account for the effect of ITN avoidance behavior, expressed as the proportion of normal exposure that would occur at times during which a human host would normally be under a net (i). This parameter can also be thought of in simple terms as the maximum proportion of normal exposure, which is directly preventable through personal protection by using an ITN. The corrected probability of a mosquito surviving the eventual host attack is calculated with the following modification of equation 13 of the original model,8 assuming that the proportion of all attacks that end in death is the sum of mortality probabilities for attacking protected and unprotected hosts, weighted according to the proportion of the availability of all hosts that they represent. The definitions of relevant terms in the model are shown in Table 1. The reduction in relative rate of exposure (RRE) to malaria transmission achieved by individual-level personal protection (ITN users), community-level protection (ITN non-users), and combined individual and communal protection (ITN users) was estimated by fixing the additional mortality probability of mosquitoes encountering an ITN at 0.825 and ITN coverage at the achievable level of 0.5, equivalent to 50% use as recorded in typical household surveys and specified by internationally agreed targets.8,9 Otherwise, the model is formulated, parameterized, and applied exactly as previously described.8 Figure 1E and F show that less than half of all human exposure to An. arabiensis in urban Dar es Salaam,Tanzania7 occurs in times and places when using an ITNs is feasible (i = 0.46). Based on these published field data, simulations predict only a slight suppression in personal relative rate of exposure to transmission (RRE = 0.59), equivalent to a 1.7-fold reduction (Figure 2). However, much greater decreases in exposure to transmission for ITN users (communal plus personal protection; RRE = 0.19) and non users (communal protection only; RRE = 0.32) are predicted at 50% community-wide coverage. Thus, even non-users receiving only communal protection can expect 3.1-fold reduction of exposure to transmission and users enjoy a 5.3-fold reduction. Extrapolating this level of communal protection horiz (...truncated)