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      Reported reasons for not using a mosquito net when one is available: a review of the published literature

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          Abstract

          Background

          A review of the barriers to mosquito net use in malaria-endemic countries has yet to be presented in the published literature despite considerable research interest in this area. This paper partly addresses this gap by reviewing one component of the evidence base; namely, published research pertaining to self-reported reasons for not using a mosquito net among net 'owning' individuals. It was anticipated that the review findings would potentially inform an intervention or range of interventions best suited to promoting greater net use amongst this group.

          Method

          Studies were sought via a search of the Medline database. The key inclusion criteria were: that study participants could be identified as owning a mosquito net or having a mosquito net available for use; that these participants on one or more occasions were identified or self-reported as not using the mosquito net; and that reasons for not using the mosquito net were reported. Studies meeting these criteria were included irrespective of mosquito net type.

          Results

          A total of 22 studies met the inclusion criteria. Discomfort, primarily due to heat, and perceived (low) mosquito density were the most widely identified reason for non-use. Social factors, such as sleeping elsewhere, or not sleeping at all, were also reported across studies as were technical factors related to mosquito net use (i.e. not being able to hang a mosquito net or finding it inconvenient to hang) and the temporary unavailability of a normally available mosquito net (primarily due to someone else using it). However, confidence in the reported findings was substantially undermined by a range of methodological limitations and a dearth of dedicated research investigation.

          Conclusions

          The findings of this review should be considered highly tentative until such time as greater quantities of dedicated, well-designed and reported studies are available in the published literature. The current evidence-base is not sufficient in scope or quality to reliably inform mosquito net promoting interventions or campaigns targeted at individuals who own, but do not (reliably) use, mosquito nets.

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          Most cited references41

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          Preventing Childhood Malaria in Africa by Protecting Adults from Mosquitoes with Insecticide-Treated Nets

          Introduction The massive malaria burden in Africa merits particular attention as the world struggles to realize a better life for the poorest [1,2]. The Anopheles mosquitoes that act as vectors for human Plasmodium parasites must access sugar, blood, and aquatic oviposition sites to complete their life cycle and maintain parasite transmission. The availability of such ecological resources to mosquitoes has long been recognized as a crucial determinant of malaria transmission [3], but quantitative understanding of this process, as well as viable means to prevent it, remain poorly developed compared with other disease [4] and pest systems [5]. Recent theoretical work highlights the enormous influence of blood source and aquatic habitat availability in determining malaria transmission intensity, disease burden, and their responsiveness to various forms of control [6–12]. Here we apply field-parameterized kinetic models of mosquito host availability [11,13] to identify important shortcomings of current global targets for delivering insecticide treated nets (ITNs) [2,14,15], the most important vector control tool in Africa today. Not only does the model outline the limitations of existing strategies that emphasize targeting of vulnerable groups such as young children and pregnant women [16–18], it also indicates how complementary strategies to promote coverage of whole populations, including nonvulnerable adults and older children [19], will achieve greater and more equitable reduction of disease burden than otherwise would be possible. Insecticide-treated nets (ITNs) represent a practical and effective means to prevent malaria in Africa [20], so scaling up coverage to at least 80% use by young children and pregnant women by 2010 is a consensus target of the Millennium Development Goals (MDGs), the Roll Back Malaria Partnership, and the US President's Malaria Initiative [2,14,15]. Targeting individual protection to these vulnerable groups [16–18] is a well-founded and explicitly accepted priority of all three initiatives, because these groups bear the highest risk of morbidity and mortality from malaria. However, this strategy largely ignores the potentially greater community-wide benefits of broader population coverage [19], and no explicit resources, targets, or strategies have been proposed to achieve these benefits. ITNs can protect not only the individuals and households that use them, but also members of the surrounding community [19,21–26]. This is because they kill adult mosquitoes directly or force them to undertake longer, more hazardous foraging expeditions in search of vertebrate blood and aquatic habits [11]. Plasmodium falciparum, the malaria parasite responsible for the bulk of deaths in Africa, requires at least 8 d to develop from imbibed gametocytes into mature sporozoites within the salivary glands of the vector mosquito. This means that most malaria transmission is carried out by mosquitoes that are at least 10 d old and have taken several previous blood meals at intervals of 2–5 d [27,28]. By even modestly increasing mosquito mortality while they attempt to feed on humans, ITNs can greatly reduce the number of mosquitoes that survive repeated hazardous encounters with protected humans [11]. Also, the excito-repellent properties of ITNs can reduce the frequency with which mosquitoes successfully acquire blood, often diverting them to feed on other mammals that do not host the malaria parasite, resulting in greatly reduced prevalence of sporozoite infection [11]. This theoretical rationale is strongly supported by detailed observations from experimental hut studies [29–34] and from larger village-scale trials: ITNs have been clearly shown to reduce malaria risk among unprotected individuals by suppressing the density [35–37], survival [35–37], human blood indices [38,39], and feeding frequency [39] of malaria vector populations. Large reductions of transmission are required to appreciably reduce malaria burden in most of Africa [17,40], particularly in the longer term as exposure and immunity re-equilibrate [41]. ITNs can address this challenging need through direct personal protection and area-wide suppression of the malaria transmission intensity that benefits even nonusers. It has been suggested that such communal benefits can make large impacts on disease burden only if appreciable levels of coverage are achieved in the human population as a whole [11,12,19], but precise coverage targets for achieving this remain to be determined. So how much coverage is enough to protect individuals who do not use an ITN? Methods Overview Here we used recently developed kinetic models of mosquito behaviour and mortality [11,13] to answer this question by considering the impact of ITNs on human host availability and feeding hazards to mosquitoes, as well as the consequences of such changes for malaria transmission intensity. Protection was estimated in terms of protection against exposure to infectious mosquito bites, expressed as the relative change in the entomological inoculation rate (EIR). EIR is a proven epidemiological indicator of malaria transmission intensity and a key determinant of disease burden [17,40]. Two common but ecologically distinct African malaria transmission systems are considered. First, we modelled an Anopheles gambiae Giles or An. arabienis Patton (sibling species from the same species complex known as An. gambiae sensu lato) population with access to human blood only. Second, we considered An. arabiensis populations in the presence of abundant cattle, which can act as alternative blood sources. An. gambiae greatly prefers humans, but An. arabiensis will readily feed upon cattle [42,43], so populations of these species respond quite differently to increasing ITN coverage, with malaria transmission by the latter typically being lower to begin with but less sensitive to control with ITNs [11]. In both transmission systems we considered ITNs with properties typical of those evaluated in rigorous clinical trials [20] or those of emerging technologies with improved operational durability [44–47]. Note that coverage is expressed as the proportion of the total human population using an ITN each night, rather than in terms of ownership, because this value is the most direct indicator of both personal and communal protection. Figure 1 provides an overview of how mosquito behaviour and survival were modelled as a function of host availability, ITN properties, compliance, and coverage. The approach described is essentially a behaviourally explicit extension of existing vector biodemography [48] models, which predict epidemiologically relevant outcomes such as exposure to transmission (the biodemography–epidemiology model). The principles and utility of the biodemography–epidemiology models we have used [27,49,50], as well as several others that are based on similar assumptions [6,18,28,51], are well established. Notably, this family of models realistically assumes that mosquito behaviour cycles between host seeking, feeding, resting, oviposition-site seeking, oviposition, and back to host seeking again [51]. Similarly to recent analyses of the importance of oviposition [7,8,10] and host acquisition [11,12] processes, here we explicitly modelled the underlying behavioural events that determine the input parameters of these biodemographic processes (the behaviour–biodemography model). Detailed consideration of mosquito behaviour and mortality upon encounter with individual hosts (the individual-level submodel) allows simulation of the impact of ITNs upon the foraging requirements and risks for mosquito populations at the community level (the community-level submodel). This hierarchical approach links individual- and community-level submodels into an integrated behaviour–biodemography model, which drives the outcome of the biodemography–epidemiology model and allows the influence of ITNs upon malaria transmission intensity to be estimated in terms of EIR experienced by both users and nonusers [11,27,50]. Figure 1 A Schematic Outline of the Two-Tier Model Used for This Analysis, Adapted from Previous Detailed Descriptions A detailed model of mosquito behaviour and survival as a function of host availability, ITN properties, compliance, and coverage [11,13] was used to estimate the key biodemographic parameters that determine malaria transmission intensity (behaviour–biodemography model). This model allowed the influence of ITN usage upon malaria transmission intensity to be estimated (biodemography–epidemiology model) in terms of EIR experienced by both users and nonusers [11,27,50]. All terms and symbols are defined in detail elsewhere [11,27,50,52] and are summarized in Methods. The specific modelling approach described here is almost identical to our recent exploration of the optimal properties of ITNs as a function of local ecology [11], apart from subtle improvements in terms calculating mosquito diversion, mortality, and feeding probabilities per host encounter. It is also similar to and consistent with the approaches of others [6,12] but accounts for the fact that ITNs can act only during times of the night when they are actually in use, so that their overall protection is also influenced by subtle variations in the behavioural interactions between humans and mosquitoes [13]. This model has already been evaluated through improved iterations in terms of sensitivity to variations in the assumed parameter values for the insecticidal and excito-repellent properties of ITNs [11], the survival rate of mosquitoes while foraging for resources [11], the innate resource preferences of vector populations [11,50,52], and the availability of those resources, including oviposition sites [50] and alternative blood meal hosts [11,50]. While the analysis outlined here could be implemented with either of the recently developed (and perhaps more elegant) alternative models [6,12], this particular form captures all of the same processes without necessitating the mathematical subtleties of integration, differentiation, equilibrium analysis, or limits. While these are inherently valuable tools for mathematical modelling, they often constitute “black boxes” to nonmathematicians, including several authors of this article. We therefore chose a model that does not require mathematical complexities that might limit accessibility to some of the field biologists and epidemiologists for whom this analysis is most relevant. The model is presented as a downloadable spreadsheet (see Protocol S1) and has proven valuable for teaching the ecological basis of malaria epidemiology and control to students in both the developed and developing world. Modelling Mosquito Behaviour and Mortality at the Individual Level Here we describe a submodel of behavioural and mortality processes that occur at the level of individual mosquitoes seeking, encountering, attacking, and feeding upon individual blood hosts. Another important simplification to consider is that, like most deterministic malaria transmission models, our approach assumed a “malaria in a bottle” scenario in which populations of identical parasites, vectors, and hosts are mixed homogenously within an enclosed system [53]. One important corollary of this assumption is that well-established variations of vulnerability to malaria infection within human populations [16,17] or associated variations in attractiveness and availability to mosquitoes [9,54–56] are not explicitly modelled. As defined previously [52], the availability (a) of any host (j) of any species (s) is the product of the rate at which individual vectors encounter it (ɛs,j) and the probability that, once encountered, they will feed upon it (φs,j): Note that this kinetic definition of availability as a rate per unit time is consistent with applications of the same term to acquisition of oviposition sites [10], the term attraction rate for blood sources [6,57], and the terms feeding rate and oviposition rate for both resources [8,12]. We considered successful feeding as just one of three possible outcomes of a host encounter by a female vector, the other two being death while attempting to feed and diversion to seek another host (Figure 1). We considered this a two-stage process in which the vector first either attacks the encountered host or is diverted away and searches for another, the probabilities of which we denote as γ and Δ, respectively. This definition of diversion includes the combined effects of noncontact repellency and contact-mediated irritancy, often referred to as excito-repellency [58,59]. Considering mean values for hosts of any given species (s), the sum of these two probabilities is: We then considered the second stage of the blood acquisition process, namely feeding. Knowing the probabilities that the vector will either feed successfully (φs) or die in the attempt (μs) per attack (rather than per encounter) allowed us to calculate the probability of a successful feed per encounter: Specifically, the cases of cattle (c) and unprotected humans (h,u) were dealt with in a straightforward manner as follows, where Δu and μu represent a common parameter value for both types of host (Table 1): Table 1 Behavioural and Host Availability Input Parameters for Both Vector Species Personal protection measures such as bed nets, repellents, or domestic insecticide use were envisaged as three possible outcomes, the probabilities of which sum to 1: For a vector that would normally choose to feed upon an encountered unprotected human with a probability of φh,u, the presence of a net or other intervention is expected to influence this probability for protected humans (φh,p) as a function of the excess probability of diverting (Δp) and killing (μp) that vector (Figure 1). The combined baseline and net-induced probabilities of diversion (Δu  + p ) or mortality (μu + p) were calculated as follows: and These parameters allowed us to calculate the feeding probability for a human who always uses and is protected by a net (φh,p): These equations are parameterized using data from experimental hut trials in which the human participants slept within the net throughout the period of data collection (Table 1). However, very few human beings spend their entire day asleep or using a net [13] so the true probability of feeding upon a typical net user ( ) is calculated by weighting φh,u and φh,p according to the proportion of normal exposure during which the host is actually covered (πi): Equations 5-7 differ slightly from those previously proposed [11], which treated diversion and killing as independent events, conditional on the host having and using a net. At low values of πi these changes relative to [11] make little difference, but the model described here is more realistic at high values of πi . Extrapolating Impacts of Insecticide-Treated Nets to the Community Level Given the above submodel for the interactions of mosquitoes with individual mammalian hosts, it was possible to extrapolate the likely large-area effects of these small-scale influences on entire vector populations and the human communities they feed upon. For any given number of cattle (Nc), unprotected humans (Nh,u), and protected humans (Nh,p), the mean seeking interval for vertebrate hosts (ηv) can be calculated as the reciprocal of total host availability (A) [52], using estimates of these feeding probabilities and their corresponding encounter rates, adapting Equation 1 from our original formulation [50]: where As refers to the total availability of all hosts of species s. In this case, the species or species categories considered were unprotected humans (h,u), protected humans (h,p), and cattle (c). Values for ac and ah,u (previously ah [50]) were estimated exactly as described previously [50] and ah,p was calculated as follows: where λp is the relative availability of protected versus unprotected hosts, estimated in terms of the ratio of their feeding probabilities: Foraging for resources is an intrinsically dangerous undertaking for mosquitoes, and it is commonly assumed that survival during these phases is lower than while resting in houses [6,60]. We adapted Equation 3 from our previous formulation [50] to estimate the survival rate per feeding cycle (Pf) as the product of the probability of surviving the eventual attack on a host that may be protected (Pγ) and the probabilities of surviving the gestation (g), oviposition site-seeking (ηo), and vertebrate host-seeking (ηv) intervals, with distinct daily survival probabilities for the resting (P), foraging for either oviposition sites or vertebrate hosts (Pov), and attacking (Pγ) phases: The mean probability of mosquitoes surviving their eventual chosen host attack (Pγ) was calculated assuming that the proportion of all attacks that end in death is the sum of the mortality probabilities for attacking protected and unprotected hosts, weighted according to the proportion of all encounters that will occur on such hosts. Assuming that protection does not affect encounter rates, and that these rates are proportional to availability when unprotected, we applied this weighting approach to estimate total attack-related mortality rate and consequent survival as follows: Similarly, the human blood index is calculated as the proportion of total host availability accounted for by humans [52], similarly to Equation 9: The EIR for protected and unprotected individuals was then calculated from the total number of infectious bites upon humans that occur in the population as a whole (β E) [27,49], the share of the total human availability represented by that group, and the population size of that group: where β is the mean number of infectious human bites each emerging mosquito takes in its lifetime and E is the emergence rate of mosquitoes [27]. Dividing Equation 16 by Equation 15, substituting with Equation 10, and rearranging also leads to an intuitively satisfactory solution, consistent with independently formulated models of personal protection [13]: Otherwise, we modelled malaria transmission exactly as previously described [50]. Note that this model has been adapted [11,50] from its original formulation [27] to account for superinfection of mosquitoes [28] and daily time increments to smooth the effects of changing host availability patterns on feeding cycle length [50]. For ease of comparison and interpretation, the impact of ITNs is presented in terms of the relative transmission intensity EIR C /EIR 0 at a given coverage level (C; note distinction from c, which denotes cattle hosts) as a result of personal and communal protection amongst users and nonusers: Baseline Mosquito Behaviour, Host Availability, and Survival Parameters The parameter definitions and values used to implement this analysis are summarized in Table 1. Namwawala, in the Kilombero Valley, southern Tanzania is the primary centre for parameterising our model because of the exceptionally detailed quantitative characterisation of malaria transmission and vector biodemography in this village and the surrounding area. This is a holoendemic village with intense seasonal transmission, stable high parasite prevalence in humans, and a heavy burden of clinical malaria [61–68]. At this site the bulk of transmission is mediated by An. gambiae sensu lato (of which the main species involved in transmission is An. arabiensis) and transmission intensity has been modelled with available field data [27,49]. As previously described [27,49], we based our estimate of human population size [62] approximately upon those reported for this particular village during the early 1990s. Nevertheless, we used a human population size of 1,000 and, where relevant, a bovine population of the same size so that the EIR experienced by users and nonusers could be easily calculated at net coverage levels approaching 0% and 100%. By setting coverage to 0.001 or 0.999, this model simulates a single user or nonuser in the population, respectively. Infectiousness of humans (κ) is set to 0.030, reflecting a more precise recent estimate [69] than was available previously [61,63]. In a typical holoendemic scenario, the infectiousness of the human population is thought to be largely insensitive to reductions in transmission intensity [69]. In the interests of making conservative and generalizable predictions, we assumed that increasing coverage with ITNs will not affect κ [69], even though reduction of κ is likely at EIR values below 10 infectious bites per person per year [56]. We set mean daily survival of the resting phase (P) at 0.90, reflecting a median value of daily survival at four well-characterised holoendemic sites [27] and estimated daily indoor survival for An. gambiae s.l. in Tanzania [70]. As previously described, the daily survival rate of mosquitoes while foraging for blood or oviposition sites (Pov) was set at 0.80, representing a median value of plausible field values [11]. The results of experimental hut studies [34] were combined with host-choice evaluations [71] and appropriate analytical models [50,52] to define the attack and mortality probabilities of An. arabiensis encountering cattle or humans: we set the probability that An. arabiensis will attack unprotected cattle or humans (γu), conditional upon encountering them, to be 0.90 and the chance that they will die in the attempt (μu) at 0.10. Using these parameters and Equation 3, we calculated that, for An. arabiensis, the overall feeding probability upon either cattle (φc) or unprotected humans (φh,u) would be 0.81, a value similar to previous estimates of approximately 0.80–0.85 for the feeding success of An. gambiae sensu lato on sleeping humans in Tanzania [34,62]. We also applied these same probabilities of attacking (γu), feeding (φh,u), and dying (μu) to An. gambiae sensu stricto encountering unprotected humans. The availabilities of unprotected humans and cattle were calculated for An. arabiensis using field measurements of the duration of the feeding cycle and were extended to An. gambiae s.s., accounting for the lower estimated relative availability of cattle (λc) to this mosquito species as previously described [52]. Note that λc is assumed to modify a c by affecting the encounter rate only, indicating that these mosquitoes can differentiate between preferred and nonpreferred hosts at long ranges [72–74]. In the case of An. arabiensis this assumption is consistent with the longer spatial range of attraction of cows relative to humans for zoophilic members of the An. gambiae complex [72–74]. Parameters Reflecting the Effects of Insecticide-Treated Bed Nets The parameter definitions and values describing the impacts of ITNs on vector behaviour and mortality at the level of individual interactions are listed in Table 1. The impacts of ITNs very much depend on their excito-repellent and insecticidal properties, which are most representatively evaluated using well-established experimental hut methodologies [59,75,76] that have been extensively applied to this particular intervention [29–34]. Furthermore, the interaction of these two properties, to yield varying levels of personal and communal protection, is complex and has crucial implications for ITN programmes across Africa [11]. Sensitivity analysis of models similar to those used in this paper [11] have previously been used to explore the influence that these properties might have upon the magnitude and equity of protection afforded by ITNs (Figure 2). In order to validate this slightly revised model (see Equations 4-8) and similarly investigate such interactions at ITN coverage levels that can be plausibly sustained, we examined usage data collected during routine socioeconomic status surveys of a long-standing demographic surveillance system in the Kilombero Valley, southern Tanzania, where social marketing programmes have been well established since 1997 [77,78]. Data from the annual ITN usage survey in 2004 were used because they overlap with detailed entomological surveys of malaria transmission (which will be reported elsewhere). These surveys of randomly sampled residents from across two rural districts indicate that 75% (11,982/16,086) net use was achieved although most of these nets were not effectively treated [79]. In this sensitivity analysis, we assumed that new long-lasting ITN technologies [44–47] will enable sustained coverage with nets that are effectively treated even under the most rigorous programmatic field conditions. Figure 2 The Simulated Protection ITNs Afford against Exposure to Malaria Transmission as a Function of Their Ability to Divert and Kill Host-Seeking Mosquitoes Protection is expressed as relative exposure to malaria transmission (EIR C /EIR o ) for individuals with (Equation 19) and without (Equation 18) nets is plotted as a function of their ability to divert (Δp) and kill (μp) mosquitoes attacking protected humans. To simulate the likely field properties of existing long-lasting insecticidal nets with a full range of insecticidal and excito-repellent properties, the parameters of this model reflecting increased mosquito mortality (μp) and diversion (Δp) were varied across a plausible range of 0–0.8. As described in the main text and previous publications, these results represent simulations in two distinctive scenarios: An. gambiae sensu lato in the absence of cattle (results for both sibling species are identical) and An. arabiensis in the presence of one head of cattle per person. The biodemographic parameters of the interacting vector and parasite are also exactly as described previously [11,13] with survival of foraging mosquitoes (Pov) set at 0.8 per day. Coverage levels of 75% net usage was assumed, consistent with the results of surveys in the Kilombero Valley, southern Tanzania (see Methods: Parameters Reflecting the Effects of Insecticide-Treated Bed Nets). Figure 2 shows that, for the comparatively zoophilic vector An. arabiensis, in the presence of alternative hosts, excito-repellency consistently enhances the benefits for both users and nonusers, regardless of the insecticidal properties of the net. Consistent with previous analyses using this model [11], this simulation suggests that nets that are purely excito-repellent and lack insecticidal properties could slightly increase exposure of nonusers to An. gambiae sensu lato by diverting mosquitoes to them where no alternative sources of blood are available. Thus, purely diversionary vector control strategies may indeed be ethically questionable, as was previously suggested [31,34,80,81]. Nevertheless, even modest insecticidal properties are expected to counterbalance this inequity and confer a useful communal reduction of EIR. While repellent properties do slightly reduce the benefits to nonusers exposed to anthropophagic vectors lacking an alternative host, this slight disadvantage is likely to be outweighed in practice by the advantage of improved personal protection for users: Excito-repellent properties and physical barriers add to the effectiveness of insecticides for personal protection because these two incentives constitute the major motivating force behind ITN uptake and use at the individual and subsequently the community level. It is also reassuring to note that the predictions and epidemiological implications of this slightly revised model are very similar to those reported for its previous iteration [11]. We therefore concluded that the simulations described in the main text should consider ITNs with both insecticidal and excito-repellent properties, consistent with those of products currently on the market that have been evaluated in a variety of settings and experimental designs. To simulate the likely properties of established ITNs under programmatic conditions, we conservatively assumed they will both divert and kill 40% more mosquitoes than an unprotected human (μp = 0.4 and Δp = 0.4). A net with such proper-ties would protect against 64% of indoor exposure (1 − [(1 − 0.4) × (1 − 0.4)] = 0.64), as measured in a typical experimental hut trial [46,76]. To explore the best possible future scenario for the development of highly durable ITNs [44–47] or regular retreatment services [82], we also simulated increasing co-verage with nets that divert and kill 80% more mosquitoes than with an unprotected human (μp = 0.8 and Δp = 0.8), providing 96% protection (1 − [(1 − 0.8) × (1 − 0.8)] = 0.96). The proportion of normal biting exposure that occurs while nets are actually in use (πi) has been estimated as 90% for A. gambiae in southern Tanzania [13], so we set πi to a value of 0.90. Results Figure 3 illustrates how increasing community-level protection of ITN nonusers and users alike combines with constant individual protection to reduce exposure to malaria. Regardless of vector species or the availability of alternative hosts, modestly effective conventional ITNs achieve much greater impact upon human exposure, even that of users, if approximately half or more of the whole human population is covered. While this principle has already been suggested by field trials [19] and two independently formulated models [11,12], here we have identified specific coverage thresholds at which communal protection becomes greater than or equal to individual personal protection. Where alternative hosts for vector mosquitoes are absent, 35% of the human population must sleep under regular ITNs to achieve equivalence of personal and communal protection mechanisms, resulting in major community-wide suppression of exposure. The same target is achieved at 55% coverage where alternative hosts such as cattle are present. Figure 3 Relative Exposure to Malaria Transmission (EIR C /EIR o ) as a Function of Increasing Coverage with Insecticide-Treated Nets We express coverage as the proportion of the total human population using an ITN each night, and protection as the proportional reduction of infectious bites to which a resident is exposed (see Methods). Individual protection afforded to users (thin solid line; Equation 20) and communal protection afforded to nonusers (thick dashed line; Equation 18), as well as their combined effect on users (thick solid line; Equation 19) are separately calculated [11,13]. Two distinct but common and broadly distributed ecological scenarios in Africa are considered: (1) An. gambiae or An. arabienis (sibling species of the same species complex known as An. gambiae sensu lato) populations in the absence of alternative blood sources and (2) vector populations dominated by An. arabiensis in the presence of abundant cattle as alternative hosts. Both scenarios are simulated with ITNs that have either standard or improved properties (See Methods). Grey shading represents an approximate absolute maximum for community-level coverage achievable by covering vulnerable under five years of age and pregnant population groups only with perfect targeting efficiency. Arrows extrapolate the thresholds at which communal and personal protection are equivalent. The insecticidal and excito-repellent properties of ITNs that define levels of personal protection also determine the extent of community-wide alleviation of exposure amongst users and nonusers alike [11], so improved ITN properties consistently result in improved overall impact. In our model, slightly higher usage rates were required to achieve equivalence of individual and communal effects, with thresholds of 40% and 64% coverage for vector populations with and without alternative hosts, respectively (Figure 3). While emerging ITN technologies with long-lasting insecticidal properties under programmatic conditions [44] would confer useful personal protection even at low coverage levels, personal protection was greatly enhanced by communal protection. At the 75% total population coverage recently achieved with largely untreated nets in southern Tanzania (Killeen et al., unpublished data), net users and nonusers are predicted to receive >98% and >90% protection, respectively, regardless of ecological scenario, if those nets were to be replaced with improved long-lasting insecticidal nets. Even for users of improved ITNs, this level of protection against African vector species is impossible without the contribution of community-level transmission suppression, because at least 10% of exposure occurs outdoors during times of the night when nets are not in use [13,83]. We conclude that modest coverage (thresholds of approximately 35%–65% use, depending on ecological scenario) of entire malaria-endemic populations, rather than just the most vulnerable minority, is needed to realize the full potential of ITNs, even with longer-lasting products or regular retreatment services [14,44]. This range of modelled thresholds is remarkably consistent with the figure of 50% suggested by large-scale field trials using approximately equivalent technology [19]. Discussion In addition to the direct impacts on vector populations explicitly modelled above, coverage of adults and older children is likely to have further benefits arising from subtleties of mosquito resource utilization that are often under-appreciated. Over 80% of human-to-mosquito transmission originates from adults and children over five years of age, because these groups constitute the bulk of the population and are more attractive to mosquitoes [56]. Where the entomological inoculation rate is fewer than ten infectious bites per person per year, the distributions of infectiousness [56,69], morbidity, and mortality will all shift into these older age groups, necessitating protection of all members of the population. Under such conditions, ITNs could suppress transmission not only through direct impacts on mosquito mortality, host choice, and feeding frequency [11], but also by limiting the prevalence, density, and infectiousness of malaria parasites in the human population [56]. An under-emphasized feature of communal protection is the enhancement of ITN programme equity, regardless of ecological scenario or ITN effectiveness: If the majority of people living in malaria-endemic Africa regularly used existing ITN technologies, nonusers would receive communal protection at least equivalent to using the only ITN in an otherwise unprotected population (Figure 3). This means that all children would equitably receive communal protection at least equivalent to the personal protection of an ITN, with users receiving multiplicative combined effects on exposure of both personal and communal benefits. While the wisdom of targeting interventions to protect at-risk individuals is based on solid scientific grounds [9,18,84] and is widely accepted [16], this approach should not preclude efforts to maximize communal protection through less selective delivery mechanisms. Targeting limited subsidies to maximize personal protection of the most vulnerable should remain a priority, but more equitable and effective suppression of risk for entire populations, including vulnerable groups, can be attained with quite modest coverage across all ages. Most field evaluations of ITNs have been conducted at reasonably high coverage levels [19], and all five mortality trials [21,85–88] that estimated that ITNs save 5.5 lives for every 1,000 children protected [20] covered large portions of entire communities rather than only the children themselves. The choice of ITN delivery strategy has proven contentious in recent years [89,90], but proponents of both market-based and public-sector approaches equally emphasize targeting strategies [9,16,84] to enhance equity and minimize leakage of subsidized ITNs beyond intended target groups [91–94]. While optimal targeting of finite subsidies is highly desirable, there are fundamental limitations to the impact that can be achieved: Even if resources were perfectly targeted, 80% coverage of pregnant women and children under five years of age could be accomplished with less than 20% coverage of the whole population, and even less of the total human host availability [11,56], as well as the infectious parasite reservoir [56,69]. Even if the ITN coverage targets of the MDGs were attained with flawless targeting efficiency, the substantial and equitable benefits of communal protection would not be achieved. Specifically, the target of 70% less exposure to transmission [13] would not be attained by the remaining minority of vulnerable individuals who are not covered and do not use an ITN, regardless of ecological scenario or ITN properties (Figure 3). We therefore highlight an important caveat to the following conclusion of the current Global Strategic Framework for ITN scaleup in Africa [95]: “In order to achieve maximum public health impact, ITN coverage needs to be maximized amongst those population groups that are most vulnerable to malaria infection and its consequences, primarily pregnant women and children under five years of age.” Specifically, we conclude that protecting the vulnerable can achieve maximum public health impact only if complemented by strategies that also achieve broad coverage of the population as a whole. In reality, the targets for coverage of vulnerable groups will not be reached without some leakage and inequity. Our analysis suggests that such concerns may be less of a problem than the targets themselves and may be minimized by extending coverage priorities to include all age groups. Fortunately, consensus is finally emerging that a range of approaches to ITN deployment merit investigation, development, and comparative evaluation at scales for which no precedent yet exists [95]. Note that this analysis supports the implementation of any of the diverse and rapidly emerging delivery strategies as long as high coverage with long-lasting ITNs is sustained across entire malaria-endemic populations on national scales. Perhaps the most important remaining question is: How can such population-wide coverage levels be affordably and cost-effectively sustained? Growing financial support for malaria control globally [14,15,95] may enable fully subsidized provision to entire populations [82] of the world's most impoverished, malaria-afflicted nations. Existing evidence, based largely on individual protection alone, indicates that ITNs are as cost-effective as childhood immunization [96], and future analyses should explicitly consider the additional benefits of communal protection. Implementing this goal may be relatively straightforward for programmes that are primarily subsidized and implemented through the public sector, such as recent successful initiatives associated with vaccination campaigns [91]. By comparison, social marketing approaches, including hybrid systems that deliver public subsidies through the private sector, may require more detailed consideration, particularly where cost sharing with the target population is substantial and biased toward the nonpregnant adults and older children who are key to communal protection. Although social marketing approaches to ITN distribution face substantial challenges [93,97,98], notable success in terms of coverage and impact have been reported in a variety of settings [94,99,100], including the KINET programme in Kilombero Valley, southern Tanzania where ITNs have been promoted and subsidized since 1996 [77,78]. Much of the essential experience generated by KINET was later integrated into the ITN promotion strategy of the National Malaria Control Programme of Tanzania, which supports private sector distribution through a voucher system that subsidizes purchase by vulnerable priority groups [101]. In the meantime, the preceding KINET pilot in Kilombero has achieved 75 % net use amongst randomly sampled residents of all ages (Killeen et al., unpublished data). It is particularly noteworthy that substantial levels of communal protection were achieved [102] (unpublished data) even though most of these nets were untreated or poorly treated at the time of evaluation [79] (unpublished data). Reassuringly, the model applied here approximately reproduces these patterns of communal protection using plausible parameter estimates for the net properties, vector behaviours, and host demographics of the area (unpublished data). We therefore recommend that the cost-effectiveness of such hybrid approaches be explicitly evaluated in terms of the complementary respective contributions of public-sector subsidies and cost-sharing by target populations to personal and communal protection. While appropriate engagement and sensitization of malaria-afflicted populations is essential to the success of any ITN promotion programme, this is likely to be especially true where cost-sharing by the target population will be needed to complement limited public subsidies. Such cost-sharing schemes may be the only affordable means to support full population coverage where available subsidies are inadequate. In such resource-limited circumstances, high levels of awareness, acceptance, and willingness to pay will be essential to enable concerted use of ITNs by adults and shared protection of all children within their communities. Overly confident extrapolation from mathematical models to set operational targets for malaria control has proved to be a grave mistake in the past [103]. A number of complications not captured by this model could emerge as ITN coverage increases, not least of which might be increased selection for insecticide resistance [104,105]. While we urge caution in interpreting the numerical results of our analysis, the phenomenon outlined is well established and has clear implications for malaria control in Africa and beyond [19]. In fact, the analysis presented here provides a generalizable rationale that strongly supports the conclusions of the most recent and meticulous evaluations of the community-level benefits of ITNs: “High coverage with ITNs will do more for public health in Africa than previously imagined” [19]. We therefore suggest that further field data, analyzed with appropriate theoretical models and cost-effectiveness frameworks, are required to verify and quantify the levels of communal protection afforded by increasing ITN use across Africa. International targets [2,14,15] should be amended to include thresholds for coverage of entire populations and monitored accordingly. By making life increasingly difficult for mosquitoes through programmes that promote ITN use by the majority of their human victims, it may be possible to protect the 15%–20% of children and pregnant women in African communities who would not otherwise be covered even if existing personal protection targets of the MDGs [2], the Roll Back Malaria Partnership [14], or the U.S. President's Malaria Initiative [15] were to be achieved. Supporting Information Protocol S1 Model Spreadsheet A Microsoft Excel spreadsheet version of all model simulations presented here is available to download. (1.1 MB XLS) Click here for additional data file.
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            Increasing Coverage and Decreasing Inequity in Insecticide-Treated Bed Net Use among Rural Kenyan Children

            Introduction The gulf between levels of childhood mortality in sub-Saharan Africa and access to simple, cost-effective interventions known to significantly reduce mortality is immoral [1]. For over ten years it has been known that insecticide-treated bed nets (ITNs) can reduce childhood mortality by 17% [2]. In 1998 the Roll Back Malaria (RBM) movement was launched with one of its primary objectives to increase ITN coverage among vulnerable groups, such as children and pregnant women, to over 60% [3]. RBM has recently revised this ITN objective to reach 80% coverage by 2010 [4]. This change in target followed the RBM publication of the current status of ITN coverage in Africa as part of its World Malaria Report [5]. Of 34 malaria-endemic countries in Africa providing recent national data, only one (Eritrea) had achieved ITN coverage among children aged less than 5 y of more than 60% [5]. Reasons for this dismal progress has been the subject of much debate [6–9] and largely centre around divergent views on optimal strategies to deliver ITNs to economically and biologically vulnerable groups across Africa. During the early days of RBM, the technical advice to countries provided by World Health Organization (WHO) was to create an “enabling environment” that allowed malaria-endemic countries to embrace multiple approaches to providing ITNs [10]. These approaches included building sustainable private for-profit markets, for example through the NETMARK initiative in nine African countries [11]; creating a not-for-profit commercial sector through social marketing, a model promoted by Population Services International (PSI) operating in 23 African countries [12]; or the less popular at the time option of providing ITNs free of charge through clinics, or as first suggested in 1995, through vaccine campaigns [13]. The best-practice debate has been driven by personal opinion [6,7] or data on temporal changes in ITN coverage associated with single delivery approaches [14–16]. Where data exist they compare information on a single delivery model against a baseline without significant intervention or iterative increases in net coverage associated with a single, nationally adopted approach to delivery. Rarely is it possible to compare incremental coverage associated with different delivery models. Here we present a serial observation of ITN coverage among rural Kenyan communities exposed at different times to the range of delivery models each with legitimate claims to improve ITN access. Our emphasis throughout this study was to examine how ITN access by the poorest sectors of rural communities might best be achieved with each approach. Methods The Kenya ITN Context Prior to the launch of Kenya's National Malaria Strategy in April 2001 [17], access to nets was limited to the private for-profit retail sector and special project-based distributions through research- or nongovernmental organization-led community development initiatives [18]. In 2000 the Kenya Ministry of Health (MoH) developed with partners an ITN strategy paper [19] that attempted to accommodate two competing views on ways to reach the government's target of 60% coverage of populations at risk by 2005. The first approach included ways to ensure that the ITN market is self-sustaining in the absence of long-term donor support by expanding the private sector through social marketing; the second approach, principally favoured by the MoH, was to provide ITNs free of charge to pregnant women and children under the age of 5 y to achieve rapid scale-up. In January 2002 the UK Department for International Development (DFID) awarded PSI-Kenya US$33 million over 5 y to socially market partially subsidised ITN within the existing retail sector. The programme, named PSI Coverage Plus, was the only major operational ITN distribution initiative between 2002 and 2004 and aimed to target urban and rural retail outlets with Supanet ITNs across all malaria-endemic districts in Kenya. A two-tier pricing system of 350 Kenya Shillings (KES) (equivalent to US$4.7) in urban settings versus KES100 (US$1.3) in rural settings was implemented. The programme's aims were to increase community awareness of the value of ITNs thus creating a “net culture”; force existing retail prices down; and increase clients' willingness to pay for nets through a sustainable, unsubsidised commercial market [20]. In June 2004, DFID approved an additional US$19 million to PSI to establish a parallel distribution system of heavily subsidised ITNs to children and pregnant women through Maternal and Child Health (MCH) clinics, recognizing that these vulnerable groups might not be able to access socially marketed commercial sector nets. The programme began in October 2004, and during the first 6 mo Supanet ITNs were bundled with separate Powertab net treatment tablets (for every 6 mo) and distributed to MCH attendees. In May 2005 an additional US$37 million was committed by DFID to PSI to procure and distribute Supanet-branded long-lasting insecticidal nets (LLINs), Olyset and Permanet. These public sector nets were heavily subsidized pretreated nets (KES50; US$0.7) and branded with the MoH logo [20]. In February 2002 the MoH responded to the first call of the Global Fund to Fight AIDS, TB and Malaria (GFATM) for funding applications to secure five million nets and net treatments to provide free of charge to children under the age of 5 y and pregnant women. This application was unsuccessful. During round four of the GFATM awards in April 2004, Kenya's application was successful and US$17 million was approved to procure and distribute 3.4 million LLINs (Olyset and Permanet brands) free of charge to children under the age of 5 y. This represented, at the time, the largest successful award for free distribution of LLINs in Africa. The implementation of the free mass distribution of LLINs was arranged in two phases during 2006. During the first phase, 21 of Kenya's 70 districts were selected for distribution of LLINs from 8 to 12 July 2006 and integrated with the national measles catch-up vaccination campaign. Health facilities and centralised non-health facility posts were identified by the Kenya Expanded Programme on Immunisation and used as delivery points of both measles vaccine and LLINs to each child under the age of 5 y. A second mass distribution of LLINs, not integrated with any other intervention, took place from 25 to 27 September 2006 in 24 additional districts using previous mass vaccine campaign delivery centres as distribution points. Study Area The study was carried out in four districts purposively sampled in collaboration with the MoH to provide detailed longitudinal milestone data on changing access to interventions proposed within the Kenya National Malaria Strategy between 2001 and 2006 [21,22]. The study districts represent the range of dominant malaria epidemiological situations that prevail across Kenya: Kwale on the coast with seasonal high-intensity malaria transmission; Bondo on the shores of Lake Victoria with perennial high-intensity transmission; Greater Kisii district (combining the new districts of Kisii Central and Gucha) with seasonal low transmission conditions of the Western highlands; and Makueni district, a semi-arid area with acutely seasonal low malaria transmission. Between 63% and 71% of households in the rural areas of each of the four districts were living below the poverty line (equivalent to US$1 per day) in 1999, compared to the national average of 54% [23]. The districts were also representative of rural districts in Kenya with respect to net delivery since 2001, with service providers including the full-cost commercial and social marketing retail sector; a research team in parts of Bondo district [24]; nongovernmental organization delivery to selected communities in Greater Kisii (Merlin and World Vision) and Kwale (Plan International and The Aga Khan Foundation); time-limited MoH provision of free nets to pregnant women in 2001 in all districts [25] and to children and pregnant women in Bondo and Gucha districts in 2005 [26]; and subsidized PSI clinic distribution since October 2004 and mass, free distribution in 2006 across all districts. Within each district, rural enumeration area (EA) boundaries were digitized with ARCGIS 9.0 (ESRI, http://www.esri.com/) and each polygon attributed to population totals derived from the last national census in 1999 [27]. A sample of 18 rural EA polygons, covering approximately 6,500 people per district, was randomly selected from each district to form the basis of the longitudinal community surveillance. Following community sensitisation, all homesteads within an EA polygon were mapped and heads of homesteads were given the purpose of the longitudinal study and asked whether they wished to participate. All de jure resident homestead members were enumerated, including details of date of birth and sex, and issued a unique identifier for follow-up. The Longitudinal Cohort During December/January of 2004/5, 2005/6, and 2006/7, just after the short rains, a cohort of children under the age of 5 y was established to track, by interviewing mothers or caretakers, the ownership and use of bed nets, including details on the net brand, where and when they were obtained, and whether nets had been treated with an insecticide during the previous 6 mo. Interviewers were instructed to observe the nets and record details of the colour, imprinted logos, and shape of the net to match the net types delivered by different partners in each district at different times. All children resident in 2004 were recruited into the cohort and exited during subsequent census rounds if they had out-migrated, homesteads or guardians subsequently refused participation, they had reached their fifth birthday, or they had died. New children were recruited into the cohort if they had migrated into the homestead between census rounds or were identified through detailed birth histories of all resident women aged 15–49 y as having been born during the interval. New infants who did not survive the interval between census rounds were included in the cohort. In-migrations that out-migrated between the census rounds were not included in the cohort and were regarded as short-term visitors not permanently resident. During the 2005/6 annual census round, representing the reference midpoint of the surveillance period, details were recorded on each homestead relating to key asset indicators, including: homestead head education level and occupation; housing characteristics (type of wall, roof, and floor); source of drinking water; type of sanitation facility; homestead size; and persons per sleeping room (see Table S1). Data Entry and Analysis Data entry and storage were undertaken using Microsoft Access, and analysis was undertaken using STATA version 9.2 (Stata, http://www.stata.com) and ARCGIS 9.0 (ESRI). All information specific to the EA, homestead, and mother or guardian were linked to the relevant child through the use of a primary homestead identifier consistent across all data sets. To account for unequal probabilities of selection of EAs, all results were weighted (weight = 1/probability of selection) and precision of proportions (95% confidence intervals [CIs]) were adjusted for clustering with EA as the primary sampling unit. A χ2 test was performed to compare net use proportions across subgroups within and between survey years. For comparisons of socioeconomic groups within a survey year, the Pearson χ2 statistic, accounting for clustering, was used. This statistic is turned into an F-statistic using the second-order Rao and Scott correction and p-values interpreted the same way as the Pearson χ2 statistic for data without clustering [28,29]. A homestead wealth index was constructed from the asset indicators using principal component analysis. Weights (scoring coefficients) derived from the first principal component were used to construct the wealth index [30]. Weights for each asset indicator from the first principal component were then applied to each homestead record to produce a wealth index. Wealth asset indices were developed separately for each district to allow for innate differences in the meaning of different assets between districts. Each homestead was then assigned to a district-specific wealth quintile. Net ownership by children in the cohort was examined serially and by source according to wealth asset quintiles. Inequity in net coverage over time and by source was analysed using the concentration index, which gives values between −1 and 1, with a value 0 indicating an absence of wealth-related inequality in net use among children [31]. Because net use is a “good” health variable, a positive value of the index indicates net use is concentrated among the wealthy. The concentration curve was plotted to illustrate changes in wealth-related inequality [31]. Ethical Approval Ethical approval was provided by the National Ethical Review Board IRB (Kenya Medical Research Institute SSC number 906). Results A total of 2,761 homesteads were selected across the 72 rural communities located in the four districts in 2004. Three homesteads refused participation in 2004 (0.01%); 11,050 observations of children under the age of 5 y were made across the three survey years in 2004/5, 2005/6, and 2006/7. Over the three years, 155 (1.4%) usually resident children were visiting elsewhere at the time of the annual surveys, 66 (0.6%) children's parents or guardians refused to be interviewed and 133 (1.2%) children died before the census rounds in 2005/6 and 2006/7. In 2004/5 the weighted proportion of children usually using a net, adjusted for clustering, was 13.9%, similar to the proportions of children using a net the night before the survey (Table 1). The small difference between usual use of a net and net use the night before survey was a consistent finding across all surveys (Table 1). We elected to restrict subsequent analysis to net use the night before survey. In 2004/5 the majority of children (65%) who slept under a net were sleeping under nets purchased from the commercial retail sector, only 7% of children slept the night before the survey under nets treated with an insecticide within the last 6 mo, and the proportion ITN use among children living in the poorest quintile homesteads was one-fifth (2.9%) to the proportion of those living in the least poor homesteads (Table 1). Table 1 Net Usage by Children across Four Districts in Three Consecutive Survey Years In December/January 2005/6, 12 mo after the baseline survey, the proportions of children sleeping under a net had increased to 32% where the dominant net source was the heavily subsidized PSI-MCH clinic nets; 58% of children using a net were using nets from this source (Table 1). The proportion of children sleeping under a net treated with an insecticide in the last 6 mo had tripled to over 23% compared to 2004/5 (p < 0.001). Children living in the poorest homesteads had proportionately the largest (six-fold) increase in ITN use over the 12 mo interval, rising from 2.9% in 2004/5 to 17.5% in 2005/6 (p < 0.001); however, children living in the least poor homesteads were still twice as likely to have slept under an ITN the previous night as those in the poorest homesteads (Table 1). These results are reinforced by the concentration indices, which remained positive (net use highest among the wealthier groups) in both rounds of the survey, although the measure of wealth-related inequality, the concentration index, fell from 0.281 in 2004/5 to 0.131 in 2005/6. By December/January 2006/7, the proportion of children sleeping under a net increased to 81%, with the two dominant sources of nets being the free mass campaign (44%) and the PSI-MCH clinics (41%) (Table 1). Within 12 mo of the previous survey, the proportion of children sleeping under an ITN had doubled to 67%; 44% of children were sleeping under an ITN provided during the mass campaign. The largest increase in the proportion of children sleeping under an ITN was among those from homesteads in the poorest quintile, from 17.5% in 2005/6 to 66.3% in 2006/7. There was no statistically significant difference in the proportion of children using an ITN between highest and lowest wealth quintiles in 2006/7 (p = 0.963). The poverty concentration index declined from 0.131 in 2005/6 to 0.000 in 2006/7 (Table 1). The concentration curve indicated, for the first time, the absence of wealth-related inequality in net use (Figure 1) further illustrated by the graph of actual proportions (Figure 2). Figure 1 Degree of Inequality in Children Sleeping under an ITN in 2004/5, 2005/6, and 2006/7 in Homesteads of Different Wealth Status in the Four Districts in Kenya The concentration curve below the line of perfect equality indicates that ITN use is concentrated among higher socioeconomic groups. When the curve is coincident on the line of perfect equality, then there is no wealth-related inequality in ITN use. Figure 2 Proportion of Children Sleeping under an ITN in 2004/5, 2005/6, and 2006/7 in Homesteads of Different Wealth Status in Four Districts in Kenya By the end of September 2006, the three principal net distribution strategies (retail social marketing, heavily subsidized clinic distribution, and free mass distribution) were all operating in parallel, providing an opportunity to examine socioeconomic targeting of each of the delivery mechanisms (Table 2). In 2006/7 2.4% and 24.3% of children from the poorest homesteads slept under a net from the retail sector and the PSI-MCH programme, respectively, compared to 6.4% and 30.8% from the least poor. Conversely, by 2006/7 the highest proportion of children from the poorest homesteads slept under nets from the free mass campaign (most poor/least poor: 36.6%/25.8%). This pattern is further illustrated by the concentration curve (Figure 3), which shows that the free mass campaign is the only delivery channel favouring the poorest children; the PSI-MCH programme was marginally in favour of the least poor, and the commercial sector was the most inequitable in favour of the least poor. Table 2 Variations in Children's Net Use the Night before the 2006/7 Survey by Source across Different Socioeconomic Groups Figure 3 Degree of Inequality in Socioeconomic Targeting by the Three Principal Net Delivery Mechanisms in Four Districts in Kenya by 2006/7 Delivery mechanisms included commercial social marketing, the PSI-MCH programme, and a free mass campaign. Discussion We have shown that a concerted, multi-pronged approach to ITN delivery in rural areas of Kenya over 3 y resulted in over 60% of children sleeping under a net treated with insecticide, surpassing the original RBM target set in Abuja in 2000 [3]. However, at the end of 2004 this target seemed almost unattainable, with only 7% of rural children reported to be sleeping under an ITN and only 3% among the poorest sectors of these communities. Radical changes in bilateral support to PSI to adapt their social marketing strategy to included MCH clinics resulted in important changes in ITN coverage (24%) by the end of 2005, but coverage still favoured the least poor children. The most dramatic increases in ITN coverage were seen during the last year of the surveillance period at the end of 2006. Through two single mass campaigns in July and September 2006, coverage of ITN use rose to over 67% and was particularly successful at reaching the poorest children (Tables 1 and 2). The concentration index of ITN coverage, which is a measure of inequality, decreased from 0.281 in 2004/5 to 0.000 in 2006/7, indicating an absence of inequality in net use (Figures 1 and 2; Table 1) coincidental with the expansion in different mechanisms of delivery. In recent years, there has been a consensus among national ministries of health, development partners, and other stakeholders that access to health interventions should be made pro-poor [30]. Although gaps in ITN coverage between the least- and most-poor groups have been declining elsewhere in Africa [5], the most-poor remain the least well covered. Our results show that ITN coverage among children was similar across all wealth groups by 2006/7. and nets provided through the free mass campaign actually preferentially covered children from the poorest-quintile homesteads while the heavily subsidised PSI-MCH clinic nets was considerably more equitable than the commercial social marketing (Figure 3; Table 2). Elsewhere in Africa pro-poor ITN interventions have been reported [32–35], but these efforts have been relatively small in scale. To the best of our knowledge this is the first time in Africa that a large-scale public health intervention, covering millions of people, has preferentially reached the most-poor quintiles of a community when compared to the least poor. Unlike single cross-sectional surveys of ITN coverage, the value of the present study is its longitudinal observations among the same homesteads exposed at different times to different systems of delivery. Such data help inform debates on whether ITN delivery should be free or subsidized and whether they should be provided through routine clinics, mass campaigns, or the private sector. Our data clearly show that the most effective means to rapidly scale up ITN coverage, particularly among the poor, is through targeted free distributions, preferably coincidental with other campaigns such as mass vaccination. However, it does not necessarily follow that this should represent the only mechanism by which treated nets are distributed to rural communities. The PSI programme of heavily subsidized net delivery through over 3,000 clinics since October 2004 has reported over 5 million sales of nets [20]. The complex distribution, ordering, and logistics of net commodities were run efficiently by an externally funded and managed system with the infrastructure and staff provided by the government and mission sectors [36]. Although there are no data to support the claim that the provision of subsidized nets at clinics increased use of health facilities, this may have occurred and is a similar argument used to increase attendance at mass Expanded Programme for Immunisation vaccine campaigns that provide free nets [15]. The PSI programme, however, did not reach nationally or internationally agreed targets of ITN coverage within the specified timelines. Similarly routine Expanded Programme for Immunisation services, provided free at clinics, often fail to reach their anticipated coverage targets [37]. We would argue that the constant availability of ITNs at clinics provides an essential early entry point for net use, particularly among young pregnant women who would otherwise not have access to ITNs if restricted to a single annual event targeting children as part of a mass distribution campaign. For vaccine-based programmes to retain effective herd immunity, periodic catch-up campaigns of single mass coverage of vulnerable populations are necessary. We would view this as an analogous position for effective ITN coverage. It is therefore not a question of choosing between the strategies but how to effectively combine them. Some sectors of our rural communities can afford subsidized ITNs, but when only these nets are available the most-poor access them least. It is likely that those bearing the brunt of the malaria burden in rural areas are those most distal to health services and the poorest. Provision of free nets would benefit these communities most. Our results are far less supportive of international donor-promoted efforts to expand the commercialization of ITN distribution in Africa [8,11]. This approach clearly failed to reach those most in need in Kenya, and despite aggressive marketing campaigns, and development of branded products and branded outlets, the incremental gains in ITN coverage were minimal. To effectively integrate routine versus mass campaign ITN distribution requires careful planning. It is important that when planning integrated free mass campaigns, each component of the package is not jeopardized by the other, for example delaying immunization to meet the needs of ITN distribution. In Kenya, funding for the donor-supported PSI programme ends in 2007. Funds are available from the GFATM and the World Bank Booster Programme during 2007 and 2008 to continue LLIN distribution through mass campaigns. Replacing or “permanently” treating existing non-LLINs, covering future vulnerable pregnant women and their infants and expanding to pockets of the country where coverage has remained low all require long-term sustainable financing planned against projected spatially defined needs. These combined approaches require long-term evaluations, modelled on the approach presented, to monitor the synergies between delivery strategies to make sure they retain the equity required to reach those most in need. Whether funding for combined models of delivery comes from national budgets, direct budgetary support from donors, or through mechanisms such as the GFATM, Presidents Malaria Initiative, or the World Bank is beyond the scope of this paper. What we can say is that if funding is not secured for clinic supply and catch-up mass campaigns for LLIN delivery beyond 2008 the impressive, rapid progress toward the RBM target of 80% coverage by 2010 in Kenya will be lost. Supporting Information Table S1 Asset Indicators and Their Weights Computed Using Principal Component Analysis to Construct Homestead Wealth Quintile Rankings for Each District (45 KB DOC) Click here for additional data file.
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              Assessment of insecticide-treated bednet use among children and pregnant women across 15 countries using standardized national surveys.

              Impact of insecticide-treated bednets (ITNs) on preventing malaria may be minimized if they are not used by vulnerable populations. Among ITN-owning households from 15 standardized national surveys from 2003 to 2006, we identify factors associated with ITN use among children younger than 5 years of age and make comparisons of ITN use among children and pregnant women across countries. Within ITN-owning households, many children and pregnant women are still not using them. Between-country analysis with linear regression showed child ITN use increases as intra-household access to ITNs increases (P = 0.020, R2 = 0.404), after controlling for season and survey year. Results from within-country logistic regression analyses were consistent with between-country analysis showing intra-household access to ITNs is the strongest and most consistent determinant of use among children. The gaps in ITN use and possession will likely persist in the absence of achieving a ratio of no more than two people per ITN.
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                Author and article information

                Journal
                Malar J
                Malaria Journal
                BioMed Central
                1475-2875
                2011
                11 April 2011
                : 10
                : 83
                Affiliations
                [1 ]Papua New Guinea Institute of Medical Research (PNGIMR), PO Box 60, Goroka, EHP 441, Papua New Guinea
                [2 ]School of Population Health, University of Queensland, Brisbane, Australia
                [3 ]Population Services International (PSI), Papua New Guinea
                [4 ]Barcelona Centre for International Health Research, Barcelona, Spain
                Article
                1475-2875-10-83
                10.1186/1475-2875-10-83
                3080352
                21477376
                30c977d0-f93e-44c1-9a3d-1ca62717deae
                Copyright ©2011 Pulford et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 4 February 2011
                : 11 April 2011
                Categories
                Review

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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