Targeting indoor residual spraying for malaria using epidemiological data: a case study of the Zambia experience

The World Health Organization (WHO) launched the Roll Back Malaria Initiative in 1998, a global partnership with the goal to halve the burden of malaria. Since 2000, worldwide, the number of annual malaria infections has decreased by 26 % (173–128 million) with a concomitant 47 % reduction in mortality [1]. To continue this progress, proven interventions, such as rapid diagnostic testing (RDT), artemisinin-based combination therapy, intermittent preventive therapy for pregnant women, long-lasting insecticidal-treated nets (LLINs), and indoor residual spraying (IRS) are recommended [2, 3]. Universal coverage with LLINs is defined as one net per two people, and is recommended by the WHO for all people at risk of malaria [4]. To complement LLIN use, IRS has been scaled up in many African countries with the aim of supporting malaria control or elimination, depending on the underlying transmission. In 2014, a total of 90 countries, 42 in the African region, recommended IRS for vector control as a primary intervention for malaria [2].

IRS operates by either repelling mosquitoes from entering sprayed houses or by killing female mosquitoes that are resting inside houses after having taken a blood meal [5, 6]. IRS is most effective for endophilic and endophagic vectors, with maximum killing potency achieved when malaria vectors rest on IRS-treated inside walls [6, 7]. A ‘mass effect’ of IRS is thought to be obtained with high, e.g., >85 %, coverage of structures in a sprayed area [6]. Scientific evidence supporting this threshold is, however, limited and the combined impact in areas of high LLIN coverage is unclear from the few rigorous studies that have been conducted [8–10]. Furthermore, impact may be modified by transmission intensity and length of the malaria transmission season [11]. The WHO currently encourages full coverage of LLINs plus supplemental IRS, but more evidence is needed [12].

Historically, IRS has generally been implemented at district level or other similar, large-scale geopolitical unit. This approach is largely due to limited availability of data on the exact geographic distribution of households and IRS coverage at sub-district levels. This status quo approach presumably developed as most countries adopted a ‘blanket spraying’ strategy to target all eligible structures. The considerable challenges of delivering IRS, however, mean achievement of 100 % coverage is often unrealistic due to logistics, refusals, absent residents, and other factors, such that 85 % coverage is recommended by the WHO [6].

Increasing levels of insecticide resistance have forced IRS programmes to adopt insecticides costing more than triple the price of pyrethroids. For example, pyrethroid lambda-cyhalothrin costs ~$2–$3 per unit (sachet/bottle equivalent), whereas carbamate bendiocarb costs ~$12 per unit, while pirimiphos-methyl, a long-lasting organophosphate, costs ~$23 per unit. With one unit able to cover ~ three houses depending on size, the need to target resources to where they will have maximum impact becomes increasingly necessary in resource-constrained settings [13]. Considering that malaria transmission is highly heterogeneous within districts and is often focalized into hotspots (<1km²) [14–16], the strategy of blanket spraying in areas of universal LLIN coverage may be unnecessary and even cost-ineffective to achieve maximum gains in the reduction of malaria transmission, particularly in resource-constrained environments [2]. Unfortunately, limited policy and little data exist to inform the best strategies for targeted IRS to achieve maximum reduction in malaria transmission, particularly in areas of documented pyrethroid resistance and universal LLIN coverage. At this time, the WHO recommends only focal IRS in elimination settings to target remaining clusters or outbreaks of transmission [6]. However, sub-district targeting of non-pyrethroid IRS in low- to medium-transmission areas with universal LLIN coverage might be considered to mitigate pyrethroid resistance and drive down transmission in ‘hot spots’ [17].

Tools sufficient to manage targeted IRS campaigns must address three issues. First, the spatial location of all structures in a district must be mapped and the structures enumerated. Second, a robust targeting strategy must be developed to determine the size of the geographical units for which targeting is feasible or desirable to achieve the greatest impact with limited resources. Third, spray operators in the field must be guided to deliver IRS to targeted structures and record spray activities structure-by-structure to determine target area coverage. Other papers outline the use of freely available satellite imagery to determine the spatial location of all eligible structures [18], and forthcoming work will outline the development of a tool to guide spray operators in the field [19]. This paper focuses on the second aspect of targeted IRS campaigns: the need to develop robust targeting methodologies for IRS. Critical issues that remain to ensure effective and efficient IRS planning and implementation are outlined.

Routine malaria incidence data were used to create an objective IRS targeting strategy via a method that is reproducible and relatively simple. In countries with a functional health management information system, this methodology does not necessarily require additional data collection. Based on the approach outlined, IRS can be targeted to high incidence, population-dense areas reducing distance necessary for spray teams to move from one structure to the next. Incorporating local knowledge and engaging district healthcare to confirm the selections and provide field-based guidance was also essential to this data-driven process.

Despite the ease of using health facility data to target IRS, there are limitations to the targeting approach used in 2014. For a number of reasons, routinely collected incidence data at the health facility may not always reflect the true underlying malaria risk. First, facility data is aggregated and therefore has very low spatial granularity. For example, a health centre catchment in Zambia may represent 8–10,000 people spread over 40 km² or more. Malaria transmission is typically heterogeneous, but identifying sub-facility pockets with an elevated or depressed risk of transmission is not possible using health facility data at this time. Second, health facility data may be delayed or inaccurate due to recording errors or the lack of diagnostic confirmation [23–25]. The freely available malaria testing and treatment at government health centres likely encourages treatment, however, individual treatment seeking behavior may bias a health facility’s risk profile. For example, centres located at major transport nodes or those that have an above average reputation may find that they attract individuals from outside their catchment increasing the calculated incidence. Further, variation in the presence and variety of alternative sources of care (e.g., private clinics which do not report data to a central Health Management Information System (HMIS) may bias incidence measures.

Even in the presence of high quality health facility incidence data, there is a dearth of scientific evidence on how best to apply limited IRS to achieve maximum impact against malaria transmission. For the methodology described here, the number of expected malaria cases per target area was used to rank target areas from highest priority to lowest. This methodology biases the ranking toward larger target areas, which are financially and logistically easier to spray than an equivalent number of houses in multiple smaller target areas. However, it is unknown whether spraying these smaller areas with higher incidence rates would have a better impact on malaria transmission than spraying the larger areas with higher case counts.

A major benefit of this method was introducing a mapped and guided IRS approach to previously unmapped areas. However, the use of objectively defined target areas in some instances led to poorly understood target-area boundaries during field operations (Fig. 1). For example, what appeared to be a continuous stretch of adjacent households would sometimes be separated into two target areas, with one receiving IRS and the other not (owing to incidence and population factors in the ranking methodology). These anomalies should have been identified and rectified through scrutiny of the selected target areas during local review. In reality, it seemed this was not always achieved either through challenges with understanding the targeting methodology or translating the map. To rectify this, for the 2015 season, an evidence-based filter was developed to ensure that proximal target areas receive the same response when biologically appropriate and feasible.

Few data exist on how to best move from the current implementation strategy (i.e., targeting IRS to maximize cost efficiency by focusing on the most accessible structures) to a strategy of targeting IRS based on epidemiological patterns. Such a data-driven approach is needed, particularly in areas of high LLIN coverage and/or insecticide resistance. The enumeration and operational aspects of targeted IRS have begun to be addressed through the use of satellite enumeration and geo-tagging IRS activities [21]. However, it is far from clear how best to identify the highest risk structures/areas to prioritize in a targeted approach.

Three ways are suggested to improve the accuracy of IRS targeting for future spray seasons. The first involves improving the quality and resolution of incidence data so that the most accurate, up-to-date, and least aggregated data are used to inform IRS targeting [26]. An example of this process may be seen throughout areas of Lusaka, central, southern and western provinces of Zambia, where malaria incidence is collected via mobile phone from a network of community health worker posts. With an average of eight health posts per health facility, community health workers have expanded care into the community and subsequently increased the spatial resolution of the HMIS data [27]. The second way to improve targeting of IRS is to incorporate malaria transmission maps that highlight entomological risk. Since the main goal of IRS is to kill and repel mosquitoes, spraying households near anopheline mosquito breeding sites, that are likely to have the highest mosquito density, may have a disproportionately higher impact on transmission. Targeting based on malaria incidence alone does not necessarily target households and populations that would benefit most from IRS. Predictive risk maps have been developed using satellite imagery and remotely sensed data to accurately characterize the location of mosquito breeding sites and high transmission risk areas [28], and further work should apply those findings to malaria intervention targeting. A third way of improving targeting is to include entomological data to account for insecticide resistance frequency and intensity, the primary vectors in the area and their seasonality and vector density. While entomological data are expensive to collect at fine scale, routine entomological surveillance systems are being employed in Zambia to build a better understanding of, and therefore better targeting of, the vector.

These three recommendations all focus on generating better data to provide a stronger platform to guide decision making for targeted IRS. However, more research is also needed to identify the specific targeting approach required to achieve the most effective IRS campaign. To that end, a comparison study of different targeted IRS approaches applied within various contexts is now being planned by this group and collaborators in order to generate evidence on the most effective and cost-efficient IRS strategies. In preparation for this study, baseline research is being collected in one of 15 districts that received targeted IRS in 2014 to understand the demographic and ecological factors associated with an effective, targeted IRS campaign.

In summary, advances in computing and GIS have opened the door to reassess and enhance the implementation of IRS. With limited malaria prevention and control tools available, it is essential that all available tools, including IRS, are used as effectively as possible. Further research to develop best-practice approaches for the implementation of IRS in environments of high LLIN coverage and also heterogeneous malaria transmission is necessary to inform malaria control programmes on the most effective and efficient IRS strategies to reduce malaria-related morbidity and mortality.