Research Article: Ecology: A Prerequisite for Malaria Elimination and Eradication

Date Published: August 3, 2010

Publisher: Public Library of Science

Author(s): Heather M. Ferguson, Anna Dornhaus, Arlyne Beeche, Christian Borgemeister, Michael Gottlieb, Mir S. Mulla, John E. Gimnig, Durland Fish, Gerry F. Killeen

Abstract: Gerry Killeen and colleagues argue that malaria eradication efforts will not be successful until a better understanding of the ecology and evolution of the mosquito vectors is gained.

Partial Text: The Global Malaria Eradication Program, launched in the middle of the last century, over-promised and under-delivered [1]. Decades of pessimism followed, during which malariologists were afraid to even mention the goal of this program by name [2]. The term eradication was often nervously referred to as “the E-word” by a disillusioned community that had learned from bitter experience that optimistic forecasts [3] had been based on an oversimplified view of transmission ecology [4]. Eradication of malaria remains beyond our grasp today, but is nevertheless firmly back on the global health agenda as a long-term target [5].

By definition, eradication of human malaria parasites globally [5] requires that intervention options are available that can eliminate transmission anywhere in the world. Leading vector control technologies such as insecticide-treated nets (ITNs) and indoor residual spraying (IRS) can suppress transmission by one or even two orders of magnitude [4],[6] and dramatically alleviate disease burden [7],[8]. Nevertheless, these measures alone are not sufficient to eliminate transmission in large tracts of tropical Africa where the entomological inoculation rate (EIR), the most direct measure of human exposure, can exceed a thousand infectious bites per person per year [9],[10]. Expressed in terms of the parasite’s reproductive number, this means that if the local parasite population were entirely eliminated by mass drug administration, for example, a single infected person moving into the area could give rise to as many as ten thousand new infections and readily re-establish stable transmission [10]. Under such conditions, simulations predict that even 100% coverage of an entire population with ITNs exhibiting near-ideal properties will fail to push the EIR below the threshold required for local elimination [11]. Although massive benefits of increasing ITN and IRS coverage have been achieved in many parts of equatorial Africa, elimination has remained elusive except for regions on the edge of stable transmission in Kenya, Tanzania and The Gambia (e.g. [12]–[14]). Evidence from the previous malaria eradication drive [4],[15] and contemporary initiatives [8],[16],[17] indicate that transmission remains robust in areas where it has been historically high. We argue here that a failure to appreciate the biological complexities that allow vector populations to resist or evade interventions has substantially impeded control efforts. In particular, we identify seven ecologically imposed obstacles that have limited the effectiveness of vector control, and must be tackled in order to move from control to eradication (Box 1).

The ecological hurdles detailed in Box 1 imply that there exists a fundamental limit to the degree of control that can be achieved with ITNs or IRS. In most settings, achieving elimination will require interventions which target mosquitoes outside of human habitations. Existing and new interventions must be combined into integrated packages [18],[19] that control mosquitoes at multiple points in the continuum from egg to adult, by targeting the key environmental resources upon which they rely to complete their life cycle: aquatic larval habitat, mates, sugar sources, blood hosts, and resting sites (Figure 1). With the exception of blood, very little is known about how mosquitoes use these resources or how to manipulate them so that malaria transmission is interrupted. We conclude that a better understanding of all aspects of vector ecology will inevitably yield numerous new and mutually complementary targets for integrated vector control. Ecology is therefore a prerequisite to eradication or elimination, and will be essential to sustaining success in the long term.

Our understanding of the ecology of mosquitoes that transmit malaria lags decades behind that of agricultural pests, endangered species, and model organisms. The reasons are multifaceted [26],[27], and disincentives include the lack of ecological representation and thus support on the funding panels of biomedical donors, limited training opportunities in fundamental ecology for medical entomologists, and the necessary ethical restrictions upon the types of experimental manipulations that are widely used to gain valuable insights into the population, community, and ecosystem dynamics of other insects [28] which do not transmit pathogens to humans. Examples of procedures which can yield crucial scientific information, but which are increasingly difficult to justify ethically include human landing catches [21] (because of the exposure risks they entail) and mark–recapture studies of mosquito demography and dispersal (because of community concerns about the re-release of potentially infectious mosquitoes that could instead have been killed). Evaluation of the potential use of alternative animal hosts to divert mosquitoes from biting humans also poses potential risks; theoretical simulations indicate there are plausible scenarios under which this may increase transmission by increasing blood availability and vector survival [29].

The overarching strategic priority for increased investment should therefore be to improve the quantitative understanding of mosquito life history, fitness, genetics, and behavioural processes as determinants of their population stability and malaria transmission intensity. Support should be directed towards delivering key outcomes, without which malaria eradication is difficult to envisage (Box 2). As such, ecology should—like other basic disciplines such as molecular biology and bioinformatics—be considered an enabling science essential for defining the target product profiles of completely new control technologies and delivery systems. To achieve these outcomes and make malaria eradication a realistic ambition, we propose key areas for specific strategic investment (Box 3).



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