A Sticky Situation: the Unexpected Stability of Malaria Elimination
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A sticky situation: the unexpected stability of malaria elimination David L. Smith1,2,3,4,5, Justin M. Cohen6, Christinah Chiyaka3, Geoffrey Johnston1,2,3, Peter W. Gething7, Roly Gosling8, Caroline O. Buckee9, 4 5,7 5,10 rstb.royalsocietypublishing.org Ramanan Laxminarayan , Simon I. Hay and Andrew J. Tatem 1Department of Epidemiology, and 2Malaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA 3Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA 4Center for Disease Dynamics, Economics and Policy, Washington, DC, USA 5Fogarty International Center, NIH, Bethesda, MD, USA Research 6Clinton Health Access Initiative, Boston, MA, USA 7Spatial Ecology, Department of Zoology, University of Oxford, Oxford, UK Cite this article: Smith DL, Cohen JM, 8Malaria Elimination Initiative, Global Health Group, University of California San Francisco, Chiyaka C, Johnston G, Gething PW, Gosling R, San Francisco, CA, USA 9 Buckee CO, Laxminarayan R, Hay SI, Tatem AJ. Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA 2013 A sticky situation: the unexpected 10Department of Geography and Environment, University of Southampton, Highfield, stability of malaria elimination. Phil Southampton, UK Trans R Soc B 368: 20120145. http://dx.doi.org/10.1098/rstb.2012.0145 Malaria eradication involves eliminating malaria from every country where transmission occurs. Current theory suggests that the post-elimination chal- lenges of remaining malaria-free by stopping transmission from imported One contribution of 15 to a Theme Issue malaria will have onerous operational and financial requirements. Although ‘Towards the endgame and beyond: resurgent malaria has occurred in a majority of countries that tried but failed complexities and challenges for the elimination to eliminate malaria, a review of resurgence in countries that successfully of infectious diseases’. eliminated finds only four such failures out of 50 successful programmes. Data documenting malaria importation and onwards transmission in these countries suggests malaria transmission potential has declined by more Subject Areas: than 50-fold (i.e. more than 98%) since before elimination. These out- ecology, health and disease and epidemiology, comes suggest that elimination is a surprisingly stable state. Elimination’s theoretical biology ‘stickiness’ must be explained either by eliminating countries starting off qualitatively different from non-eliminating countries or becoming different once elimination was achieved. Countries that successfully eliminated were Keywords: wealthier and had lower baseline endemicity than those that were unsuc- malaria elimination, malaria eradication, cessful, but our analysis shows that those same variables were at best backwards bifurcation incomplete predictors of the patterns of resurgence. Stability is reinforced by the loss of immunity to disease and by the health system’s increasing Author for correspondence: capacity to control malaria transmission after elimination through routine treatment of cases with antimalarial drugs supplemented by malaria out- David L. Smith break control. Human travel patterns reinforce these patterns; as malaria e-mail: [email protected] recedes, fewer people carry malaria from remote endemic areas to remote areas where transmission potential remains high. Establishment of an inter- national resource with backup capacity to control large outbreaks can make elimination stickier, increase the incentives for countries to eliminate, and ensure steady progress towards global eradication. Although available evidence supports malaria elimination’s stickiness at moderate-to-low trans- mission in areas with well-developed health systems, it is not yet clear if such patterns will hold in all areas. The sticky endpoint changes the pro- jected costs of maintaining elimination and makes it substantially more attractive for countries acting alone, and it makes spatially progressive elim- ination a sensible strategy for a malaria eradication endgame. Electronic supplementary material is available at http://dx.doi.org/10.1098/rstb.2012.0145 or via http://rstb.royalsocietypublishing.org. & 2013 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited. 1. Introduction been achieved, either by sustaining control measures even 2 after elimination or through intense surveillance to identify rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20120145 Malaria was the first human disease formally scheduled for and cure all imported and subsequent infections before they global eradication, when a vote of the 8th World Health Con- can lead to the resumption of transmission [18,19]. These con- gress in 1955 made it the official policy and launched the tinued measures make even the medium-term projected costs Global Malaria Eradication Programme (GMEP), so malaria of elimination higher than maintaining existing control pro- has a special place in the history of human disease eradica- grammes [20]. Failure to sustain elimination following loss of tion. By 1969, however, the GMEP had collapsed and the immunity would leave populations vulnerable and raise the World Health Organization changed the malaria agenda for risk of a deadly resurgent malaria epidemic [21]. Elimination countries from imminent elimination to indefinite control is thus regarded as a risky and, often, unwise strategy [22]. [1,2]. Malaria was then neglected for decades. Bill and A major long-term issue for malaria elimination planning Melinda Gates’ call for eradication [3] has reoriented strategic is thus the risk posed by malaria importation and how it can thinking about malaria since 2007, and global eradication be managed. In Zanzibar, for example, the feasibility assess- was reinstated as the long-term policy goal by a consensus ment showed that importation rates were the primary decision of the Roll Back Malaria Partnership (RBMP) in determinant of the cost and overall feasibility of sustainable 2008 [4,5]. Decisions about elimination are taken at the elimination [7]. Many countries have insufficient capacity to national level, with advice given to formally assess the feasi- organize the long-term operations needed to maintain bility of malaria elimination [6]. Zanzibar conducted the first malaria elimination, insufficient funds or competing priori- (and still only) malaria elimination feasibility assessment in ties [23]. The GMEP had assumed that malaria elimination 2009 [7]. Meanwhile, of the 99 countries that still have ende- would be coordinated globally and, consequently, post-elim- mic malaria, 36 have already made plans to eliminate malaria ination planning for malaria importation was not prioritized [8]. The basis for making appropriate decisions about elimin- since most countries could assume that their neighbours ation policy and practice remains one of the most important would also soon be eliminating malaria [12]. Without a cam- research topics in malaria [5,9,10]. paign, some coordination is occurring through bilateral Malaria elimination involves stopping transmission in a agreements or regional initiatives [24,25], but these efforts defined region until no parasites remain [11,12]; eradication remain limited. The need to mitigate ongoing risks of malaria is elimination on a global scale. Elimination is currently importation is, perhaps, the most basic difference between guided by a theory of malaria transmission dynamics and the endgame of a globally coordinated malaria eradication control based largely on work by Macdonald [13–15]. The campaign and that of national/regional elimination plans potential intensity of transmission under baseline conditions based on decisions of individual countries. is described by the basic reproductive number, R0, the Strategic decisions facing countries involve whether to expected number of new human malaria cases arising from eliminate malaria or minimize the burden through malaria a single human malaria case [16]. Baseline entomological control. Minimizing burden and eliminating malaria both determinants of transmission are described by vectorial involve sharply reducing transmission, but discussions capacity in a population with no vector control, V0, and epi- about elimination and eradication are often seen as being in demiological aspects of baseline transmission are described conflict with the ongoing efforts to minimize the burden of by the net infectiousness of a human case with no immunity malaria, particularly in sub-Saharan Africa [22,26]. The and no antimalarial drug use, D0, so that R0 is proportional rising tide of funding for malaria control has been stemmed to V0D0. Elimination must be achieved by interrupting trans- by the global economic recession that started in late 2008. mission through implementation of vector control, treatment In the short-term, outside donor funding for malaria is of infected individuals and usage of other available interven- expected to plateau at around 1.5 billion US dollars per tions, such as larval source management or active case year, far short of the amounts required to eradicate malaria detection. Vector control changes vectorial capacity to VC, [27]. With inadequate funding, it becomes more important and drugs and immunity change net infectiousness of than ever to prioritize