Sustaining elimination of malaria in areas with high receptivity and vulnerability will require effective strategies to prevent reestablishment of local transmission, yet there is a dearth of evidence about this phase. Mauritius offers a uniquely informative history, with elimination of local transmission in 1969, re-emergence in 1975, and second elimination in 1998. Towards this end, Mauritius's elimination and prevention of reintroduction (POR) programs were analyzed via a comprehensive review of literature and government documents, supplemented by program observation and interviews with policy makers and program personnel. The impact of the country's most costly intervention, a passenger screening program, was assessed quantitatively using simulation modeling.
On average, Mauritius spent $4.43 per capita per year (pcpy) during its second elimination campaign from 1982 to 1988. The country currently spends $2.06 pcpy on its POR program that includes robust surveillance, routine vector control, and prompt and effective treatment and response. Thirty-five percent of POR costs are for a passenger screening program. Modeling suggests that the estimated 14% of imported malaria infections identified by this program reduces the annual risk of indigenous transmission by approximately 2%. Of cases missed by the initial passenger screening program, 49% were estimated to be identified by passive or reactive case detection, leaving an estimated 3.1 unidentified imported infections per 100,000 inhabitants per year.
The Mauritius experience indicates that ongoing intervention, strong leadership, and substantial predictable funding are critical to consistently prevent the reestablishment of malaria. Sustained vigilance is critical considering Mauritius's enabling conditions. Although the cost of POR is below that of elimination, annual per capita spending remains at levels that are likely infeasible for countries with lower overall health spending. Countries currently embarking on elimination should quantify and plan for potentially similar POR operations and costs.
Citation: Tatarsky A, Aboobakar S, Cohen JM, Gopee N, Bheecarry A, Moonasar D, et al. (2011) Preventing the Reintroduction of Malaria in Mauritius: A Programmatic and Financial Assessment. PLoS ONE 6(9): e23832. https://doi.org/10.1371/journal.pone.0023832
Editor: Abdisalan Mohamed Noor, Kenya Medical Research Institute - Wellcome Trust Research Programme, Kenya
Received: March 2, 2011; Accepted: July 26, 2011; Published: September 2, 2011
Copyright: © 2011 Tatarsky et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This case study was funded by grants from the Bill and Melinda Gates Foundation and ExxonMobil to the Global Health Group. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The corresponding author had full access to all the data in the study and had final responsibility for the decision to submit for publication.
Competing interests: AT, JC, BM, and OS work within or assist the malaria program at the Clinton Health Access Initiative, which is supporting malaria elimination in southern Africa. SA, NG, AB, and DM are actively involved in the management of elimination or prevention of reintroduction programmes in Mauritius (SA, NG, and AB) and South Africa (DM). AP works at The Global Health Group of the University of California, San Francisco; the Global Health Group exists in part to document and disseminate evidence from malaria elimination efforts, and is funded by the Bill & Melinda Gates Foundation and ExxonMobil. DM, AP, BM, DS, and OS are members of the Malaria Elimination Group. JK has a paid consultancy with the bednet manufacturer, Vestergaard Frandsen. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials. The findings and conclusions in this paper are those of the authors and do not necessarily represent the views of their employing organizations nor the sources of funding.
Recently, a growing number of countries have experienced dramatic reductions in malaria transmission and have set short-term goals for elimination . Among this group are a number of countries in sub-Saharan Africa and other regions where baseline malaria transmission is high . Several countries, including Morocco, Oman, and the United Arab Emirates, have recently achieved elimination and others are on the verge of doing so . The recent surge of interest in and pursuit of elimination requires a close examination of post-elimination, or prevention of reintroduction (POR), activities. While recent recommendations suggest that countries should thoroughly assess the feasibility of preventing reintroduction prior to embarking on a serious elimination effort , many outstanding questions surrounding malaria elimination and POR remain. What is the cost structure of successful elimination and POR programs? Can malaria-free status be maintained in areas with an efficient vector and frequent importation of new cases? What is an effective combination of interventions to sustain elimination?
Despite the fact that several countries have been actively preventing the reintroduction of malaria over the past several decades , there continues to be a dearth of evidence about this phase. POR was considered only superficially during the Global Malaria Eradication Program (GMEP) since a global campaign by definition implied that importation and resurgence were not of significant concern. Since then, most evidence generated has focused on control in high endemic areas or the process of interrupting transmission , . As a result, only a limited empirical foundation is available today to guide strategic decision-making in countries that may successfully achieve elimination without the benefit of their neighbors and the wider malaria endemic world doing the same.
To help close this evidence gap, the elimination and prevention of reintroduction experience on the island nation of Mauritius was closely analyzed. The Republic of Mauritius consists of several reefed islands in the Indian Ocean, including the larger populated islands of Mauritius and Rodrigues with a total population of 1,288,000 in 2009 . The islands experience subtropical climate year round and heavy rainfall from December to May during the hot, wet summer with frequent and often destructive cyclones . Total expenditure on health as a percentage of GDP in 2009 was 5.7% .
Plasmodium vivax and Plasmodium falciparum and their vectors, Anopheles funestus and Anopheles arabiensis, were most likely imported into Mauritius by ships with slaves and indentured laborers arriving from malaria-endemic East Africa and South Asia during colonization from early 1800 to 1860 . In 1867, a violent malaria epidemic erupted in Mauritius that resulted in 40,000 deaths of a population 330,000, with 6,000 deaths occurring in just one month in urban Port Louis . Mauritius was globally notorious for its malariousness after the epidemic, making the achievement of elimination that much more remarkable more than 100 years later .
Mauritius's experience is well suited to generate lessons for the current wave of countries today that are pursuing or considering elimination. It is one of only two sub-Saharan African countries to have fully eliminated malaria and has historically faced malaria transmission equivalent to many mainland countries . Mauritius, a country that interrupted local transmission in 1969, saw it reemerge in 1975, and once again ended transmission in 1998, continues to receive high volumes of travelers from malaria endemic countries despite its relative isolation.
This paper examines the history of malaria elimination in Mauritius, with a particular focus on the country's POR programs. The composition and costs of both elimination and POR programs are analyzed and the impact of its single most costly component, a passenger screening program, is examined quantitatively to provide evidence on its effectiveness and cost-efficiency. Finally, recommendations are presented based on the Mauritius experience to inform decision-making in other countries embarking on malaria elimination.
Literature review and interviews
To identify all available information on the history of malaria epidemiology, control, and elimination in Mauritius, a systematic literature review was conducted. PubMed (United States National Library of Medicine), OVID (Ovid Technologies, Inc.), and Google Scholar databases were searched using the keywords “malaria”, “Mauritius”, and “eradication” or “elimination.” Relevant citations contained in resulting publications were also included, as well as published government and WHO reports and digitized books. In addition, all gray literature available at the National Archives, Health Statistics Unit, Mauritius Institute of Health, and Communicable Disease Control Unit (CDCU) of the Ministry of Health and Quality of Life was searched for reference to malaria, malaria control, or elimination. Only literature dated from 1860, the time of emergence of malaria in Mauritius, was included in the review. All narratives, health statistics, and financial budgets related to malaria in Mauritius were extracted from this subset of reports and publications and compiled for analysis by AT.
Direct observation of ongoing surveillance and vector control activities furnished additional insights, and visits to major implementing institutions in Mauritius and the ports of entry allowed closer examination of the passenger screening program. Further information was collected through approximately 50 interviews using semi-structured questionnaires with key technical experts, policy makers, and operational personnel from past and present malaria programs. All individuals were purposively selected based on their professional affiliation in public health, most of whom had current or past involvement in malaria financing, program management, or implementation. Information was verified through document review, and, when possible, from additional individuals with identical rank and responsibility.
All identified costs from budgets, technical reports, and program reviews were allocated to specific activities within four main intervention categories – surveillance and diagnosis; treatment; prevention; and management. Within each activity, costs were classified as personnel, consumables, capital equipment, training, or services.
Comprehensive costing data were available for both elimination campaigns, 1948–1951 and 1982–1988. Costs were also available for 1960–1961, 1990–1991, and 2008. Although local transmission was not interrupted until 1968 and re-interrupted until 1998, interventions and strategies in 1960 and 1990 were very similar to those during POR. Malaria incidence had virtually reached zero during these years ,  and strategies were in place that continued until reemergence (1975)  and through the early 1990s . Therefore, costs for these two years and for 2008 are considered representative of POR and are analyzed as such in this paper.