Elimination of Malaria, Comoros Archipelago | CDC EID

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Volume 16, Number 11–November 2010
Research
Genetic Structure of Plasmodium falciparum and Elimination of Malaria, Comoros Archipelago

Stanislas Rebaudet,1 Hervé Bogreau,1 Rahamatou Silaï, Jean-François Lepère, Lionel Bertaux, Bruno Pradines, Jean Delmont, Philippe Gautret, Philippe Parola, and Christophe Rogier Comments to Author
Author affiliations: Institute for Biomedical Research of the French Army, Marseille, France (S. Rebaudet, H. Bogreau, L. Bertaux, B. Pradines, C. Rogier); Université de la Méditerranée, Marseille (J. Delmont, P. Parola); Assistance Publique–Hôpitaux de Marseille, Marseille (P. Gautret); Programme National de Lutte contre le Paludisme, Moroni, Comoros (R. Silaï); and Dispensaire de Bandraboua, Mayotte, France (J.-F. Lepère)

Suggested citation for this article

Abstract
The efficacy of malaria control and elimination on islands may depend on the intensity of new parasite inflow. On the Comoros archipelago, where falciparum malaria remains a major public health problem because of spread of drug resistance and insufficient malaria control, recent interventions for malaria elimination were planned on Moheli, 1 of 4 islands in the Comoros archipelago. To assess the relevance of such a local strategy, we performed a population genetics analysis by using multilocus microsatellite and resistance genotyping of Plasmodium falciparum sampled from each island of the archipelago. We found a contrasted population genetic structure explained by geographic isolation, human migration, malaria transmission, and drug selective pressure. Our findings suggest that malaria elimination interventions should be implemented simultaneously on the entire archipelago rather than restricted to 1 island and demonstrate the necessity for specific chemoresistance surveillance on each of the 4 Comorian islands.

Plasmodium falciparum causes malaria worldwide; 250 million cases and ≈1 million deaths occur annually, mostly in sub-Saharan Africa. However, recently increased international financial commitment has revived hope for malaria elimination from selected areas to which it is endemic, and the feasibility of elimination has become a topic of research (1). The successful elimination of malaria from several Caribbean islands, Cyprus, Reunion, Mauritius, Maldives, Taiwan, and Singapore in the context of the Global Malaria Eradication Program (1955–1968) (2) suggests that islands are prime targets for elimination interventions. Because most parasites among neighboring areas are exchanged through human migrations, the geographic isolation of islands can limit malaria importation and may make control easier (3,4).

Several molecular epidemiologic studies have shown that P. falciparum populations are more or less homogeneous within malaria-endemic areas and may exhibit genetic structure patterns shaped by various transmission rates and geographic isolation levels (4–6). Although geographic isolation may be more relevant on islands than within continents, the role of parasite genetic structure in malaria-endemic archipelagos or among malaria-endemic islands and the nearest continent remains unknown. Past failures of malaria elimination in Zanzibar off the coast of mainland Tanzania; in Sri Lanka (1); or in Mayotte, a France-administered island of the Comoros archipelago (7), raise the question of the minimal geographic isolation level and the optimal size of intervention area required for malaria elimination success. Analysis of malaria epidemiology in Comoros archipelago, where a limited malaria elimination program is ongoing, may help to answer this question.

Falciparum malaria remains a major public health problem on the 4 islands of the Comoros archipelago (Grande Comore, Moheli, Anjouan, and Mayotte) (Table 1) in the Indian Ocean between Madagascar and the eastern coast of Africa. Malaria control has been hampered by the emergence of P. falciparum resistance to chloroquine and to pyrimethamine/sulfadoxine in the early 1980s (7,10) and of Anopheles mosquitoes resistance to DDT. Malaria control also has had recurrent political, economic, and structural weaknesses in the Union of the Comoros (the state comprising Grande Comore, Moheli, and Anjouan islands). Under stable political and economic conditions, notable efforts in case management and vector control in Mayotte failed to eliminate falciparum malaria and to prevent recurrent epidemics (Table 1). During the past 6 years Since 2004, health authorities in Grande Comore and France have introduced an artemisinin-based combined therapy (artemether plus lumefantrin) as first-line treatment for uncomplicated falciparum malaria (7,10). Large-scale distribution of insecticide-treated mosquito nets also has been gradually implemented on Grande Comore, Moheli, and Anjouan (8), with the goal of reaching up to 89.1% and 46.3% of the households with at least 1 mosquito net and 1 insecticide-impregnated mosquito net, respectively, among 1,620 households from the 3 islands (Comoran National Malaria Control Program, unpub. data, 2007).

In Mayotte, anti–Anopheles spp. mosquito larvae measures have been strengthened. Finally, by late 2007, a controversial malaria elimination project was launched on the sole island of Moheli with assistance from China. Mass treatment of the residing and disembarking population with artemisinin plus piperaquine (Artequick; Artepharm Co., Guangzhou, People's Republic of China) and primaquine was initiated without enhancement of vector control. Because of continual human travel across the archipelago, the long-term success of such a spatially limited elimination attempt is questionable.

In addition, surveillance of P. falciparum chemosusceptibility has been chaotic and unequal among the islands of the archipelago, and results of the few available therapeutic efficacy tests and in vitro and molecular resistance studies often have been discordant. A more rational and efficient surveillance system is urgently needed. Because Marseille, France, houses a Comorian community of 50,000–80,000 persons who annually import several hundred malaria cases, the city was proposed as a relevant surveillance site for chemosusceptibility of P. falciparum imported from Comoros (11). However, extrapolating these chemoresistance data to the entire archipelago remains difficult.

As already proposed for Borneo (12) and the Philippines (13), our main objective was to analyze the genetic structure of P. falciparum on the Comoros islands to 1) forecast the chances of middle-term and long-term success for the current elimination program focalized in Moheli, 2) guide future malaria elimination programs on the archipelago, and 3) adjust its chemoresistance monitoring and treatment policies. Study results also would provide a pertinent model for determining which other malaria-endemic areas might be eligible for malaria elimination. A secondary objective was to assess whether the diversity of the P. falciparum strains imported into Marseille were representative of the P. falciparum populations from Comoros so we could evaluate the relevance of distant chemoresistance surveillance from Marseille.

We characterized P. falciparum populations from each of the 4 islands and from Marseille (imported from the archipelago) by multilocus microsatellite genotyping. The genetic polymorphism of 3 genes involved in P. falciparum resistance to chloroquine, pyrimethamine and cycloguanil, or sulfadoxine was also investigated.

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Elimination of Malaria, Comoros Archipelago | CDC EID

Suggested Citation for this Article

Rebaudet S, Bogreau H, Silaï R, Lepère J-F, Bertaux L, Pradines B, et al. Genetic structure of Plasmodium falciparum and malaria elimination, Comoros archipelago. Emerg Infect Dis [serial on the Internet]. 2010 Nov [date cited]. http://www.cdc.gov/EID/content/16/11/1686.htm

DOI: 10.3201/eid1611.100694

1These authors contributed equally to this article.