In the sixties, the relative seriousness of malaria and the seasonal transmission of Plasmodium falciparum by Anopheles gambiae s.l. in Dakar were reported in different studies 1234. Immunity was acquired quite slowly during the first 20 years of life 5. Malaria-infected individuals came from rural areas to Dakar and contributed to the start of transmission, which culminated in October-November after the end of the rainy period 6. In the eighties, an entomological survey proved that malaria transmission occurred in Pikine in the suburb of Dakar and that Anopheles arabiensis was the main vector in this area 6. In the nineties, malaria transmission persisted in Pikine and in the surrounding villages of Dakar, always with An. arabiensis as the vector 7. During the same period, two parasitological and entomological studies conducted in two sanitary districts of Dakar showed that the prevalence of malaria was very low; a few An. arabiensis were caught, and none of them were infected by P. falciparum 8910. Based on these results, many practitioners thought that there was no malaria transmission in Dakar intra-muros (i.e. in the down-town area) and that the infections occurred in the suburbs or inland. Nevertheless, human malaria cases were reported in autochthonous people who had not been outside Dakar for at least one year, suggesting that malaria was transmitted in Dakar 10. At the same time, French military doctors were confronted with malaria cases in expatriates, who were visiting a malaria endemic country for the first time, but had never left downtown Dakar. To assess the reality of malaria transmission in Dakar, an entomological evaluation was conducted at the French military bases of Dakar from May 2005 to October 2006, over two winters.

Malaria transmission is a reality in Dakar. P. falciparum-infected Anopheles have been caught during two rainy periods consecutively in two quarters of the town. All infected An. gambiae s.l. were caught only during the rainy period. The seasonal transmission occurs in the end of the rainy season from September to November. In August 2005, very heavy rains (278 mm of water in six days) flooded many parts of the city. Many potential breeding sites were created, and the An gambiae s.l. aggressiveness was high, with a peak of almost 200 bites per person per night in September. This abnormal situation in Dakar, due to an exceptional climatic event, could have led to an exceptional malaria transmission. However, the catch of infected Anopheles during the 2006 winter proved that malaria transmission is not exceptional and occurred each year during this period. These data agree with clinical data from a Senegalese military Hospital of Dakar (Hospital Principal), where most malaria cases occur between October and December.

Only specimens of An. arabiensis were infected. Anopheles arabiensis is the main member of the gambiae complex in Dakar and, according to its abundance and to the results of this study, is the main malaria vector. The presence of An. melas was detected in Dakar for the first time in the present study. Nevertheless, this vector was not found to be infected with P. falciparum. Until now, An. melas had been reported only in the mangrove swamps of the Delta's Saloum (south Senegal) and in the Senegal River delta (north Senegal) 1819. In addition, neither Anopheles pharoensis nor An. gambiae molecular form M caught in Dakar were infected with P. falciparum. The aggressiveness of An. arabiensis was higher in Bel-air than in Ouakam, but EIRs were very high in the two quarters. An. arabiensis is more endophagic in Ouakam. This behavior allows for an easier access to a human blood meal that may explain the similar EIRs observed for the two quarters.

The seasonal character of transmission allows us to calculate mean annual EIR for the two years of study. In Bel-air, the mean annual EIR fell from 9.5 in 2005 to 4 in 2006. In Ouakam, a similar mean annual EIR of 3 was estimated for 2005 and 2006. Our observations are consistent with the results of a meta-analysis of studies of malaria transmission in sub-Saharan Africa, which found a mean annual EIR of 7.1 in the city centers, with more than two-thirds of the studies reporting EIRs < 4/year 20. In 1996, the number of infective bites per person was estimated to 0.05/year for the central area of Dakar, i.e., one infective bite every 20 years 10. This work was conducted on a very large area with 13 study sites but with only two catching points per site and human landing collections performed once every month. Ten years later, the risk of malaria transmission seemed to be 60 to 80 times higher. The peak of An. gambiae s.l. aggressiveness lasts for a little longer than one month (Figure 3). With a monthly rhythm of capture, the previous study could have missed this peak. Nevertheless, a modification of the entomological situation over ten years cannot be excluded. There is some evidence that anopheline species may be adapting to urban ecosystems. Adaptation of An. gambiae s.s. to urban aquatic habitats, such as water-filled domestic containers, has been observed in Accra, Ghana 21. In addition, adaptations of the anopheline vectors to new breeding sites (tree holes, polluted water) are reported from many urban areas in Africa 222324. The impact of urbanization on the composition of the vector system and malaria transmission dynamics has been highlighted in many studies 2526. Urban farming provides ample aquatic habitats for mosquitoes, which are responsible for the persistence of anopheline populations in many African towns 272829. In Ouakam and Bel-air, as in other places in Dakar, market gardens are present with or without water wells (cement wells or traditional wells called "ceanes"). The urban area of Dakar contains more than 5,000 market-garden wells, which provide permanent sites for mosquito larvae, in particular An. Arabiensis 30. The increase of the An. arabiensis population size during the 2005 winter is an argument to highlight the major role of temporary pools in malaria transmission in Dakar. Further specific study is necessary to understand the impact wells and urban farming on anopheline density and malaria transmission.

This situation questions the origins of these anopheline populations. Are there autochthonous populations from Dakar growing during the rainy season, or are they coming in from other areas of Senegal? Populations of An. arabiensis in West Africa are considered to be continuous throughout the year, with many individuals surviving through the dry season, perhaps in a physiologically altered state rather than through extinction or a severe bottleneck during the dry season, followed by re-colonization by a few individual survivors or immigrants in the subsequent rainy season 31. In Barkedji, Senegal, Simard et al did not detect any difference in measures of genetic diversity and linkage disequilibrium between the dry and rainy seasons 32. They concluded that, despite extreme minima in local density, malaria transmission in this area was due to autochthonous population of An. arabiensis. They also found a low differentiation between two populations, which were 250 Km apart, suggesting extensive gene flow across this distance. These results suggest that An. arabiensis maintains a large permanent deme over a large area. The situation in Dakar seems similar to that in Barkedji: a long dry season where no An. arabiensis (or only a few) are caught 33. Further genetic studies will be necessary to confirm the hypothesis that malaria transmission is due to an autochthonous An. arabiensis population, and to assess the gene flow between the urban and rural populations of Senegalese An. arabiensis.

Pyrethroids are the main insecticide used in malaria vector control, including indoor residual spraying and impregnated materials (bednets, curtains, plastic sheeting). Pyrethroids have the advantage of acting very rapidly as insecticides, with both knockdown and lethal effects at dosages under the threshold of mammalian toxicity 34. Since 1970s, pyrethroids have been extensively used in urban areas and for agricultural purpose in rural areas. Detected in the 1990s, knock-down resistance (Kdr) to pyrethroids and DDT of An. gambiae s.l is an increasing problem. Two mutations at the same locus in the voltage-gated sodium channel are known to confer knock-down resistance to a wide range of pyrethroids and DDT 353637. These mutations were previously described in west and east Africa (Kdr-w and Kdr-e) in An. gambiae s.s. as well in An. arabiensis 38394041. There are few studies of An. arabiensis insecticide susceptibility in the area of Dakar. In 1987, bioassays were conducted in two places in the suburbs of Pikine and of Thiaroye 42, where in vivo resistance to DDT was observed. The agricultural use of DDT in market gardens was incriminated. In 1999, a normal susceptibility of An. arabiensis was found in Dakar 43. Our data show a Kdr-w frequency of 0.12 in Bel-air and 0.09 in Ouakam. The populations were not at Hardy-Weinberg equilibrium for Kdr in either site (P < 0.0001). This disequilibrium could be due to local selection pressure by the agricultural use of pyrethroids in market gardens.

The Kdr mutation has been shown to be closely associated with DDT and pyrethroid resistance in several An. gambiae populations (particularly the molecular S form) 353637. However, the role of Kdr in conferring resistance in An. arabiensis remains unclear 4445 As a result, insecticide susceptibility tests should be carried out to assess physiological resistance levels in An. arabiensis in Dakar. However, this is the first report of the Kdr-w mutation in An. arabiensis in Dakar. Resistance to carbamate and organophosphate insecticides is also widespread in West Africa. The presence of an insensitive acetylcholinesterase in populations of An. gambiae s.s. of both forms was revealed by biochemical assays. The ACE-1-R mutation has also been detected in the two molecular forms of An. gambiae s.s in many West African countries 1746. This mutation has not been detected in An. arabiensis at present. Our results are consistent with these data.

In terms of effective vector control at the military camps and in town, choice of insecticide should depend on the results of susceptibility tests on An. arabiensis.

Malaria prevalence is very low in Dakar and its urban periphery 7810. Nevertheless, cerebral malaria is the first etiology of neuromeningeal diseases in Dakar 47. Extensive genetic diversity was observed in P. falciparum isolates collected in Dakar 484950. Significant linkage disequilibrium was observed with microsatellite loci in urban parasites. Two non-exclusive hypothesis could explain the situation in Dakar: (i) a global non-panmictic structure of Dakar malaria population due to a high predominance of selfing; (ii) a structuration in subpopulations of several malaria foci in Dakar. The entomological findings of the present study are consistent with seasonal transmission leading to an increase of cases in the October end of the rainy season. There is a concern about the origin of Plasmodium falciparum infections observed in Dakar during the rainy season. Are they due to autochthonous parasites transmitted during the winter or to parasites imported from the suburbs by commuters, as suggested by Vercruysse? 6 In Senegalese people employed by the French army, the first malaria cases are diagnosed in commuters at the beginning of the rainy season, and cases in residents occur later in the season. The movement of populations from the suburbs or rural areas to Dakar must be considered to understand malaria epidemiology in Dakar 5152.

Urban malaria is considered to be an emerging problem in Africa. In 2003, 39% of Africa's people lived in urban settings; by 2030, 54% of Africans are expected to do so 53. With the increase of people living in urban dwellings, it's important to develop and validate new approaches for rapid appraisal of malaria risk. The rapid urban malaria appraisal (RUMA) methodology has been develop to provide a cost effective tool to conduct assessment of the malaria situation in urban sub-Saharan Africa and to improve the understanding of urban malaria 54. The only entomological point required is in this evaluation is the mapping of breeding sites. Considered very time-consuming, this task has been done only in Ouagadougou 27.

The results of this study confirm that the vector complex situation in African towns is always changing, with the description of An melas and An gambiae s.s. in Dakar. Entomological studies are long, difficult and require time and special expertise but they are indispensable to understand the dynamics of malaria transmission in urban settlements and to monitor the increase of the insecticide resistance in urban mosquitoes. The study showed a difference in host finding behaviour between the two quarters: An. arabiensis are more endophagic in Ouakam than in Bel air. This difference of behaviour has an impact on the malaria transmission level. With a lower biting activity during the transmission season, the Annual EIR in Ouakam remains as high than in Bel air. Indoor vector control measures will probably not have the same impact in the two quarters. The misuse of impregnated bed nets during this period is probably riskier in Ouakam.

Malaria is transmitted in Dakar. This seasonal transmission occurs only during the two last months of the rainy season. The transmission level could be very high. Further studies have to be conducted in other parts of Dakar to assess the risk of transmission, to understand the role of permanent and temporary pools, the impact of urban farming and to discover the origin of the Dakar anopheline populations.

The authors declare that they have no competing interests.

FP was responsible for the study design, supervision of data collection, analysis, interpretation and production of the final manuscript and revisions. GT contributed to the supervision of data collection, the data analysis, interpretation and production of final manuscript. BP contributed to the supervision of data collection, to the data analysis, interpretation and production of final manuscript. LG contributed to the supervision of data collection, to the data analysis, interpretation and production of final manuscript. VM contributed to the data analysis and to the preparation of the final manuscript. FJ contributed to the supervision of data collection, to the data analysis. KP contributed to the supervision of data collection, to the data analysis. FB contributed to the supervision of data collection, to the data analysis. JFT was contributed to overall scientific management, analysis, interpretation and preparation of the final manuscript and revisions. CR was contributed to overall scientific management, analysis, interpretation and preparation of the final manuscript and revisions. CS was responsible for overall scientific management, analysis, interpretation and preparation of the final manuscript and revisions. All authors read and approved the final manuscript.