Transmission of Leishmania infantum in the Canine Leishmaniasis Focus of Mont-Rolland, Senegal: Ecological, Parasitological and Molecular Evidence for a Possible Role of Sergentomyia Sand Flies

Leishmania (L.) infantum is the causative agent in an endemic focus of canine leishmaniasis in the Mont-Rolland district (Thiès, Senegal). In this area, the transmission cycle is well established and more than 30% of dogs and 20% of humans are seropositive for L. infantum. However, the sand fly species involved in L. infantum transmission cycle are still unknown. Between 2007 and 2010, 3654 sand flies were collected from different environments (indoor, peridomestic, farming and sylvatic areas) to identify the main L. infantum vector(s). Nine sand fly species were identified. The Phlebotomus genus (n = 54 specimens; Phlebotomus (Ph) duboscqi and Phlebotomus (Ph). rodhaini) was markedly under-represented in comparison to the Sergentomyia genus (n = 3600 specimens; Sergentomyia (Se) adleri, Se. clydei, Se. antennata, Se. buxtoni, Se. dubia, Se. schwetzi and Se. magna). Se. dubia and Se. schwetzi were the dominant species indoor and in peridomestic environments, near humans and dogs. Blood-meal analysis indicated their anthropophilic behavior. Some Se. schwetzi specimens fed also on dogs. The dissection of females in the field allowed isolating L. infantum from sand flies of the Sergentomyia genus (0.4% of Se. dubia and 0.79% of Se. schwetzi females). It is worth noting that one Se. dubia female not engorged and not gravid revealed highly motile metacyclic of L. infantum in the anterior part of the midgut. PCR-based diagnosis and sequencing targeting Leishmania kinetoplast DNA (kDNA) highlighted a high rate of L. infantum-positive females (5.38% of Se. dubia, 4.19% of Se. schwetzi and 3.64% of Se. magna). More than 2% of these positive females were unfed, suggesting the parasite survival after blood-meal digestion or egg laying. L. infantum prevalence in Se. schwetzi was associated with its seroprevalence in dogs and humans and L. infantum prevalence in Se. dubia was associated with its seroprevalence in humans. These evidences altogether strongly suggest that species of the Sergentomyia genus are probably the vectors of canine leishmaniasis in the Mont-Rolland area and challenge one more time the dogma that in the Old World, leishmaniasis is exclusively transmitted by species of the Phlebotomus genus.
Author Summary Leishmaniases, neglected tropical vector-borne diseases, remain today a problem of public health. Classically, the sand flies involved in Leishmania transmission belong either to the Phlebotomus genus (Old World) or to the Lutzomyia genus (New World). In the rural community of Mont-Rolland (Senegal, West Africa), Leishmania infantum is the causative agent in an endemic focus of canine leishmaniasis. Recent surveys revealed more than 30% of dogs and 20% of humans with a positive serological test for Leishmania in this community. However, the sand fly species involved in L. infantum transmission were still unknown. Between 2007 and 2010, we carried out a study in this community to identify the sand fly species responsible for L. infantum transmission. We collected nine species belonging mainly to Sergentomyia genus and in low proportion to Phlebotomus genus. The abundance around dogs and humans, the detection of live and mature parasites in anterior midgut, the high rate of L. infantum-positive females using molecular analyses and the identification of dog and human blood in the fed females incriminates Se. schwetzi and Se. dubia as possible vectors of L. infantum. This hypothesis is strongly supported by statistical analyses performed to compare the prevalence of infected sand flies with the seroprevalence data in humans and dogs.