Ecology of Phlebotomine Sand Flies in the Rural Community of Mont Rolland (Thiès Region, Senegal): Area of Transmission of Canine Leishmaniasis

BACKGROUND: Different epidemiological studies previously indicated that canine leishmaniasis is present in the region of Thiès (Senegal). However, the risks to human health, the transmission cycle and particularly the implicated vectors are unknown. METHODOLOGY/PRINCIPAL FINDINGS: To improve our knowledge on the population of phlebotomine sand flies and the potential vectors of canine leishmaniasis, sand flies were collected using sticky traps, light traps and indoor spraying method using pyrethroid insecticides in 16 villages of the rural community of Mont Rolland (Thiès region) between March and July 2005. The 3788 phlebotomine sand flies we collected (2044 males, 1744 females) were distributed among 9 species of which 2 belonged to the genus Phlebotomus: P. duboscqi (vector of cutaneous leishmaniasis in Senegal) and P. rodhaini. The other species belonged to the genus Sergentomyia: S. adleri, S. clydei, S. antennata, S. buxtoni, S. dubia, S. schwetzi and S. magna. The number of individuals and the species composition differed according to the type of trap, suggesting variable, species-related degrees of endophily or exophily. The two species of the genus Phlebotomus were markedly under-represented in comparison to the species of the genus Sergentomyia. This study also shows a heterogeneous spatial distribution within the rural community that could be explained by the different ecosystems and particularly the soil characteristics of this community. Finally, the presence of the S. dubia species appeared to be significantly associated with canine leishmaniasis seroprevalence in dogs. CONCLUSIONS/SIGNIFICANCE: Our data allow us to hypothesize that the species of the genus Sergentomyia and particularly the species S. dubia and S. schwetzi might be capable of transmitting canine leishmaniasis. These results challenge the dogma that leishmaniasis is exclusively transmitted by species of the genus Phlebotomus in the Old World. This hypothesis should be more thoroughly evaluated

Sand fly species caught in the Mont Rolland rural community.

<p>This table presents the nine species of sand flies caught in the Mont Rolland rural community, the number of females and males and their percentage in the whole population.</p><p>*Differently from females, the distinction between males of <i>S. dubia</i> and males of <i>S. antennata</i> was difficult. Therefore we calculated the ratio between <i>S. dubia</i> and <i>S. antennata</i> females (2.19) and then we used the same ratio to estimate the number of males in each of the two species.</p

Sand fly species collected in each type of traps.

<p>The table presents the number of individual of each species (the number of males (M), females (F), total and percentage) collected in each type of trap (sticky traps; CDC light traps; Indoor Spraying).</p

Discriminant analysis showing the relations between sand fly species and the three ecosystems.

<p>Each dot represents one village. Villages were classified in the ecosystem (LG, S and SC) they belong to. Sand fly captures were used to compute the coordinates of the dots (dimensionless units). Confidence ellipses materialized the variability of capture data across ecosystems. The Ndiaye Bopp (NB) village was excluded from this analysis because it is the only village with an intermediate ecosystem between S and SC (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0014773#pone-0014773-g001" target="_blank">Figure 1</a>).</p

Distribution of sand fly species and leishmaniasis seropositive dogs in the rural community of Mont Rolland.

<p>The map shows the rural community of Mont Rolland (the villages are represented by their initials), the distribution of the different species of phlebotomine sand flies in each village and, in between brackets, the number of seropositive dogs out of the total number of tested dogs in each village <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0014773#pone.0014773-Faye1" target="_blank">[7]</a>.</p

Ecosystems, number of traps and number of sand flies in each trap in the different villages.

<p>The table presents the number of phlebotomine sand flies collected in each of the 16 villages:</p><p>Guidieur (G), Khaye Diagal (KaD), Fouloum (Fm), Sambaye Karang (SK), Twin Djassa (TD), Ndiaye Bopp (NB), Loukhouss (L), Pallo Dial (PD), Pallo Youga (PY), Paham Kouye (PK), Kémaye (K), Fouloune (Fne), Keur Daouda (KeD), Colobane Thiombane (CT), Keur Lat Diop (KLD) and Nguith Fall (NF); the different traps used [light traps (CDC), sticky traps (ST) and indoor residual spraying (IRS)]; the number of traps (No.T) and in bracket the number of sand flies caught <b>(</b>No.flies) in each village with that type of trap; the mean number of sand flies/trap (Mean No.flies/T). Eco, Ecosystem; SC, sandy clay soil; S, sandy soil; LG, lateritic gravel soil.</p><p>*The Ndiaye Bopp village presents intermediate ecological features between S and SC.</p

Leishmaniasis prevalence in dogs and sand fly captures.

<p>Odds ratios are computed simultaneously using multiple logistic regression analysis (all species included), <i>P. duboscqi</i> (PD), <i>S. antennata</i>(SA), <i>S. schwetzi</i> (SS), <i>S. dubia</i> (SD), <i>S. magna</i> (SM), <i>S. clydei</i> (SC), <i>S</i>. <i>adleri</i> (SA.1), <i>S. buxtoni</i> (SB), <i>P</i>-values corresponding to likelihood ratio tests. (* ≤5%, ** <1%).</p

Ecosystems and sand fly captures.

<p>Odds ratios are computed by multiple logistic regression analysis (all species included). <i>P. duboscqi</i> (PD), <i>S. antennata</i> (SA), <i>S. schwetzi</i> (SS), <i>S. dubia</i> (SD), <i>S. magna</i> (SM), <i>S. clydei</i> (SC), <i>S</i>. <i>adleri</i> (SA.1), <i>S. buxtoni.</i> The indicated <i>P</i>-values result from likelihood ratio tests. Stars denote the degree of significance (* ≤5%, ** <1%, *** <0.1%).</p

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., 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.PubMedWoSScopu