Home sweet home: sand flies find a refuge in remote indigenous villages in north-eastern Brazil, where leishmaniasis is endemic

Abstract

BackgroundFrom 2012 to 2013, an outbreak of cutaneous leishmaniasis by Leishmania braziliensis was detected in indigenous villages located in a remote rural area of Pernambuco state, north-eastern Brazil. Considering that the principal activities of this indigenous community are farming and crop plantation, and also that the outbreak involved many children, we investigated the presence of sand fly vectors inside human houses and also the exposure of dogs to leishmanial parasites. Our general objective was to gather epidemiological data that could indicate the occurrence of a peri-domestic/domestic transmission cycle of L. braziliensis in these indigenous villages.MethodsFrom March 2015 to March 2016, sand flies were collected using light traps in the indoor and immediate outdoor environments in the three indigenous villages that reported the most cutaneous leishmaniasis cases during the 2012–2013 outbreak. Moreover, samples obtained from 300 dogs living in the outbreak villages and two nearby villages were tested by a rapid immunochromatographic test and by a real-time PCR for detecting anti-Leishmania antibodies and Leishmania DNA, respectively.ResultsIn total, 5640 sand flies belonging to 11 species were identified. Males (n = 3540) predominated over females (n = 2100). Migonemyia migonei (84.3%) was the most abundant species, followed by Evandromyia lenti (5.5%), Lutzomyia longipalpis (4.1%), Nyssomyia intermedia (1.6%) and Micropygomyia capixaba (1.4%), representing together ~97% of the sand flies collected. Nine out of the 11 species identified in this study were found indoors, including M. migonei, L. longipalpis and N. intermedia, which are proven vectors of Leishmania spp. Out of 300 dogs tested, 26 (8.7%) presented anti-Leishmania antibodies and six (2%) were Leishmania DNA-positive. The level of exposure in dogs living in the indigenous villages where the 2012–2013 outbreak of human CL was detected was almost 2-fold higher than in the two nearby villages (11.0 vs 6.2% for serology and 2.6 vs 1.4% for real-time PCR).ConclusionsThe results suggest that different sand fly vectors may be adapted to human dwellings, thus increasing the risk of transmission in the indoor and immediate outdoor environments. The adaptation of sand flies to the indoor environment in the studied indigenous villages may be partly explained by the poor housing conditions and the proximity of the houses to crop plantations and forest fragments.Electronic supplementary materialThe online version of this article (10.1186/s13071-019-3383-1) contains supplementary material, which is available to authorized users.

Fast multiplex real-time PCR assay for simultaneous detection of dog and human blood and Leishmania parasites in sand flies

“…While our multiplex real-time PCR assay was tested with sand flies collected from a CL focus, it is also suitable for other epidemiological settings, namely VL endemic regions, considering that the primers and probe used also efficiently detected L. infantum kDNA [18,19]. The identification of humans as the most frequent host of M. migonei females in this study, also reinforces their high attractiveness for humans [34] as well as the hypothesis that this species may be adapted to feed indoors [22]. It has been shown that human CL patients that have been treated and clinically cured may harbour viable parasites in their scars [36] and it has been suggested that they could eventually act as a source of infection to sand flies [37].…”

“…Interestingly, eight out of 44 females fed on humans were also positive for Leishmania spp. Leishmania-positive sand flies were collected in human dwellings (four indoors and eight outdoors), where human cases of CL by L. braziliensis were previously recorded [22]. Altogether, these findings strongly suggest that M. migonei is a vector of L. braziliensis for humans in the indigenous villages, where sand flies were collected.…”

“…A total of 97 engorged female sand flies collected in the context of a previous study [22] were tested individually by the newly developed multiplex real-time PCR. These females belonged to two species: M. migonei (n = 95); and Nyssomyia intermedia (n = 2).…”

“…These females belonged to two species: M. migonei (n = 95); and Nyssomyia intermedia (n = 2). Details regarding sand fly collection, identification and processing are described elsewhere [22]. Females were collected both indoors (n = 23) and outdoors (n = 74).…”

Sandflies in an endemic area for Visceral Leishmaniasis in Northeastern Brazil

“…Over the last few years, great efforts have been made through the Brazilian national health system to control the spreading of leishmaniasis. Nonetheless, in some areas, the numbers of cases have increased, and outbreaks have been described in regions where the disease had been considered absent (SALES et al, 2019). This spreading has been related to degradation of natural habitats that may force sandflies to adapt to the modified environment (ANTONINI et al, 2017).…”