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

Abstract

Background: From 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.

Methods: From 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.

Results: In 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).

Conclusions: The 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.

Keywords: Cutaneous leishmaniasis; Dogs; Phlebotomine sand fly; Rural area.

Fig. 1

Location of the three indigenous villages (V1, Guarda; V2, Santana; and V3, Afetos) studied herein. Pesqueira, Pernambuco, Brazil. Copyright: Creative Commons Attribution-ShareAlike 3.0 Licence (https://creativecommons.org/licenses/by-sa/3.0/). The map was created using QGIS and publicly available shapefiles from QGIS web site [55]

Fig. 2

Species accumulation curve (Mao’s tau function) (red line) and 95% confidence interval (blue lines) for sand flies in Pesqueira, Pernambuco, Brazil

Fig. 3

Monthly relative frequency of sand flies (number of individuals per hour of trapping) collected indoors (a and b) and outdoors (c and d) according to species (a and c Migonemyia migonei; b and d remaining species), Pesqueira, Pernambuco, Brazil

Fig. 4

Monthly relative frequency of sand flies (number of individuals per hour of trapping) collected in Pesqueira, Pernambuco, Brazil (a the five most common species; b the remaining species)

Fig. 5

Monthly relative frequency of sand flies (number of individuals per hour of trapping) in relation to rainfall (a) and temperature (b) in Pesqueira, Pernambuco, Brazil