One piece of the puzzle: Modeling vector presence and environment reveals seasonality, distribution, and prevalence of sandflies and Leishmania in an expansion area

Abstract

The recent geographic spread of Leishmania infantum along the borders of Argentina, Brazil and Paraguay has been highlighted. In our previous study, Lutzomyia longipalpis was found in 55 of 123 patches surveyed, and in some patches, sandflies were found at higher densities, forming hotspots. Based on the One Health approach, we investigated the seasonality of the vector, the presence of parasite DNA, and the environmental factors that contribute to vector and parasite dispersal in these previously described hotspots in Foz do Iguaçu, Brazil. Entomological surveys were conducted monthly for one year. Fourteen hotspots peridomicile and six intradomicile were sampled. PCR was used to assess the prevalence of Leishmania DNA in sandflies. Zero-inflated negative binomial regression was used to determine the association of micro- and mesoscale environmental variables with the occurrence and abundance of the three most abundant sandfly species sampled. A total of 3543 species were captured, with Lutzomyia longipalpis being the predominant species (71.78%) of the 13 species found. Evandromyia edwardsi, Expapillata firmatoi, Micropygomyia ferreirana and Pintomyia christenseni were reported for the first time in the region. NDVI, distance to water, precipitation, west-to-east wind, wind speed, maximum and minimum relative humidity, and sex were significant variables associated with vector presence/abundance in the environment. Vector presence/abundance in the peridomicile was associated with precipitation, altitude, maximum temperature, minimum and maximum relative humidity, west-to-east wind, wind speed, and sex. Leishmania DNA was detected in an average of 21% of Lu. longipalpis throughout the year. Vector abundance is concentrated in urban and peri-urban areas, with some specimens present in different parts of the city and some sites with high vector abundance. This distribution suggests that the risk of actual contact between humans and parasite vectors in urban areas during the epidemic period is associated with patches of peri-urban vegetation and then extends into urban areas.

Keywords: Dispersion; Environment; Epidemiology; Leishmaniasis; Modeling; Psychodidae.

Graphical abstract

Fig. 1

Hotspots surveyed for sandflies and infection by Leishmania. Blue dots represent peridomicile sampling, red and blue dots represent peridomicile and intradomicile sampling. Unit A: 415 (−25°30.430/−54°35.177), 421 (−54°35.177/−54°35.241), 448 (−25°31.240/−54°32.563) and 470 (−25°31.057/−54°31.547). Unit B: 458 (−25°31.091/−54°32.563), 463 (−25°31.057/−54°31.547), and 551 (−25°32.233/−54°33.119). Unit C: 27 (−25°26.433/−54°34.389), 264 (−25°28.511/−54°30.292), 329 (−25°29.175/−54°32.174), and 321 (−25°29.321/−54°34.117). Unit D: 597 (−25°33.178/−54°34.374), 613 (−25°33.598/−54°35.055) and 616 (−25°34.139/−54°34.538). The maps were made using the ArcGIS® PRO software developed by Esri. Map data ©OpenStreetMap, scale 1:90,000. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Correlation matrix for the environmental variables measured in the intradomicile (A) and peridomicile (B) traps used in this study. Colors represents positive (blue) and negative (red) correlations, and white represents the absence of correlation. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

Environmental parameters and seasonal density of sand flies captured for one year from November 2014 to October 2015 in Foz do Iguaçu, Paraná, Brazil. The left side shows the comparison of climatic and surface cover parameters (A) Temperature, (B) Humidity, (C) Cumulative rainfall, and (D) Surface cover – Normalized Difference Vegetation Index (NDVI) and Normalized Difference Water Index (NDWI). The right side shows the total number of sandflies collected per species, sex, and capture site – intra- and peridomicile, (E) Total specimens, (F) Lutzomyia longipalpis, (G) Nyssomyia whitmani, (H) Nyssomyia neivai.