Microsatellite based molecular epidemiology of Leishmania infantum from re-emerging foci of visceral leishmaniasis in Armenia and pilot risk assessment by ecological niche modeling.

Katrin Kuhls,Anja Jaeschke,Hripsime Apresyan,Gayane Melik-Andreasyan,Marcus Frohme,Ara Keshishyan,Anna Sukiasyan,Margarita Strelkova,Ralf Wieland,Liana Atshemyan,Sofia Cortes,Olga Moskalenko,Dezdemonia Manukyan

doi:10.1371/journal.pntd.0009288

Abstract

BackgroundVisceral leishmaniasis (VL) is re-emerging in Armenia since 1999 with 167 cases recorded until 2019. The objectives of this study were (i) to determine for the first time the genetic diversity and population structure of the causative agent of VL in Armenia; (ii) to compare these genotypes with those from most endemic regions worldwide; (iii) to monitor the diversity of vectors in Armenia; (iv) to predict the distribution of the vectors and VL in time and space by ecological niche modeling.Methodology/Principal findingsHuman samples from different parts of Armenia previously identified by ITS-1-RFLP as L. infantum were studied by Multilocus Microsatellite Typing (MLMT). These data were combined with previously typed L. infantum strains from the main global endemic regions for population structure analysis. Within the 23 Armenian L. infantum strains 22 different genotypes were identified. The combined analysis revealed that all strains belong to the worldwide predominating MON1-population, however most closely related to a subpopulation from Southeastern Europe, Maghreb, Middle East and Central Asia. The three observed Armenian clusters grouped within this subpopulation with strains from Greece/Turkey, and from Central Asia, respectively. Ecological niche modeling based on VL cases and collected proven vectors (P. balcanicus, P. kandelakii) identified Yerevan and districts Lori, Tavush, Syunik, Armavir, Ararat bordering Georgia, Turkey, Iran and Azerbaijan as most suitable for the vectors and with the highest risk for VL transmission. Due to climate change the suitable habitat for VL transmission will expand in future all over Armenia.ConclusionsGenetic diversity and population structure of the causative agent of VL in Armenia were addressed for the first time. Further genotyping studies should be performed with samples from infected humans, animals and sand flies from all active foci including the neighboring countries to understand transmission cycles, re-emergence, spread, and epidemiology of VL in Armenia and the entire Transcaucasus enabling epidemiological monitoring.

Highlights

Leishmaniasis, a vector-borne disease caused by obligatory intracellular protozoan parasites of the genus Leishmania, is endemic in about 98 countries of the World [1]
Genetic diversity and population structure of the causative agent of visceral leishmaniasis (VL) in Armenia were addressed for the first time
Further genotyping studies should be performed with samples from infected humans, animals and sand flies from all active foci including the neighboring countries to understand transmission cycles, re-emergence, spread, and epidemiology of VL in Armenia and the entire Transcaucasus enabling epidemiological monitoring

Summary

Introduction

Leishmaniasis, a vector-borne disease caused by obligatory intracellular protozoan parasites of the genus Leishmania, is endemic in about 98 countries of the World [1]. There are about 18 species of sand flies in Armenia occurring in different frequencies as reported by different authors (S1 Table) [8,11,12,13,14,15,16] Of these only P. kandelakii and P. balcanicus were considered as the most likely vectors for VL in the Caucasus region based on their wide distribution, the presence in places with VL cases, and their ability to feed on humans and dogs [8,17,18,19]. In 2012, molecular evidence of P. balcanicus and P. kandelakii infected by L. infantum was provided for specimens collected in neighbouring Georgia [20] Apart from these two species, P. tobbi, P. neglectus, P. transcaucasicus and P. perfilievi (all subgenus Larroussius), as well as P. brevis and P. simici (both subgenus Adlerius) were considered to transmit VL in the Southern Caucasus [21,22]. The objectives of this study were (i) to determine for the first time the genetic diversity and population structure of the causative agent of VL in Armenia; (ii) to compare these genotypes with those from most endemic regions worldwide; (iii) to monitor the diversity of vectors in Armenia; (iv) to predict the distribution of the vectors and VL in time and space by ecological niche modeling

Objectives

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Results

Conclusion