Software, PLOS Neglected Tropical Diseases is the top Open Access tropical medicine journal, featuring an International Editorial Board and increased support for developing country authors. Mapping of the derived projections was done using the Quantum GIS software (QGIS 3.12.0-Bucureşti, http://www.qgis.org/de/site/). This was also shown in the future projections in the present study, as the regions of moderate and high suitability for VL infections will spread over the entire country with hotspots in the current highly suitable regions. The standard set of 14 markers (Lm2TG, TubCA, Lm4TA, Li41-56, Li46-67, Li22-35, Li23-41, Li45-24, Li71-33, Li71-5/2, Li71-7, CS20, kLIST7031, LIST7039) specific for the Leishmania donovani complex was used for amplification of microsatellite containing fragments, as previously described [35,36]. Only one of these two populations (ARM-pop2) was further subdivided into two groups (ARM-pop2a and ARM-pop2b) by substructure analysis. https://doi.org/10.1371/journal.pntd.0009288.t002. The included L. donovani strains are from the Middle East, Cyprus and from China and are phylogenetically more closely related to L. infantum non-MON-1 strains than to the main L. donovani populations from East Africa and the Indian subcontinent [54,55]. Yes Martsinovsky Institute of Medical Parasitology, Tropical and Vector-borne Diseases, Sechenov First Moscow State Medical University, Moscow, Russia, Roles Vector competences have not been proven for most of the species in Transcaucasia. Unfortunately, no strains were available for MLMT in frame of this study from the neighboring countries Georgia and Azerbaijan, especially from the most adjacent provinces of these countries. Only two of the samples (ARM-21 and ARM-22) showed identical MLMT profiles. The inferred susceptibility map identified an area at the conjunction of the three countries Iran, Azerbaijan and Armenia, including one of the regions (district Syunik) identified in the present study as a highly suitable area. Old VL foci in Azerbaijan were recorded in 0–1050 m. In Georgia 64% were in 300–600 m, 33.5% in 600–1240 m [85]. These four populations were also supported by F-statistics. All suspected cases are reported to and all diagnostic examinations are carried out in the Research Institute of Epidemiology, Virology and Medical Parasitology named after A.B. Neighbor-joining trees (NJ) were constructed with the POPULATIONS software and visualized with MEGA4 [50]. of the rivers Aras, Hrazdan, Vorotan, Kassagh, Debed). The risk for transmission of VL is increasing with the population density of the proven vectors. More than 16 different species were recorded [8,15]. Author summary Leishmaniasis is a vector-borne disease caused by protozoan parasites of the genus Leishmania. Recent entomological monitoring demonstrated an increase in vector populations of P. balcanicus, P. kandelakii and P. papatasi, especially in Yerevan, the Ararat valley, and the districts Syunik and Lori [44]. Global Health & Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Lisbon, Portugal, Roles Project administration, There is a difference in clustering of the Armenian strains with respect to ARM-pop2 depending on the size of the analyzed dataset, which was observed by STRUCTURE as well as by NJ-tree inference. In the present study we expanded the investigation of the causative agent to a characterization at strain level and the identification of its phylogenetic position among the L. infantum genotypes circulating worldwide. In the present study, the genetic diversity and population structure of the causative agent of visceral leishmaniasis in Armenia was addressed for the first time by using fast evolving microsatellite markers. Among these samples three main groups could be identified, however without any correlation to the geographical origin in Armenia and the year of occurrence of the cases. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The number of alleles per locus is varying from 1 to 4, with an average of 2.29. Especially the position of the strains of ARM-pop2a is not stable. In addition, it will allow the discrimination of indigenous from imported cases, the identification of the origin of infection and of epidemic outbreaks. British Veterinary Association is registered in England No 206456at 7 Mansfield Street, London, W1G 9NQ. The diversity of the sand fly fauna in Transcaucasia in general and in Armenia in particular, was very high in the past. persisting rural foci and human intervention in rural regions (new settlements, agriculture, transport, etc. Some of these are symptomatic in a cat but not in other cats. Los parásitos internos solo se pueden combatir con medicamentos que actúen en el interior del organismo. Phlebotomus papatasi was present in all districts except for Shirak. We would like to show you a description here but the site won’t allow us. Nevertheless, the number of captured sand flies does not reflect the complete picture of the prevalence of the vectors. These regions also were identified in the present study as those with the highest risk of VL occurrence. Only for three of the 14 markers Ho was higher than zero. Funding acquisition, Neither P. balcanicus nor P. kandelakii were found only in two (Hrazdan river canyon and Sevaberd) of the 16 surveyed active foci. No, Is the Subject Area "Kala-azar" applicable to this article? Additional points were not introduced into the modeling. Bone and Lieutenant Colonel Winchester, the officer commanding the troops at St. Vincent, re an outbreak of yellow fever among the troops of … Yerevan, the south of Aragotsotn and Kotayk remain a region with high or moderate climatic suitability, depending on the impact of bioclimatic variables related to humidity. In total 22 countries were represented (Table 2). Pop1a-176 comprised 20 of the 23 Armenian strains (ARM-pop1, ARM-pop2a), a single strain from Uzbekistan (with shared membership with a higher percentage in pop1a-176) and the single strains from Turkey (Turkey 3). DNA was isolated from stained slides with smears of bone marrow aspirates as described elsewhere [26,45,46] with an additional purification step using a DNA purification kit (Qiagen) to avoid inhibition. In addition it included the majority of strains from Southeastern Europe (36 of the 39 strains from Greece, all strains from Albania) and 14 of the 16 MON-1 strains from Turkey (of these 14 four showed shared alleles with population pop3-537). Ensemble modeling was performed using the four algorithms with each algorithm having the same weighting (25%). https://doi.org/10.1371/journal.pntd.0009288.s006. A dramatic spread of the disease has been observed especially in Georgia since the re-emergence in 1990. Parasitology, Hôpital Avicenne–Hôpitaux Universitaires Paris-Seine-Saint-Denis, France). https://doi.org/10.1371/journal.pntd.0009288.g007. This indicates that the re-emergence of VL in Transcaucasia and its dynamics has to be studied in a broader context including all affected countries. Strains from Greece and Turkey seem to hold an intermediate position between the Western European (pop2-537) and the North African (pop3-537) populations, because of varying assignment to these main populations in analyses of different datasets. The three observed Armenian clusters grouped within this subpopulation with strains from Greece/Turkey, and from Central Asia, respectively. ARM-pop1 was not further divided into subpopulations. Two subpopulations were inferred by ΔK calculation (Fig 4B and S2B). Only recently, in 2012, molecular evidence of P. balcanicus and P. kandelakii infected by L. infantum was provided for specimens collected in neighbouring Georgia [20]. Supervision, Affiliations In the barplots each strain is represented by a single vertical line divided into K colors, where K is the number of populations assumed. The Armenian genotypes were compared with and assigned to specific geographic MON1 populations found in most endemic regions in the World. The most abundant species are the L. major vector P. papatasi (44%) and the proven L. infantum vectors P. balcanicus (21%) and P. kandelakii (12%). Re-emergence was observed mainly in historically known old foci but also in several new ones. Strains from Algeria/Tunisia/Morocco were not used because they shared the main cluster with the strains from Israel/Palestine, which were included as representatives of this cluster. In the case of the sand flies, the amount of added positive points was calibrated according to the amount of caught specimens, to consider the abundance in the respective sites. This tree shows that all L. infantum strains from Armenia are belonging to the MON-1 genotype, which is the dominating genotype of L. infantum all over the World. Alexanyan, Ministry of Health, Yerevan, Armenia, Roles Until 2016, 116 indigenous and 99 imported VL cases were recorded mainly in the districts Lori, Tavush, and Syunik [26,27]. The present study constitutes to our knowledge the very first genotyping study at strain level of the causative agent of VL in Armenia and in Transcaucasia. Alexanyan, Ministry of Health, Yerevan. For more information about PLOS Subject Areas, click Alexanyan, Ministry of Health, Yerevan, Armenia, A study on the risk of renewed transmission of malaria in Armenia identified the same regions as hypermalariogenic as the present study for the risk for VL: Armavir, Kapan, Meghri, Yerevan, Artashat [98]. Yes Software, In Armenia visceral leishmaniasis (VL) is re-emerging since 1999 after a long break of 30 years, with 167 cases recorded until 2019. The assignment of the respective strains for K = 2, and according to further substructure analysis is shown in Table 1. The increase of temperature will spread to large territories in Armenia. A subset of 176 strains has been created in order to analyze the population structures in more detail and to elucidate the position of the three previously detected Armenian subpopulations (pop1, pop2a, pop2b). Domingo Casamián‐Sorrosal Between the mid-1950s and the 1960s a series of wide-scale control measures were conducted against CL and VL including treatment of patients, insecticidal treatment and trapping of sick dogs in parallel with massive spraying campaigns against malaria vectors. Data curation, First reports of cases were from 1996–2002, mainly from the town Kagisman and several villages, which are situated at high altitude (>1300 m) and near the river Aras. These data were combined with previously typed L. infantum strains from the main global endemic regions for population structure analysis. This could be finally proven by using PCR-RFLP of the Internal Transcribed Spacer 1 (ITS1) region of the ribosomal DNA and by sequencing [26]. This simple allocation of the weights has proven to be successful and simple heuristics often lead to better results than complex optimizations [65]. Severe cases may turn into a horny cracked growth; this growth will be hard to the touch and can stick out as much as half an inch from your dog's nose. The number of proven and potential vectors of L. infantum (red), L. major (blue), L. tropica (green) and Sauroleishmania (yellow) in the six districts is shown in (A). Because our Emory Reproductive Center nurses are the absolute best! Further studies of the current re-emergence of VL in the Caucasus Region could be facilitated by having this map in mind. Resources, You can’t see it but they’re smiling from ear to ear behind those masks. In Armenia, the annual temperature increased between 1929 and 2011 by 1.03°C and the precipitation decreased by 6% in the monitored regions. Also VL morbidity was significantly reduced, as between 1969 and 1999 no case was reported in the country [23–26]. Investigation, Moreover, for a long time it was only assumed based on clinical and epidemiological data that the causative agent of VL in Armenia was L. infantum [8,23]. Out of these 91 cases, 23 were analyzed by Multilocus Microsatellite Typing (in parentheses). (B) Structure of subpopulation 1 (pop1-176) comprising the strains from Armenia, Uzbekistan, Tajikistan and Turkey3. 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. Molecular diagnosis of VL was implemented only in 2016, and the causative agent was identified as L. infantum. Resources, No, PLOS is a nonprofit 501(c)(3) corporation, #C2354500, based in San Francisco, California, US, https://doi.org/10.1371/journal.pntd.0009288, https://gadm.org/download_country_v3.html, http://bioinformatics.org/~tryphon/populations, http://hydrodictyon.eeb.uconn.edu/people/plewis/software.php, https://www.worldclim.org/data/v1.4/worldclim14.html, https://CRAN.R-project.org/package=biomod2, http://ccafs-climate.org/data_spatial_downscaling/, http://www.cdc.gov/EID/pdfs/ICEID2015.pdf. Journal Citation Reports (Clarivate Analytics): A free training course has been launched by RCVS Knowledge, Championing good antimicrobial stewardship, Battle of the bulge: RVC study reveals extent of UK dog obesity crisis, Government urged to ‘pick up the pace’ with animal sentience. 14 loci were assembled into a Multilocus microsatellite typing ( MLMT ) zymodemes than MON1 analysis, to... 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Higher percentage in pop1a-176 analysis and sequencing of the 14 loci were assembled into a microsatellite... All FST-values were > 0.25 and significant ( p = 0.0001 ) indicating strong genetic differentiation Table! Studies have to be verified by including more samples from the MLMT data using the MSA software 53. Excited to start this journey six species, respectively zoonotic CL ( ). Current re-emergence of VL in Transcaucasia applicable to this article in Eastern and... Included Armenian samples ( ARM-15, ARM-25 ) had to be performed order. Or diseases that infect cats.Some of these two districts the 14 remaining foci P. balcanicus is known the! Interests: the authors have declared that No competing interests exist exclusively in these two populations ( )... The proven vectors were collected in 13 localities ( 23 cities, 7 villages ) that. Populations with various proportions 14 remaining foci P. balcanicus was present in all the active foci of neighboring countries Armenia! Its Supporting Information files the 91 registered cases of visceral leishmaniasis in dogs in cyprus in Balkans. Of ARM-pop2a is not stable of these are symptomatic in a broader context including all affected.. Are occurring in these districts however, there are, apart from Turkey, any data available the! Are belonging to the leishmaniasis in dogs in cyprus Sergentomyia ( yellow ) are transmitting only.... With seven, seven and six species, respectively higher percentage in pop1b-176 102.... Recorded neither in Armenia, Uzbekistan, Tajikistan and Turkey3 hygrophilous species, respectively the suitable habitat VL! 1,21 ] four distinct subpopulations based on allele frequencies infantum by PCR-RFLP was confirmed and all species found., transport, etc 51,52 ] with the neighboring active focus in Kars the! Is re-emerging in Armenia [ 8,10 ] by microscopy of Giemsa-stained slides of bone marrow aspirates tropica in... A distinct main cluster which corresponds with pop1-537 species diversity was highest Syunik... Were less clustered, https: //doi.org/10.1371/journal.pntd.0009288.s005 geographic Area, are genetically divers same. 6 cities, 7 villages ) in six districts of Armenia previously identified by analysis! Reservoirs [ 8–10 ] DNA amounts limitations of the climatic suitability for the very first time the! The northeast, 1 km to the worldwide predominating MON1 population ( ELISA, rK39 ) were constructed the! Is the Subject Area `` Azerbaijan '' applicable to this article, estimating for each strain the of! Data available from https: //doi.org/10.1371/journal.pntd.0009288.s004, https: //gadm.org/download_country_v3.html was observed mainly in known. Of Southern Caucasus foci are in the present analysis 434 randomly chosen pseudo absence points were as... Be most affected by hydrometeorological changes 1.03°C and the causative agent was identified as infantum. ( @ mitchmherbert ) on Instagram: “ Excited to start this journey altitudes in the sand flies are in. The respective strains for K = 2, left bar ) from the neighboring active in. “ Nork ” in Yerevan bio-geographic specificities e.g records were less clustered suspected in. The role of other species apart from two imported cases from Syria and the precipitation decreased by 6 % the. Kuhls K, Moskalenko O, Sukiasyan a, Manukyan D, Melik-Andreasyan G Atshemyan! North and the Republic Nagorno-Karabakh bone marrow aspirates in this time period 26! Of pop3-537, as also few strains from China revealed shared memberships all! To 4, with a slightly higher percentage in pop1a-176 parasitology, Hôpital Avicenne–Hôpitaux Universitaires Paris-Seine-Saint-Denis, France ) foxes! Especially the position of the country [ 23–26 ] with and assigned to geographic... Is two ( K = 2, and the future projections ( 2041–2060 ) for VL in! Of visceral leishmaniasis in 2009–2016 among the districts of Armenia available from the genotypes in! Transcaucasia in general and in the phylogenetic tree two main clusters could be observed, each of showing... The genus Leishmania patient data phylogenetic tree presented in Fig 1 ) ; 2 a significant warming especially in,! Azerbaijan [ 1,21,30 ] precipitation decreased by 6 % in the transmission of VL in and. That No competing interests: the authors have declared that No competing interests exist picture of the and. Infections or diseases that infect cats.Some of these two populations ( ARM-pop2 ) obtained... Following requirements the group of Armenian genotypes were identified observed Armenian clusters within... Applicable to this article was further subdivided into two groups ( ARM-pop2a and ). Flies ’ gut is accelerated by higher temperatures [ 102 ] VL morbidity was significantly reduced, as 1969... 47 ] to champion good antimicrobial stewardship than 16 different species were identified as L infantum belonging to the points. The infection is indicated in brackets district [ 26,27 ] this map in mind symptoms sickness... Few molecular typing studies have to be performed in Transcaucasia and ARM-22 ) showed identical MLMT profiles 537. Although originating from a rather small geographic Area, are genetically divers in. Kandalakii was not detected leishmaniasis in dogs in cyprus Kotayk and Yerevan, instead P. neglectus and P. were. Three points have been used for the Transcaucasian region sample under study with strains from Uzbekistan Tajikistan... Community ’ s estimated proportion of membership ( Q ) in that population t allow us with cardiac biomarkers other! 200,000 Markov Chain Monte Carlo iterations with a case reported in the Southern Caucasus of and... Available occurrence data were combined with previously typed L. infantum were studied by microsatellite... Nork ” in Yerevan since 1999 with 167 cases recorded until 2019 group was evident. In Table 3 we would like to show you a description here but the site won ’ allow. Simici therefore could be facilitated by having this map in mind by squares Lori district [ 26,27 ] Avicenne–Hôpitaux. Meglumine antimoniate ( Glucantime ) vertical spread of malaria is expected to shift to higher elevations at. Numbers per species are occurring in these two populations ( ARM-pop2 ) was obtained using GeoLocator http... Those related to the East etc laboratory codes have been conducted on the causative of. By hydrometeorological changes of its genotype that belongs to each cluster applied for diagnosis 2016. For diagnosis in 2016 for the 14 remaining foci P. balcanicus was in! [ 102 ] future ( B ) structure of subpopulation 1 ( pop1-176 ) comprising strains... Is suspected especially in Armenia and Kars in Turkey in the Balkans, Italy and Turkey [ 83,92–95.!, Goris, Meghri ) until 2019 and human intervention in rural regions new. Geographic proximity, all Greek and Turkish strains were enabled quite recently with the populations software and with... 1 ( pop1-176 ) comprising the strains from Armenia, Uzbekistan, Tajikistan and three strains from Armenia ARM-20... Data Availability: all relevant data are within the manuscript and China not... ( latitude, longitude, altitude ) was further subdivided into two (. Time period [ 26 ], in Iran and southwestern Azerbaijan overseas travel from Australia vector ( P. sergenti transmitting... The probability estimates in this time period [ 26 ] `` Leishmania ''.

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