The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination era

Abstract Background Visceral leishmaniasis (VL), a life-threatening neglected tropical disease, is targeted for elimination from Nepal by the year 2026. The national VL elimination program is still confronted with many challenges including the increasingly widespread distribution of the disease over...

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Main Authors: Lalita Roy, Kristien Cloots, Surendra Uranw, Keshav Rai, Narayan R. Bhattarai, Tom Smekens, Rik Hendrickx, Guy Caljon, Epco Hasker, Murari L. Das, Wim Van Bortel
Format: Article
Language:English
Published: BMC 2023-11-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-023-05986-9
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author Lalita Roy
Kristien Cloots
Surendra Uranw
Keshav Rai
Narayan R. Bhattarai
Tom Smekens
Rik Hendrickx
Guy Caljon
Epco Hasker
Murari L. Das
Wim Van Bortel
author_facet Lalita Roy
Kristien Cloots
Surendra Uranw
Keshav Rai
Narayan R. Bhattarai
Tom Smekens
Rik Hendrickx
Guy Caljon
Epco Hasker
Murari L. Das
Wim Van Bortel
author_sort Lalita Roy
collection DOAJ
description Abstract Background Visceral leishmaniasis (VL), a life-threatening neglected tropical disease, is targeted for elimination from Nepal by the year 2026. The national VL elimination program is still confronted with many challenges including the increasingly widespread distribution of the disease over the country, local resurgence and the questionable efficacy of the key vector control activities. In this study, we assessed the status and risk of Leishmania donovani transmission based on entomological indicators including seasonality, natural Leishmania infection rate and feeding behavior of vector sand flies, Phlebotomus argentipes, in three districts that had received disease control interventions in the past several years in the context of the disease elimination effort. Methods We selected two epidemiologically contrasting settings in each survey district, one village with and one without reported VL cases in recent years. Adult sand flies were collected using CDC light traps and mouth aspirators in each village for 12 consecutive months from July 2017 to June 2018. Leishmania infection was assessed in gravid sand flies targeting the small-subunit ribosomal RNA gene of the parasite (SSU-rRNA) and further sequenced for species identification. A segment (~ 350 bp) of the vertebrate cytochrome b (cytb) gene was amplified from blood-fed P. argentipes from dwellings shared by both humans and cattle and sequenced to identify the preferred host. Results Vector abundance varied among districts and village types and peaks were observed in June, July and September to November. The estimated Leishmania infection rate in vector sand flies was 2.2% (1.1%–3.7% at 95% credible interval) and 0.6% (0.2%–1.3% at 95% credible interval) in VL and non-VL villages respectively. The common source of blood meal was humans in both VL (52.7%) and non-VL (74.2%) villages followed by cattle. Conclusions Our findings highlight the risk of ongoing L. donovani transmission not only in villages with VL cases but also in villages not reporting the presence of the disease over the past several years within the districts having disease elimination efforts, emphasize the remaining threats of VL re-emergence and inform the national program for critical evaluation of disease elimination strategies in Nepal. Graphical Abstract
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spelling doaj.art-e5a34f5dfdb847eea910318fad6141062023-11-12T12:08:08ZengBMCParasites & Vectors1756-33052023-11-0116111110.1186/s13071-023-05986-9The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination eraLalita Roy0Kristien Cloots1Surendra Uranw2Keshav Rai3Narayan R. Bhattarai4Tom Smekens5Rik Hendrickx6Guy Caljon7Epco Hasker8Murari L. Das9Wim Van Bortel10Tropical and Infectious Disease Centre, BP Koirala Institute of Health SciencesDepartment of Public Health, Institute of Tropical MedicineDepartment of Internal Medicine, BP Koirala Institute of Health SciencesDepartment of Microbiology, BP Koirala Institute of Health SciencesDepartment of Microbiology, BP Koirala Institute of Health SciencesDepartment of Public Health, Institute of Tropical MedicineDepartment of Biomedical Sciences, University of Antwerp, AntwerpDepartment of Biomedical Sciences, University of Antwerp, AntwerpDepartment of Public Health, Institute of Tropical MedicineDepartment of Microbiology, BP Koirala Institute of Health SciencesDepartment of Biomedical Sciences and Outbreak Research Team, Institute of Tropical MedicineAbstract Background Visceral leishmaniasis (VL), a life-threatening neglected tropical disease, is targeted for elimination from Nepal by the year 2026. The national VL elimination program is still confronted with many challenges including the increasingly widespread distribution of the disease over the country, local resurgence and the questionable efficacy of the key vector control activities. In this study, we assessed the status and risk of Leishmania donovani transmission based on entomological indicators including seasonality, natural Leishmania infection rate and feeding behavior of vector sand flies, Phlebotomus argentipes, in three districts that had received disease control interventions in the past several years in the context of the disease elimination effort. Methods We selected two epidemiologically contrasting settings in each survey district, one village with and one without reported VL cases in recent years. Adult sand flies were collected using CDC light traps and mouth aspirators in each village for 12 consecutive months from July 2017 to June 2018. Leishmania infection was assessed in gravid sand flies targeting the small-subunit ribosomal RNA gene of the parasite (SSU-rRNA) and further sequenced for species identification. A segment (~ 350 bp) of the vertebrate cytochrome b (cytb) gene was amplified from blood-fed P. argentipes from dwellings shared by both humans and cattle and sequenced to identify the preferred host. Results Vector abundance varied among districts and village types and peaks were observed in June, July and September to November. The estimated Leishmania infection rate in vector sand flies was 2.2% (1.1%–3.7% at 95% credible interval) and 0.6% (0.2%–1.3% at 95% credible interval) in VL and non-VL villages respectively. The common source of blood meal was humans in both VL (52.7%) and non-VL (74.2%) villages followed by cattle. Conclusions Our findings highlight the risk of ongoing L. donovani transmission not only in villages with VL cases but also in villages not reporting the presence of the disease over the past several years within the districts having disease elimination efforts, emphasize the remaining threats of VL re-emergence and inform the national program for critical evaluation of disease elimination strategies in Nepal. Graphical Abstracthttps://doi.org/10.1186/s13071-023-05986-9Visceral leishmaniasisVectorPhlebotomus argentipesSeasonalityLeishmania donovani transmissionInfection rate
spellingShingle Lalita Roy
Kristien Cloots
Surendra Uranw
Keshav Rai
Narayan R. Bhattarai
Tom Smekens
Rik Hendrickx
Guy Caljon
Epco Hasker
Murari L. Das
Wim Van Bortel
The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination era
Parasites & Vectors
Visceral leishmaniasis
Vector
Phlebotomus argentipes
Seasonality
Leishmania donovani transmission
Infection rate
title The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination era
title_full The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination era
title_fullStr The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination era
title_full_unstemmed The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination era
title_short The ongoing risk of Leishmania donovani transmission in eastern Nepal: an entomological investigation during the elimination era
title_sort ongoing risk of leishmania donovani transmission in eastern nepal an entomological investigation during the elimination era
topic Visceral leishmaniasis
Vector
Phlebotomus argentipes
Seasonality
Leishmania donovani transmission
Infection rate
url https://doi.org/10.1186/s13071-023-05986-9
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