Cargando…

Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites

BACKGROUND: Human schistosomiasis is the second most important tropical disease and occurs in two forms in Africa (intestinal and urogenital) caused by the digenetic trematodes Schistosoma mansoni and Schistosoma haematobium, respectively. A proposed recent shift of schistosomiasis above a previousl...

Descripción completa

Detalles Bibliográficos
Autores principales: Tumwebaze, Immaculate, Clewing, Catharina, Dusabe, Marie Claire, Tumusiime, Julius, Kagoro-Rugunda, Grace, Hammoud, Cyril, Albrecht, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6882369/
https://www.ncbi.nlm.nih.gov/pubmed/31775865
http://dx.doi.org/10.1186/s13071-019-3811-2
_version_ 1783474145678327808
author Tumwebaze, Immaculate
Clewing, Catharina
Dusabe, Marie Claire
Tumusiime, Julius
Kagoro-Rugunda, Grace
Hammoud, Cyril
Albrecht, Christian
author_facet Tumwebaze, Immaculate
Clewing, Catharina
Dusabe, Marie Claire
Tumusiime, Julius
Kagoro-Rugunda, Grace
Hammoud, Cyril
Albrecht, Christian
author_sort Tumwebaze, Immaculate
collection PubMed
description BACKGROUND: Human schistosomiasis is the second most important tropical disease and occurs in two forms in Africa (intestinal and urogenital) caused by the digenetic trematodes Schistosoma mansoni and Schistosoma haematobium, respectively. A proposed recent shift of schistosomiasis above a previously established altitudinal threshold of 1400 m above sea level in western Ugandan crater lakes has triggered more research interest there. METHODS: Based on extensive field sampling in western Uganda and beyond and employing an approach using sequences of the mitochondrial barcoding gene cytochrome c oxidase subunit 1 (cox1) this study aims were: (i) identification and establishment of the phylogenetic affinities of Bulinus species as potential hosts for Schistosoma spp.; (ii) determining diversity, frequency and distribution patterns of Bulinus spp.; and (iii) establishing genetic variability and phylogeographical patterns using Bayesian inference and parsimony network analyses. RESULTS: Out of the 58 crater lakes surveyed, three species of Bulinus snails were found in 34 crater lakes. Bulinus tropicus was dominating, Bulinus forskalii was found in two lakes and Bulinus truncatus in one. The latter two species are unconfirmed potential hosts for S. haematobium in this region. However, Bulinus tropicus is an important species for schistosomiasis transmission in ruminants. Bulinus tropicus comprised 31 haplotypes while both B. forskalii and B. truncatus exhibited only a single haplotype in the crater lakes. All species clustered with most of the haplotypes from surrounding lake systems forming source regions for the colonization of the crater lakes. CONCLUSIONS: This first detailed malacological study of the crater lakes systems in western Uganda revealed presence of Bulinus species that are either not known or not regionally known to be hosts for S. haematobium, the causing agent of human urogenital schistosomiasis. Though this disease risk is almost negligible, the observed dominance of B. tropicus in the crater lakes shows that there is a likelihood of a high risk of infections with Schistosoma bovis. Thus, extra attention should be accorded to safeguard wild and domestic ruminants in this region as the population benefits from these animals.
format Online
Article
Text
id pubmed-6882369
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-68823692019-12-03 Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites Tumwebaze, Immaculate Clewing, Catharina Dusabe, Marie Claire Tumusiime, Julius Kagoro-Rugunda, Grace Hammoud, Cyril Albrecht, Christian Parasit Vectors Research BACKGROUND: Human schistosomiasis is the second most important tropical disease and occurs in two forms in Africa (intestinal and urogenital) caused by the digenetic trematodes Schistosoma mansoni and Schistosoma haematobium, respectively. A proposed recent shift of schistosomiasis above a previously established altitudinal threshold of 1400 m above sea level in western Ugandan crater lakes has triggered more research interest there. METHODS: Based on extensive field sampling in western Uganda and beyond and employing an approach using sequences of the mitochondrial barcoding gene cytochrome c oxidase subunit 1 (cox1) this study aims were: (i) identification and establishment of the phylogenetic affinities of Bulinus species as potential hosts for Schistosoma spp.; (ii) determining diversity, frequency and distribution patterns of Bulinus spp.; and (iii) establishing genetic variability and phylogeographical patterns using Bayesian inference and parsimony network analyses. RESULTS: Out of the 58 crater lakes surveyed, three species of Bulinus snails were found in 34 crater lakes. Bulinus tropicus was dominating, Bulinus forskalii was found in two lakes and Bulinus truncatus in one. The latter two species are unconfirmed potential hosts for S. haematobium in this region. However, Bulinus tropicus is an important species for schistosomiasis transmission in ruminants. Bulinus tropicus comprised 31 haplotypes while both B. forskalii and B. truncatus exhibited only a single haplotype in the crater lakes. All species clustered with most of the haplotypes from surrounding lake systems forming source regions for the colonization of the crater lakes. CONCLUSIONS: This first detailed malacological study of the crater lakes systems in western Uganda revealed presence of Bulinus species that are either not known or not regionally known to be hosts for S. haematobium, the causing agent of human urogenital schistosomiasis. Though this disease risk is almost negligible, the observed dominance of B. tropicus in the crater lakes shows that there is a likelihood of a high risk of infections with Schistosoma bovis. Thus, extra attention should be accorded to safeguard wild and domestic ruminants in this region as the population benefits from these animals. BioMed Central 2019-11-27 /pmc/articles/PMC6882369/ /pubmed/31775865 http://dx.doi.org/10.1186/s13071-019-3811-2 Text en © The Author(s) 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Tumwebaze, Immaculate
Clewing, Catharina
Dusabe, Marie Claire
Tumusiime, Julius
Kagoro-Rugunda, Grace
Hammoud, Cyril
Albrecht, Christian
Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites
title Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites
title_full Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites
title_fullStr Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites
title_full_unstemmed Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites
title_short Molecular identification of Bulinus spp. intermediate host snails of Schistosoma spp. in crater lakes of western Uganda with implications for the transmission of the Schistosoma haematobium group parasites
title_sort molecular identification of bulinus spp. intermediate host snails of schistosoma spp. in crater lakes of western uganda with implications for the transmission of the schistosoma haematobium group parasites
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6882369/
https://www.ncbi.nlm.nih.gov/pubmed/31775865
http://dx.doi.org/10.1186/s13071-019-3811-2
work_keys_str_mv AT tumwebazeimmaculate molecularidentificationofbulinussppintermediatehostsnailsofschistosomasppincraterlakesofwesternugandawithimplicationsforthetransmissionoftheschistosomahaematobiumgroupparasites
AT clewingcatharina molecularidentificationofbulinussppintermediatehostsnailsofschistosomasppincraterlakesofwesternugandawithimplicationsforthetransmissionoftheschistosomahaematobiumgroupparasites
AT dusabemarieclaire molecularidentificationofbulinussppintermediatehostsnailsofschistosomasppincraterlakesofwesternugandawithimplicationsforthetransmissionoftheschistosomahaematobiumgroupparasites
AT tumusiimejulius molecularidentificationofbulinussppintermediatehostsnailsofschistosomasppincraterlakesofwesternugandawithimplicationsforthetransmissionoftheschistosomahaematobiumgroupparasites
AT kagororugundagrace molecularidentificationofbulinussppintermediatehostsnailsofschistosomasppincraterlakesofwesternugandawithimplicationsforthetransmissionoftheschistosomahaematobiumgroupparasites
AT hammoudcyril molecularidentificationofbulinussppintermediatehostsnailsofschistosomasppincraterlakesofwesternugandawithimplicationsforthetransmissionoftheschistosomahaematobiumgroupparasites
AT albrechtchristian molecularidentificationofbulinussppintermediatehostsnailsofschistosomasppincraterlakesofwesternugandawithimplicationsforthetransmissionoftheschistosomahaematobiumgroupparasites