Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley

Abstract Background Urogenital schistosomiasis, caused by infection with Schistosoma haematobium, is endemic in Niger but complicated by the presence of Schistosoma bovis, Schistosoma curassoni and S. haematobium group hybrids along with various Bulinus snail intermediate host species. Establishing...

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Main Authors: Tom Pennance, Fiona Allan, Aidan Emery, Muriel Rabone, Jo Cable, Amadou Djirmay Garba, Amina Amadou Hamidou, Joanne P. Webster, David Rollinson, Bonnie L. Webster
Format: Article
Language:English
Published: BMC 2020-05-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-020-04136-9
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spelling doaj-33aa1aa9806d4eb9b5edccc3451188b72020-11-25T03:17:53ZengBMCParasites & Vectors1756-33052020-05-0113111510.1186/s13071-020-04136-9Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River ValleyTom Pennance0Fiona Allan1Aidan Emery2Muriel Rabone3Jo Cable4Amadou Djirmay Garba5Amina Amadou Hamidou6Joanne P. Webster7David Rollinson8Bonnie L. Webster9Department of Life Sciences, Natural History MuseumDepartment of Life Sciences, Natural History MuseumDepartment of Life Sciences, Natural History MuseumDepartment of Life Sciences, Natural History MuseumSchool of Biosciences, Cardiff UniversityRéseau International Schistosomoses, Environnement, Aménagement et Lutte (RISEAL-Niger)Réseau International Schistosomoses, Environnement, Aménagement et Lutte (RISEAL-Niger)London Centre for Neglected Tropical Disease Research, Imperial College London, School of Public HealthDepartment of Life Sciences, Natural History MuseumDepartment of Life Sciences, Natural History MuseumAbstract Background Urogenital schistosomiasis, caused by infection with Schistosoma haematobium, is endemic in Niger but complicated by the presence of Schistosoma bovis, Schistosoma curassoni and S. haematobium group hybrids along with various Bulinus snail intermediate host species. Establishing the schistosomes and snails involved in transmission aids disease surveillance whilst providing insights into snail-schistosome interactions/compatibilities and biology. Methods Infected Bulinus spp. were collected from 16 villages north and south of the Niamey region, Niger, between 2011 and 2015. From each Bulinus spp., 20–52 cercariae shed were analysed using microsatellite markers and a subset identified using the mitochondrial (mt) cox1 and nuclear ITS1 + 2 and 18S DNA regions. Infected Bulinus spp. were identified using both morphological and molecular analysis (partial mt cox1 region). Results A total of 87 infected Bulinus from 24 sites were found, 29 were molecularly confirmed as B. truncatus, three as B. forskalii and four as B. globosus. The remaining samples were morphologically identified as B. truncatus (n = 49) and B. forskalii (n = 2). The microsatellite analysis of 1124 cercariae revealed 186 cercarial multilocus genotypes (MLGs). Identical cercarial genotypes were frequently (60%) identified from the same snail (clonal populations from a single miracidia); however, several (40%) of the snails had cercariae of different genotypes (2–10 MLG’s) indicating multiple miracidial infections. Fifty-seven of the B. truncatus and all of the B. forskalii and B. globosus were shedding the Bovid schistosome S. bovis. The other B. truncatus were shedding the human schistosomes, S. haematobium (n = 6) and the S. haematobium group hybrids (n = 13). Two B. truncatus had co-infections with S. haematobium and S. haematobium group hybrids whilst no co-infections with S. bovis were observed. Conclusions This study has advanced our understanding of human and bovid schistosomiasis transmission in the Niger River Valley region. Human Schistosoma species/forms (S. haematobium and S. haematobium hybrids) were found transmitted only in five villages whereas those causing veterinary schistosomiasis (S. bovis), were found in most villages. Bulinus truncatus was most abundant, transmitting all Schistosoma species, while the less abundant B. forskalii and B. globosus, only transmitted S. bovis. Our data suggest that species-specific biological traits may exist in relation to co-infections, snail-schistosome compatibility and intramolluscan schistosome development.http://link.springer.com/article/10.1186/s13071-020-04136-9Schistosoma haematobiumSchistosoma bovisHybridsUrogenital schistosomiasisBulinus globosusBulinus truncatus
collection DOAJ
language English
format Article
sources DOAJ
author Tom Pennance
Fiona Allan
Aidan Emery
Muriel Rabone
Jo Cable
Amadou Djirmay Garba
Amina Amadou Hamidou
Joanne P. Webster
David Rollinson
Bonnie L. Webster
spellingShingle Tom Pennance
Fiona Allan
Aidan Emery
Muriel Rabone
Jo Cable
Amadou Djirmay Garba
Amina Amadou Hamidou
Joanne P. Webster
David Rollinson
Bonnie L. Webster
Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley
Parasites & Vectors
Schistosoma haematobium
Schistosoma bovis
Hybrids
Urogenital schistosomiasis
Bulinus globosus
Bulinus truncatus
author_facet Tom Pennance
Fiona Allan
Aidan Emery
Muriel Rabone
Jo Cable
Amadou Djirmay Garba
Amina Amadou Hamidou
Joanne P. Webster
David Rollinson
Bonnie L. Webster
author_sort Tom Pennance
title Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley
title_short Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley
title_full Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley
title_fullStr Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley
title_full_unstemmed Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley
title_sort interactions between schistosoma haematobium group species and their bulinus spp. intermediate hosts along the niger river valley
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2020-05-01
description Abstract Background Urogenital schistosomiasis, caused by infection with Schistosoma haematobium, is endemic in Niger but complicated by the presence of Schistosoma bovis, Schistosoma curassoni and S. haematobium group hybrids along with various Bulinus snail intermediate host species. Establishing the schistosomes and snails involved in transmission aids disease surveillance whilst providing insights into snail-schistosome interactions/compatibilities and biology. Methods Infected Bulinus spp. were collected from 16 villages north and south of the Niamey region, Niger, between 2011 and 2015. From each Bulinus spp., 20–52 cercariae shed were analysed using microsatellite markers and a subset identified using the mitochondrial (mt) cox1 and nuclear ITS1 + 2 and 18S DNA regions. Infected Bulinus spp. were identified using both morphological and molecular analysis (partial mt cox1 region). Results A total of 87 infected Bulinus from 24 sites were found, 29 were molecularly confirmed as B. truncatus, three as B. forskalii and four as B. globosus. The remaining samples were morphologically identified as B. truncatus (n = 49) and B. forskalii (n = 2). The microsatellite analysis of 1124 cercariae revealed 186 cercarial multilocus genotypes (MLGs). Identical cercarial genotypes were frequently (60%) identified from the same snail (clonal populations from a single miracidia); however, several (40%) of the snails had cercariae of different genotypes (2–10 MLG’s) indicating multiple miracidial infections. Fifty-seven of the B. truncatus and all of the B. forskalii and B. globosus were shedding the Bovid schistosome S. bovis. The other B. truncatus were shedding the human schistosomes, S. haematobium (n = 6) and the S. haematobium group hybrids (n = 13). Two B. truncatus had co-infections with S. haematobium and S. haematobium group hybrids whilst no co-infections with S. bovis were observed. Conclusions This study has advanced our understanding of human and bovid schistosomiasis transmission in the Niger River Valley region. Human Schistosoma species/forms (S. haematobium and S. haematobium hybrids) were found transmitted only in five villages whereas those causing veterinary schistosomiasis (S. bovis), were found in most villages. Bulinus truncatus was most abundant, transmitting all Schistosoma species, while the less abundant B. forskalii and B. globosus, only transmitted S. bovis. Our data suggest that species-specific biological traits may exist in relation to co-infections, snail-schistosome compatibility and intramolluscan schistosome development.
topic Schistosoma haematobium
Schistosoma bovis
Hybrids
Urogenital schistosomiasis
Bulinus globosus
Bulinus truncatus
url http://link.springer.com/article/10.1186/s13071-020-04136-9
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