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Schistosoma Haematobium Group Species and Their Bulinus Spp

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Schistosoma Haematobium Group Species and Their Bulinus Spp Pennance et al. Parasites Vectors (2020) 13:268 https://doi.org/10.1186/s13071-020-04136-9 Parasites & Vectors RESEARCH Open Access Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley Tom Pennance1,2,3* , Fiona Allan1,3, Aidan Emery1,3, Muriel Rabone1,3, Jo Cable2, Amadou Djirmay Garba4,5, Amina Amadou Hamidou4, Joanne P. Webster3,6, David Rollinson1,3 and Bonnie L. Webster1,3* 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 identifed using the mitochondrial (mt) cox1 and nuclear ITS1 2 and 18S DNA regions. Infected Bulinus spp. were identifed 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 confrmed as B. truncatus, three as B. forskalii and four as B. globosus. The remaining samples were morphologically identifed 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%) identifed from the same snail (clonal populations from a single miracidia); however, several (40%) of the snails had cercariae of diferent 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 fve 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 *Correspondence: [email protected]; [email protected] 1 Department of Life Sciences, Natural History Museum, Cromwell Road, South Kensington, London SW7 5BD, UK Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Pennance et al. Parasites Vectors (2020) 13:268 Page 2 of 15 and B. globosus, only transmitted S. bovis. Our data suggest that species-specifc biological traits may exist in relation to co-infections, snail-schistosome compatibility and intramolluscan schistosome development. Keywords: Schistosoma haematobium, Schistosoma bovis, Hybrids, Urogenital schistosomiasis, Bulinus globosus, Bulinus truncatus, Bulinus forskalii, Cercariae, Niger, Molecular identifcation Background Health Organisation as critical actions necessary for Schistosomiasis is a snail-borne neglected tropical dis- reaching the goal of eliminating schistosomiasis as a ease (NTD) associated with poverty, poor sanitation and public health problem by 2030 [19]. lack of safe water [1, 2]. An estimated 180–200 million Of the estimated 3–4 million people at risk of human people are infected, primarily from tropical low and mid- schistosomiasis in Niger, the majority of the disease is dle-income countries [3]. Schistosomes are diverse, with urogenital, caused by Schistosoma haematobium (includ- 25 species currently recognised within the genus Schisto- ing S. haematobium group hybrids), with transmission soma, and exhibit preferences for both their intermediate relying on freshwater Bulinus spp. snails [20, 21]. Tere snail and mammalian hosts, both of which governs their is also a relatively unknown burden of veterinary schis- distribution. In sub-Saharan Africa, there are four species tosomiasis caused by the schistosomes Schistosoma bovis that cause human schistosomiasis, whilst there are many and Schistosoma curassoni, and also S. bovis-curassoni more that infect livestock and/or wildlife [4]. hybrids [22–24], all of which are transmitted by Bulinus Schistosomes can be identifed by species-specifc phe- spp. [22, 23, 25]. Additionally, the occurrence of S. hae- notypic characteristics, particularly associated with the matobium group hybrids, involving a mixture of human adult worms and their eggs. Additionally, epidemiological and veterinary schistosome species (S. haematobium-S. and ecological characteristics, such as geographical region bovis, S. haematobium-S. curassoni, S. haematobium- and intermediate snail and defnitive mammalian host S. bovis-S. curassoni) have been reported from humans associations, are used as proxies for species identifca- in Niger [10, 24, 26], and are reported in other African tion at a given focus [5]. Supported by new feld collection countries [9, 11, 27–31]. Tis complicates transmission and sample preservation methods [6, 7], molecular data and epidemiology, while raising many questions regard- from schistosome collections have revealed new species ing the general biology of both snail and mammalian host distributions [8], interspecies hybridisation [9–12], and specifcities of these closely related schistosome species. unexpected host associations [13], all of which highlight Our current understanding of S. haematobium and S. the need to incorporate molecular analyses into disease bovis interactions with the intermediate hosts in Niger surveillance. Molecular data are particularly pertinent for is based on morphological identifcations (cercariae and free-living schistosome cercarial larvae, which have lim- their snail host), cercarial emergence patterns, and exper- ited species-specifc morphologies [14] and also for schis- imental infections. Regarding the intermediate hosts of tosomes that overlap in their snail intermediate host use. human schistosomiasis, Bulinus senegalensis, Bulinus Aside from schistosomes, snail host identifcation can forskalii and Bulinus truncatus have previously been pose complications as it often relies on species-specifc reported to transmit S. haematobium [32–36] while Buli- morphological characteristics, including shell charac- nus umbilicatus and B. senegalensis have been reported teristics, morphology of reproductive organs and chro- as shedding the veterinary schistosomes, S. curassoni and mosome counts [15]. However, morphologically similar S. bovis, respectively [25, 34]. However, molecular data snails can be very difcult to identify, with phenotypic are needed to support these predominantly morphologi- plasticity, including overlap in shell morphology poten- cal observations for both snail and schistosome, provid- tially confounding accurate identifcations [16]. Molec- ing a more accurate assessment of snail-schistosome ular analyses provide greater accuracy and also enable relations and epidemiology [10, 32]. interrelationship, phylogenetic and population diver- Using a combination of methods, this study investi- sity analyses [17]. Moreover, precise snail identifca- gates the snail-schistosome relationships of S. haemato- tions are needed to determine the true hosts involved in bium group species and their Bulinus snail hosts along Schistosoma spp. transmission. Tis is vital for mapping the Niger River Valley to: (i) identify the Bulinus species and monitoring disease transmission and determining involved in schistosomiasis transmission in the Niamey infection risk to human and livestock populations sur- region of Niger; (ii) identify the schistosome species rounding snail habitats [18], which in addition will also being transmitted by specifc Bulinus spp. in these areas; aid in determining suitable localities for targeted snail and (iii) investigate schistosome single- and multiple spe- control, both of these points being listed
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