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      Transmission and diversity of Schistosoma haematobium and S. bovis and their freshwater intermediate snail hosts Bulinus globosus and B. nasutus in the Zanzibar Archipelago, United Republic of Tanzania

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          Abstract

          Background

          The Zanzibar Archipelago (Pemba and Unguja islands) is targeted for the elimination of human urogenital schistosomiasis caused by infection with Schistosoma haematobium where the intermediate snail host is Bulinus globosus. Following multiple studies, it has remained unclear if B. nasutus (a snail species that occupies geographically distinct regions on the Archipelago) is involved in S. haematobium transmission on Zanzibar. Additionally, S. haematobium was thought to be the only Schistosoma species present on the Zanzibar Archipelago until the sympatric transmission of S. bovis, a parasite of ruminants, was recently identified. Here we re-assess the epidemiology of schistosomiasis on Pemba and Unguja together with the role and genetic diversity of the Bulinus spp. involved in transmission.

          Methodology/Principal findings

          Malacological and parasitological surveys were conducted between 2016 and 2019. In total, 11,116 Bulinus spp. snails were collected from 65 of 112 freshwater bodies surveyed. Bulinus species identification were determined using mitochondrial cox1 sequences for a representative subset of collected Bulinus (n = 504) and together with archived museum specimens (n = 6), 433 B. globosus and 77 B. nasutus were identified. Phylogenetic analysis of cox1 haplotypes revealed three distinct populations of B. globosus, two with an overlapping distribution on Pemba and one on Unguja. For B. nasutus, only a single clade with matching haplotypes was observed across the islands and included reference sequences from Kenya. Schistosoma haematobium cercariae (n = 158) were identified from 12 infected B. globosus and one B. nasutus collected between 2016 and 2019 in Pemba, and cercariae originating from 69 Bulinus spp. archived in museum collections. Schistosoma bovis cercariae (n = 21) were identified from seven additional B. globosus collected between 2016 and 2019 in Pemba. By analysing a partial mitochondrial cox1 region and the nuclear ITS (1–5.8S-2) rDNA region of Schistosoma cercariae, we identified 18 S. haematobium and three S. bovis haplotypes representing populations associated with mainland Africa and the Indian Ocean Islands (Zanzibar, Madagascar, Mauritius and Mafia).

          Conclusions/Significance

          The individual B. nasutus on Pemba infected with S. haematobium demonstrates that B. nasutus could also play a role in the local transmission of S. haematobium. We provide preliminary evidence that intraspecific variability of S. haematobium on Pemba may increase the transmission potential of S. haematobium locally due to the expanded intermediate host range, and that the presence of S. bovis complicates the environmental surveillance of schistosome infections.

          Author summary

          Schistosomiasis is a snail-borne neglected tropical disease caused by parasitic blood flukes of the genus Schistosoma. Human urogenital schistosomiasis is targeted for elimination on the Zanzibar Archipelago, United Republic of Tanzania, with multiple interventions being implemented to curtail transmission of the parasite to humans on the islands since 2012. Environmental surveillance for schistosomiasis transmission by collecting intermediate host snails, checking snails for Schistosoma infection, and preserving collected snails and Schistosoma parasites offers the possibility for molecular analyses to investigate the evolutionary/genetic relationships of both snails and parasites. Schistosome transmission on Zanzibar was believed to involve a single schistosome species ( Schistosoma haematobium) transmitted via a single intermediate host species ( Bulinus globosus). However, our findings demonstrate the locally established presence of S. bovis, responsible for bovine intestinal schistosomiasis, and an extended intermediate host compatibility of S. haematobium with the snail B. nasutus on Pemba. Increased parasite diversity and intermediate host species compatibility may increase the transmission of Schistosoma species on Zanzibar and stretch resources for public health interventions with the need for Schistosoma species specific surveillance.

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: Project administration
                Role: InvestigationRole: Project administration
                Role: InvestigationRole: Project administration
                Role: Funding acquisitionRole: Project administrationRole: Supervision
                Role: Funding acquisitionRole: Project administrationRole: Supervision
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                5 July 2022
                July 2022
                : 16
                : 7
                : e0010585
                Affiliations
                [1 ] Department of Science, Natural History Museum, London, United Kingdom
                [2 ] School of Biosciences, Cardiff University, Cardiff, United Kingdom
                [3 ] London Centre for Neglected Tropical Disease Research, London, United Kingdom
                [4 ] Department of Basic Medical Sciences, College of Osteopathic Medicine of the Pacific–Northwest, Western University of Health Sciences, Lebanon, Oregon, United States of America
                [5 ] Public Health Laboratory-Ivo de Carneri, Pemba, United Republic of Tanzania
                [6 ] Neglected Diseases Program, Ministry of Health Zanzibar, United Republic of Tanzania
                [7 ] The Scottish Oceans Institute, Gatty Marine Laboratory, University of St Andrews, East Sands, St Andrews, United Kingdom
                [8 ] Swiss Tropical and Public Health Institute, Allschwil, Switzerland
                [9 ] University of Basel, Basel, Switzerland
                University of Oxford, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0003-4898-462X
                Article
                PNTD-D-21-01740
                10.1371/journal.pntd.0010585
                9286283
                35788199
                392b47e2-09c0-44d4-9d9b-8837dcaae273
                © 2022 Pennance et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 December 2021
                : 14 June 2022
                Page count
                Figures: 4, Tables: 1, Pages: 21
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 207728
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000270, Natural Environment Research Council;
                Award ID: NE/L002434/1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;
                Award ID: 50816
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 104958/Z/14/Z
                Award Recipient :
                The study was partially funded by a Wellcome Trust Seed Award ( https://wellcome.org) grant number 207728 (awarded to BLW). TP was funded by the NERC GW4+ DTP ( https://www.nercgw4plus.ac.uk) and the Natural Environmental Research Council ( https://www.nerc.com), number NE/L002434/1. Data and samples from the ZEST project were also used in the current study, ZEST was funded by the University of Georgia Research Foundation Inc., which is funded by the Bill & Melinda Gates Foundation (https://www. gatesfoundation.org/) for the Schistosomiasis Consortium for Operational Research and Evaluation (SCORE; https://score.uga.edu/) projects (prime award no. 50816, subaward no. RR374-053/4893206 to DR). FA, AE and MR were funded by the Wellcome Trust ( https://wellcome.org), for the SCAN: Schistosomiasis Collection at the Natural History Museum, grant number 104958/Z/14/Z, in which many of the ZEST samples were accessioned. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Schistosoma
                Schistosoma Haematobium
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Helminths
                Schistosoma
                Schistosoma Haematobium
                Biology and Life Sciences
                Genetics
                Heredity
                Genetic Mapping
                Haplotypes
                People and Places
                Geographical Locations
                Africa
                Tanzania
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Helminths
                Schistosoma
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Helminths
                Schistosoma
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Islands
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Molting
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Helminth Infections
                Schistosomiasis
                Medicine and Health Sciences
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Schistosomiasis
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Fresh Water
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Fresh Water
                Custom metadata
                vor-update-to-uncorrected-proof
                2022-07-15
                All DNA sequence files are available from the GenBank database (accession numbers MT380520-MT380560). All other relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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