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Keywords = Schistosoma bovis

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16 pages, 2771 KiB  
Review
Livestock Reservoir Hosts: An Obscured Threat to Control of Human Schistosomiasis in Nigeria
by Hammed Oladeji Mogaji, Olaitan Olamide Omitola, Adedotun Ayodeji Bayegun, Uwem Friday Ekpo and Andrew W. Taylor-Robinson
Zoonotic Dis. 2023, 3(1), 52-67; https://doi.org/10.3390/zoonoticdis3010006 - 17 Feb 2023
Cited by 7 | Viewed by 6202
Abstract
Schistosomiasis is one of the leading neglected tropical diseases in sub-Saharan Africa. Recorded case numbers of this chronic and debilitating helminth disease indicate Nigeria to be the most endemic country within this region. National control efforts have focused intensively on restricting human contact [...] Read more.
Schistosomiasis is one of the leading neglected tropical diseases in sub-Saharan Africa. Recorded case numbers of this chronic and debilitating helminth disease indicate Nigeria to be the most endemic country within this region. National control efforts have focused intensively on restricting human contact with freshwater sources of intermediate host snails. However, limited attention has been paid to the role of livestock as reservoir hosts and the prevalence of transmission of schistosomes to humans via farmed animals. The West African nations of Mali, Senegal, and the neighbouring Niger, Benin, and Cameroon have all reported the hybridization of the closely related species of Schistosoma haematobium, which infects humans, and S. bovis, which infects cattle. As these countries share the Niger and Benue rivers, with their tributaries, there is a distinct possibility of aquatic snails infected with hybrid schistosomes migrating to become established in the Nigerian river system. Here, we report on the current state of research in Nigeria that aims to elucidate key aspects of zoonotic schistosomiasis epidemiology. Factors promoting the hybridization of Schistosoma species are highlighted, and how available control measures can be optimized to address the emergence of schistosome hybrids is discussed. Full article
(This article belongs to the Special Issue Feature Papers of Zoonotic Diseases 2021–2022)
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14 pages, 1696 KiB  
Article
Prevalence and Molecular Identification of Schistosoma haematobium among Children in Lusaka and Siavonga Districts, Zambia
by Rabecca Tembo, Walter Muleya, John Yabe, Henson Kainga, King S. Nalubamba, Mildred Zulu, Florence Mwaba, Shereen Ahmed Saad, Moses Kamwela, Andrew N. Mukubesa, Ngula Monde, Simegnew Adugna Kallu, Natalia Mbewe and Andrew M. Phiri
Trop. Med. Infect. Dis. 2022, 7(9), 239; https://doi.org/10.3390/tropicalmed7090239 - 10 Sep 2022
Cited by 5 | Viewed by 4818
Abstract
Schistosomiasis remains a public health concern in Zambia. Urinary schistosomiasis caused by Schistosoma haematobium is the most widely distributed infection. The aim of the current study was to determine the prevalence and risk factors of urinary schistosomiasis and identify the strain of S. [...] Read more.
Schistosomiasis remains a public health concern in Zambia. Urinary schistosomiasis caused by Schistosoma haematobium is the most widely distributed infection. The aim of the current study was to determine the prevalence and risk factors of urinary schistosomiasis and identify the strain of S. haematobium among children in the Siavonga and Lusaka districts in Zambia. Urine samples were collected from 421 primary school children and S. haematobium eggs were examined under light microscopy. A semi-structured questionnaire was used to obtain information on the socio-demographic characteristics and the potential risk factors for urinary schistosomiasis. DNA of the parasite eggs was extracted from urine samples and the internal transcribed spacer gene was amplified, sequenced and phylogenetically analysed. The overall prevalence of S. haematobium was 9.7% (41/421) (95% CI: 7.16–13.08), male participants made up 6.2% (26/232) (95% CI: 4.15–9.03), having a higher burden of disease than female participants who made up 3.5% (15/421) (95% CI: 2.01–5.94). The age group of 11–15 years had the highest overall prevalence of 8.3% (35/421) (5.94–11.48). Participants that did not go fishing were 0.008 times less likely to be positive for schistosomiasis while participants whose urine was blood-tinged or cloudy on physical examination and those that lived close to water bodies were 9.98 and 11.66 times more likely to test positive for schistosomiasis, respectively. A phylogenetic tree analysis indicated that S. haematobium isolates were closely related to pure S. haematobium from Zimbabwe and hybrids of S. haematobium × S. bovis from Benin, Senegal and Malawi. The current study shows that urinary schistosomiasis is endemic in the study areas and is associated with water contact, and S. haematobium isolated is closely related to hybrids of S. bovis × S. haematobium strain, indicating the zoonotic potential of this parasite. Full article
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10 pages, 302 KiB  
Article
Mating Interactions between Schistosoma bovis and S. mansoni and Compatibility of Their F1 Progeny with Biomphalaria glabrata and Bulinus truncatus
by Amos Mathias Onyekwere, Alejandra De Elias-Escribano, Julien Kincaid-Smith, Sarah Dametto, Jean-François Allienne, Anne Rognon, Maria Dolores Bargues and Jérôme Boissier
Microorganisms 2022, 10(6), 1251; https://doi.org/10.3390/microorganisms10061251 - 19 Jun 2022
Cited by 4 | Viewed by 3592
Abstract
Contrary to the majority of other Trematoda, Schistosoma species are gonochoric. Consequently, in endemic areas where several schistosome species overlap and can co-infect the same definitive host, there may be frequent opportunities for interspecific pairing. Our experimental study provides novel insight on the [...] Read more.
Contrary to the majority of other Trematoda, Schistosoma species are gonochoric. Consequently, in endemic areas where several schistosome species overlap and can co-infect the same definitive host, there may be frequent opportunities for interspecific pairing. Our experimental study provides novel insight on the pairing behavior between Schistosoma bovis and S. mansoni in mixed infections in mice. We used six mate choice experiments to assess mating interactions between the two schistosome species. We show that mating between the two Schistosoma species is not random and that S. mansoni exhibits greater mate recognition compared to S. bovis. We also performed reciprocal crosses (male S. mansoni × female S. bovis) and (female S. mansoni × male S. bovis) that produce active swimming miracidia. These miracidia were genotyped by ITS2 sequencing and proposed for mollusc infection. Molecular analyses show that all the miracidia are parthenogenetically produced (i.e., their harbor the mother ITS2 genotype) and as a consequence can only infect the mollusc of the maternal species. Offspring produced by male S. mansoni × female S. bovis pairing can only infect Bulinus truncatus whereas offspring produced by female S. mansoni × male S. bovis can only infect Biomphalaria glabrata snails. Evolutionary and epidemiological consequences are discussed. Full article
(This article belongs to the Section Parasitology)
15 pages, 7421 KiB  
Article
Population Genetic Structure and Hybridization of Schistosoma haematobium in Nigeria
by Amos Mathias Onyekwere, Olivier Rey, Jean-François Allienne, Monday Chukwu Nwanchor, Moses Alo, Clementina Uwa and Jerome Boissier
Pathogens 2022, 11(4), 425; https://doi.org/10.3390/pathogens11040425 - 31 Mar 2022
Cited by 21 | Viewed by 3646
Abstract
Background: Schistosomiasis is a major poverty-related disease caused by dioecious parasitic flatworms of the genus Schistosoma with a health impact on both humans and animals. Hybrids of human urogenital schistosome and bovine intestinal schistosome have been reported in humans in several of Nigeria’s [...] Read more.
Background: Schistosomiasis is a major poverty-related disease caused by dioecious parasitic flatworms of the genus Schistosoma with a health impact on both humans and animals. Hybrids of human urogenital schistosome and bovine intestinal schistosome have been reported in humans in several of Nigeria’s neighboring West African countries. No empirical studies have been carried out on the genomic diversity of Schistosoma haematobium in Nigeria. Here, we present novel data on the presence and prevalence of hybrids and the population genetic structure of S. haematobium. Methods: 165 Schistosoma-positive urine samples were obtained from 12 sampling sites in Nigeria. Schistosoma haematobium eggs from each sample were hatched and each individual miracidium was picked and preserved in Whatman® FTA cards for genomic analysis. Approximately 1364 parasites were molecularly characterized by rapid diagnostic multiplex polymerase chain reaction (RD-PCR) for mitochondrial DNA gene (Cox1 mtDNA) and a subset of 1136 miracidia were genotyped using a panel of 18 microsatellite markers. Results: No significant difference was observed in the population genetic diversity (p > 0.05), though a significant difference was observed in the allelic richness of the sites except sites 7, 8, and 9 (p < 0.05). Moreover, we observed two clusters of populations: west (populations 1–4) and east (populations 7–12). Of the 1364 miracidia genotyped, 1212 (89%) showed an S. bovis Cox1 profile and 152 (11%) showed an S. haematobium cox1 profile. All parasites showed an S. bovis Cox1 profile except for some at sites 3 and 4. Schistosoma miracidia full genotyping showed 59.3% of the S. bovis ITS2 allele. Conclusions: This study provides novel insight into hybridization and population genetic structure of S. haematobium in Nigeria. Our findings suggest that S. haematobium x S. bovis hybrids are common in Nigeria. More genomic studies on both human- and animal-infecting parasites are needed to ascertain the role of animals in schistosome transmission. Full article
(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)
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21 pages, 6735 KiB  
Article
Engineering a Pseudo-26-kDa Schistosoma Glutathione Transferase from bovis/haematobium for Structure, Kinetics, and Ligandin Studies
by Neo Padi, Blessing Oluebube Akumadu, Olga Faerch, Chinyere Aloke, Vanessa Meyer and Ikechukwu Achilonu
Biomolecules 2021, 11(12), 1844; https://doi.org/10.3390/biom11121844 - 7 Dec 2021
Cited by 11 | Viewed by 3335
Abstract
Glutathione transferases (GSTs) are the main detoxification enzymes in schistosomes. These parasitic enzymes tend to be upregulated during drug treatment, with Schistosoma haematobium being one of the species that mainly affect humans. There is a lack of complete sequence information on the closely [...] Read more.
Glutathione transferases (GSTs) are the main detoxification enzymes in schistosomes. These parasitic enzymes tend to be upregulated during drug treatment, with Schistosoma haematobium being one of the species that mainly affect humans. There is a lack of complete sequence information on the closely related bovis and haematobium 26-kDa GST isoforms in any database. Consequently, we engineered a pseudo-26-kDa S. bovis/haematobium GST (Sbh26GST) to understand structure–function relations and ligandin activity towards selected potential ligands. Sbh26GST was overexpressed in Escherichia coli as an MBP-fusion protein, purified to homogeneity and catalyzed 1-chloro-2,4-dinitrobenzene-glutathione (CDNB-GSH) conjugation activity, with a specific activity of 13 μmol/min/mg. This activity decreased by ~95% in the presence of bromosulfophthalein (BSP), which showed an IC50 of 27 µM. Additionally, enzyme kinetics revealed that BSP acts as a non-competitive inhibitor relative to GSH. Spectroscopic studies affirmed that Sbh26GST adopts the canonical GST structure, which is predominantly α-helical. Further extrinsic 8-anilino-1-naphthalenesulfonate (ANS) spectroscopy illustrated that BSP, praziquantel (PZQ), and artemisinin (ART) might preferentially bind at the dimer interface or in proximity to the hydrophobic substrate-binding site of the enzyme. The Sbh26GST-BSP interaction is both enthalpically and entropically driven, with a stoichiometry of one BSP molecule per Sbh26GST dimer. Enzyme stability appeared enhanced in the presence of BSP and GSH. Induced fit ligand docking affirmed the spectroscopic, thermodynamic, and molecular modelling results. In conclusion, BSP is a potent inhibitor of Sbh26GST and could potentially be rationalized as a treatment for schistosomiasis. Full article
(This article belongs to the Section Biomacromolecules: Proteins, Nucleic Acids and Carbohydrates)
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18 pages, 1255 KiB  
Article
Hybridized Zoonotic Schistosoma Infections Result in Hybridized Morbidity Profiles: A Clinical Morbidity Study amongst Co-Infected Human Populations of Senegal
by Cheikh B. Fall, Sébastien Lambert, Elsa Léger, Lucy Yasenev, Amadou Djirmay Garba, Samba D. Diop, Anna Borlase, Stefano Catalano, Babacar Faye, Martin Walker, Mariama Sene and Joanne P. Webster
Microorganisms 2021, 9(8), 1776; https://doi.org/10.3390/microorganisms9081776 - 20 Aug 2021
Cited by 17 | Viewed by 3921
Abstract
Hybridization of infectious agents is a major emerging public and veterinary health concern at the interface of evolution, epidemiology, and control. Whilst evidence of the extent of hybridization amongst parasites is increasing, their impact on morbidity remains largely unknown. This may be predicted [...] Read more.
Hybridization of infectious agents is a major emerging public and veterinary health concern at the interface of evolution, epidemiology, and control. Whilst evidence of the extent of hybridization amongst parasites is increasing, their impact on morbidity remains largely unknown. This may be predicted to be particularly pertinent where parasites of animals with contrasting pathogenicity viably hybridize with human parasites. Recent research has revealed that viable zoonotic hybrids between human urogenital Schistosoma haematobium with intestinal Schistosoma species of livestock, notably Schistosoma bovis, can be highly prevalent across Africa and beyond. Examining human populations in Senegal, we found increased hepatic but decreased urogenital morbidity, and reduced improvement following treatment with praziquantel, in those infected with zoonotic hybrids compared to non-hybrids. Our results have implications for effective monitoring and evaluation of control programmes, and demonstrate for the first time the potential impact of parasite hybridizations on host morbidity. Full article
(This article belongs to the Special Issue Schistosoma and Schistosomiasis)
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19 pages, 3539 KiB  
Review
Natural Intra- and Interclade Human Hybrid Schistosomes in Africa with Considerations on Prevention through Vaccination
by Ursula Panzner and Jerome Boissier
Microorganisms 2021, 9(7), 1465; https://doi.org/10.3390/microorganisms9071465 - 8 Jul 2021
Cited by 21 | Viewed by 4947
Abstract
Causal agents of schistosomiasis are dioecious, digenean schistosomes affecting mankind in 76 countries. Preventive measures are manifold but need to be complemented by vaccination for long-term protection; vaccine candidates in advanced pre-clinical/clinical stages include Sm14, Sm-TSP-2/Sm-TSP-2Al®, Smp80/SchistoShield®, and Sh28GST/Bilhvax [...] Read more.
Causal agents of schistosomiasis are dioecious, digenean schistosomes affecting mankind in 76 countries. Preventive measures are manifold but need to be complemented by vaccination for long-term protection; vaccine candidates in advanced pre-clinical/clinical stages include Sm14, Sm-TSP-2/Sm-TSP-2Al®, Smp80/SchistoShield®, and Sh28GST/Bilhvax®. Natural and anthropogenic changes impact on breaking species isolation barriers favoring introgressive hybridization, i.e., allelic exchange among gene pools of sympatric, interbreeding species leading to instant large genetic diversity. Phylogenetic distance matters, thus the less species differ phylogenetically the more likely they hybridize. PubMed and Embase databases were searched for publications limited to hybridale confirmation by mitochondrial cytochrome c oxidase (COX) and/or nuclear ribosomal internal transcribed spacer (ITS). Human schistosomal hybrids are predominantly reported from West Africa with clustering in the Senegal River Basin, and scattering to Europe, Central and Eastern Africa. Noteworthy is the dominance of Schistosoma haematobium interbreeding with human and veterinary species leading due to hybrid vigor to extinction and homogenization as seen for S. guineensis in Cameroon and S. haematobium in Niger, respectively. Heterosis seems to advantage S. haematobium/S. bovis interbreeds with dominant S. haematobium-ITS/S. bovis-COX1 profile to spread from West to East Africa and reoccur in France. S. haematobium/S. mansoni interactions seen among Senegalese and Côte d’Ivoirian children are unexpected due to their high phylogenetic distance. Detecting pure S. bovis and S. bovis/S. curassoni crosses capable of infecting humans observed in Corsica and Côte d’Ivoire, and Niger, respectively, is worrisome. Taken together, species hybridization urges control and preventive measures targeting human and veterinary sectors in line with the One-Health concept to be complemented by vaccination protecting against transmission, infection, and disease recurrence. Functional and structural diversity of naturally occurring human schistosomal hybrids may impact current vaccine candidates requiring further research including natural history studies in endemic areas targeted for clinical trials. Full article
(This article belongs to the Special Issue Schistosoma and Schistosomiasis)
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11 pages, 7599 KiB  
Article
Bulinus senegalensis and Bulinus umbilicatus Snail Infestations by the Schistosoma haematobium Group in Niakhar, Senegal
by Papa Mouhamadou Gaye, Souleymane Doucoure, Bruno Senghor, Babacar Faye, Ndiaw Goumballa, Mbacké Sembène, Coralie L’Ollivier, Philippe Parola, Stéphane Ranque, Doudou Sow and Cheikh Sokhna
Pathogens 2021, 10(7), 860; https://doi.org/10.3390/pathogens10070860 - 8 Jul 2021
Cited by 9 | Viewed by 3738
Abstract
Thorough knowledge of the dynamics of Bulinus spp. infestation could help to control the spread of schistosomiasis. This study describes the spatio-temporal dynamics of B. senegalensis and B. umbilicatus infestation by the Schistosoma haematobium group of blood flukes in Niakhar, Senegal. Molecular identification [...] Read more.
Thorough knowledge of the dynamics of Bulinus spp. infestation could help to control the spread of schistosomiasis. This study describes the spatio-temporal dynamics of B. senegalensis and B. umbilicatus infestation by the Schistosoma haematobium group of blood flukes in Niakhar, Senegal. Molecular identification of the S. haematobium group was performed by real-time PCR, targeting the Dra 1 gene in 810 samples of Bulinus spp. collected during the schistosomiasis transmission season in 2013. In addition to Dra 1 PCR, a rapid diagnostic-PCR was performed on a sub-group of 43 snails to discriminate S. haematobium, S. bovis, and S. mattheei. Out of 810 snails, 236 (29.1%) were positive for Dra 1 based on the PCR, including 96.2% and 3.8% of B. senegalensis and B. umbilicatus, respectively. Among the sub-group, 16 samples were confirmed to be S. haematobium while one was identified as a mixture of S. haematobium and S. bovis. Snails infestations were detected in all villages sampled and infestation rates ranged from 15.38% to 42.11%. The prevalence of infestation was higher in the north (33.47%) compared to the south (25.74%). Snail populations infestations appear early in the rainy season, with a peak in the middle of the season, and then a decline towards the end of the rainy season. Molecular techniques showed, for the first time, the presence of S. bovis in the Bulinus spp. population of Niakhar. The heterogeneity of snail infestations at the village level must be taken into account in mass treatment strategies. Further studies should help to improve the characterizations of the schistosome population. Full article
(This article belongs to the Special Issue Schistosomiasis: Host-Pathogen Biology)
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13 pages, 1594 KiB  
Article
Application of a Genus-Specific LAMP Assay for Schistosome Species to Detect Schistosoma haematobium x Schistosoma bovis Hybrids
by Beatriz Crego-Vicente, Pedro Fernández-Soto, Begoña Febrer-Sendra, Juan García-Bernalt Diego, Jérôme Boissier, Etienne K. Angora, Ana Oleaga and Antonio Muro
J. Clin. Med. 2021, 10(6), 1308; https://doi.org/10.3390/jcm10061308 - 22 Mar 2021
Cited by 8 | Viewed by 3796
Abstract
Schistosomiasis is a disease of great medical and veterinary importance in tropical and subtropical regions caused by different species of parasitic flatworms of the genus Schistosoma. The emergence of natural hybrids of schistosomes indicate the risk of possible infection to humans and [...] Read more.
Schistosomiasis is a disease of great medical and veterinary importance in tropical and subtropical regions caused by different species of parasitic flatworms of the genus Schistosoma. The emergence of natural hybrids of schistosomes indicate the risk of possible infection to humans and their zoonotic potential, specifically for Schistosoma haematobium and S. bovis. Hybrid schistosomes have the potential to replace existing species, generate new resistances, pathologies and extending host ranges. Hybrids may also confuse the serological, molecular and parasitological diagnosis. Currently, LAMP technology based on detection of nucleic acids is used for detection of many agents, including schistosomes. Here, we evaluate our previously developed species-specific LAMP assays for S. haematobium, S. mansoni, S. bovis and also the genus-specific LAMP for the simultaneous detection of several Schistosoma species against both DNA from pure and, for the first time, S. haematobium x S. bovis hybrids. Proper operation was evaluated with DNA from hybrid schistosomes and with human urine samples artificially contaminated with parasites’ DNA. LAMP was performed with and without prior DNA extraction. The genus-specific LAMP properly amplified pure Schistosoma species and different S. haematobium-S. bovis hybrids with different sensitivity. The Schistosoma spp.-LAMP method is potentially adaptable for field diagnosis and disease surveillance in schistosomiasis endemic areas where human infections by schistosome hybrids are increasingly common. Full article
(This article belongs to the Special Issue Epidemiology, Immunology, and Control of Schistosomiasis)
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17 pages, 3186 KiB  
Article
Development of a Molecular Snail Xenomonitoring Assay to Detect Schistosoma haematobium and Schistosoma bovis Infections in their Bulinus Snail Hosts
by Tom Pennance, John Archer, Elena Birgitta Lugli, Penny Rostron, Felix Llanwarne, Said Mohammed Ali, Amour Khamis Amour, Khamis Rashid Suleiman, Sarah Li, David Rollinson, Jo Cable, Stefanie Knopp, Fiona Allan, Shaali Makame Ame and Bonnie Lee Webster
Molecules 2020, 25(17), 4011; https://doi.org/10.3390/molecules25174011 - 2 Sep 2020
Cited by 26 | Viewed by 5238
Abstract
Schistosomiasis, a neglected tropical disease of medical and veterinary importance, transmitted through specific freshwater snail intermediate hosts, is targeted for elimination in several endemic regions in sub-Saharan Africa. Multi-disciplinary methods are required for both human and environmental diagnostics to certify schistosomiasis elimination when [...] Read more.
Schistosomiasis, a neglected tropical disease of medical and veterinary importance, transmitted through specific freshwater snail intermediate hosts, is targeted for elimination in several endemic regions in sub-Saharan Africa. Multi-disciplinary methods are required for both human and environmental diagnostics to certify schistosomiasis elimination when eventually reached. Molecular xenomonitoring protocols, a DNA-based detection method for screening disease vectors, have been developed and trialed for parasites transmitted by hematophagous insects, such as filarial worms and trypanosomes, yet few have been extensively trialed or proven reliable for the intermediate host snails transmitting schistosomes. Here, previously published universal and Schistosoma-specific internal transcribed spacer (ITS) rDNA primers were adapted into a triplex PCR primer assay that allowed for simple, robust, and rapid detection of Schistosoma haematobium and Schistosoma bovis in Bulinus snails. We showed this two-step protocol could sensitively detect DNA of a single larval schistosome from experimentally infected snails and demonstrate its functionality for detecting S. haematobium infections in wild-caught snails from Zanzibar. Such surveillance tools are a necessity for succeeding in and certifying the 2030 control and elimination goals set by the World Health Organization. Full article
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13 pages, 252 KiB  
Review
Schistosome Vaccines for Domestic Animals
by Hong You, Pengfei Cai, Biniam Mathewos Tebeje, Yuesheng Li and Donald P. McManus
Trop. Med. Infect. Dis. 2018, 3(2), 68; https://doi.org/10.3390/tropicalmed3020068 - 19 Jun 2018
Cited by 42 | Viewed by 5864
Abstract
Schistosomiasis is recognized as a tropical disease of considerable public health importance, but domestic livestock infections due to Schistosoma japonicum, S. bovis, S. mattheei and S. curassoni are often overlooked causes of significant animal morbidity and mortality in Asia and Africa. [...] Read more.
Schistosomiasis is recognized as a tropical disease of considerable public health importance, but domestic livestock infections due to Schistosoma japonicum, S. bovis, S. mattheei and S. curassoni are often overlooked causes of significant animal morbidity and mortality in Asia and Africa. In addition, whereas schistosomiasis japonica is recognized as an important zoonosis in China and the Philippines, reports of viable schistosome hybrids between animal livestock species and S. haematobium point to an underappreciated zoonotic component of transmission in Africa as well. Anti-schistosome vaccines for animal use have long been advocated as part of the solution to schistosomiasis control, benefitting humans and animals and improving the local economy, features aligning with the One Health concept synergizing human and animal health. We review the history of animal vaccines for schistosomiasis from the early days of irradiated larvae and then consider the recombinant DNA technology revolution and its impact in developing schistosome vaccines that followed. We evaluate the major candidates tested in livestock, including the glutathione S-transferases, paramyosin and triose-phosphate isomerase, and summarize some of the future challenges that need to be overcome to design and deliver effective anti-schistosome vaccines that will complement current control options to achieve and sustain future elimination goals. Full article
(This article belongs to the Special Issue Prospects for Schistosomiasis Elimination)
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