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Mapping of schistosome hybrids of the haematobium group in West and Central Africa

Published online by Cambridge University Press:  18 September 2024

P. Agniwo
Affiliation:
Department of Epidemiology of Infectious Diseases, Faculty of Pharmacy, University of Sciences, Techniques and Technologies of Bamako IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, Franceand Centre de Recherche pour la lutte contre les Maladies Infectieuses Tropicales (CReMIT/TIDRC), Université d’Abomey-Calavi, Benin
B.A.E.S. Savassi
Affiliation:
IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, Franceand Centre de Recherche pour la lutte contre les Maladies Infectieuses Tropicales (CReMIT/TIDRC), Université d’Abomey-Calavi, Benin
J. Boissier
Affiliation:
IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, Franceand
M. Dolo
Affiliation:
Department of Epidemiology of Infectious Diseases, Faculty of Pharmacy, University of Sciences, Techniques and Technologies of Bamako
M. Ibikounlé
Affiliation:
Centre de Recherche pour la lutte contre les Maladies Infectieuses Tropicales (CReMIT/TIDRC), Université d’Abomey-Calavi, Benin
A. Dabo*
Affiliation:
Department of Epidemiology of Infectious Diseases, Faculty of Pharmacy, University of Sciences, Techniques and Technologies of Bamako
*
Corresponding author: A. Dabo; Email: [email protected]

Abstract

Hybridization of parasitic species is an emerging health problem in the evolutionary profile of infectious disease, particularly within trematodes of the genus Schistosoma. Because the consequences of this hybridization are still relatively unknown, further studies are needed to clarify the epidemiology of the disease and the biology of hybrid schistosomes. In this article, we provide a detailed review of published results on schistosome hybrids of the haematobium group. Using a mapping approach, this review describes studies that have investigated hybridization in human (S. haematobium, S. guineensis, and S. intercalatum) and animal (S. bovis and S. curassoni) schistosome species in West Africa (Niger, Mali, Senegal, Côte d’Ivoire, Benin, Nigeria) and in Central Africa (Cameroon, Gabon, Democratic Republic of Congo), as well as their limitations linked to the underestimation of their distribution in Africa. This review provides information on studies that have highlighted hybrid species of the haematobium group and the regions where they have been found, notably in West and Central Africa.

Type
Review Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Abdulkadir, A., Ahmed, M., Abubakar, B., Suleiman, I., Yusuf, I., Imam, I., and Musa, B. M. (2017) Prevalence of urinary schistosomiasis in Nigeria, 1994–2015: Systematic review and meta-analysis. African Journal of Urology 23(3), 228239. https://doi.org/10.1016/j.afju.2016.11.004Google Scholar
Agi, P. I., and Okafor, E. J. (2005) ‘The epidemiology of Schistosoma haematobium in Odau community in the Niger Delta Area of Nigeria.Journal of Applied Sciences and Environmental Management 9.3, 3743.Google Scholar
Angora, E. K., Allienne, J. F., Rey, O., Menan, H., Touré, A. O., Coulibaly, J. T., and Boissier, J. (2020) High prevalence of Schistosoma haematobium× Schistosoma bovis hybrids in schoolchildren in Côte d’Ivoire. Parasitology 147(3), 287294.Google Scholar
Angora, E, Boissier, J., Menan, H., Rey, O., Tuo, K., Touré, A. O., and Balmer, O. (2019a) Prevalence and risk factors for Schistosomiasis among schoolchildren in two settings of Côte d’Ivoire. Tropical Medicine and Infectious Diseases 23; 4(3):11. doi: 10.3390/tropicalmed4030110. PMID: 31340504; PMCID: PMC6789509.). https://doi.org/10.3390/tropicalmed4030110Google Scholar
Angora, E., Allienne, J., Rey, O., Menan, H., Touré, A. O., Coulibaly, J. T., and Boissier, J. (2019b) High prevalence of Schistosoma haematobium × Schistosoma bovis hybrids in schoolchildren in Côte d’Ivoire. Parasitology 147(3):287294.Google Scholar
Angora, Etienne K., Vangraefschepe, A., Allienne, J.-F., Menan, H., Coulibaly, J. T., Meïté, A., Boissier, J. (2022) Population genetic structure of Schistosoma haematobium and Schistosoma haematobium × Schistosoma bovis hybrids among school-aged children in Côte d’Ivoire. Parasite 29, 23. https://doi.org/10.1051/parasite/2022023Google Scholar
Aula, O. P., McManus, D. P., Jones, M. K., and Gordon, C. A. (2021) Schistosomiasis with a focus on Africa. Tropical Medicine and Infectious Disease 6(3), 140.Google Scholar
Biu, A.A., Kolo, H.B., and Agbadu, E.T. (2009) Prevalence of Schistosoma haematobium infection in school aged children of Konduga Local Government Area, Northeastern Nigeria. African Studies 5(4), 181184.Google Scholar
Blin, M., Dametto, S., Agniwo, P., Webster, B. L., and Angora, E. (2023) A duplex tetra-primer ARMS-PCR assay to discriminate three species of the Schistosoma haematobium group: Schistosoma curassoni, S. bovis, S. haematobium and their hybrids. Parasites & Vectors 16, 121.Google Scholar
Boissier, J., Kincaid-smith, J., Berry, A., Allienne, J., Fillaux, J., Toulza, E., and Fillaux, J. (2016) Changements globaux et infections parasitaires à mollusques vecteurs. Un schistosome hybride atteint l’Europe. Médecine/Sciences, EDP Sciences 31(11):962964.Google Scholar
Boon, A., Mbow, M., Paredis, L., Moris, P., Sy, I., Maes, T., and Huyse, T. (2019) No barrier breakdown between human and cattle schistosome species in the Senegal River Basin in the face of hybridisation. International Journal for Parasitology, 49(13–14), 10391048.Google Scholar
Boon, N. A. M., Van Den Broeck, F., Faye, D., Volckaert, F. A. M., Mboup, S., Polman, K., and Huyse, T. (2018) Barcoding hybrids: heterogeneous distribution of Schistosoma haematobium × Schistosoma bovis hybrids across the Senegal River Basin. Parasitology 145(5), 634645.Google Scholar
Boon, N. A. M., Fannes, W., Rombouts, S., Polman, K., Volckaert, F. A. M., and Huyse, T. (2017) Detecting hybridization in African schistosome species: does egg morphology complement molecular species identification? Parasitology 144(7). https://doi.org/10.1017/S0031182017000087Google Scholar
Brémond, P., Mouchet, F., Chevallier, P., Sellin, E., Vera, C., and Sellin, B. (1990) Flux genique entre Schistosoma bovis et S. curassoni au Niger. Bull Soc Française Parasitology, 8, 708.Google Scholar
Bremond, P., Sellin, B., Sellin, E., Nameoua, B., Labbo, R., and Theron, A. (1993) [Arguments for the modification of the genome (introgression) of the human parasite Schistosoma haematobium by genes from. S bovis, in Niger]. Comptes Rendus de l’Academie Des Sciences. Serie III, Sciences de La Vie, 316(7), 667670.Google Scholar
Briand, V., Watier, L., Le Hesran, J. Y., Garcia, A., and Cot, M. (2005) Coinfection with Plasmodium falciparum and Schistosoma haematobium: additional evidence of the protective effect of schistosomiasis on malaria in Senegalese children. American Journal of Tropical Medicine and Hygiene 72(6), 702707.Google Scholar
Burchard, G., and Kern, P. (1985) Probable hybridization between S. intercalatum and S. haematobium in western Gabun. Tropical and Geographical Medicine 37(2):119123.Google Scholar
Catalano, S., Sène, M., Diouf, N. D., and Fall, C. B. (2018) Rodents as natural hosts of zoonotic Schistosoma species and hybrids : an epidemiological and evolutionary perspective from West Africa. The Journal of Infectious Diseases 218(1), 429433.Google Scholar
Chammartin, F., Houngbedji, C. A., Hürlimann, E., Yapi, R. B., Silué, K. D., Soro, G., Kouamé, F. N., N’Goran, R. K., Utzinger, J., Raso, G., and Vounatsou, P. (2014) Bayesian risk mapping and model-based estimation of Schistosoma haematobium–Schistosoma mansoni co-distribution in Côte d′Ivoire. PLoS Neglected Tropical Diseases 8(12).Google Scholar
Chiti, L., De Bont, J., Fransen, J., Kane, R. A., Mwase, M., Southgate, V. R., and Vercruysse, J. (2000) Natural infection with schistosomes of the Schistosoma haematobium group in a dog in Zambia. Journal of Comparative Pathology 122(2–3), 229233.Google Scholar
Clements, A. C. A., Bosqué-Oliva, E., Sacko, M., Landouré, A., and Dembélé, R. (2009) A comparative study of the spatial distribution of schistosomiasis in Mali in 1984-1989 and 2004-2006. PLoS Neglected Tropical Diseases 3(5), 111.Google Scholar
Cnops, L., Huyse, T., Maniewski, U., Soentjens, P., Bottieau, E., Van Esbroeck, M., and Clerinx, J. (2021) Acute schistosomiasis with a Schistosoma mattheei × Schistosoma haematobium hybrid species in a cluster of 34 travelers infected in South Africa. Clinical Infectious Diseases 72(10), 16931698.Google Scholar
Coulibaly, J. T., N’Gbesso, Y. K., Knopp, S., Keiser, J., N’Goran, E. K., and Utzinger, J. (2012) Efficacy and safety of praziquantel in preschool-aged children in an area co-endemic for Schistosoma mansoni and S. haematobium. PLoS Neglected Tropical Diseases, 6(12).Google Scholar
Crego-Vicente, B., Fernández-Soto, P., Febrer-Sendra, B., Diego, J. G. B., Boissier, J., Angora, E. K., and Muro, A. (2021) Application of a genus-specific LAMP assay for schistosome species to detect Schistosoma haematobium x Schistosoma bovis hybrids. Journal of Clinical Medicine 10(6), 113.Google Scholar
Dabo, A, Diarra, A., Machault, V., Touré, O., Niambélé, D. S., Kanté, A., and Doumbo, O. (2015) Urban schistosomiasis and associated determinant factors among school children in Bamako, Mali, West Africa. Infectious Diseases of Poverty 4(1).Google Scholar
Dabo, A., Bary, B., Kouriba, B., Sankaré, O., and Doumbo, O. (2013) Factors associated with coverage of praziquantel for schistosomiasis control in the community- direct intervention (CDI) approach in Mali (West Africa ). Infectious Diseases of Poverty 2(11), 111.Google Scholar
Dabo, Abdoulaye, Durand, P., Morand, S., Diakite, M., Langand, J., Imbert-Establet, D., and Jourdane, J. (1997) Distribution and genetic diversity of Schistosoma haematobium within its bulinid intermediate hosts in Mali. Acta Tropica 66(1), 1526.Google Scholar
Dabo, A., Mahamat Badawi, H., Bary, B., and Doumbo, O. K. (2011) Urinary schistosomiasis among preschool-aged children in Sahelian rural communities in Mali. Parasites & Vectors 4, 17.Google Scholar
Dawet, A., Yakubu, D., Longmut, R., Benjamin, C., Nannim, Y., and Daburum, N. (2012) Prevalence and intensity of Schistosoma haematobium among residents of Gwong and Kabong in Jos North Local Government Area, Plateau State, Nigeria. International Journal of Biological and Chemical Sciences 6(4).Google Scholar
De Bont, J., Vercruysse, J., Southgate, V. R., Rollinson, D., and Kaukas, A. (1994) Cattle schistosomiasis in Zambia. Journal of Helminthology 68(4), 295299.Google Scholar
De Bont, J., and Vercruysse, J. (1998). Schistosomiasis in cattle. Advances in Parasitology 41, 285364.Google Scholar
De Clercq, D., Rollinson, D., Diarra, A., Sacko, M., Coulibaly, G., Landouré, A., and Vercruysse, J. (1994) Schistosomiasis in Dogon country, Mali: identification and prevalence of the species responsible for infection in the local community. Transactions of the Royal Society of Tropical Medicine and Hygiene 88(6), 653656.Google Scholar
De Clercq, D., Vercruysse, J., Picquet, M., Shaw, D. J., Diop, M., Ly, A., and Gryseels, B. (1999) The epidemiology of a recent focus of mixed Schistosoma haematobium and Schistosoma mansoni infections around the ‘Lac de Guiers’ in the Senegal River Basin, Senegal. Tropical Medicine and International Health 4(8), 544–450.Google Scholar
Dejon-Agobé, J. C., Edoa, J. R., Adegnika, A. A., and Grobusch, M. P. (2022) Schistosomiasis in Gabon from 2000 to 2021-a review. Acta Tropica 228(106317).Google Scholar
Detwiler, J. T., and Criscione, C. D. (2010) An infectious topic in reticulate evolution: introgression and hybridization in animal parasites. Genes 1, 102123.Google Scholar
Ekpo, U. F., Hürlimann, E., Schur, N., Oluwole, A. S., Abe, E. M., Mafe, M. A., and Vounatsou, P. (2013) Mapping and prediction of schistosomiasis in Nigeria using compiled survey data and Bayesian geospatial modelling. Geospatial Health 7(2), 355366.Google Scholar
Ezeh, O. C., Chibuike Onyekwelu, K., Phebian Akinwale, O., Shan, L., and Wei, H. (2019) Urinary schistosomiasis in Nigeria: a 50 year review of prevalence, distribution and disease burden. Parasite 26, 19.Google Scholar
Huyse, T., Webster, B. L., Geldof, S., Stothard, J. R., Diaw, O. T., and Rollinson, D. (2009) Bidirectional introgressive hybridization between a cattle and human schistosome species. PLOS Pathogens 5(9).Google Scholar
Irwin, D. E. (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution 56(12), 23832394.Google Scholar
Ivoke, N., Ivoke, O. N., Nwani, C. D., Ekeh, F. N., Asogwa, C. N., Atama, C. I., and Eyo, J. E. (2014) Prevalence and transmission dynamics of Schistosoma haematobium infection in a rural community of southwestern Ebonyi State, Nigeria. Tropical Biomedicine 31(1), 7788.Google Scholar
King, K. C., Stelkens, R. B., Webster, J. P., Smith, D. F., and Brockhurst, M. A. (2015) Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world. PLoS Pathogens 11(9).Google Scholar
Kouriba, B., Traoré, H. A., Dabo, A., Sangaré, L., Guindo, H., Keita, A. S., and Dessein, A. J. (2005) Urinary disease in 2 Dogon populations with different exposure to Schistosoma haematobium infection: progression of bladder and kidney diseases in children and adults. Journal of Infectious Diseases 192(12), 21522159.Google Scholar
Kruger, F., and Hamilton-Attwell, V. (1988) Scanning electron microscope studies of miracidia suggest introgressive hybridization between Schistosoma haematobium and S. haematobium × S. mattheei in the Eastern Transvaal. Journal of Helminthology 62, 141147.Google Scholar
Lai, Y. S., Biedermann, P., Ekpo, U. F., Garba, A., Mathieu, E., Midzi, N., and Vounatsou, P. (2015) Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis. The Lancet Infectious Diseases 15(8), 927940.Google Scholar
Léger, E., Garba, A., Hamidou, A. A., Webster, B. L., Pennance, T., Rollinson, D., and Webster, J. P. (2016) Introgressed animal Schistosomes Schistosoma curassoni and S. bovis. Emerging Infectious Diseases 22(12), 22122214.Google Scholar
Léger, E., and Webster, J. P. (2017) Hybridizations within the genus Schistosoma : implications for evolution, epidemiology and control. Parasitology 65–80.Google Scholar
Léger, E., Borlase, A., Fall, C.B., Diouf, N.D., Diop, S.D., Yasenev, L., Catalano, S., Thiam, C.T., Ndiaye, A., Emery, A., Morrell, A., Rabone, M., Ndao, M., Faye, B., Rollinson, D., Rudge, JW., Sène, M., and Webster, JP. (2020) Prevalence and distribution of schistosomiasis in human, livestock, and snail populations in northern Senegal: a One Health epidemiological study of a multi-host system. Lancet Planet Health, 4(8):e330e342.Google Scholar
Lyke, K. E., Dabo, A., Arama, C., Daou, M., Diarra, I., Wang, A., and Sztein, M. B. (2012a). Reduced T regulatory cell response during acute plasmodium falciparum infection in malian children co-infected with Schistosoma haematobium. PLoS ONE 7(2).Google Scholar
Lyke, K. E., Dabo, A., Sangare, L., Arama, C., Daou, M., Diarra, I., and Sztein, M. B. (2006) Effects of concomitant Schistosoma haematobium infection on the serum cytokine levels elicited by acute Plasmodium falciparum malaria infection in malian children. Infection and Immunity 74(10), 57185724.Google Scholar
Lyke, K. E., Wang, A., Dabo, A., Arama, C., Daou, M., Diarra, I., and Sztein, M. B. (2012b) Antigen-specific B memory cell responses to Plasmodium falciparum malaria antigens and Schistosoma haematobium antigens in co-infected Malian children. PLoS ONE 7(6).Google Scholar
Madinga, J., Linsuke, S., Mpabanzi, L., Meurs, L., Kanobana, K., Speybroeck, N., Polman, K. (2015) Schistosomiasis in the Democratic Republic of Congo: a literature review. Parasites & Vectors 8, 110.Google Scholar
McSorley, H. J., and Maizels, R. M. (2012) Helminth infections and host immune regulation. Clinical Microbiology Reviews, 25(4), 585608.Google Scholar
Meurs, L., Mbow, M., Boon, N., Van Den Broeck, F., Vereecken, K., Ndiaye Diè Ye, T., and Polman, K. (2013) Micro-geographical heterogeneity in Schistosoma mansoni and S. haematobium infection and morbidity in a co-endemic community in Northern Senegal. PLoS Neglected Tropical Diseases.Google Scholar
de la Santé, Ministère. (2017) Plan directeur de lutte contre les Maladies Tropicales Négligées (2016 - 2020). Rapport du programme national intégré de lutte contre les maladies tropicales négligées du Niger. Available at: https://espen.afro.who.int/system/files/content/resources/NIGER_.Google Scholar
de la Santé, Ministère. (2021) Plan stratégique national de lutte contre les Maladies Tropicales Négligées (2022 - 2025). Rapport du Ministère de la Santé et de l’Action Sociale du Sénégal. Available at: https://espen.afro.who.int/system/files/content/resources/VFF%20Plan%20national%20.Google Scholar
de la Santé, Ministère. (2016) Plan directeur national de lutte contre les Maladies Tropicales Négligées (2016 - 2020). Rapport du Ministère de la Santé et de la lutte contre le sida en Côte d’Ivoire. Available at: https://espen.afro.who.int/system/files/content/resources/COTE_DIVOIRE_.Google Scholar
Ministry of Public Health of Cameroun. (2019). Contrôle de la schistosomiase et des helminthiases intestinales. Progress Report 2003–2019 of National Programme for the Control of Schistosomiasis and Soil transmitted Helminthiasis, 165p.Google Scholar
Mintsa Nguema, R, Mavoungou, J. F., Mengue Me Ngou-Milama, K., Mabicka Mamfoumbi, M., Koumba, A. A., Sani Lamine, M., Diarra, A., and Bouyou Akotet, M. K. (2018) Baseline mapping of schistosomiasis and soil transmitted helminthiasis in the Northern and Eastern health regions of Gabon, Central Africa: Recommendations for preventive chemotherapy. Tropical Medicine and Infectious Disease 3(4), 119.Google Scholar
Moné, H., Holtfreter, M. C., Allienne, J. F., Mintsa-nguéma, R., Ibikounlé, M., and Boissier, J. (2015)Introgressive hybridizations of Schistosoma haematobium by Schistosoma bovis at the origin of the first case report of schistosomiasis in Corsica(France, Europe). Springer-Verlag Berlin Heidelberg, 41274133.Google Scholar
Moné, Hélène, Minguez, S., Ibikounlé, M., Allienne, J.-F., Massougbodji, A., and Mouahid, G. (2012) Natural interactions between S. haematobium and S. guineensis in the Republic of Benin. The Scientific World Journal 793420.Google Scholar
Mouchet, F., Theron, A., Brémond, P., Sellin, E., and Sellin, B. (1992) Pattern of cercarial emergence of Schistosoma curassoni from Niger and comparison with three sympatric species of schistosomes. The Journal of Parasitology, 6163.Google Scholar
Mouchet, F., Labo, R., Develoux, M., and Sellin, B. (1987) Enquete sur les schistosomoses dans l’arrondissement de Gaya (République du Niger). Annual Society of Belgian Medicine and the Tropics, 67(1), 2329.Google Scholar
Mouchet, F., and Bremond, P. (1989) Preliminary observations on Schistosoma curassoni Brumpt, 1931 in Niger. Transactions of the Royal Society of Tropical Medicine and Hygiene 83(6), 811.Google Scholar
Mouchet, Francois, Develoux, M., and Magasa, M. B. (1988) Schistosoma bovis in human stools in republic of Niger. Transactions of the Royal Society of Tropical Medicine and Hygiene 82(2), 257.Google Scholar
Ndifon, G. T., Betterton, C., and Rollinson, D. (1988) Schistosoma curassoni Brumpt, 1931 and S. bovis (Sonsino, 1876) in cattle in northern Nigeria. Journal of Helminthology 7, 3334.Google Scholar
Nguema, R. M., Milama, K. M. N., Kombila, M., Richard-Lenoble, D., Tisseyre, P., Ibikounlé, M., and Mouahid, G. (2010) Morphometric and molecular characterizations of schistosome populations in Estuaire province Gabon. Journal of Helminthology 84(1), 8185.Google Scholar
Niangaly, H., Djimde, A. A., Traore, B., Sangare, C. P. O., Guindo, D., Konate, D., and Doumbo, O. K. (2012) Variations saisonnières de l’infestation par les helminthes intestinaux et Schistosoma haematobium en zone rurale sahélienne au Mali. Médecine et Santé Tropicales 22(4), 430434.Google Scholar
Onyekwere, A., Rey, O., Allienne, J., Nwanchor, M. C., Alo, M., Uwa, C., and Boissier, J. (2022a) Population genetic structure and hybridization of Schistosoma haematobium in Nigeria. Pathogens 11(4).Google Scholar
Onyekwere, A., Rey, O., Nwanchor, M. C., Alo, M., Angora, E. K., Allienne, J. F., and Boissier, J. (2022b) Prevalence and risk factors associated with urogenital schistosomiasis among primary school pupils in Nigeria. Parasite Epidemiology and Control 18, e00255.Google Scholar
Onzo-Aboki, A., Ibikounlé, M., Boko, P. M., Savassi, B. S., Doritchamou, J., Siko, E. J., and Kaboré, A. (2019) Human schistosomiasis in Benin: countrywide evidence of Schistosoma haematobium predominance. Acta Tropica 191, 185197.Google Scholar
Ossai, P. O., Dankoli, R., Nwodo, C., Tukur, D., Nsubuga, P., Ogbuabor, D., and Eze, G. (2014) Bacteriuria and urinary schistosomiasis in primary school children in rural communities in Enugu State, Nigeria, 2012. Pan African Medical Journal 18, 15.Google Scholar
Pagès, J., Jourdane, J., Southgate, V., and Tchuem Tchuenté, L.A. (2003) Reconnaissance de deux espèces jumelles au sein du taxon Schistosoma intercalatum Fisher, 1934, agent de la schistosomosa humaine rectale en Afrique. Description de Schistosoma Guineen_sis. Pp. 139 147 in Combes, C. & Jourdane, J. (Eds) Taxonomy, Ecology.Google Scholar
Panzner, U. and Boissier, J. (2021) Natural intra- and interclade human hybrid schistosomes in Africa with considerations on prevention through vaccination. Microorganisms 9(7), 1465.Google Scholar
Pennance, T., Allan, F., Emery, A., Rabone, M., Cable, J., Garba, A. D., and Webster, B. L. (2020) Interactions between Schistosoma haematobium group species and their Bulinus spp. intermediate hosts along the Niger River Valley. Parasites and Vectors 13(1), 115.Google Scholar
Pitchford, R. J. (1961) Observations on a possible hybrid between the two schistosomes S. haematobium and S. mattheei. Tropical Medicine and Hygiene 74(3), 55, 4451.Google Scholar
Platt, R. N., McDew-White, M., Le Clec’H, W., Chevalier, F. D., Allan, F., Emery, A. M., and Shapiro, B. (2019) Ancient hybridization and adaptive introgression of an invadolysin gene in schistosome parasites. Molecular Biology and Evolution 36(10), 21272142.Google Scholar
Rey, O., Webster, B. L., Huyse, T., Rollinson, D., Van den Broeck, F., Kincaid-Smith, J., and Boissier, J. (2021) Population genetics of African Schistosoma species. Infection, Genetics and Evolution 89, 104727.Google Scholar
Rollinson, D., and Southgate, V. R. (1985) Schistosome and snail populations: genetic variability and parasite transmission. In Ecology and Genetics of Host-Parasite Interactions, Linnean Society Symposium Series (ed. Rollinson, D. and Anderson, R. M.). Academic Press, London, 91109.Google Scholar
Rollinson, D., Southgate, V. R., Vercruysse, J., and Moore, P. J. (1990) Observations on natural and experimental interactions between Schistosoma bovis and S. curassoni from West Africa. Acta Tropicalis 47, 101114.Google Scholar
Sangho, H., Dabo, A., Sidibé, A., Dembélé, R., Diawara, A., Diallo, A., and Konaté, S. (2009) Satisfaction des populations après traitement de masse au praziquantel et a l’albendazole au Mali. Mali Médical 24(2), 2124.Google Scholar
Savassi, B. A. E. S., Dobigny, G., Etougbétché, J. R., Avocegan, T. T., Quinsou, F. T., Gauthier, P., and Mouahid, G. (2021) Mastomys natalensis (Smith, 1834) as a natural host for Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 x Schistosoma bovis Sonsino, 1876 introgressive hybrids. Parasitology Research 120(5), 17551770.Google Scholar
Savassi, B. A. E. S., Mouahid, G., Lasica, C., Mahaman, S. K., Garcia, A., Courtin, D., and Moné, H. (2020) Cattle as natural host for Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 x Schistosoma bovis Sonsino, 1876 interactions, with new cercarial emergence and genetic patterns. Parasitology Research 119(7), 21892205.Google Scholar
Sene-wade, M., Marchand, B., Rollinson, D., and Webster, B. L. (2018) Urogenital schistosomiasis and hybridization between Schistosoma haematobium and Schistosoma bovis in adults living in, 2016–2019. Parisitology 145(13), 17231726.Google Scholar
Senghor, B., Diallo, A., Sylla, S. N., Doucoure, S., Ndiath, M. O., Gaayeb, L.., and Ba, C. T. (2014) Prevalence and intensity of urinary schistosomiasis among school children in the district of Niakhar, region of Fatick, Senegal. Parasites and Vectors 7(1).Google Scholar
Senghor, B., Webster, B., Pennance, T., Sène, M., Doucouré, S., Sow, D., and Sokhna, C. (2023) Molecular characterization of schistosome cercariae and their Bulinus snail hosts from Niakhar, a seasonal transmission focus in central Senegal. Current Research in Parasitology and Vector-Borne Diseases, 3.Google Scholar
Sissoko, M. S., Dabo, A., Traoré, H., Diallo, M., Traoré, B., Konaté, D., and Doumbo, O. K. (2009) Efficacy of artesunate + sulfamethoxypyrazine/ pyrimethamine versus praziquantel in the treatment of Schistosoma haematobium in Children. PLoS One 4(10), e6732.Google Scholar
Soentjens, P., Cnops, L., Huyse, T., Yansouni, C., De Vos, D., De Bottieau, E., Van Esbroeck, M. (2016) Diagnosis and clinical management of Schistosoma haematobium – Schistosoma bovis hybrid infection in a cluster of travelers returning from Mali. Clinical Infectious Diseases 63, 1518.Google Scholar
Southgate, V. R., van Wijk, H. B., and Wright, C. A. (1976) Schistosomiasis at Loum, Cameroun; Schistosoma haematobium, S. intercalatum and their natural hybrid. Z Parasitenkd, 49, 145159.Google Scholar
Tchuem Tchuenté, L. A., Southgate, V. R., Njiokou, F., Njine, T., Kouemeni, L., and Jourdane, J. (1997) The evolution of schistosomiasis at Loum, Cameroon: replacement of Schistosoma intercalatum by S. haematobium through introgressive hybridization. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 664665.Google Scholar
Tchuenté, L. T., Southgate, V. R., Vercruysse, J., Kaukas, A., Kane, R., Mulumba, M. P., and Jourdane, J. (1997) Epidemiological and genetic observations on human schistosomiasis in Kinshasa, Zaire. Transactions of the Royal Society of Tropical Medicine and Hygiene 91(3), 263269.Google Scholar
Ten Hove, R. J., Verweij, J. J., Vereecken, K., Polman, K., Dieye, L., and van Lieshout, L. (2008) Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Transactions of the Royal Society of Tropical Medicine and Hygiene 102(2), 179185.Google Scholar
Teukeng, F. F. D., Blin, M., Bech, N., Gomez, M. R., Zein-Eddine, R., Simo, A. M. K., Allienne, J.-F., Tchuem-Tchuenté, L. A., and Boissier, J. (2022) Hybridization increases genetic diversity in Schistosoma haematobium populations infecting humans in Cameroon. Infectious Diseases of Poverty 11(1), 111.Google Scholar
Tian-Bi, Y. N. T., Konan, J. N. K., Sangaré, A., Ortega-Abboud, E., Utzinger, J., N’Goran, E. K., and Jarne, P. (2019a) Spatio-temporal population genetic structure, relative to demographic and ecological characteristics, in the freshwater snail Biomphalaria pfeifferi in Man, western Côte d’Ivoire. Genetica 147(1), 3345.Google Scholar
Tian-Bi, Y. N. T., Webster, B., Konan, C. K., Allan, F., Diakité, N. R., Ouattara, M., Salia, D., Koné, A., Kakou, A. K., Rabone, M., Coulibaly, J. T., Knopp, S., Meité, A., Utzinger, J., N’Goran, E. K., and Rollinson, D. (2019b) Molecular characterization and distribution of Schistosoma cercariae collected from naturally infected bulinid snails in northern and central Côte d’Ivoire. Parasites and Vectors 12(1), 110.Google Scholar
Toews, D. P. L., and Brelsford, A. (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21(16), 39073930.Google Scholar
Vera, C., Mouchet, F., Bremond, P., Sidiki, A., Sellin, E., and Sellin, B. (1992) Natural infection of bulinus senegalensis by Schistosoma haematobium in a temporary pool focus in Niger: characterization by cercarial emergence patterns. Tropical Medicine and Hygiene 86(1), 62.Google Scholar
Vercruysse, J., Southgate, V. R., and Rollinson, D. (1984) Schistosoma curassoni brumpt, 1931 in sheep and goats in senegal. Journal of Natural History 18(6), 969976.Google Scholar
Webster, B., Diaw, O., Seye, M., Webster, J., and Rollinson, D. (2013) Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLoS Neglected Tropical Diseases 4, 19.Google Scholar
Webster, J., Gower, C., Knowles, S. C., Molyneux, D., and Fenton, A. (2016) One health - an ecological and evolutionary framework for tackling Neglected Zoonotic Diseases. Evol. Appl., 9, 313333.Google Scholar
Webster, B. L., Alharbi, M. H., Kayuni, S., Makaula, P., Halstead, F., Christiansen, R., and Stothard, J. R. (2019) Schistosome interactions within the Schistosoma haematobium Group, Malawi. Emerging Infectious Diseases 25(6), 1245.Google Scholar
Webster, B. L, Southgate, V. R., and Tchuem Tchuenté, L. A. (2003) Isoenzyme analysis of Schistosoma haematobium, S. intercalatum and their hybrids and occurrences of natural hybridization in Cameroon. Journal of Helminthology 77, 269274.Google Scholar
Webster, B. L., Tchuem Tchuenté, L. A., Jourdane, J., and Southgate, V. R. (2005) The interaction of Schistosoma haematobium and S. guineensis in Cameroon. Journal of Helminthology 79(3), 193197.Google Scholar
Webster, Bonnie L., and Littlewood, D. T. J. (2012) Mitochondrial gene order change in Schistosoma (Platyhelminthes: Digenea: Schistosomatidae). International Journal for Parasitology 42(3), 313321.Google Scholar
WHO. (2022) Schistosomiase et géohelminthiases: rapport de situation, 2021, december 2022,. Available at: http://www.who.int/werGoogle Scholar
Wright, C. A., and Ross, C. (1980). Hybrids between Schistosoma haematobium and S. mattheei and their identification by isoelectric focusing of enzymes. Transactions of the Royal Society of Tropical Medicine and Hygiene 74(3), 326332.Google Scholar
Wright, C. A., Southgate, V. R., Van Wijk, H. B., and Moore, P. J. (1974) Hybrids between Schistosoma haematobium and S. intercalatum in Cameroon. Transactions of the Royal Society of Tropical Medicine and Hygiene 68(5), 413414.Google Scholar
Zwingenberger, K., Feldmeier, H., Bienzle, U., and Steiner, A. (1990) Mixed Schistosoma haematobium/Schistosoma intercalatum infection. Annals of Tropical Medicine and Parasitology 84, 8587.Google Scholar