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High prevalence of Schistosoma haematobium × Schistosoma bovis hybrids in schoolchildren in Côte d'Ivoire

Published online by Cambridge University Press:  21 November 2019

Etienne K. Angora
Affiliation:
Swiss Tropical and Public Health Institute, Basel, Switzerland University of Basel, Basel, Switzerland Unité de Formation et de Recherche Sciences Pharmaceutiques et Biologiques, Université Félix Houphouët-Boigny, Abidjan, Côte d'Ivoire
Jean-François Allienne
Affiliation:
IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, France
Olivier Rey
Affiliation:
IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, France
Hervé Menan
Affiliation:
Unité de Formation et de Recherche Sciences Pharmaceutiques et Biologiques, Université Félix Houphouët-Boigny, Abidjan, Côte d'Ivoire
André O. Touré
Affiliation:
Institut Pasteur de Côte d'Ivoire, Abidjan, Côte d'Ivoire
Jean T. Coulibaly
Affiliation:
Swiss Tropical and Public Health Institute, Basel, Switzerland University of Basel, Basel, Switzerland Unité de Formation et de Recherche Biosciences, Université Félix Houphouët-Boigny, Abidjan, Côte d'Ivoire Centre Suisse de Recherches Scientifiques en Côte d'Ivoire, Abidjan, Côte d'Ivoire
Giovanna Raso
Affiliation:
Swiss Tropical and Public Health Institute, Basel, Switzerland University of Basel, Basel, Switzerland
William Yavo
Affiliation:
Unité de Formation et de Recherche Sciences Pharmaceutiques et Biologiques, Université Félix Houphouët-Boigny, Abidjan, Côte d'Ivoire
Eliézer K. N'Goran
Affiliation:
Unité de Formation et de Recherche Biosciences, Université Félix Houphouët-Boigny, Abidjan, Côte d'Ivoire Centre Suisse de Recherches Scientifiques en Côte d'Ivoire, Abidjan, Côte d'Ivoire
Jürg Utzinger
Affiliation:
Swiss Tropical and Public Health Institute, Basel, Switzerland University of Basel, Basel, Switzerland
Oliver Balmer
Affiliation:
Swiss Tropical and Public Health Institute, Basel, Switzerland University of Basel, Basel, Switzerland
Jérôme Boissier*
Affiliation:
IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, France
*
Author for correspondence: Jérôme Boissier, E-mail: boissier@univ-perp.fr

Abstract

Schistosomiasis is a neglected tropical disease, though it is highly prevalent in many parts of sub-Saharan Africa. While Schistosoma haematobium-bovis hybrids have been reported in West Africa, no data about Schistosoma hybrids in humans are available from Côte d'Ivoire. This study aimed to identify and quantify S. haematobium-bovis hybrids among schoolchildren in four localities of Côte d'Ivoire. Urine samples were collected and examined by filtration to detect Schistosoma eggs. Eggs were hatched and 503 miracidia were individually collected and stored on Whatman® FTA cards for molecular analysis. Individual miracidia were molecularly characterized by analysis of mitochondrial cox1 and nuclear internal transcribed spacer 2 (ITS 2) DNA regions. A mitochondrial cox1-based diagnostic polymerase chain reaction was performed on 459 miracidia, with 239 (52.1%) exhibiting the typical band for S. haematobium and 220 (47.9%) the S. bovis band. The cox1 and ITS 2 amplicons were Sanger sequenced from 40 randomly selected miracidia to confirm species and hybrids status. Among the 33 cox1 sequences analysed, we identified 15 S. haematobium sequences (45.5%) belonging to seven haplotypes and 18 S. bovis sequences (54.5%) belonging to 12 haplotypes. Of 40 ITS 2 sequences analysed, 31 (77.5%) were assigned to pure S. haematobium, four (10.0%) to pure S. bovis and five (12.5%) to S. haematobium-bovis hybrids. Our findings suggest that S. haematobium-bovis hybrids are common in Côte d'Ivoire. Hence, intense prospection of domestic and wild animals is warranted to determine whether zoonotic transmission occurs.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019

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Footnotes

*

These authors contributed equally to this work.

References

Achi, YL, Zinsstag, J, Yéo, N, Dea, V and Dorchies, PH (2003) Les nématodes gastro-intestinaux des bovins de la région des savanes de la Côte-d'Ivoire: enquête d'abattoir. Revue de Médecine Vétérinaire 154, 105112.Google Scholar
Angora, EK, Boissier, J, Menan, H, Rey, O, Tuo, K, Touré, AO, Coulibaly, JT, Méité, A, Raso, G, N'Goran, EK, Utzinger, J and Balmer, O (2019) Prevalence and risk factors for schistosomiasis among schoolchildren in two settings of Côte d'Ivoire. Tropical Medicine and Infectious Disease 4, 110.CrossRefGoogle ScholarPubMed
Assaré, RK, Lai, Y-S, Yapi, A, Tian-Bi, Y-NT, Ouattara, M, Yao, PK, Knopp, S, Vounatsou, P, Utzinger, J and N'Goran, EK (2015) The spatial distribution of Schistosoma mansoni infection in four regions of western Côte d'Ivoire. Geospatial Health 10, 345.CrossRefGoogle ScholarPubMed
Barber, KE, Mkoji, GM and Loker, ES (2000) PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. bovis from Kenya. American Journal of Tropical Medicine and Hygiene 62, 434440.CrossRefGoogle ScholarPubMed
Boissier, J, Grech-Angelini, S, Webster, BL, Allienne, J-F, Huyse, T, Mas-Coma, S, Toulza, E, Barré-Cardi, H, Rollinson, D, Kincaid-Smith, J, Oleaga, A, Galinier, R, Foata, J, Rognon, A, Berry, A, Mouahid, G, Henneron, R, Moné, H, Noel, H and Mitta, G (2016) Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study. Lancet Infectious Diseases 16, 971979.CrossRefGoogle ScholarPubMed
Chammartin, F, Houngbedji, CA, Hürlimann, E, Yapi, RB, Silué, KD, Soro, G, Kouamé, FN, N'Goran, EK, 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, e3407.CrossRefGoogle ScholarPubMed
Colley, DG, Bustinduy, AL, Secor, WE and King, CH (2014) Human schistosomiasis. Lancet 383, 22532264.CrossRefGoogle ScholarPubMed
Cook, GC and Zumla, A (2009) Manson's Tropical Diseases, 22nd Edn.Elsevier Health Sciences 1830p.Google Scholar
Coulibaly, JT, N'Gbesso, YK, N'Guessan, NA, Winkler, MS, Utzinger, J and N'Goran, EK (2013) Epidemiology of schistosomiasis in two high-risk communities of south Côte d'Ivoire with particular emphasis on pre-school–aged children. American Journal of Tropical Medicine and Hygiene 89, 3241.CrossRefGoogle ScholarPubMed
Djuikwo-Teukeng, FF, Kouam Simo, A, Allienne, J-F, Rey, O, Njayou Ngapagna, A, Tchuem-Tchuenté, LA and Boissier, J (2019) Population genetic structure of Schistosoma bovis in Cameroon. Parasites & Vectors 12, 56.CrossRefGoogle ScholarPubMed
GBD 2017 DALYs and HALE Collaborators (2018) Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392, 17361788.Google Scholar
Gower, CM, Gouvras, AN, Lamberton, PHL, Deol, A, Shrivastava, J, Mutombo, PN, Mbuh, JV, Norton, AJ, Webster, BL, Stothard, JR, Garba, A, Lamine, MS, Kariuki, C, Lange, CN, Mkoji, GM, Kabatereine, NB, Gabrielli, AF, Rudge, JW, Fenwick, A, Sacko, M, Dembelé, R, Lwambo, NJS, Tchuem Tchuenté, L-A, Rollinson, D and Webster, JP (2013) Population genetic structure of Schistosoma mansoni and Schistosoma haematobium from across six sub-Saharan African countries: implications for epidemiology, evolution and control. Acta Tropica 128, 261274.CrossRefGoogle ScholarPubMed
Hotez, PJ, Alvarado, M, Basáñez, M-G, Bolliger, I, Bourne, R, Boussinesq, M, Brooker, SJ, Brown, AS, Buckle, G, Budke, CM, Carabin, H, Coffeng, LE, Fèvre, EM, Fürst, T, Halasa, YA, Jasrasaria, R, Johns, NE, Keiser, J, King, CH, Lozano, R, Murdoch, ME, O'Hanlon, S, Pion, SDS, Pullan, RL, Ramaiah, KD, Roberts, T, Shepard, DS, Smith, JL, Stolk, WA, Undurraga, EA, Utzinger, J, Wang, M, Murray, CJL and Naghavi, M (2014) The Global Burden of Disease Study 2010: interpretation and implications for the neglected tropical diseases. PLoS Neglected Tropical Diseases 8, e2865.CrossRefGoogle ScholarPubMed
Huyse, T, Webster, BL, Geldof, S, Stothard, JR, Diaw, OT, Polman, K and Rollinson, D (2009) Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathogens 5, e1000571.CrossRefGoogle ScholarPubMed
King, KC, Stelkens, RB, Webster, JP, Smith, DF and Brockhurst, MA (2015) Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world. PLoS Pathogens 11, e1005098.CrossRefGoogle Scholar
Krauth, SJ, Musard, C, Traoré, SI, Zinsstag, J, Achi, LY, N'Goran, EK and Utzinger, J (2015) Access to, and use of, water by populations living in a schistosomiasis and fascioliasis co-endemic area of northern Côte d'Ivoire. Acta Tropica 149, 179185.CrossRefGoogle Scholar
Lai, Y-S, Biedermann, P, Ekpo, UF, Garba, A, Mathieu, E, Midzi, N, Mwinzi, P, N'Goran, EK, Raso, G, Assaré, RK, Sacko, M, Schur, N, Talla, I, Tchuem-Tchuenté, L-A, Touré, S, Winkler, MS, Utzinger, J and Vounatsou, P (2015) Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis. Lancet Infectious Diseases 15, 927940.CrossRefGoogle ScholarPubMed
Le Govic, Y, Kincaid-Smith, J, Allienne, J-F, Rey, O, de Gentile, L and Boissier, J (2019) Schistosoma haematobium-Schistosoma mansoni hybrid parasite in migrant boy, France, 2017. Emerging Infectious Diseases 25, 365367.CrossRefGoogle Scholar
Leger, E and Webster, JP (2017) Hybridizations within the genus Schistosoma: implications for evolution, epidemiology and control. Parasitology 144, 6580.CrossRefGoogle ScholarPubMed
Lockyer, AE, Olson, PD, Ostergaard, P, Rollinson, D, Johnston, DA, Attwood, SW, Southgate, VR, Horak, P, Snyder, SD, Le, TH, Agatsuma, T, McManus, DP, Carmichael, AC, Naem, S and Littlewood, DTJ (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma weinland, 1858. Parasitology 126, 203224.CrossRefGoogle ScholarPubMed
M'Bra, RK, Koné, B, Yapi, YG, Silué, KD, Sy, I, Vienneau, D, Soro, N, Cissé, G and Utzinger, J (2018) Risk factors for schistosomiasis in an urban area in northern Côte d'Ivoire. Infectious Diseases of Poverty 7, 47.CrossRefGoogle Scholar
Moné, H, Holtfreter, MC, Allienne, J-F, Mintsa-Nguéma, R, Ibikounlé, M, Boissier, J, Berry, A, Mitta, G, Richter, J and Mouahid, G (2015) Introgressive hybridizations of Schistosoma haematobium by Schistosoma bovis at the origin of the first case report of schistosomiasis in Corsica (France, Europe). Parasitology Research 114, 41274133.CrossRefGoogle Scholar
Mott, KE, Baltes, R, Bambagha, J and Baldassini, B (1982) Field studies of a reusable polyamide filter for detection of Schistosoma haematobium eggs by urine filtration. Tropenmedizin und Parasitologie 33, 227228.Google ScholarPubMed
N'Guessan, N, Acka, CA, Utzinger, J and N'Goran, EK (2007) Identification des régions à haut risque de schistosomoses en Côte d'Ivoire. Bulletin de la Société de Pathologie Exotique 100, 119123.Google Scholar
Raso, G, Matthys, B, N'Goran, EK, Tanner, M, Vounatsou, P and Utzinger, J (2005) Spatial risk prediction and mapping of Schistosoma mansoni infections among schoolchildren living in western Côte d'Ivoire. Parasitology 131, 97108.CrossRefGoogle ScholarPubMed
Rozas, J, Ferrer-Mata, A, Sánchez-DelBarrio, JC, Guirao-Rico, S, Librado, P, Ramos-Onsins, SE and Sánchez-Gracia, A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34, 32993302.CrossRefGoogle ScholarPubMed
Tian-Bi, Y-NT, Webster, B, Konan, CK, Allan, F, Diakité, NR, Ouattara, M, Salia, D, Koné, A, Kakou, AK, Rabone, M, Coulibaly, JT, Knopp, S, Meïté, A, Utzinger, J, N'Goran, EK and Rollinson, D (2019) Molecular characterization and distribution of Schistosoma cercariae collected from naturally infected bulinid snails in northern and central Côte d'Ivoire. Parasites & Vectors 12, 117.CrossRefGoogle ScholarPubMed
Webster, BL, Emery, AM, Webster, JP, Gouvras, A, Garba, A, Diaw, O, Seye, MM, Tchuem-Tchuente, LA, Simoonga, C, Mwanga, J, Lange, C, Kariuki, C, Mohammed, KA, Stothard, JR and Rollinson, D (2012) Genetic diversity within Schistosoma haematobium: DNA barcoding reveals two distinct groups. PLoS Neglected Tropical Diseases 6, e1882.CrossRefGoogle ScholarPubMed
Webster, BL, Diaw, OT, Seye, MM, Webster, JP 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 7, e2110.CrossRefGoogle ScholarPubMed
Webster, BL, Rabone, M, Pennance, T, Emery, AM, Allan, F, Gouvras, A, Knopp, S, Garba, A, Hamidou, AA, Mohammed, KA, Ame, SM, Rollinson, D and Webster, JP (2015) Development of novel multiplex microsatellite polymerase chain reactions to enable high-throughput population genetic studies of Schistosoma haematobium. Parasites & Vectors 8, 432.CrossRefGoogle ScholarPubMed
Webster, BL, Alharbi, MH, Kayuni, S, Makaula, P, Halstead, F, Christiansen, R, Juziwelo, L, Stanton, MC, LaCourse, EJ, Rollinson, D, Kalua, K and Stothard, JR (2019) Schistosome interactions within the Schistosoma haematobium group, Malawi. Emerging Infectious Diseases 25, 12451247.CrossRefGoogle ScholarPubMed
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