Skip to main content
SpringerLink
Log in

Introgressive hybridizations of Schistosoma haematobium by Schistosoma bovis at the origin of the first case report of schistosomiasis in Corsica (France, Europe)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

This study concerns the first urinary schistosomiasis case observed in Corsica (France, Europe) occurring in a 12-year-old German boy. The aim was to identify the relationship between this Schistosoma haematobium infection and other schistosomes of the Schistosoma group with terminal-spined ova. Morphological and molecular analyses were conducted on the ova. The results showed that the schistosome responsible for the emergence of schistosomiasis in Corsica was due to S. haematobium introgressed by genes from S. bovis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Beltran S, Galinier R, Allienne JF, Boissier J (2008) Cheap, rapid and efficient DNA extraction method to perform multilocus microsatellite genotyping on all Schistosoma mansoni stages. Mem Inst Oswaldo Cruz 103(5):501–503

    Article  CAS  PubMed  Google Scholar 

  • Berry A, Moné H, Iriart X, Mouahid G, Abbo O, Boissier J, Fillaux J, Cassaing S, Debuisson C, Valentin A, Mitta G, Théron A, Magnaval JF (2014) Schistosomiasis haematobium, Corsica, France [letter]. Emerg Infect Dis [Internet]. Sep [date cited]. http://dx.doi.org/10.3201/eid2009.140928

  • Boissier J, Moné H, Mitta G, Bargues MD, Molyneux D, Mas-Coma S (2015) Schistosomiasis reaches Europe. Lancet Inf Dis 15(7):757–758

    Article  Google Scholar 

  • Brémond P, Sellin B, Sellin E, Naméoua B, Labro R, Théron A, Combes C (1993) Arguments en faveur d’une modification du génome (introgression) du parasite humain Schistosoma haematobium par des gènes de S. bovis, au Niger. C R Acad Sciences Série III Sciences de la Vie 316(7):667–670

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552

    Article  CAS  PubMed  Google Scholar 

  • Davis A (2009) Schistosomiasis. In: Cook GC, Zumla AI (eds) Manson’s tropical diseases, 22nd edn. Saunders, Elsevier, Edinburgh, pp 1425–1460

    Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucl Acids Res 36(Web Server issue):W465–W469. doi:10.1093/nar/gkn180

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dereeper A, Audic S, Claverie JM, Blanc G (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10:8. doi:10.1186/1471-2148-10-8

    Article  PubMed Central  PubMed  Google Scholar 

  • Doby JM, Rault B, Deblock S, Chabaud A (1966) Snails and bilharziasis in Corsica. Distribution, frequency and biology of Bulinus truncatus. Ann Parasitol Hum Comp 41(4):337–349

    CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32(5):1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gautret P, Mockenhaupt FP, von Sonnenburg F, Rothe C, Libman M, Van De Winkel K et al. (2015) Local and international implications of schistosomiasis acquired in Corsica, France. Emerg Infect Dis. doi:10.3201/eid2110.150881

  • Holtfreter MC, Moné H, Müller-Stöver I, Mouahid G, Richter J (2014) Schistosoma haematobium infections acquired in Corsica, France, August 2013. Eurosurveillance;19(22): http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20821

  • Huyse T, Webster BL, Geldof S, Stothard R, Diaw OT, Polman K, Rollinson D (2009) Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathog 5(9):e1000571

    Article  PubMed Central  PubMed  Google Scholar 

  • Ibikounlé M, Mouahid G, Mintsa Nguéma R, Sakiti N, Massougbodji A, Moné H (2012) Snail intermediate host/Schistosoma haematobium relationships from three transmission sites in Benin (West Africa). Parasitol Res 112(1):227–233

    Article  PubMed  Google Scholar 

  • Kane RA, Bartley J, Stothard JR, Vercruysse J, Rollinson D, Southgate VR (2002) Application of single strand conformational polymorphism (SSCP) analysis with fluorescent primers for differentiation of Schistosoma haematobium group. Trans R Soc Trop Med Hyg 96(1):235–241

    Article  CAS  Google Scholar 

  • Lockyer AE, Olson PD, Østergaard P, Rollinson D, Johnston DA, Attwood SW, Southgate VR, Horak P, Snyder SD, Le TH, Agatsuma T, McManus DP, Carmichael AC, Naem S, Littlewood DT (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126(3):203–224

    Article  CAS  PubMed  Google Scholar 

  • Loker ES (1983) A comparative study of the life-histories of mammalian schistosomes. Parasitology 87(2):343–369

    Article  PubMed  Google Scholar 

  • Mintsa Nguéma R, Mengué Ngou Milama K, Kombila M, Richard-Lenoble D, Tisseyre P, Ibikounlé M, Moné H, Mouahid G (2010) Morphometric and molecular characterizations of schistosome populations in Estuaire province Gabon. J Helminthol 84(1):81–85

    Article  PubMed  Google Scholar 

  • Moné H, Minguez S, Ibikounlé M, Allienne J-F, Massougbodji A, Mouahid G (2012) Natural interactions between S. haematobium and S. guineensis in the Republic of Benin. Scientific World J 793420:8. doi:10.1100/2012/793420

    Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Pitchford R (1965) Differences in the egg morphology and certain biological characteristics of some African and Middle Eastern schistosomes, genus Schistosoma, with terminal-spined eggs. Bull World Health Organ 32(1):105–120

    PubMed Central  CAS  PubMed  Google Scholar 

  • Richard-Lenoble D, Kombila M, Duong TH, Gendrel D (1993) Schistosoma intercalatum schistosomiasis. A recent and forgotten schistosomiasis. Revue du Praticien 43(4):432–439

    CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tchuem Tchuenté LA, Southgate VR, Njiokou F, Njiné T, Kouemeni LE, Jourdane J (1997) The evolution of schistosomiasis at Loum, Cameroon: replacement of Schistosoma intercalatum by S. haematobium through introgressive hybridization. T Roy Soc Trop Med Hyg 91(6):664–665

    Article  Google Scholar 

  • Webster BL, Tchuem Tchuenté LA, Southgate VR (2007) A single-strand conformation polymorphism (SSCP) approach for investigating genetic interactions of Schistosoma haematobium and Schistosoma guineensis in Loum, Cameroon. Parasitol Res 100(4):739–745

    Article  CAS  PubMed  Google Scholar 

  • Webster BL, Diaw OT, Seye MM, Webster JP, Rollinson D (2013) Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLoS Negl Trop Dis 7(4):e2110. doi:10.1371/journal.pntd.0002110

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the CNRS, UPVD, and WHO for their valuable financial support.

Consent

Written informed consent was obtained from the patient’s parents for the publication of this report.

Author information

Authors and Affiliations

  1. University Perpignan Via Domitia, IHPE UMR 5244, CNRS, IFREMER, University Montpellier, 58 avenue Paul Alduy, Bât. R, F-66860, Perpignan, France

    Hélène Moné, Jean-François Allienne, Jérôme Boissier, Guillaume Mitta & Gabriel Mouahid

  2. Tropical Medicine Unit, Department of Gastroenterology, Hepatology and Infectious Diseases, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany

    Martha C. Holtfreter & Joachim Richter

  3. Institut de Recherche en Écologie Tropicale (IRET)/CENAREST., BP 13354, Libreville, Gabon

    Rodrigue Mintsa-Nguéma

  4. Faculté des Sciences et Techniques, Université d’Abomey-Calavi, 01BP526, Cotonou, Benin

    Moudachirou Ibikounlé

  5. Service de Parasitologie-Mycologie, CHU Toulouse and Centre de Physiopathologie de Toulouse Purpan, INSERM U1043, CNRS UMR5282, Université de Toulouse, Toulouse, France

    Antoine Berry

Authors
  1. Hélène Moné
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martha C. Holtfreter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-François Allienne
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rodrigue Mintsa-Nguéma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Moudachirou Ibikounlé
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jérôme Boissier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Antoine Berry
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guillaume Mitta
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Joachim Richter
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gabriel Mouahid
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joachim Richter.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moné, H., Holtfreter, M.C., Allienne, JF. et al. Introgressive hybridizations of Schistosoma haematobium by Schistosoma bovis at the origin of the first case report of schistosomiasis in Corsica (France, Europe). Parasitol Res 114, 4127–4133 (2015). https://doi.org/10.1007/s00436-015-4643-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4643-4

Keywords

Search

Navigation