Skip to main content

Cattle as natural host for Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 x Schistosoma bovis Sonsino, 1876 interactions, with new cercarial emergence and genetic patterns

Abstract

Schistosomiasis remains a parasitic infection which poses serious public health consequences around the world, particularly on the African continent where cases of introgression/hybridization between human and cattle schistosomiasis are being discovered on a more frequent basis in humans, specifically between Schistosoma haematobium and S. bovis. The aim of this paper is to analyze the occurrence of S. bovis in cattle and its relationship with S. haematobium in an area where cattle and humans share the same site in Benin (West Africa). We used the chronobiology of cercarial emergence as an ecological parameter and both molecular biology (COI mtDNA and ITS rDNA) of the larvae and morphology of the eggs as taxonomic parameters. The results showed a chronobiological polymorphism in the cercarial emergence rhythm. They showed for the first time the presence of S. bovis in Benin, the presence of introgressive hybridization between S. bovis and S. haematobium in domestic cattle, and the presence of atypical chronobiological patterns in schistosomes from cattle, with typical S. haematobium shedding pattern, double-peak patterns, and nocturnal patterns. Our results showed that the chronobiological life-history trait is useful for the detection of new hosts and also may reveal the possible presence of introgressive hybridization in schistosomes. Our results, for the first time, place cattle as reservoir host for S. haematobium and S. bovis x S. haematobium. The consequences of these results on the epidemiology of the disease, the transmission to humans, and the control of the disease are very important.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Abou M, Yabi I, Yolou I, Ogouwale E (2018) Caractérisation des systèmes de production sur les sites d’aménagements hydro-agricoles dans le doublet Dangbo-Adjohoun au sud du Bénin. Int J Biol Chem Sci 12:462–478

    Article  Google Scholar 

  • Alves W (1949) The eggs of Schistosoma bovis, S. mattheei and S. haematobium. J Helminthol 23:127–134

    CAS  PubMed  Article  Google Scholar 

  • Angora EK, Allienne J-F, Rey O, Menan H, Touré AO, Coulibaly JT, Raso G, Yavo W, N'Goran EK, Utzinger J, Balmer O, Boissier J (2019) High prevalence of Schistosoma haematobium× Schistosoma bovis hybrids in schoolchildren in Côte d'Ivoire. Parasitology 147:287–294

    PubMed  Article  CAS  Google Scholar 

  • Barber K, Mkoji G, Loker E (2000) PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. bovis from Kenya. Am J Trop Med Hyg 62:434–440

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  • 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, Mitta G (2016) Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study. Lancet Infect Dis. https://doi.org/10.1016/S1473-3099(16)00175-4

  • Boko PM, Ibikounlé M, Onzo-Aboki A, Tougoue J-J, Sissinto Y, Batcho W, Kindé-Gazard D, Kabore A (2016) Schistosomiasis and soil transmitted helminths distribution in Benin : a baseline prevalence survey in 30 districts. PLoS One 11:e0162798

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Boon NAM, Mbow M, Paredis L, Moris P, Sy I, Maes T, Webster BL, Sacko M, Volckaert FAM, Polman K, Huyse T (2019) No barrier breakdown between human and cattle schistosome species in the Senegal River Basin in the face of hybridisation. Int J Parasitol 49:1039–1048

    CAS  PubMed  Article  Google Scholar 

  • Brémond P, Sellin B, Sellin E, Naméoua B, Labbo R, Théron A, Combes C (1993) Arguments for the modification of the genome (introgression) of the human parasite Schistosoma haematobium by genes from S. bovis, in Niger. C R Acad Sci Série III, Sciences de la vie 316:667–670

    Google Scholar 

  • Brown DS (1994) Freshwater snails of Africa and their medical importance, revised 2nd edition. Taylor & Francis Ltd, London, pp 608

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

    CAS  PubMed  Article  Google Scholar 

  • Catalano S, Sene M, Diouf ND, Fall CB, Borlase A, Leger E, Ba K, Webster JP (2018) Rodents as natural hosts of zoonotic Schistosoma species and hybrids: an epidemiological and evolutionary perspective from West Africa. J Infect Dis 218:429–433

    PubMed  Article  Google Scholar 

  • Chitsulo L, Engels D, Montresor A, Savioli L (2000) The global status of schistosomiasis and its control. Acta Trop 77:41–51

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • De Bont J, Vercruysse J (1997) The epidemiology and control of cattle schistosomiasis. Parasitol Today 13:255–262

    PubMed  Article  Google Scholar 

  • De Bont J, Vercruysse J (1998) Schistosomiasis in cattle. Adv Parasitol 41:285–364

    PubMed  Article  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. https://doi.org/10.1186/1471-2148-10-8

    CAS  Article  PubMed  PubMed Central  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. Nucleic Acids Res 36(Web Server issue):W465–W469. https://doi.org/10.1093/nar/gkn180

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Engels D, Chitsulo L, Montresor A, Savioli L (2002) The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Trop 82:139–146

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Ibikounlé M, Moné H, Abou Y, Kinde-Gazard D, Sakiti NG, Mouahid G, Massougbodji A (2012) Premier cas de chronobiologie des émissions cercariennes de type infradien chez Schistosoma mansoni dans deux foyers du sud-Bénin. Int J Biol Chem Sci 6:1081–1089

    Google Scholar 

  • Ibikounlé M, Mouahid G, Mintsa-Nguema R, Sakiti N, Massougbodji A, Moné H (2013) Snail intermediate host/Schistosoma haematobium relationships from three transmission sites in Benin (West Africa). Parasitol Res 112:227–233

    PubMed  Article  Google Scholar 

  • Kéchemir N, Théron A (1997) Intraspecific variation in Schistosoma haematobium from Algeria. J Helminthol 71:29–33

    PubMed  Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. Mol Biol Evol 33:1870–1874

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Leger E, Garba A, Hamidou AA, Webster BL, Pennance T, Rollinson D, Webster JP (2016) Introgressed animal schistosomes Schistosoma curassoni and S. bovis naturally infecting humans. EID 22:2212

    Google Scholar 

  • Lockyer A, Olson P, Østergaard P, Rollinson D, Johnston D, Attwood S, Southgate V, Horak P, Snyder S, Le T (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126:203–224

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Mintsa-Nguema R, Moné H, Ibikounlé M, Mengué-Ngou-Milama K, Kombila M, Mouahid G (2014) Cercarial emergence pattern of Schistosoma haematobium from Libreville, Gabon. Parasite 21:3. https://doi.org/10.1051/parasite/2014004

    Article  PubMed  PubMed Central  Google Scholar 

  • Moné H, Holtfreter MC, Allienne J-F, Mintsa-Nguema R, Ibikounlé M, Boissier J, Berry A, Mitta G, Richter J, 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). Parasitol Res 114:4127–4133

    PubMed  Article  Google Scholar 

  • Moné H, Ibikounlé M, Massougbodji A, Mouahid G (2010) Human schistosomiasis in the Economic Community of West African States; epidemiology and control. Adv Parasitol 71:33–91

    Article  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. Sci World J 2012:793420

    Article  Google Scholar 

  • Moné H, Mouahid G, Morand S (1999) The distribution of Schistosoma bovis Sonsino, 1876 in relation to intermediate host mollusc-parasite relationships. Adv Parasitol 44:99–138

    PubMed  Article  Google Scholar 

  • Mouahid A, Théron A (1986) Schistosoma bovis: patterns of cercarial emergence from snails of the genera Bulinus and Planorbarius. Exp Parasitol 62:389–393

    CAS  PubMed  Article  Google Scholar 

  • Mouahid A, Théron A (1987) Schistosoma bovis: variability of cercarial production as related to the snail hosts: Bulinus truncatus, B. wrighti and Planorbarius metidjensis. Int J Parasitol 17:1431–1434

    CAS  PubMed  Article  Google Scholar 

  • Mouahid G, Idris MA, Verneau O, Théron A, Shaban MM, Moné H (2012) A new chronotype of Schistosoma mansoni: adaptive significance. Tropical Med Int Health 17:727–732

    CAS  Article  Google Scholar 

  • Mouahid A, Moné H, Arru E, Chassé J-L, Théron A, Combes C (1987) Analyse comparative du rythme d’émission des cercaires de trois souches de Schistosoma bovis. Parassitologia 29:79–85

    CAS  PubMed  Google Scholar 

  • Mouahid A, Moné H, Chaïb A, Théron A (1991) Cercarial shedding patterns of Schistosoma bovis and Schistosoma haematobium from single and mixed infections of Bulinus truncatus. J Helminthol 65:8–14

    CAS  PubMed  Article  Google Scholar 

  • Mouchet F, Théron A, Brémond P, Sellin E, Sellin B (1992) Pattern of cercarial emergence of Schistosoma curassoni from Niger and comparison with three sympatric species of schistosomes. J Parasitol 78:61–63

    CAS  PubMed  Article  Google Scholar 

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

    Google Scholar 

  • Onzo-Aboki A, Ibikounlé M, Boko PM, Savassi BS, Doritchamou J, Siko EJ, Daré A, Batcho W, Massougbodji A, Tougoue JJ (2019) Human Schistosomiasis in Benin: countrywide evidence of Schistosoma haematobium predominance. Acta Trop 191:185–197

    PubMed  Article  Google Scholar 

  • Pagès J, Théron A (1990) Analysis and comparison of cercarial emergence rhythms of Schistosoma haematobium, S. intercalatum, S. bovis, and their hybrid progeny. Int J Parasitol 20:193–197

    PubMed  Article  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 32:105–120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Platt RN, McDew-White M, Le Clec’h W, Chevalier F, Allan F, Emery AM, Garba A, Hamidou AA, Ame SM, Webster JP, Rollinson D, Webster BL, Anderson TJC (2019) Ancient hybridization and adaptive introgression of an invadolysin gene in schistosome parasites. Mol Biol Evol 36:2127–2142

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Raymond K, Probert AJ (1991) The daily cercarial emission rhythm of Schistosoma margrebowiei with particular reference to dark period stimuli. J Helminthol 65:159–168

    CAS  PubMed  Article  Google Scholar 

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

    CAS  Google Scholar 

  • Sang T, Crawford DJ, Stuessy TF (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proc Natl Acad Sci U S A 92:6813–6817

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Soentjens P, Cnops L, Huyse T, Yansouni C, De Vos D, Bottieau E, Clerinx J, Van Esbroeck M (2016) Diagnosis and clinical management of Schistosoma haematobiumSchistosoma bovis hybrid infection in a cluster of travelers returning from Mali. Clin Infect Dis 63:1626–1629

    PubMed  Article  Google Scholar 

  • Théron A, Combes C (1988) Genetic analysis of cercarial emergence rhythms of Schistosoma mansoni. Behavior Gen 18:201–209

    Article  Google Scholar 

  • Théron A, Mouahid G, Moné H (1997) Schistosoma mansoni : cercarial shedding patterns from a mixed infection of Biomphalaria glabrata with two (early and late) chronobiological variants. Parasitol Res 83:356–358

    PubMed  Article  Google Scholar 

  • Van den Broeck F, Geldof S, Polman K, Volckaert F, Huyse T (2011) Optimal sample storage and extraction procotols for reliable multilocus genotyping of the human parasite Schistosoma mansoni. Infect Genet Evol 11:1413–1418

    PubMed  Article  CAS  Google Scholar 

  • Webster BL, Southgate VR (2003) Compatibility of Schistosoma haematobium, S. intercalatum and their hybrids with Bulinus truncatus and B. forskalii. Parasitology 127:231–242

    CAS  PubMed  Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Webster BL, Rollinson D, Stothard JR, Huyse T (2010) Rapid diagnostic multiplex PCR (RD-PCR) to discriminate Schistosoma haematobium and S. bovis. J Helminthol 84(107):114

    Google Scholar 

  • World Health Organization (2019) Schistosomiasis. Fact sheet 17 April 2019

  • Wright C, Ross G (1980) Hybrids between Schistosoma haematobium and S. mattheei and their identification by isoelectric focusing of enzymes. Trans R Soc Trop Med Hyg 74:326–332

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

We would like to thank M. Marius CODJO, chief of Kessounou village and all the breeders and also M. Jean-Pierre TOKPO, Director of Kessounou school and all the schoolchildren for their participation to the study.

Funding

This research was funded by the French Ministry of Foreign Affairs, the “Laboratoire Mixte International” (Mixed International Laboratory) on the project CONS-HELM « Infections helminthiques: traitements et conséquences sur la santé et le développement au Sud », and the French National Agency for Research (ANR) [grant ANR-17-CE12-0005-01] CHRONOGET and CNRS. BS is a student fellow from the SCAC (Service de Coopération et d’Action Culturelle), French Embassy in Benin; CL is a student fellow from the Occitanie Region, France.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Hélène Moné, Gabriel Mouahid, Moudachirou Ibikounlé.

Material preparation, data collection and analysis: Boris A.E.S. Savassi, Gabriel Mouahid, Chrystelle Lasica, Samoussou-Dine K. Mahaman, Jean-François Allienne, Moudachirou Ibikounlé, Hélène Moné.

Funding acquisition: Gabriel Mouahid, André Garcia, David Courtin, Moudachirou Ibikounlé, Hélène Moné.

Investigation: Boris A.E.S. Savassi, Gabriel Mouahid, Chrystelle Lasica, Samoussou-Dine K. Mahaman, Jean-François Allienne, Moudachirou Ibikounlé, Hélène Moné.

Methodology: Hélène Moné, Gabriel Mouahid, Moudachirou Ibikounlé.

Project administration: Gabriel Mouahid, André Garcia, David Courtin, Moudachirou Ibikounlé, Hélène Moné.

Resources: Boris A.E.S. Savassi, Gabriel Mouahid, Chrystelle Lasica, Samoussou-Dine K. Mahaman, André Garcia, David Courtin, Jean-François Allienne, Moudachirou Ibikounlé, Hélène Moné.

Supervision: Gabriel Mouahid, Hélène Moné.

Validation: Gabriel Mouahid, Hélène Moné.

Visualization: Gabriel Mouahid, Hélène Moné.

Writing–original draft: Boris A.E.S. Savassi, Gabriel Mouahid, Hélène Moné.

Writing–review & editing: Boris A.E.S. Savassi, Gabriel Mouahid, Chrystelle Lasica, André Garcia, David Courtin, Jean-François Allienne, Moudachirou Ibikounlé, Hélène Moné.

All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hélène Moné.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Ethical permission (No119, 17/07/2019/CER-ISBA) was obtained from the Ethic Committee of the « Institut des Sciences Biomédicales Appliquées, Faculté de Médecine, Université d’Abomey-Calavi, 01BP526, Cotonou, Benin.

Informed consent

The Director of Kessounou school obtained informed consent from the parents of all the schoolchildren who participated to the study.

Data set availability

Sequence data were deposited in the NCBI GenBank database under the accession numbers MT159589 to MT159601 for COI mtDNA and MT158872 to MT158882 for ITS rDNA.

Additional information

Section Editor: Hiroshi Sato

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Savassi, B.A., Mouahid, G., Lasica, C. et al. Cattle as natural host for Schistosoma haematobium (Bilharz, 1852) Weinland, 1858 x Schistosoma bovis Sonsino, 1876 interactions, with new cercarial emergence and genetic patterns. Parasitol Res 119, 2189–2205 (2020). https://doi.org/10.1007/s00436-020-06709-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06709-0

Keywords

  • Schistosoma bovis
  • Schistosoma haematobium
  • Introgressive hybridization
  • Cercarial emergence pattern
  • Cattle
  • Benin