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Genetic diversity of schistosomes and snails: implications for control

Published online by Cambridge University Press:  27 July 2009

DAVID ROLLINSON ,
JOANNE P. WEBSTER ,
BONNIE WEBSTER ,
SILVESTER NYAKAANA ,
ASLAK JØRGENSEN  and
J. RUSSELL STOTHARD
DAVID ROLLINSON*
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, LondonSW7 5BD, UK
JOANNE P. WEBSTER
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London, W2 1PG
BONNIE WEBSTER
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, LondonSW7 5BD, UK
SILVESTER NYAKAANA
Affiliation:
Makerere University, P.O. Box 7062, Kampala, Uganda
ASLAK JØRGENSEN
Affiliation:
DBL Parasitology, Health and Development, University of Copenhagen, Thorvaldsensvej 57, 1871 Frederiksburg C, Denmark
J. RUSSELL STOTHARD
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, LondonSW7 5BD, UK
*
*Corresponding author: David Rollinson, Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, LondonSW7 5BD, UK. Tel: +44 20 7942 518. Fax: +44 20 7942 5518. E-mail: [email protected]
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Summary

Molecular approaches are providing new insights into the genetic diversity of schistosomes and their intermediate snail hosts. For instance, molecular tools based on the polymerase chain reaction are being developed for the diagnosis of schistosomiasis and the detection of prepatent schistosome infections in snails at transmission sites. Robust phylogenies of the different species of Schistosoma, Bulinus and Biomphalaria have been determined and novel methods are available to identify the different and cryptic taxa involved. Microsatellite analyses and mitochondrial DNA sequencing methods have been developed and are contributing to a better understanding of the genetic structure of both schistosome and snail populations. New sampling procedures to capture DNA of eggs and larval stages of schistosomes in field situations are facilitating more detailed and ethically advantageous studies on parasite heterogeneity. Knowledge of the genetic diversity of schistosome and snail populations adds a further dimension to the monitoring and surveillance of disease, and the implementation of new molecular-based approaches will be of increasing importance in helping to assess the impact of schistosomiasis control strategies.

Keywords

SchistosomessnailsMtDNAmicrosatellitesdiagnosispopulation geneticscontrolAfrica
Type
SECTION 4 MONITORING AND EVALUATION OF INTERVENTIONS
Information
Parasitology , Volume 136 , Special Issue 13: Control of schistosomiasis in sub-Saharan Africa , November 2009 , pp. 1801 - 1811
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Abbasi, I., King, C. H., Sturrock, R. F., Kariuki, C., Muchiri, E. and Hamburger, J. (2007). Differentiation of Schistosoma haematobium from related schistosomes by PCR amplifying an inter-repeat sequence. American Journal of Tropical Medicine and Hygiene 76, 950–955.CrossRefGoogle ScholarPubMed
Agatsuma, T., Iwagami, M., Liu, C. X., Rajapakse, R. P., Mondal, M. M., Kitikoon, V., Ambu, S., Agatsuma, Y., Blair, D. and Higuchi, T. (2002). Affinities between Asian non-human Schistosoma species, the group, and the African human schistosomes. Journal of Helminthology 76, 7–19.CrossRefGoogle Scholar
Agola, L. E., Mburu, D. N., DeJong, R. J., Mungai, B. N., Muluvi, G. M., Njagi, E. N., Loker, E. S. and Mkoji, G. M. (2006). Microsatellite typing reveals strong genetic structure of Schistosoma mansoni from localities in Kenya. Infection Genetics and Evolution 6, 484–490.CrossRefGoogle ScholarPubMed
ANON, (2007). A turning point for neglected tropical disease control. Lancet 369, 1404.CrossRefGoogle Scholar
Balen, J., Stothard, J. R., Kabatereine, N. B., Tukahebwa, E. M., Kazibwe, F., Whawell, S., Webster, J. P., Utzinger, J. and Fenwick, A. (2006). Morbidity due to Schistosoma mansoni: an epidemiological assessment of distended abdomen syndrome in Ugandan school children with observations before and 1-year after anthelminthic chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 1039–1048.CrossRefGoogle ScholarPubMed
Barber, K. E., Mkoji, G. M. and Loker, E. S. (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, 434–440.CrossRefGoogle ScholarPubMed
Blair, L., Webster, J. P. and Barker, G. C. (2001). Isolation and characterization of polymorphic microsatellite markers in Schistosoma mansoni from Africa. Molecular Ecology Notes 1, 93–95.CrossRefGoogle Scholar
Bogh, H. O., Zhu, X. Q., Qian, B. Z. and Gasser, R. B. (1999). Scanning for nucleotide variations in mitochondrial DNA fragments of Schistosoma japonicum by single-strand conformation polymorphism. Parasitology 118, 73–82.CrossRefGoogle ScholarPubMed
Boisier, P., Ramarokoto, C. E., Ravoniarimbinina, P., Rabarijaona, L. and Ravaoalimalala, V. E. (2001). Geographic differences in hepatosplenic complications of schistosomiasis mansoni and explanatory factors of morbidity. Tropical Medicine and International Health 6, 699–706.CrossRefGoogle ScholarPubMed
Brant, S. V. and Loker, E. S. (2005). Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS Pathogens 1, 167–169.CrossRefGoogle ScholarPubMed
Brouwer, K. C., Ndhlovu, P. D., Wagatsuma, Y., Munatsi, A. and Shiff, C. J. (2003). Urinary tract pathology attributed to Schistosoma haematobium: Does parasite genetics play a role? American Journal of Tropical Medicine and Hygiene 68, 456–462.CrossRefGoogle ScholarPubMed
Curtis, J., Sorensen, R. E. and Minchella, D. J. (2002). Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology 125 (Suppl), S51–S59.CrossRefGoogle ScholarPubMed
Davies, C. M., Webster, J. P. and Woolhouse, M. E. J. (2001). Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proceedings of the Royal Society of London Series B-Biological Sciences 268, 251–257.CrossRefGoogle Scholar
Durand, P., Sire, C. and Theron, A. (2000). Isolation of microsatellite markers in the digenetic trematode Schistosoma mansoni from Guadeloupe island. Molecular Ecology 9, 997–998.CrossRefGoogle ScholarPubMed
Gasser, R. B. (1998). What's in that band? International Journal for Parasitology 28, 989–996.CrossRefGoogle ScholarPubMed
Golan, R., Gower, C. M., Emery, A. M., Rollinson, D., and Webster, J. P. (2008). Isolation and characterization of the first polymorphic microsatellite markers for Schistosoma haematobium and their application in multiplex reactions. Molecular Ecology Resources 8, 647–649.CrossRefGoogle ScholarPubMed
Gomes, A. L., Melo, F. L., Werkhauser, R. P. and Abath, F. G. (2006). Development of a real time polymerase chain reaction for quantitation of Schistosoma mansoni DNA. Memorias do Instituto Oswaldo Cruz 101 (Suppl 1), 133–136.CrossRefGoogle ScholarPubMed
Gower, C. M., Shrivastava, J., Lamberton, P. H. L., Rollinson, D., Webster, B. L., Emery, A., Kabatereine, N. B. and Webster, J. P. (2007). Development and application of an ethically and epidemiologically advantageous assay for the multi-locus microsatellite analysis of Schistosoma mansoni. Parasitology 134, 523–536.CrossRefGoogle ScholarPubMed
Hamburger, J., He, N., Xin, X. Y., Ramzy, R. M., Jourdane, J. and Ruppel, A. (1998 a). A polymerase chain reaction assay for detecting snails infected with bilharzia parasites (Schistosoma mansoni) from very early prepatency. American Journal of Tropical Medicine and Hygiene 59, 872–876.CrossRefGoogle ScholarPubMed
Hamburger, J., Xu, Y. X., Ramzy, R. M., Jourdane, J. and Ruppel, A. (1998 b). Development and laboratory evaluation of a polymerase chain reaction for monitoring Schistosoma mansoni infestation of water. American Journal of Tropical Medicine and Hygiene 59, 468–473.CrossRefGoogle ScholarPubMed
Hamburger, J., Hoffman, O., Kariuki, H. C., Muchiri, E. M., Ouma, J. H., Koech, D. K., Sturrock, R. F. and King, C. H. (2004). Large-scale, polymerase chain reaction-based surveillance of Schistosoma haematobium DNA in snails from transmission sites in coastal Kenya: a new tool for studying the dynamics of snail infection. American Journal of Tropical Medicine and Hygiene 71, 765–773.CrossRefGoogle Scholar
Jørgensen, A., Kristensen, T. K. and Stothard, J. R. (2007). Phylogeny and biogeography of African Biomphalaria (Gastropoda: Planorbidae) with special emphasis on the endemic species of the great East African lakes. Zoological Journal of the Linnean Society 151, 337–349.CrossRefGoogle Scholar
Jolly, E., Chin, C., Miller, S., Baghat, M., Lim, K., DeRisis, J. and McKerrow, J. (2007). Gene expression patterns during adaptation of a parasite helminth to different environmental niches. Genome Biology 8, R65.CrossRefGoogle ScholarPubMed
Kane, R. A., Bartley, J., Stothard, J. R., Vercruysse, J., Rollinson, D. and Southgate, V. R. (2002). Application of single strand conformational polymorphism (SSCP) analysis with fluorescent primers for differentiation of Schistosoma haematobium group species. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 235–241.CrossRefGoogle ScholarPubMed
Kane, R. A., Stothard, J. R., Emery, A. M. and Rollinson, D. (2008). Molecular characterization of freshwater snails in the genus Bulinus: a role for barcodes? Parasites and Vectors 1:15 doi:10.1186/1756-3305-1-15.CrossRefGoogle ScholarPubMed
King, C. H., Sturrock, R. F., Kariuki, H. C. and Hamburger, J. (2006). Transmission control for schistosomiasis – why it matters now. Trends in Parasitology 22, 575–582.CrossRefGoogle ScholarPubMed
Le, T. H., Blair, D. and McManus, D. P. (2000). Mitochondrial DNA sequences of human schistosomes: the current status. International Journal for Parasitology 30, 283–290.CrossRefGoogle ScholarPubMed
Le, T. H., Blair, D. and McManus, D. P. (2002 a). Revisiting the question of limited genetic variation within Schistosoma japonicum. Annals of Tropical Medicine and Parasitology 96, 155–164.CrossRefGoogle ScholarPubMed
Le, T. H., Blair, D. and McManus, D. P. (2002 b). Mitochondrial genomes of parasitic flatworms. Trends in Parasitology 18, 206–213.CrossRefGoogle ScholarPubMed
Le, T. H., Humair, P. F., Blair, D., Agatsuma, T., Littlewood, D. T. and McManus, D. P. (2001). Mitochondrial gene content, arrangement and composition compared in African and Asian schistosomes. Molecular and Biochemical Parasitology 117, 61–71.CrossRefGoogle ScholarPubMed
Lier, T., Simonsen, G. S., Haaheim, H., Hjelmevoll, S. O., Vennervald, B. J. and Johansen, M. V. (2006). Novel real-time PCR for detection of Schistosoma japonicum in stool. South East Asian Journal of Tropical Medicine and Public Health 37, 257–264.Google ScholarPubMed
Littlewood, D. T., Lockyer, A. E., Webster, B. L., Johnston, D. A. and Le, T. H. (2006). The complete mitochondrial genomes of Schistosoma haematobium and Schistosoma spindale and the evolutionary history of mitochondrial genome changes among parasitic flatworms. Molecular Phylogenetics and Evolution 39, 452–467.CrossRefGoogle ScholarPubMed
Lockyer, A. E., Olson, P. D., Ostergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., Southgate, V. R., Horak, P., Snyder, S. D., Le, T. H., Agatsuma, T., McManus, D. P., Carmichael, A. C., Naem, S. and Littlewood, D. T. J. (2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203–224.CrossRefGoogle ScholarPubMed
Lockyer, A. E., Spinks, J., Noble, L. R., Rollinson, D. and Jones, C. S. (2007). Identification of genes involved in interactions between Biomphalaria glabrata and Schistosoma mansoni by suppression subtractive hybridization. Molecular and Biochemical Parasitology 151, 18–27.CrossRefGoogle ScholarPubMed
Melo, F. L., Gomes, A. L., Barbosa, C. S., Werkhauser, R. P. and Abath, F. G. (2006). Development of molecular approaches for the identification of transmission sites of schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 1049–1055.CrossRefGoogle ScholarPubMed
Morgan, J. A., Dejong, R. J., Adeoye, G. O., Ansa, E. D., Barbosa, C. S., Bremond, P., Cesari, I. M., Charbonnel, N., Correa, L. R., Coulibaly, G., D'Andrea, P. S., De Souza, C. P., Doenhoff, M. J., File, S., Idris, M. A., Incani, R. N., Jarne, P., Karanja, D. M., Kazibwe, F., Kpikpi, J., Lwambo, N. J., Mabaye, A., Magalhaes, L. A., Makundi, A., Mone, H., Mouahid, G., Muchemi, G. M., Mungai, B. N., Sene, M., Southgate, V. R., Tchuente, L. A. T., Theron, A., Yousif, F., Zanotti-Magalhaes, E. M., Mkoji, G. M. and Loker, E. S. (2005). Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology 14, 3889–3902.CrossRefGoogle ScholarPubMed
Morgan, J. A., DeJong, R. J., Kazibwe, F., Mkoji, G. M. and Loker, E. S. (2003). A newly-identified lineage of Schistosoma. International Journal for Parasitology 33, 977–985.CrossRefGoogle ScholarPubMed
Morgan, J. A., Dejong, R. J., Snyder, S. D., Mkoji, G. M. and Loker, E. S. (2001). Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology 123 (Suppl), S211–S228.CrossRefGoogle ScholarPubMed
Prugnolle, F., De Meeus, T., Durand, P., Sire, C. and Theron, A. (2002). Sex-specific genetic structure in Schistosoma mansoni: evolutionary and epidemiological implications. Molecular Ecology 11, 1231–1238.CrossRefGoogle ScholarPubMed
Prugnolle, F., Theron, A., Durand, P. and De Meeus, T. (2004). Test of pangamy by genetic analysis of Schistosoma mansoni pairs within its natural murine host in Guadeloupe. Journal of Parasitology 90, 507–509.CrossRefGoogle ScholarPubMed
Quinnell, R. J. (2003). Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33, 1219–1231.CrossRefGoogle ScholarPubMed
Rodrigues, N. B., Coura Filho, P., de Souza, C. P., Jannoti Passos, L. K., Dias-Neto, E. and Romanha, A. J. (2002). Populational structure of Schistosoma mansoni assessed by DNA microsatellites. International Journal for Parasitology 32, 843–851.CrossRefGoogle ScholarPubMed
Rollinson, D. and Southgate, V. R. (1987). The genus Schistosoma: a taxonomic appraisal. In The Biology of Schistosomes: from Genes to Latrines (eds. Rollinson, D. and Simpson, A. J. G.), pp. 1–49, London: Academic Press.Google Scholar
Rollinson, D., Stothard, J. R. and Southgate, V. R. (2001). Interactions between intermediate snail hosts of the genus Bulinus and schistosomes of the Schistosoma haematobium group. Parasitology 123, S245–S260.CrossRefGoogle ScholarPubMed
Rudge, J. W., Carabin, H., Balolong, E. Jr., Tallo, V., Shrivastava, J., Lu, D-B, Basáñez, M-G, Olveda, R., McGarvey, S. T. and Webster, J. P. (2008). Population genetics of Schistosoma japonicum within the Philippines suggest high levels of transmission between humans and dogs. PloS Neglected Tropical Diseases 2: e340.CrossRefGoogle ScholarPubMed
Rudge, J. W., Lu, D-B, Feng, G-W, Wang, T-P, Basáñez, M-G. and Webster, J. P. (2009). Parasite genetic differentiation by host species and habitat type: molecular epidemiology of Schistosoma japonicum in hilly and marshland areas of Anhui Province, China. Molecular Ecology 18, 2134–47.CrossRefGoogle ScholarPubMed
Sandoval, N., Siles-Lucas, M., Lopez Aban, J., Perez-Arellano, J. L., Garate, T. and Muro, A. (2006 a). Schistosoma mansoni: a diagnostic approach to detect acute schistosomiasis infection in a murine model by PCR. Experimental Parasitology 114, 84–88.CrossRefGoogle Scholar
Sandoval, N., Siles-Lucas, M., Perez-Arellano, J. L., Carranza, C., Puente, S., Lopez-Aban, J. and Muro, A. (2006 b). A new PCR-based approach for the specific amplification of DNA from different Schistosoma species applicable to human urine samples. Parasitology 133, 581–587.CrossRefGoogle ScholarPubMed
Sene, M., Southgate, V. R. and Vercruysse, J. (2004). Bulinus truncatus, intermediate host of Schistosoma haematobium in the Senegal River Basin (SRB)]. Bulletin de la Societe de Pathologie Exotique 97, 29–32.Google ScholarPubMed
Shrivastava, J., Barker, G. C., Johansen, M. V., Xiaonong, Z., Aligui, G. D., McGarvey, S. T. and Webster, J. P. (2003). Isolation and characterization of polymorphic DNA microsatellite markers from Schistosoma japonicum. Molecular Ecology Notes 3, 406–408.CrossRefGoogle Scholar
Shrivastava, J., Gower, C. M., Balolong, E. Jr., Wang, T. P., Qian, B. Z. and Webster, J. P. (2005). Population genetics of multi-host parasites – the case for molecular epidemiological studies of Schistosoma japonicum using larval stages from naturally infected hosts. Parasitology 131, 617–626.CrossRefGoogle ScholarPubMed
Southgate, V. R., de Clercq, D., Sene, M., Rollinson, D., Ly, A. and Vercruysse, J. (2000). Observations on the compatibility between Bulinus spp. and Schistosoma haematobium in the Senegal River basin. Annals of Tropical Medicine and Parasitology 94, 157–164.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Agola, L. E., Mwangi, I. N., Mkoji, G. M. and Loker, E. S. (2008 a). Molecular epidemiology of Schistosoma mansoni: A robust, high-throughput method to assess multiple microsatellite markers from individual miracidia. Infection, Genetics and Evolution 8, 68–73.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Hanelt, B., Mwangi, I. N., Maina, G. M., Agola, L. E., Kinthuia, J. M., Mutuku, M. W., Mungal, B. N., Wilson, W. D., Mkoji, G. M. and Loker, E. S. (2008 b). Introgressive hybridization of human and rodent schistosome parasites in western Kenya. Molecular Ecology 17, 5062–5074.CrossRefGoogle ScholarPubMed
Stothard, J. R., Bartley, J., Griffin, C. S., Hubbard, S. J., Kristensen, T. K. and Rollinson, D. (2002 a). Identification of snails within the Bulinus africanus group from East Africa by multiplex SNaPshot™ analysis of single nucleotide polymorphisms within the cytochrome oxidase subunit I. Memorias do Instituto Oswaldo Cruz. 97, 31–36.CrossRefGoogle ScholarPubMed
Stothard, J. R. and Gabrielli, A. F. (2007). Schistosomiasis in African infants and preschool children: to treat or not to treat? Trends in Parasitology 23, 83–86.CrossRefGoogle ScholarPubMed
Stothard, J. R., Mgeni, A. F., Khamis, S., Seto, E., Ramsan, M., Hubbard, S. J., Kristensen, T. K. and Rollinson, D. (2002 b). New insights into the transmission biology of urinary schistosomiasis in Zanzibar. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 470–475.CrossRefGoogle ScholarPubMed
Suzuki, T., Osada, Y., Kumagai, T., Hamada, A., Okuzawa, E. and Kanazawa, T. (2006). Early detection of Schistosoma mansoni infection by touchdown PCR in a mouse model. Parasitology International 55, 213–218.CrossRefGoogle ScholarPubMed
Ten Hove, R. J., Verweij, J. C., 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, 179–185.CrossRefGoogle ScholarPubMed
Van de Vijver, K. K., Colpaert, C. G., Jacobs, W., Kuypers, K., Hokke, C. H., Deelder, A. M. and Van Marck, E. A. (2006). The host's genetic background determines the extent of angiogenesis induced by schistosome egg antigens. Acta Tropica 99, 243–251.CrossRefGoogle ScholarPubMed
Wang, T. P., Shrivastava, J., Johansen, M. V., Zhang, S. Q., Wang, F. F. and Webster, J. P. (2006). Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host species. International Journal for Parasitology 36, 1317–1325.CrossRefGoogle ScholarPubMed
Webster, B. L., Rollinson, D., Stothard, J. R. and Huyse, T. (2009). Rapid diagnostic multiplex PCR (RDPCR) to discriminate Schistosoma haematobium and S. bovis. Journal of Helminthlogy. In pressGoogle ScholarPubMed
Webster, B. L., Southgate, V. R. and Littlewood, D. T. (2006). A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. International Journal for Parasitology 36, 947–955.CrossRefGoogle ScholarPubMed
Webster, B. L., Tchuente, L. A. T., Jourdane, J. and Southgate, V. R. (2005). The interaction of Schistosoma haematobium and S. guineensis in Cameroon. Journal of Helminthology 79, 193–197.CrossRefGoogle ScholarPubMed
Webster, B. L., Tchuente, L. A. T. and Southgate, V. R. (2007). A single-strand conformation polymorphism (SSCP) approach for investigating genetic interactions of Schistosoma haematobium and Schistosoma guineensis in Loum, Cameroon. Parasitology Research 100, 739–745.CrossRefGoogle ScholarPubMed
Wilson, R. A., Ashton, P. D., Braschi, S., Dillon, G. P., Berriman, M. and Ivens, A. (2007). ‘Oming’ in on schistosomes: prospects and limitations for post-genomics. Trends in Parasitology 23, 14–20.CrossRefGoogle Scholar
Zarowiecki, M., Huyse, T. and Littlewood, D. T. J. (2007). Making the most of mitochondrial genomes – markers for phylogeny, molecular ecology and barcodes in Schistosoma (Platyhelminthes: Digenea). International Journal for Parasitology 37, 1401–1418.CrossRefGoogle ScholarPubMed
Zhang, S. M., Adema, C. M., Kepler, T. B. and Loker, E. S. (2004). Diversification of Ig superfamily genes in an invertebrate. Science 305, 251–254.CrossRefGoogle Scholar