Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-23T06:45:56.773Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantial genetic diversity within Lake Albert and Lake Victoria populations

Published online by Cambridge University Press:  23 July 2009

J. R. STOTHARD ,
B. L. WEBSTER ,
T. WEBER ,
S. NYAKAANA ,
J. P. WEBSTER ,
F. KAZIBWE ,
N. B. KABATEREINE  and
D. ROLLINSON
J. R. STOTHARD*
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, London, SW7 5BD, UK
B. L. WEBSTER
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, London, SW7 5BD, UK
T. WEBER
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, London, SW7 5BD, UK Department of Infectious Disease Epidemiology, Imperial College London, Norfolk Place, London W2 1PG, UK
S. NYAKAANA
Affiliation:
Institute of Environment and Natural Resources (Genetics Laboratory), Makerere University, Kampala, Uganda
J. P. WEBSTER
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College London, Norfolk Place, London W2 1PG, UK
F. KAZIBWE
Affiliation:
Vector Control Division, Ministry of Health, Kampala, Uganda
N. B. KABATEREINE
Affiliation:
Vector Control Division, Ministry of Health, Kampala, Uganda
D. ROLLINSON
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, London, SW7 5BD, UK
*
*Corresponding author: J. Russell Stothard. Tel: +44 207 942 5490. Fax: +44 207 942 5518. E-mail: R.Stothard@nhm.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Representative samples of Ugandan Schistosoma mansoni from Lake Albert and Lake Victoria were examined using DNA barcoding, sequence analysis of two partially overlapping regions – ASMIT (396 bp) & MORGAN (617 bp) – of the mitochondrial cytochrome oxidase subunit I (cox1). The Victorian sample exhibited greater nucleotide diversity, 1·4% vs. 1·0%, and a significant population partition appeared as barcodes did not cross-over between lakes. With one exception, Lake Albert populations were more mixed by sampled location, while those from Lake Victoria appeared more secluded. Using statistical parsimony, barcode ASMIT 1 was putatively ancestral to all others and analysis of MORGAN cox1 confirmed population diversity. All samples fell into two of five well-resolved lineages; sub-lineages therein broadly partitioning by lake. It seems that barcode ASMIT 1 (and close variants) was likely widely dispersed throughout the Nilotic environment but later diversified in situ, and in parallel, within Lake Albert and Lake Victoria. The genetic uniformity of Ugandan S. mansoni can no longer be assumed, which might better explain known epidemiological heterogeneities. While it appears plausible that locally evolved heritable traits could spread through most of the Lake Albert populations, it seems unlikely they could quickly homogenise into Lake Victoria or amongst populations therein.

Keywords

schistosomiasisSchistosoma mansoniDNA barcodingphylogeographycox1controlpraziquantelUganda
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. 1813 - 1824
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

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
Besansky, N. J., Severson, D. W. and Ferdig, M. T. (2003). DNA barcoding of parasites and invertebrate disease vectors: what you don't know can hurt you. Trends in Parasitology 19, 545–546.CrossRefGoogle ScholarPubMed
Blair, D., Le, T. H., Despres, L. and McManus, D. P. (1999). Mitochondrial genes of Schistosoma mansoni. Parasitology 119, 303–313.CrossRefGoogle ScholarPubMed
Brown, D. S. (1994). Freshwater Snails of Africa and their Medical Importance, 2nd edn., London, Taylor and Francis.CrossRefGoogle Scholar
Clement, M., Posada, D. and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.CrossRefGoogle ScholarPubMed
de Moira, A. P., Fulford, A. J. C., Kabatereine, N. B., Kazibwe, F., Ouma, J. H., Dunne, D. W. and Booth, M. (2007). Microgeographical and tribal variations in water contact and Schistosoma mansoni exposure within a Ugandan fishing community. Tropical Medicine and International Health 12, 724–735.CrossRefGoogle Scholar
Dunne, D. W., Vennervald, B. J., Booth, M., Joseph, S., Fitzsimmons, C. M., Cahen, P., Sturrock, R. F., Ouma, J. H., Mwatha, J. K., Kimani, G., Kariuki, H. C., Kazibwe, F., Tukahebwa, E. and Kabatereine, N. B. (2006). Applied and basic research on the epidemiology, morbidity, and immunology of schistosomiasis in fishing communities on Lake Albert, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 216–223.CrossRefGoogle ScholarPubMed
Frezal, L. and Leblois, R. (2008). Four years of DNA barcoding: current advances and prospects. Infection Genetics and Evolution 8, 727–736.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
Jannotti-Passos, L. K., Souza, C. P., Parra, J. C. and Simpson, A. J. G. (2001). Biparental mitochondrial DNA inheritance in the parasitic trematode Schistosoma mansoni. Journal of Parasitology 87, 79–82.CrossRefGoogle ScholarPubMed
John, R., Ezekiel, M., Philbert, C. and Andrew, A. (2008). Schistosomiasis transmission at high altitude crater lakes in Western Uganda. BMC Infectious Diseases 8, 110–116.CrossRefGoogle ScholarPubMed
Jorgensen, A., Kristensen, T. K. and Stothard, J. R. (2007). Phylogeny and biogeography of African Biomphalaria (Gastropoda: Planorbidae), with emphasis on endemic species of the great East African lakes. Zoological Journal of the Linnean Society 151, 337–349.CrossRefGoogle Scholar
Kabatereine, N. B., Brooker, S., Koukounari, A., Kazibwe, F., Tukahebwa, E. M., Fleming, F. M., Zhang, Y. B., Webster, J. P., Stothard, J. R. and Fenwick, A. (2007). Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bulletin of the World Health Organization 85, 91–99.Google ScholarPubMed
Kabatereine, N. B., Brooker, S., Tukahebwa, E. M., Kazibwe, F. and Onapa, A. W. (2004). Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control. Tropical Medicine and International Health 9, 372–380.CrossRefGoogle ScholarPubMed
Kabatereine, N. B., Tukahebwa, E., Kazibwe, F., Namwangye, H., Zaramba, S., Brooker, S., Stothard, J. R., Kamenka, C., Whawell, S., Webster, J. P. and Fenwick, A. (2006). Progress towards countrywide control of schistosomiasis and soil-transmitted helminthiasis in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 208–215.CrossRefGoogle ScholarPubMed
Kane, R. A. and Rollinson, D. (1994). Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheei. Molecular and Biochemical Parasitology 63, 153–156.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, 15CrossRefGoogle Scholar
Koukounari, A., Fenwick, A., Whawell, S., Kabatereine, N. B., Kazibwe, F., Tukahebwa, E. M., Stothard, J. R., Donnelly, C. A. and Webster, J. P. (2006). Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. American Journal of Tropical Medicine and Hygiene 75, 278–286.CrossRefGoogle ScholarPubMed
Le, T. H., Blair, D., Agatsuma, T., Humair, P. F., Campbell, N. J. H., Iwagami, M., Littlewood, D. T. J., Peacock, B., Johnston, D. A., Bartley, J., Rollinson, D., Herniou, E. A., Zarlenga, D. S. and McManus, D. P. (2000). Phylogenies inferred from mitochondrial gene orders – a cautionary tale from the parasitic flatworms. Molecular Biology and Evolution 17, 1123–1125.CrossRefGoogle Scholar
Morgan, J. A. T., Dejong, R. J., Adeoye, G. O., Ansa, E. D. O., 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. S., Kazibwe, F., Kpikpi, J., Lwambo, N. J. S., Mabaye, A., Magalhaes, L. A., Makundi, A., Mone, H., Mouahid, G., Muchemi, G. M., Mungai, B. N., Sene, M., Southgate, V., Tchuente, L. A. T., Theron, A., Yousif, F., Magalhaes, E. M. Z., 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. T., 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. T., 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, S211–S228.CrossRefGoogle ScholarPubMed
Odogwu, S. E., Ramamurthy, N. K., Kabatereine, N. B., Kazibwe, F., Tukahebwa, E., Webster, J. P., Fenwick, A. and Stothard, J. R. (2006). Schistosoma mansoni in infants (aged <3 years) along the Ugandan shoreline of Lake Victoria. Annals of Tropical Medicine and Parasitology 100, 315–326.CrossRefGoogle ScholarPubMed
Odongo-Aginya, E. I., Grigull, L., Schweigmann, U., Loroni-Lakwo, T., Enrich, J. H. H., Gryseels, B. and Doehring, E. (2002). High prevalence and morbidity of Schistosoma mansoni along the Albert Nile in Uganda. African Health Science 2, 99–106.Google ScholarPubMed
Pitchford, R. J. and Visser, P. S. (1975). A simple and rapid technique for quantitative estimation of helminth eggs in human and animal excreta with special reference to Schistosoma sp. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 318–322.CrossRefGoogle ScholarPubMed
Plam, M., Jorgensen, A., Kristensen, T. K. and Madsen, H. (2008). Sympatric Biomphalaria species (Gastropoda: Planorbidae) in Lake Albert, Uganda, show homoplasies in shell morphology. African Zoology 43, 34–44.CrossRefGoogle Scholar
Smithers, S. R. and Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695–700.CrossRefGoogle ScholarPubMed
Stensgaard, A. S., Jorgensen, A., Kabatereine, N. B., Rahbek, C. and Kristensen, T. K. (2006). Modeling freshwater snail habitat suitability and areas of potential snail-borne disease transmission in Uganda. Geospatial Health 1, 93–104.CrossRefGoogle ScholarPubMed
Stothard, J. R. and Gabrielli, A. F. (2007 a). Schistosomiasis in African infants and preschool children: to treat or not to treat? Trends in Parasitology 23, 83–86.CrossRefGoogle ScholarPubMed
Stothard, J. R. and Gabrielli, A. F. (2007 b). Response to Johansen et al.: Leave children untreated and sustain inequity! Trends in Parasitology 23, 569–570.CrossRefGoogle Scholar
Stothard, J. R. and Rollinson, D. (1997). Partial DNA sequences from the mitochondrial cytochrome oxidase subunit I (COI) gene can differentiate the intermediate snail hosts Bulinus globosus and B. nasutus (Gastropoda: Planorbidae). Journal of Natural History 31, 727–737.CrossRefGoogle Scholar
Webster, J. P., Gower, C. M. and Norton, A. J. (2008). Evolutionary concepts in predicting and evaluating the impact of mass chemotherapy schistosomiasis control programmes on parasites and their hosts. Evolutionary Applications 1, 66–83.CrossRefGoogle ScholarPubMed
WHO (2008). World Health Statistics 2008. Geneva, Switzerland. ISBN 978 92 4 156359 8 (NLM classification: WA 900.1).Google Scholar
Zarowlecki, M. Z., 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 Scholar
Zhang, Y., Koukounari, A., Kabatereine, N., Fleming, F., Kazibwe, F., Tukahebwa, E., Stothard, J. R., Webster, J. P. and Fenwick, A. (2007). Parasitological impact of 2-year preventive chemotherapy on schistosomiasis and soil-transmitted helminthiasis in Uganda. BMC Medicine 5, 11–22.CrossRefGoogle ScholarPubMed