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Population genetics of Schistosoma haematobium: development of novel microsatellite markers and their application to schistosomiasis control in Mali

Published online by Cambridge University Press:  17 June 2011

C. M. GOWER ,
A. F. GABRIELLI ,
M. SACKO ,
R. DEMBELÉ ,
R. GOLAN ,
A. M. EMERY ,
D. ROLLINSON  and
J. P. WEBSTER
C. M. GOWER*
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine (St Mary's Campus), Norfolk Place, London W2 1PG, UK
A. F. GABRIELLI
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine (St Mary's Campus), Norfolk Place, London W2 1PG, UK
M. SACKO
Affiliation:
Institut National de Recherche en Santé Publique, Ministère de la Santé, Bamako, Mali; Service de Radiologie, Hôpital National du Point G, Bamako, Mali
R. DEMBELÉ
Affiliation:
Institut National de Recherche en Santé Publique, Ministère de la Santé, Bamako, Mali; Service de Radiologie, Hôpital National du Point G, Bamako, Mali
R. GOLAN
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine (St Mary's Campus), Norfolk Place, London W2 1PG, UK
A. M. EMERY
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
D. ROLLINSON
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
J. P. WEBSTER
Affiliation:
Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine (St Mary's Campus), Norfolk Place, London W2 1PG, UK
*
*Corresponding author: DIDE, School of Public Health, Imperial College Faculty of Medicine, St Mary's Campus, Norfolk Place, London W2 1PG. Tel: 020 7594 3819. E-mail: c.gower@imperial.ac.uk
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Summary

The recent implementation of mass drug administration (MDA) for control of uro-genital schistosomiasis has identified an urgent need for molecular markers to both directly monitor the impact of MDA, for example to distinguish re-infections from uncleared infections, as well as understand aspects of parasite reproduction and gene flow which might predict evolutionary change, such as the development and spread of drug resistance. We report the development of a novel microsatellite tool-kit allowing, for the first time, robust genetic analysis of individual S. haematobium larvae collected directly from infected human hosts. We genotyped the parasite populations of 47 children from 2 schools in the Ségou region of Mali, the first microsatellite study of this highly neglected parasite. There was only limited evidence of population subdivision between individual children or between the two schools, suggesting that few barriers to gene flow exist in this population. Complex relationships between parasite reproductive success, infection intensity and host age and gender were identified. Older children and boys harboured more diverse infections, as measured by the number of unique adult genotypes present. Individual parasite genotypes had variable reproductive success both across hosts, a pre-requisite for evolutionary selection, and, phenotypically, in hosts of different ages and genders. These data serve as a baseline against which to measure the effect of treatment on parasite population genetics in this region of Mali, and the tools developed are suitable to further investigate this important pathogen, and its close relatives, throughout their range.

Keywords

Schistosoma haematobiumdiversityneglected tropical diseasemicrosatelliteintensityparasitemonitoringevolution
Type
Research Article
Information
Parasitology , Volume 138 , Issue 8 , July 2011 , pp. 978 - 994
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Agola, L. E., Steinauer, M. L., Mburu, D. N., Mungai, B. N., Mwangi, I. N., Magoma, G. N., Loker, E. S. and Mkoji, G. M. (2009). Genetic diversity and population structure of Schistosoma mansoni within human infrapopulations in Mwea, central Kenya assessed by microsatellite markers. Acta Tropica 111, 219–225.CrossRefGoogle ScholarPubMed
Botros, S., Sayed, H., Amer, N., El-Ghannam, M., Bennett, J. L. and Day, T. A. (2005). Current status of sensitivity to praziquantel in a focus of potential drug resistance in Eygpt. International Journal for Parasitology 35, 787–791.CrossRefGoogle Scholar
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
Cavalli-Sforza, L. L. and Edwards, A. W. F. (1967). Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics 19, 233–257.Google ScholarPubMed
Chunge, R. N., Karumba, N., Ouma, J. H., Thiongo, F. W., Sturrock, R. F. and Butterworth, A. E. (1995). Polyparasitism in two rural communities with endemic Schistosoma mansoni infection in Mackakos district, Kenya. American Journal of Tropical Medicine and Hygiene 98, 440–444.Google ScholarPubMed
Criscione, C. D., Poulin, R. and Blouin, M. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257.CrossRefGoogle ScholarPubMed
Cunin, P., Tchuem Tchuente, L. A., Poste, B., Djibrilla, K. and Martin, P. M. (2003). Interactions between Schistosoma haematobium and Schistosoma mansoni in humans in north Cameroon. Tropical Medicine and International Health 8, 1110–1117.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, S51–59.CrossRefGoogle ScholarPubMed
Davies, C. M., Fairbrother, E. and Webster, J. P. (2002). Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 31–38.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, B 268, 251–257.CrossRefGoogle Scholar
Fenwick, A., Webster, J. P., Bosque-Oliva, E., Blair, L., Fleming, F. M., Zhang, Y., Garba, A., Stothard, J. R., Gabrielli, A. F., Clements, A. C. A., Kabatereine, N. B., Toure, S., Dembele, R., Nyandindi, U., Mwansa, J. and Koukounari, A. (2009). The Schistosomaisis Control Initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology 136, 1719–1730.CrossRefGoogle Scholar
Ferreira, M. U., Nair, S., Hyunh, T. V., Kawamoto, F. and Anderson, T. J. C. (2002). Microsatellite characterisation of Plasmodium falciparum from cerebral and uncomplicated malaria patients in Southern Vietnam. Journal of Clinical Microbiology 40, 1854–1857.CrossRefGoogle ScholarPubMed
Golan, R., Gower, C. M., Emery, A. M., Rollinson, D. and Webster, J. P. (2007). Isolation and characterization of the first polymorphic microsatellite markers for Schistosoma haematobium and their application in multiplex reactions of larval stages. Molecular Ecology Resources 8, 647–649.CrossRefGoogle Scholar
Goudet, J. (2002). FSTAT: A Computer Program to Calculate F Statistics. Version 2.9.3·2. http://www2.unil.ch/popgen/softwares/fstat.htm.Google Scholar
Gouvras, A. N. (2010). Intestinal and urinary schistosomiasis dynamics in sub-Saharan Africa. Ph.D. thesis. Imperial College, London, UK.Google Scholar
Gower, C. M., Shrivastava, J., Lamberton, P. H. L., Rollinson, D., Emery, A. M., Webster, B. L., Kabatereine, N. B. and Webster, J. P. (2007). Development and application of an ethical and epidemiologically appropriate assay for the multi-locus analysis of Schistosoma mansoni. Parasitology 134, 523–536.CrossRefGoogle Scholar
Gower, C. M. and Webster, J. P. (2004). Fitness of indirectly-transmitted pathogens: restraint and constraint. Evolution 58, 1178–1184.Google ScholarPubMed
Guo, S. and Thompson, E. (1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48, 361–372.CrossRefGoogle ScholarPubMed
Huyse, T., Webster, B. L., Gelhof, S., Stothard, J. R., Diaw, O. T., Polman, K. and Rollinson, D. (2009). Bidirectional introgressive hybridization between cattle and human schistosome species. PLos Pathogens 5, e1000571.CrossRefGoogle ScholarPubMed
Kane, R. A., Southgate, V. R., Rollinson, D., Littlewood, D. T., Lockyer, A. E., Pagès, J. R., Tchuem Tchuentè, L. A. and Jourdane, J. (2003). A phylogeny based on three mitochondrial genes supports the division of Schistosoma intercalatum into two separate species. Parasitology 127, 131–137.CrossRefGoogle ScholarPubMed
King, C. H., Blanton, R. E., Muchiri, E. M., Ouma, J. H., Kariuki, H. C., Mungai, P., Magak, P., Kadzo, H., Ireri, E. and Koech, D. K. (2004). Low heritable component of risk for infection intensity and infection-associated disease in urinary schistosomiasis among Wadigo village populations in Coast Province, Kenya. American Journal of Tropical Medicine and Hygiene 70, 57–62.CrossRefGoogle ScholarPubMed
Koukounari, A., Donnelly, C. A., Sacko, M., Keita, A. D., Landoure, A., Dembele, R., Bosque-Oliva, E., Gabrielli, A. F., Gouvras, A., Traore, M., Fenwick, A. and Webster, J. P. (2010). The impact of single versus mixed schistosome species infections on liver, spleen and bladder morbidity within Malian children pre- and post-praziquantel treatment. BMC Infectious Diseases 10, 227.CrossRefGoogle ScholarPubMed
Koukounari, A., Sacko, M., Keita, A. D., Gabrielli, A. F. and Landoure, A. (2006). Assessment of ultrasound morbidity indicators of schistosomiasis in the context of large-scale programs illustrated with experiences from Malian children. American Journal of Tropical Medicine and Hygiene 75, 1042–1052.CrossRefGoogle ScholarPubMed
Langella, O. (1999). Populations: 1.2.28 (23/5/2002). CNRS UPR9034.Google Scholar
Lewis, P. O. and Zaykin, D. (2001). Genetic Data Analysis: Computer Program for the Analysis of Allelic Data. Version 1.0 (d16c). http://lewis.eeb.uconn.edu/lewishome/software.html.Google Scholar
Lu, D. B., Rudge, J. W., Wang, T. P., Donnelly, C. A., Fang, G. R. and Webster, J. P. (2010). Transmission of Schistosoma japonicum in marshland and hilly regions of China: parasite population genetic and sibship structure. Plos Neglected Tropical Diseases 4, e781.CrossRefGoogle ScholarPubMed
Nelson, G. S. and Saoud, M. F. A. (1968). A comparison of the pathogenecity of two geographical strains of Schistosoma mansoni in rhesus monkeys. Journal of Helminthology 17, 339–362.CrossRefGoogle Scholar
Norton, A. J., Gower, C. M., Lamberton, P. H. L., Webster, B. L., Lwambo, N. J. S., Blair, L., Fenwick, A. and Webster, J. P. (2010). Genetic consequences of mass human chemotherapy for Schistosoma mansoni: population structure pre- and post-praziquantel treatment in Tanzania. American Journal of Tropical Medicine and Hygiene 83, 951–957.CrossRefGoogle ScholarPubMed
Rollinson, D. (2009). A wake up call for urinary schistosomiasis: reconciling research effort with public health importance. Parasitology 136, 1801–1811.CrossRefGoogle ScholarPubMed
Rudge, J. W., Carabin, H., Balolong, E. J., Tallo, V., Shrivastava, J., Lu, D-B., Basanez, M. G., Olveda, R., McGarvey, S. T. and Webster, J. P. (2008). Population genetics of Schistosoma japonicum within the Phillipines suggest high levels of transmission between humans and dogs. Plos Neglected Tropical Diseases 2, e340.CrossRefGoogle ScholarPubMed
Schneider, S., Roesli, D. and Excoffier, L. (2000). Arlequin Ver 2.0: A Software for Population Genetic Analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland.Google Scholar
Schwab, A. E., Churcher, T. S., Schwab, A. J., Basanez, M. G. and Pritchard, R. K. (2006). Population genetics of concurrent selection with albendazole and invermectin or diethylcarbamazine on the possible spread of albendazole resistance in Wuchereria bancrofti. Parasitology 133, 589–601.CrossRefGoogle ScholarPubMed
Shrivastava, J., Gower, C. M., Balolong, E. J., 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 naturally sampled larval stages. Parasitology 131, 617–626.CrossRefGoogle ScholarPubMed
Sire, C., Durand, P. and Pointier, J. P. (1999). Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. Journal of Parasitology 85, 436–441.CrossRefGoogle Scholar
Sorensen, R. E., Rodrigues, N. B., Oliveira, G., Romanha, A. J. and Minchella, D. J. (2006). Genetic filtering and optimal sampling of Schistosoma mansoni populations. Parasitology 133, 443–451.CrossRefGoogle ScholarPubMed
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Diseases 6, 411–425.CrossRefGoogle ScholarPubMed
Stothard, J. R., French, M. D., Khamis, I. S., Basanez, M. G. and Rollinson, D. (2009). The epidemiology and control of urinary schistosomiasis and soil-transmitted helminthiasis in schoolchildren on Unguja Island, Zanzibar. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 1031–1044.CrossRefGoogle ScholarPubMed
Thiongo, F. W., Madsen, H., Ouma, J. H., Andreassen, J. and Christensen, N. O. (1997). Host-parasite relationships in infections with two Kenyan isolates of Schistosoma mansoni in NMRI mice. Journal of Parasitology 83, 330–332.CrossRefGoogle ScholarPubMed
van der Werf, M. J., de Vlas, S. J., Brooker, S., Looman, C. W., Nagelkerke, N. J., Habbema, J. D. and Engels, D. (2003). Quantification of clincial morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica 86, 125–139.CrossRefGoogle Scholar
van Wyk, J. A. (2001). Refugia – overlooked as perhaps the most potent factor concerning the development of anthelminthich resistance. Onderstepoort Journal of Veterinary Research 68, 55–67.Google ScholarPubMed
Wang, J. (2004). Sibship reconstruction from genetic data with typing errors. Genetics 166, 1963–1979.CrossRefGoogle ScholarPubMed
Wang, J. and Whitlock, M. C. (2003). Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163, 429–446.CrossRefGoogle ScholarPubMed
Webster, B. L. (2009). Isolation and preservation of schistosome eggs and larvae in RNA later® facilitates genetic profiling of individuals. Parasite and Vectors 2, 50.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
Webster, J. P., Koukounari, A., Lamberton, P. H., Stothard, J. R. and Fenwick, A. (2009). Evaluation and application of potential schistosome-associated morbidity markers within large-scale mass chemotherapy programmes. Parasitology 136, 1789–1799.CrossRefGoogle ScholarPubMed
Webster, J. P., Oliveira, G., Rollinson, D. and Gower, C. M. (2010). Schistosome genomes: a wealth of information. Trends in Parasitology 26, 103–106.CrossRefGoogle ScholarPubMed
Zerlotini, A. and Oliveira, G. (2010). The contributions of the Genome Project to the study of schistosomiasis. Memorias do Insitituto Oswaldo Cruz 105, 367–369.CrossRefGoogle Scholar