Skip to main content Accessibility help
×
Home

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

  • C. M. GOWER (a1), A. F. GABRIELLI (a1), M. SACKO (a2), R. DEMBELÉ (a2), R. GOLAN (a1), A. M. EMERY (a3), D. ROLLINSON (a3) and J. P. WEBSTER (a1)...

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.

Copyright

Corresponding author

*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

References

Hide All
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, 219225.
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, 787791.
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, 456462.
Cavalli-Sforza, L. L. and Edwards, A. W. F. (1967). Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics 19, 233257.
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, 440444.
Criscione, C. D., Poulin, R. and Blouin, M. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 22472257.
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, 11101117.
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, S5159.
Davies, C. M., Fairbrother, E. and Webster, J. P. (2002). Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 3138.
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, 251257.
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, 17191730.
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, 18541857.
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, 647649.
Goudet, J. (2002). FSTAT: A Computer Program to Calculate F Statistics. Version 2.9.3·2. http://www2.unil.ch/popgen/softwares/fstat.htm.
Gouvras, A. N. (2010). Intestinal and urinary schistosomiasis dynamics in sub-Saharan Africa. Ph.D. thesis. Imperial College, London, UK.
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, 523536.
Gower, C. M. and Webster, J. P. (2004). Fitness of indirectly-transmitted pathogens: restraint and constraint. Evolution 58, 11781184.
Guo, S. and Thompson, E. (1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48, 361372.
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.
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, 131137.
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, 5762.
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.
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, 10421052.
Langella, O. (1999). Populations: 1.2.28 (23/5/2002). CNRS UPR9034.
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.
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.
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, 339362.
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, 951957.
Rollinson, D. (2009). A wake up call for urinary schistosomiasis: reconciling research effort with public health importance. Parasitology 136, 18011811.
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.
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.
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, 589601.
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, 617626.
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, 436441.
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, 443451.
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, 411425.
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, 10311044.
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, 330332.
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, 125139.
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, 5567.
Wang, J. (2004). Sibship reconstruction from genetic data with typing errors. Genetics 166, 19631979.
Wang, J. and Whitlock, M. C. (2003). Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163, 429446.
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.
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, 6683.
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, 17891799.
Webster, J. P., Oliveira, G., Rollinson, D. and Gower, C. M. (2010). Schistosome genomes: a wealth of information. Trends in Parasitology 26, 103106.
Zerlotini, A. and Oliveira, G. (2010). The contributions of the Genome Project to the study of schistosomiasis. Memorias do Insitituto Oswaldo Cruz 105, 367369.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed