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Hydrological modelling of snail dispersal patterns in Msambweni, Kenya and potential resurgence of Schistosoma haematobium transmission

Published online by Cambridge University Press:  11 December 2006

J. A. CLENNON*
Affiliation:
Department of Pathobiology, University of Illinois, 2001 South Lincoln Avenue, Urbana, Illinois 61801, USA
C. H. KING
Affiliation:
Center for Global Health and Diseases, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, Ohio 44106, USA
E. M. MUCHIRI
Affiliation:
Division of Vector Borne Diseases, Ministry of Health, Nairobi, Kenya
U. KITRON
Affiliation:
Department of Pathobiology, University of Illinois, 2001 South Lincoln Avenue, Urbana, Illinois 61801, USA
*
*Corresponding author and current address: Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, 615 North Wolfe Street, Baltimore, MD 21205, USA. Tel: +410 955 3708. Fax: +410 955 0105. E-mail: jclennon@jhsph.edu

Summary

Urinary schistosomiasis is an important source of human morbidity in Msambweni, Kenya, where the intermediate host snail, Bulinus nasutus is found in ponds and water pools. In the past, aquatic habitats in the area have been studied separately; however, recent collections of B. nasutus snails and shells indicated that many of these ponds are in fact connected during and following sufficient rains. Satellite imagery and a geographical information system (GIS) were used to survey the main water courses and potential drainage routes, to locate potential source populations of snails and to determine probable snail dispersal routes. The 2 water bodies implicated as being the most important Schistosoma haematobium transmission foci in the area were found to differ in their degree of connectivity to other B. nasutus source habitats. One pond becomes connected even after normal rains, while the other pond requires prolonged rains or flooding to become connected with source habitats. Consequently, the transmission foci differ in their susceptibility to snail population control measures. Spatially explicit dispersal models that consider the spatial and temporal patterns of connectivity between aquatic habitats will contribute to improved snail surveillance and more focused control for urinary schistosomiasis at a local level.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

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References

REFERENCES

Abdel-Rahman, M. S., El-Bahy, M. M., Malone, J. B., Thompson, R. A. and El Bahy, N. M. (2001). Geographic information systems as a tool for control program management for schistosomiasis in Egypt. Acta Tropica 79, 4957. DOI: 10.1016/S0001-706X(01)00102-4CrossRefGoogle ScholarPubMed
Brown, D. (1994). Freshwater Snails of Africa and Their Medical Importance. Taylor and Francis Ltd, London.CrossRefGoogle Scholar
Bavia, M. E., Hale, L. F., Malone, J. B., Braud, D. H. and Shane, S. M. (1999). Geographic information systems and the environmental risk of schistosomiasis in Bahia, Brazil. American Journal of Tropical Medicine and Hygiene 60, 566572.CrossRefGoogle ScholarPubMed
Bavia, M. E., Malone, J. B., Hale, L., Dantas, A., Marroni, L. and Reis, R. (2001). Use of thermal and vegetation index data from earth observing satellites to evaluate the risk of schistosomiasis in Bahia, Brazil. Acta Tropica 79, 7985. DOI: 10.1016/S0001-706X(01)00105-XCrossRefGoogle ScholarPubMed
Bergquist, R., Malone, J. B. and Kristensen, T. K. (2000). Schistosomiasis information systems and control of snail-borne diseases. Parasitology Today 16, 363364. DOI: 10.1016/S0169-4758(00)01745-2CrossRefGoogle ScholarPubMed
Chlyeh, G., Henry, P. Y., Sourrouille, P., Delay, B., Khallaayoune, K. and Jarne, P. (2002). Population genetics and dynamics at short spatial scale in Bulinus truncatus, the intermediate host of Schistosoma haematobium in Morocco. Parasitology 125, 349357. doi: 10.1017/S0031182002002123CrossRefGoogle ScholarPubMed
Clennon, J. A., King, C. H., Muchiri, E. M., Kariuki, H. C., Ouma, J. H., Mungai, P. and Kitron, U. (2004). Spatial patterns of urinary schistosomiasis infection in a highly endemic area of coastal Kenya. American Journal of Tropical Medicine and Hygiene 70, 443448.CrossRefGoogle Scholar
Cummins, R. H. (1994). Taphonomic processes in modern freshwater molluscan death assemblages: Implications for the fossil record. Palaeogeography, Palaeoclimatology, Palaeoecology 108, 5573.CrossRefGoogle Scholar
Donnelly, F. A., Appleton, C. C. and Schutte, C. H. J. (1983). The influence of salinity on certain aspects of the biology of Bulinus (Physopsis) africanus. International Journal for Parasitology 13, 539545.CrossRefGoogle ScholarPubMed
Garbrecht, J. and Martz, L. W. (1997). The assignment of drainage direction over flat surfaces in raster digital elevation models. Journal of Hydrology 193, 204213.CrossRefGoogle Scholar
Gracio, M. A. A. (1988). A comparative laboratory study of Bulinus (Physopsis) globosus uninfected and infected with Schistosoma haematobium. Malacological Review 21, 123127.Google Scholar
Guo, J. G., Vounatsou, P., Cao, C. L., Utzinger, J., Zhu, H. Q., Anderegg, D., Zhu, R., He, Z. Y., Li, D., Hu, F., Chen, M. G. and Tanner, M. (2005). A geographic information and remote sensing based model for prediction of Oncomelania hupensis habitats in the Poyang Lake area, China. Acta Tropica 96, 213222. DOI: 10.1016/j.actatropica.2005.07.029CrossRefGoogle 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, 765773.CrossRefGoogle Scholar
Jordon, P. and Webbe, G. (1993). Epidemiology. In Human Schistosomiasis, (ed.Jordon, P., Webbe, G. and Sturrock, R. F.), pp. 87158. CAB International, Oxon, UK.Google Scholar
Kariuki, H. C., Clennon, J. A., Brady, M. S., Kitron, U., Sturrock, R. F., Ouma, J. H., Ndzovu, S. T. M., Mungai, P., Hoffman, O., Hamburger, J., Pellegrini, C., Muchiri, E. M. and King, C. H. (2004). Distribution patterns and cercarial shedding of Bulinus nasutus and other snails in the Msambweni area, coast province, Kenya. American Journal of Tropical Medicine and Hygiene 70, 449456.CrossRefGoogle ScholarPubMed
King, C. H., Muchiri, E., Ouma, J. H. and Koech, D. (1991). Chemotherapy-based control of schistosomiasis haematobia. IV. Impact of repeated annual chemotherapy on prevalence and intensity of Schistosoma haematobium infection in an endemic area of Kenya. American Journal of Tropical Medicine and Hygiene 45, 498508.CrossRefGoogle Scholar
Kitron, U. (2000). Risk maps: Transmission and burden of vector borne diseases. Parasitology Today 16, 324325.CrossRefGoogle ScholarPubMed
Kitron, U., Clennon, J. A., Gürtler, R. E., King, C. K., Cecere, M. C., Vázquez-Prokopec, G., Thornhill, J. and Beck, L. (2006). Application of fine resolution satellite data to spatial analysis and control of infectious diseases: Schistosomiasis in Kenya and Chagas disease in Argentina. In Remote Sensing and the Control of Infectious Diseases: Proceedings from an Interamerican Workshop (ed.Confalonieri, U. E. C. and Marinho, D. P.). SOLGRAF Publisher, Rio de Janeiro.Google Scholar
Malone, J. B., Huh, O. K., Fehler, D. P., Wilson, P. A., Wilensky, D. E., Holmes, R. A. and Elmagdoub, A. I. (1994). Temperature data from satellite imagery and the distribution of schistosomiasis in Egypt. American Journal of Tropical Medicine and Hygiene 50, 714722.CrossRefGoogle ScholarPubMed
Marti, H. P., Tanner, M., Degremont, A. A. and Freyvogel, T. A. (1985). Studies on the ecology of Bulinus globosus, the intermediate host of Schistosoma haematobium in the Ifakara Area, Tanzania. Acta Tropica 42, 171187.Google ScholarPubMed
Maszle, D. R., Whitehead, P. G., Johnson, R. C. and Spear, R. C. (1998). Hydrological studies of schistosomiasis transport in Sichuan Province, China. Science of the Total Environment 216, 193203.CrossRefGoogle ScholarPubMed
Mavarez, J., Amarista, M., Pointier, J. P. and Jarne, P. (2002). Fine-scale population structure and dispersal in Biomphalaria glabrata, the intermediate snail host of Schistosoma mansoni, in Venezuela. Molecular Ecology 11, 879889.CrossRefGoogle ScholarPubMed
McCullough, F. S., Eyakuze, V. M., Msinde, J. and Nditi, H. (1968). Water resources and bilharziasis transmission in the Misungwi area, Mwanza District, north-west Tanzania. East African Medical Journal 45, 295308.Google ScholarPubMed
Muchiri, E. M., Ouma, J. H. and King, C. H. (1996). Dynamics and control of Schistosoma haematobium transmission in Kenya: An overview of the Msambweni Project. American Journal of Tropical Medicine and Hygiene 55, 127134.CrossRefGoogle ScholarPubMed
Mzuga, J. M., Tole, M. P. and Ukakuwun, E. K. (1998). The impact of geology and pit latrines on groundwater quality in Kwale District. In Dunes, Groundwater, Mangroves and Birdlife in Coastal Kenya Coastal Ecology Series No. 4 (ed.Hoorweg, J.), pp. 8596. Moi University, Eldoret.Google Scholar
O'Keefe, J. H. (1985). Population biology of the freshwater snail Bulinus globosus on the Kenya coast: I. Population fluctuations in relation to climate. Journal of Applied Ecology 22, 7384.CrossRefGoogle Scholar
Rock, B. N., Vogelmann, J. E., Williams, D. L., Vogelmann, A. F. and Hoshizaki, T. (1986). Remote detection of forest damage. BioScience 36, 439445.CrossRefGoogle 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, S245S260. doi: 10.1017/S0031182001008046CrossRefGoogle ScholarPubMed
Satayathum, S. A., Muchiri, E. M., Ouma, J. H., Whalen, C. C. and King, C. H. (2006). Factors affecting infection or reinfection with schistosoma haematobium in coastal Kenya: survival analysis during a nine-year, school-based treatment program. American Journal of Tropical Medicine and Hygiene 75, 8392.CrossRefGoogle ScholarPubMed
Shaman, J. and Day, J. F. (2005). Achieving operational hydrologic monitoring of mosquitoborne disease. Emerging Infectious Diseases 11, 13431350.CrossRefGoogle ScholarPubMed
Shaman, J., Stieglitz, M., Stark, C., Le Blancq, S. and Cane, M. (2002). Using a dynamic hydrology model to predict mosquito abundances in flood and swamp water. Emerging Infectious Diseases 8, 613.CrossRefGoogle ScholarPubMed
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water development: systematic review, meta-analysis, and estimates of people at risk. The Lancet Infectious Diseases 6, 411425.CrossRefGoogle ScholarPubMed
Stothard, J. R., Loxton, N., Rollinson, D., Mgeni, A. F., Khamis, S., Ameri, H., Ramsan, M. and Savioli, L. (2000). The transmission status of Bulinus on Zanzibar Island (Unguja), with implications for control of urinary schistosomiasis. Annals of Tropical Medical Parasitology 94, 8794.CrossRefGoogle ScholarPubMed
Stothard, J. R., Bremond, P., Andriamaro, L., Sellin, B., Sellin, E. and Rollinson, D. (2001). Bulinus species on Madagascar: molecular evolution, genetic markers and compatibility with Schistosoma haematobium. Parasitology 123, S261S275.CrossRefGoogle ScholarPubMed
Stothard, J. R., Llewellyn-Hughes, J., Griffin, C. E., Hubbard, S. J., Kristensen, T. K. and Rollinson, D. (2002 b). Identification of snails within the Bulinus africanus group from East Africa by multiplex SNaPshot (TM) analysis of single nucleotide polymorphisms within the cytochrome oxidase subunit I. Memorias do Instituto Oswaldo Cruz 97, 3136.CrossRefGoogle Scholar
Stothard, J. R., Mgeni, A. F., Khamis, S., Seto, E., Ramsan, M. and Rollinson, D. (2002 a). Urinary schistosomiasis in schoolchildren on Zanzibar Island (Unguja), Tanzania: a parasitological survey supplemented with questionnaires. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 507514.CrossRefGoogle ScholarPubMed
Sturrock, R. F., Kinyanjui, H., Thiongo, F. W., Tosha, S., Ouma, J. H., King, C. H., Koech, D., Siongok, T. K. and Mahmoud, A. A. (1990). Chemotherapy-based control of schistosomiasis haematobia. 3. Snail studies monitoring the effect of chemotherapy on transmission in the Msambweni area, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 257261.CrossRefGoogle ScholarPubMed
Sturrock, R. F. (1993). The intermediate hosts and host-parasite relationships. In Human Schistosomiasis (ed.Jordan, P., Webbe, G. and Sturrock, R. F.), pp. 3385. CAB International, Oxon, UK.Google Scholar
Tarboton, D. G. (1997). A new method for the determination of flow directions and upslope areas in grid digital elevation models. Water Resources Research 33, 309319.CrossRefGoogle Scholar
Thomas, J. D. and Tait, A. I. (1984). Control of the snail hosts of schistosomiasis by environmental manipulation – a field and laboratory appraisal in the Ibadan Area, Nigeria. Philosophical Transactions of the Royal Society of London, Series B 305, 201253.Google ScholarPubMed
Utzinger, J., Mayombana, C., Smith, T. and Tanner, M. (1997). Spatial microhabitat selection by Biomphalaria pfeifferi in a small perennial river in Tanzania. Hydrobiologica 356, 5360.CrossRefGoogle Scholar
Utzinger, J. and Tanner, M. (2000). Microhabitat preferences of Biomphalaria pfeifferi and Lymnaea natalensis in a natural and a man-made habitat in Southeastern Tanzania. Memorias do Instituto Oswaldo Cruz 95, 287294.CrossRefGoogle Scholar
Webbe, G. and Msangi, A. S. (1958). Observations on three species of Bulinus on the east coast of Africa. Annals of Tropical Medicine and Parasitology 52, 302314.CrossRefGoogle ScholarPubMed
Woolhouse, M. E. J. (1992). Population biology of the fresh-water snail Biomphalaria pfeifferi in the Zimbabwe Highveld. Journal of Applied Ecology 29, 687694.CrossRefGoogle Scholar
Zhang, Z. Y., Xu, D. Z., Zhou, X. N., Zhou, Y. and Liu, S. J. (2005). Remote sensing and spatial statistical analysis to predict the distribution of Oncomelania hupensis in the marshlands of China. Acta Tropica 96, 205212. DOI: 10.1016/j.actatropica.2005.07.027CrossRefGoogle Scholar
Zhou, X. N., Malone, J. B., Kristensen, T. K. and Bergquist, N. R. (2001). Application of geographic information systems and remote sensing to schistosomiasis control in China. Acta Tropica 79, 97106. DOI: 10.1016/S0001-706X(01)00107-3CrossRefGoogle ScholarPubMed
Zhou, X., Dandan, L., Huiming, Y., Honggen, C., Leping, S., Guojing, Y., Qingbiao, H., Brown, L. and Malone, J. B. (2002). Use of landsat TM satellite surveillance data to measure the impact of the 1998 flood on snail intermediate host dispersal in the lower Yangtze River Basin. Acta Tropica 82, 199205. DOI: 10.1016/S0001-706X(02)00011-6CrossRefGoogle ScholarPubMed