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Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution

Published online by Cambridge University Press:  11 November 2009

J. UTZINGER*
Affiliation:
Department of Public Health and Epidemiology, Swiss Tropical Institute, P.O. Box, CH–4002 Basel, Switzerland
G. RASO
Affiliation:
Division of Epidemiology and Social Medicine, School of Population Health, The University of Queensland, Public Health Building, Herston Road, Brisbane, Queensland 4006, Australia Molecular Parasitology Laboratory, Queensland Institute of Medical Research, 300 Herston Road, Brisbane, Queensland 4006, Australia Centre Suisse de Recherches Scientifiques, 01 BP 1303, Abidjan 01, Côte d'Ivoire
S. BROOKER
Affiliation:
Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London WC1E 7HT, United Kingdom Malaria Public Health and Epidemiology Group, KEMRI/Wellcome Trust Research Programme, P.O. Box 43640–00100, Nairobi, Kenya
D. DE SAVIGNY
Affiliation:
Department of Public Health and Epidemiology, Swiss Tropical Institute, P.O. Box, CH–4002 Basel, Switzerland
M. TANNER
Affiliation:
Department of Public Health and Epidemiology, Swiss Tropical Institute, P.O. Box, CH–4002 Basel, Switzerland
N. ØRNBJERG
Affiliation:
DBL – Centre for Health Research and Development, Faculty of Life Sciences, University of Copenhagen, Thorvaldsensvej 57, DK-1871 Frederiksberg C, Denmark
B. H. SINGER
Affiliation:
Office of Population Research, Princeton University, Princeton, NJ 08544, USA
E. K. N'GORAN
Affiliation:
Centre Suisse de Recherches Scientifiques, 01 BP 1303, Abidjan 01, Côte d'Ivoire UFR Biosciences, Université d'Abidjan-Cocody, 22 BP 582, Abidjan 22, Côte d'Ivoire
*
*Corresponding author: Jürg Utzinger, Department of Public Health and Epidemiology, Swiss Tropical Institute, P.O. Box, CH–4002 Basel, Switzerland. Tel.: +41 61 284-8129; Fax: +41 61 284-8105; E-mail: juerg.utzinger@unibas.ch

Summary

In May 2001, the World Health Assembly (WHA) passed a resolution which urged member states to attain, by 2010, a minimum target of regularly administering anthelminthic drugs to at least 75% and up to 100% of all school-aged children at risk of morbidity. The refined global strategy for the prevention and control of schistosomiasis and soil-transmitted helminthiasis was issued in the following year and large-scale administration of anthelminthic drugs endorsed as the central feature. This strategy has subsequently been termed ‘preventive chemotherapy’. Clearly, the 2001 WHA resolution led the way for concurrently controlling multiple neglected tropical diseases. In this paper, we recall the schistosomiasis situation in Africa in mid-2003. Adhering to strategic guidelines issued by the World Health Organization, we estimate the projected annual treatment needs with praziquantel among the school-aged population and critically discuss these estimates. The important role of geospatial tools for disease risk mapping, surveillance and predictions for resource allocation is emphasised. We clarify that schistosomiasis is only one of many neglected tropical diseases and that considerable uncertainties remain regarding global burden estimates. We examine new control initiatives targeting schistosomiasis and other tropical diseases that are often neglected. The prospect and challenges of integrated control are discussed and the need for combining biomedical, educational and engineering strategies and geospatial tools for sustainable disease control are highlighted. We conclude that, for achieving integrated and sustainable control of neglected tropical diseases, a set of interventions must be tailored to a given endemic setting and fine-tuned over time in response to the changing nature and impact of control. Consequently, besides the environment, the prevailing demographic, health and social systems contexts need to be considered.

Type
SECTION 5 TOWARDS FUTURE USE OF PRAZIQUANTEL
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Adamson, P. B. (1976). Schistosomiasis in antiquity. Medical History 20, 176188.Google Scholar
Baltussen, R. (2006). Priority setting of public spending in developing countries: do not try to do everything for everybody. Health Policy 78, 149156.Google Scholar
Bergquist, R., Johansen, M. V. and Utzinger, J. (2009). Diagnostic dilemmas in helminthology: what tools to use and when? Trends in Parasitology 25, 151156.Google Scholar
Bergquist, R., Utzinger, J. and McManus, D. P. (2008). Trick or treat: the role of vaccines in integrated schistosomiasis control. PLoS Neglected Tropical Diseases 2, e244.Google Scholar
Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., Lacerda, D., Macedo, C. D., McVeigh, P., Ning, Z., Oliveira, G., Overington, J. P., Parkhill, J., Pertea, M., Pierce, R. J., Protasio, A. V., Quail, M. A., Rajandream, M. A., Rogers, J., Sajid, M., Salzberg, S. L., Stanke, M., Tivey, A. R., White, O., Williams, D. L., Wortman, J., Wu, W., Zamanian, M., Zerlotini, A., Fraser-Liggett, C. M., Barrell, B. G. and El-Sayed, N. M. (2009). The genome of the blood fluke Schistosoma mansoni. Nature 460, 352358.Google Scholar
Bliss, K. E. (2009). Enhancing U.S. leadership on drinking water and sanitation: opportunities within global health programs. A report of the CSIS Global Health Policy Center. Centre for Strategic and International Studies, Washington, D.C.Google Scholar
Brady, M. A., Hooper, P. J. and Ottesen, E. A. (2006). Projected benefits from integrating NTD programs in sub-Saharan Africa. Trends in Parasitology 22, 285291.Google Scholar
Brooker, S. and Clements, A. C. A. (2009). Spatial heterogeneity of parasite co-infection: determinants and geostatistical prediction at regional scales. International Journal for Parasitology 39, 591597.Google Scholar
Brooker, S., Kabatereine, N. B., Fleming, F. and Devlin, N. (2008). Cost and cost-effectiveness of nationwide school-based helminth control in Uganda: intra-country variation and effects of scaling-up. Health Policy and Planning 23, 2435.Google Scholar
Brooker, S., Kabatereine, N. B., Gyapong, J. O., Stothard, J. R. and Utzinger, J. (2009 a). Rapid mapping of schistosomiasis and other neglected tropical diseases in the context of integrated control programmes in Africa. Parasitology 136, 17071718.Google Scholar
Brooker, S., Kabatereine, N. B., Smith, J. L., Mupfasoni, D., Mwanje, M. T., Ndayishimiye, O., Lwambo, N. J. S., Mbotha, D., Karanja, P., Mwandawiro, C., Muchiri, E., Clements, A. C. A., Bundy, D. A. P. and Snow, R. W. (2009 b). An updated atlas of human helminth infections: the example of East Africa. International Journal of Health Geographics 8, 42.Google Scholar
Brooker, S. and Utzinger, J. (2007). Integrated disease mapping in a polyparasitic world. Geospatial Health 1, 141146.Google Scholar
Bundy, D. A. P., Shaeffer, S., Jukes, M., Beegle, K., Gillespie, A., Drake, L., Lee, S. H. F., Hoffman, A. M., Jones, J., Mitchell, A., Wright, C., Barcelona, D., Camara, B., Golmar, C., Savioli, L., Takeuchi, T. and Sembene, M. (2006). School based health and nutrition programs. In Disease Control Priorities for Developing Countries (Ed. Breman, J. G., Measham, A. R., Alleyne, G., Claeson, M., Evans, D., Jha, P., Mills, A. and Musgrove, P.), Oxford University Press, Oxford, pp. 10911108.Google Scholar
Clements, A. C. A., Bosque-Oliva, E., Sacko, M., Landoure, A., Dembele, R., Traore, M., Coulibaly, G., Gabrielli, A. F., Fenwick, A. and Brooker, S. (2009). A comparative study of the spatial distribution of schistosomiasis in Mali in 1984–1989 and 2004–2006. PLoS Neglected Tropical Diseases 3, e431.Google Scholar
Clements, A. C. A., Garba, A., Sacko, M., Toure, S., Dembele, R., Landoure, A., Bosque-Oliva, E., Gabrielli, A. F. and Fenwick, A. (2008). Mapping the probability of schistosomiasis and associated uncertainty, West Africa. Emerging Infectious Diseases 14, 16291632.Google Scholar
Clements, A. C. A., Lwambo, N. J. S., Blair, L., Nyandindi, U., Kaatano, G., Kinung'hi, S., Webster, J. P., Fenwick, A. and Brooker, S. (2006). Bayesian spatial analysis and disease mapping: tools to enhance planning and implementation of a schistosomiasis control programme in Tanzania. Tropical Medicine and International Health 11, 490503.Google Scholar
Colley, D. G., LoVerde, P. T. and Savioli, L. (2001). Medical helminthology in the 21st century. Science 293, 14371438.Google Scholar
Colley, D. G. and Secor, W. E. (2004). Immunoregulation and World Health Assembly resolution 54.19: why does treatment control morbidity? Parasitology International 53, 143150.Google Scholar
Davis, A. (2009). Schistosomiasis. In Manson's Tropical Diseases (Ed. Cook, G. C. and Zumla, A. I.), Saunders, Elsevier, pp. 14251460.Google Scholar
El-Khoby, T., Galal, N., Fenwick, A., Barakat, R., El-Hawey, A., Nooman, Z., Habib, M., Abdel-Wahab, F., Gabr, N. S., Hammam, H. M., Hussein, M. H., Mikhail, N. N., Cline, B. L. and Strickland, G. T. (2000). The epidemiology of schistosomiasis in Egypt: summary findings in nine governorates. American Journal of Tropical Medicine and Hygiene 62 (2 Suppl.), 8899.Google Scholar
Engels, D., Chitsulo, L., Montresor, A. and Savioli, L. (2002). The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Tropica 82, 139146.Google Scholar
Fenwick, A. (2006). Waterborne infectious diseases – could they be consigned to history? Science 313, 10771081.Google Scholar
Fenwick, A., Savioli, L., Engels, D., Bergquist, N. R. and Todd, M. H. (2003). Drugs for the control of parasitic diseases: current status and development in schistosomiasis. Trends in Parasitology 19, 509515.Google 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., Kabatereine, N. B., Toure, S., Dembele, R., Nyandindi, U., Mwansa, J. and Koukounari, A. (2009). The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology 136, 17191730.Google Scholar
Finkelstein, J. L., Schleinitz, M. D., Carabin, H. and McGarvey, S. T. (2008). Decision-model estimation of the age-specific disability weight for schistosomiasis japonica: a systematic review of the literature. PLoS Neglected Tropical Diseases 2, e158.Google Scholar
French, M. D., Rollinson, D., Basáñez, M. G., Mgeni, A. F., Khamis, I. S. and Stothard, J. R. (2007). School-based control of urinary schistosomiasis on Zanzibar, Tanzania: Monitoring micro-haematuria with reagent strips as a rapid urological assessment. Journal of Pediatric Urology 3, 364368.Google Scholar
Frost, L. J., Reich, M. R., Fenwick, A. and Thompson, H. (2008). Praziquantel: access to medicines. In Access: How do good health technologies get to poor people in poor countries? (Ed. Frost, L. J. and Reich, M. R.). Harvard Center for Population and Development Studies, Cambridge, USA.Google Scholar
Grépin, K. A. and Reich, M. R. (2008). Conceptualizing integration: a framework for analysis applied to neglected tropical disease control partnerships. PLoS Neglected Tropical Diseases 2, e174.Google Scholar
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. Lancet 368, 11061118.Google Scholar
Guo, J. G., Cao, C. L., Hu, G. H., Lin, H., Li, D., Zhu, R. and Xu, J. (2005). The role of ‘passive chemotherapy’ plus health education for schistosomiasis control in China during maintenance and consolidation phase. Acta Tropica 96, 177183.Google Scholar
Gurarie, D. and Seto, E. Y. W. (2009). Connectivity sustains disease transmission in environments with low potential for endemicity: modelling schistosomiasis with hydrologic and social connectivities. Journal of the Royal Society Interface 6, 495508.Google Scholar
Hillyer, G. V., Tsang, V. C., Vivas-Gonzalez, B. E., Noh, J., Ahn, L. H. and Vorndam, V. (1999). Age-specific decrease in seroprevalence of schistosomiasis in Puerto Rico. American Journal of Tropical Medicine and Hygiene 60, 313318.Google Scholar
Holveck, J. C., Ehrenberg, J. P., Ault, S. K., Rojas, R., Vasquez, J., Cerqueira, M. T., Ippolito-Shepherd, J., Genovese, M. A. and Periago, M. R. (2007). Prevention, control, and elimination of neglected diseases in the Americas: pathways to integrated, inter-programmatic, inter-sectoral action for health and development. BMC Public Health 7, 6.Google Scholar
Hotez, P. (2007). A new voice for the poor. PLoS Neglected Tropical Diseases 1, e77.Google Scholar
Hotez, P., Raff, S., Fenwick, A., Richards, F. Jr. and Molyneux, D. H. (2007 a). Recent progress in integrated neglected tropical disease control. Trends in Parasitology 23, 511514.Google Scholar
Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J. and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 13111321.Google Scholar
Hotez, P. J. and Fenwick, A. (2009). Schistosomiasis in Africa: an emerging tragedy in our new global health decade. PLoS Neglected Tropical Diseases 3, e485.Google Scholar
Hotez, P. J., Fenwick, A., Savioli, L. and Molyneux, D. H. (2009). Rescuing the bottom billion through control of neglected tropical diseases. Lancet 373, 15701575.Google Scholar
Hotez, P. J., Molyneux, D. H., Fenwick, A., Kumaresan, J., Ehrlich Sachs, S., Sachs, J. D. and Savioli, L. (2007 b). Control of neglected tropical diseases. New England Journal of Medicine 357, 10181027.Google Scholar
Hotez, P. J., Molyneux, D. H., Fenwick, A., Ottesen, E., Ehrlich Sachs, S. and Sachs, J. D. (2006). Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS Medicine 3, e102.Google Scholar
Hotez, P. J. and Yamey, G. (2009). The evolving scope of PLoS Neglected Tropical Diseases. PLoS Neglected Tropical Diseases 3, e379.Google Scholar
James, C. E., Hudson, A. L. and Davey, M. W. (2009). Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in Parasitology 25, 328335.Google Scholar
Jia, T. W., Zhou, X. N., Wang, X. H., Utzinger, J., Steinmann, P. and Wu, X. H. (2007). Assessment of the age-specific disability weight of chronic schistosomiasis japonica. Bulletin of the World Health Organization 85, 458465.Google Scholar
Jordan, P. (2000). From Katayama to the Dakhla Oasis: the beginning of epidemiology and control of bilharzia. Acta Tropica 77, 940.Google Scholar
Keiser, J. and Utzinger, J. (2007). Advances in the discovery and development of novel trematocidal drugs. Expert Opinion on Drug Discovery 2 (Suppl. 1), S923.Google Scholar
King, C. H. and Bertino, A. M. (2008). Asymmetries of poverty: why global burden of disease valuations underestimate the burden of neglected tropical diseases. PLoS Neglected Tropical Diseases 2, e209.Google Scholar
King, C. H. and Dangerfield-Cha, M. (2008). The unacknowledged impact of chronic schistosomiasis. Chronic Illness 4, 6579.Google Scholar
King, C. H., Dickman, K. and Tisch, D. J. (2005). Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 15611569.Google Scholar
Kolaczinski, J. H., Kabatereine, N. B., Onapa, A. W., Ndyomugyenyi, R., Kakembo, A. S. L. and Brooker, S. (2007). Neglected tropical diseases in Uganda: the prospects and challenge of integrated control. Trends in Parasitology 23, 485493.Google Scholar
Laamrani, H., Khallaayoune, K., Madsen, H., Mahjour, J. and Gryseels, B. (2000). New challenges in schistosomiasis control in Morocco. Acta Tropica 77, 6167.Google Scholar
Lammie, P. J., Fenwick, A. and Utzinger, J. (2006). A blueprint for success: integration of neglected tropical disease control programmes. Trends in Parasitology 22, 313321.Google Scholar
Lengeler, C., Utzinger, J. and Tanner, M. (2002). Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa. Bulletin of the World Health Organization 80, 235242.Google Scholar
Lerer, L. B. and Scudder, T. (1999). Health impacts of large dams. Environmental Impact Assessment Review 19, 113123.Google Scholar
Li, Y. S., Raso, G., Zhao, Z. Y., He, Y. K., Ellis, M. K. and McManus, D. P. (2007). Large water management projects and schistosomiasis control, Dongting Lake region, China. Emerging Infectious Diseases 13, 973979.Google Scholar
Lopez, A. D., Mathers, C. D., Ezzati, M., Jamison, D. T. and Murray, C. J. L. (2006). Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 367, 17471757.Google Scholar
Martens, W. J. M., Jetten, T. H. and Focks, D. A. (1997). Sensitivity of malaria, schistosomiasis and dengue to global warming. Climatic Change 35, 145156.Google Scholar
Melman, S. D., Steinauer, M. L., Cunningham, C., Kubatko, L. S., Mwangi, I. N., Barker Wynn, N., Mutuku, M. W., Karanja, D. M. S., Colley, D. G., Black, C. L., Secor, W. E., Mkoji, G. M. and Loker, E. S. (2009). Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Neglected Tropical Diseases 3, e504.Google Scholar
Molyneux, D. H., Hotez, P. J. and Fenwick, A. (2005). “Rapid-impact interventions”: how a policy of integrated control for Africa's neglected tropical diseases could benefit the poor. PLoS Medicine 2, e336.Google Scholar
Moran, M. (2005). A breakthrough in R&D for neglected diseases: new ways to get the drugs we need. PLoS Medicine 2, e302.Google Scholar
Murray, C. J. L., Lopez, A. D., Black, R., Mathers, C. D., Shibuya, K., Ezzati, M., Salomon, J. A., Michaud, C. M., Walker, N. and Vos, T. (2007). Global burden of disease 2005: call for collaborators. Lancet 370, 109110.Google Scholar
Prüss-Üstün, A., Bos, R., Gore, F. and Bartram, J. (2008). Safer water, better health: costs, benefits and sustainability of interventions to protect and promote health. World Health Organization, Geneva.Google Scholar
Raso, G., Luginbühl, A., Adjoua, C. A., Tian-Bi, N. T., Silue, K. D., Matthys, B., Vounatsou, P., Wang, Y., Dumas, M. E., Holmes, E., Singer, B. H., Tanner, M., N'Goran, E. K. and Utzinger, J. (2004). Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Côte d'Ivoire. International Journal of Epidemiology 33, 10921102.Google Scholar
Raso, G., Matthys, B., N'Goran, E. K., Tanner, M., Vounatsou, P. and Utzinger, J. (2005). Spatial risk prediction and mapping of Schistosoma mansoni infections among schoolchildren living in western Côte d'Ivoire. Parasitology 131, 97108.Google Scholar
Raso, G., Vounatsou, P., Gosoniu, L., Tanner, M., N'Goran, E. K. and Utzinger, J. (2006 a). Risk factors and spatial patterns of hookworm infection among schoolchildren in a rural area of western Côte d'Ivoire. International Journal for Parasitology 36, 201210.Google Scholar
Raso, G., Vounatsou, P., McManus, D. P. and Utzinger, J. (2007). Bayesian risk maps for Schistosoma mansoni and hookworm mono-infections in a setting where both parasites co-exist. Geospatial Health 2, 8596.Google Scholar
Raso, G., Vounatsou, P., Singer, B. H., N'Goran, E. K., Tanner, M. and Utzinger, J. (2006 b). An integrated approach for risk profiling and spatial prediction of Schistosoma mansoni-hookworm coinfection. Proceedings of the National Academy of Sciences, USA 103, 69346939.Google Scholar
Reddy, M., Gill, S. S., Kalkar, S. R., Wu, W., Anderson, P. J. and Rochon, P. A. (2007). Oral drug therapy for multiple neglected tropical diseases: a systematic review. JAMA 298, 19111924.Google Scholar
Richards, F. O. Jr., Eigege, A., Miri, E. S., Jinadu, M. Y. and Hopkins, D. R. (2006). Integration of mass drug administration programmes in Nigeria: the challenge of schistosomiasis. Bulletin of the World Health Organization 84, 673676.Google Scholar
Rumunu, J., Brooker, S., Hopkins, A., Chane, F., Emerson, P. and Kolaczinski, J. (2009). Southern Sudan: an opportunity for NTD control and elimination? Trends in Parasitology 25, 301307.Google Scholar
Savioli, L., Gabrielli, A. F., Montresor, A., Chitsulo, L. and Engels, D. (2009). Schistosomiasis control in Africa: 8 years after World Health Assembly Resolution 54.19. Parasitology 136, 16771681.Google Scholar
Scherrer, A. U., Sjöberg, M. K., Allangba, A., Traoré, M., Lohourignon, L. K., Tschannen, A. B., N'Goran, E. K. and Utzinger, J. (2009). Sequential analysis of helminth egg output in human stool samples following albendazole and praziquantel administration. Acta Tropica 109, 226231.Google Scholar
Singer, B. H. and Castro, M. C. (2007). Bridges to sustainable tropical health. Proceedings of the National Academy of Sciences, USA 104, 1603816043.Google Scholar
Smits, H. L. (2009). Prospects for the control of neglected tropical diseases by mass drug administration. Expert Review of Anti-Infective Therapy 7, 3756.Google Scholar
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.Google Scholar
Stiles, C. W. (1939). Early history, in part esoteric of the hookworm (uncinariasis) campaign in our southern United States. Journal of Parasitology 25, 283308.Google Scholar
Stothard, J. R. (2009). Improving control of African schistosomiasis: towards effective use of rapid diagnostic tests within an appropriate disease surveillance model. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 325332.Google Scholar
Stothard, J. R., Chitsulo, L., Kristensen, T. K. and Utzinger, J. (2009). Control of schistosomiasis in sub-Saharan Africa: progress made, new opportunities and remaining challenges. Parasitology 136, 16651675.Google Scholar
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, 8386.Google Scholar
Stothard, J. R., Mook, P., Mgeni, A. F., Khamis, I. S., Khamis, A. N. and Rollinson, D. (2006). Control of urinary schistosomiasis on Zanzibar (Unguja Island): a pilot evaluation of the educational impact of the Juma na Kichocho health booklet within primary schools. Memórias do Instituto Oswaldo Cruz 101 (Suppl. 1), 119124.Google Scholar
Tanaka, H. and Tsuji, M. (1997). From discovery to eradication of schistosomiasis in Japan: 1847–1996. International Journal for Parasitology 27, 14651480.Google Scholar
Tchuem Tchuenté, L. A. and N'Goran, E. K. (2009). Schistosomiasis and soil-transmitted helminthiasis control in Cameroon and Côte d'Ivoire: implementing control on a limited budget. Parasitology 136, 17391745.Google Scholar
The Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium (2009). The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460, 345351.Google Scholar
Utzinger, J., Bergquist, R., Xiao, S. H., Singer, B. H. and Tanner, M. (2003). Sustainable schistosomiasis control – the way forward. Lancet 362, 19321934.Google Scholar
Utzinger, J. and de Savigny, D. (2006). Control of neglected tropical diseases: integrated chemotherapy and beyond. PLoS Medicine 3, e112.Google Scholar
Utzinger, J., Zhou, X. N., Chen, M. G. and Bergquist, R. (2005). Conquering schistosomiasis in China: the long march. Acta Tropica 96, 6996.Google Scholar
Vounatsou, P., Raso, G., Tanner, M., N'Goran, E. K. and Utzinger, J. (2009). Bayesian geostatistical modelling for mapping schistosomiasis transmission. Parasitology 136, 16951705.Google Scholar
Wang, L., Utzinger, J. and Zhou, X. N. (2008). Schistosomiasis control: experiences and lessons from China. Lancet 372, 17931795.Google Scholar
Wang, L. D., Chen, H. G., Guo, J. G., Zeng, X. J., Hong, X. L., Xiong, J. J., Wu, X. H., Wang, X. H., Wang, L. Y., Xia, G., Hao, Y., Chin, D. P. and Zhou, X. N. (2009 b). A strategy to control transmission of Schistosoma japonicum in China. New England Journal of Medicine 360, 121128.Google Scholar
Wang, L. D., Guo, J. G., Wu, X. H., Chen, H. G., Wang, T. P., Zhu, S. P., Zhang, Z. H., Steinmann, P., Yang, G. J., Wang, S. P., Wu, Z. D., Wang, L. Y., Hao, Y., Bergquist, R., Utzinger, J. and Zhou, X. N. (2009 a). China's new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Tropical Medicine and International Health 14, doi:10.1111/j.1365-3156.2009.02403.x.Google Scholar
WHO (2002). Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Technical Report Series No. 912, 157.Google Scholar
WHO (2004). The world health report 2004: changing history. World Health Organization, Geneva.Google Scholar
WHO (2006 a). Neglected tropical diseases: hidden successes, emerging opportunities, World Health Organization Geneva.Google Scholar
WHO (2006 b). Preventive chemotherapy in human helminthiasis: coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. World Health Organization, Geneva.Google Scholar
WHO (2008). Soil-transmitted helminthiasis. Progress report on number of children treated with anthelminthic drugs: an update towards the 2010 global target. Weekly Epidemiological Record 82, 237252.Google Scholar
World Bank (1993). World Development Report 1993: Investing in Health. Oxford University Press, New York.Google Scholar
Yang, G. J., Vounatsou, P., Zhou, X. N., Tanner, M. and Utzinger, J. (2005). A potential impact of climate change and water resource development on the transmission of Schistosoma japonicum in China. Parassitologia 47, 127134.Google Scholar
Zhou, X. N., Yang, G. J., Yang, K., Wang, X. H., Hong, Q. B., Sun, L. P., Malone, J. B., Kristensen, T. K., Bergquist, N. R. and Utzinger, J. (2008). Potential impact of climate change on schistosomiasis transmission in China. American Journal of Tropical Medicine and Hygiene 78, 188194.Google Scholar