Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-26T06:34:22.912Z Has data issue: false hasContentIssue false

Rapid mapping of schistosomiasis and other neglected tropical diseases in the context of integrated control programmes in Africa

Published online by Cambridge University Press:  19 May 2009

S. BROOKER*
Affiliation:
Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, LondonWC1E 7HT, United Kingdom Malaria Public Health and Epidemiology Group, KEMRI/Wellcome Trust Collaborative Programme, P.O. Box 43640 – 00100, Nairobi, Kenya
N. B. KABATEREINE
Affiliation:
National Schistosomiasis and Soil-Transmitted Helminthiasis Control Programme, Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
J. O. GYAPONG
Affiliation:
Health Research Unit, Ghana Health Service, P.O. Box MB-190, Accra, Ghana
J. R. STOTHARD
Affiliation:
Department of Zoology, Natural History Museum, Cromwell Road, LondonSW7 5BD, United Kingdom
J. UTZINGER
Affiliation:
Department of Public Health and Epidemiology, Swiss Tropical Institute, P.O. Box, CH–4002Basel, Switzerland
*
*Corresponding author: Simon Brooker, Malaria Public Health and Epidemiology Group, Kenya Medical Research Institute/Wellcome Trust Collaborative Programme, P.O. Box 43640 – 00100, Nairobi, Kenya. E-mail: simon.brooker@lshtm.ac.uk

Summary

There is growing interest and commitment to the control of schistosomiasis and other so-called neglected tropical diseases (NTDs). Resources for control are inevitably limited, necessitating assessment methods that can rapidly and accurately identify and map high-risk communities so that interventions can be targeted in a spatially-explicit and cost-effective manner. Here, we review progress made with (1) mapping schistosomiasis across Africa using available epidemiological data and, more recently, climate-based risk prediction; (2) the development and use of morbidity questionnaires for rapid identification of high-risk communities of urinary schistosomiasis; and (3) innovative sampling-based approaches for intestinal schistosomiasis, using the lot quality assurance sampling technique. Experiences are also presented for the rapid mapping of other NTDs, including onchocerciasis, loiasis and lymphatic filariasis. Future directions for an integrated rapid mapping approach targeting multiple NTDs simultaneously are outlined, including potential challenges in developing an integrated survey tool. The lessons from the mapping of human helminth infections may also be relevant for the rapid mapping of malaria as its control efforts are intensified.

Type
SECTION 1 ADVOCACY AND DEFINING AREAS IN NEED OF CONTROL
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

Ansell, J. and Guyatt, H. L. (2002). Comparative cost-effectiveness of diagnostic tests for urinary schistosomiasis and the implications for school health programmes. Annals of Tropical Medicine and Parasitology 96, 145153.Google Scholar
Ansell, J., Guyatt, H., Hall, A., Kihamia, C. and Bundy, D. A. P. (2001). The effects of sex and age of responders on the reliability of self-diagnosed infection: a study of self-reported urinary schistosomiasis in Tanzanian school children. Social Science and Medicine 53, 957967.CrossRefGoogle ScholarPubMed
Ayele, B., Erko, B., Legesse, M., Hailu, A. and Medhin, G. (2008). Evaluation of circulating cathodic antigen (CCA) strip for diagnosis of urinary schistosomiasis in Hassoba school children, Afar, Ethiopia. Parasite 15, 6975.CrossRefGoogle ScholarPubMed
Ayong, L. S., Tume, C. B., Wembe, F. E., Simo, G., Asonganyi, T., Lando, G. and Ngu, J. L. (2005). Development and evaluation of an antigen detection dipstick assay for the diagnosis of human onchocerciasis. Tropical Medicine and International Health 10, 228233.CrossRefGoogle ScholarPubMed
Beau de Rochars, M. V., Milord, M. D., St Jean, Y., Désormeaux, A. M., Dorvil, J. J., Lafontant, J. G., Addiss, D. G. and Streit, T. G. (2004). Geographic distribution of lymphatic filariasis in Haiti. American Journal of Tropical Medicine and Hygiene 71, 598601.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
Birrie, H., Medhin, G. and Jemaneh, L. (1995). Comparison of urine filtration and a chemical reagent strip in the diagnosis of urinary schistosomiasis in Ethiopia. East African Medical Journal 72, 180185.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. (2007). Spatial epidemiology of human schistosomiasis in Africa: risk models, transmission dynamics and control. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 18.Google Scholar
Brooker, S. and Clements, A. C. A. (2009). Spatial heterogeneity of parasite co-infection: determinants and geostastical prediction at regional scales. International Journal for Parasitology 39, 591597.Google Scholar
Brooker, S., Clements, A. C. A. and Bundy, D. A. P. (2006). Global epidemiology, ecology and control of soil-transmitted helminth infections. Advances in Parasitology 62, 223265.Google ScholarPubMed
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., Myatt, M., Stothard, J. R. and Fenwick, A. (2005). Rapid assessment of Schistosoma mansoni: the validity, applicability and cost-effectiveness of the lot quality assurance sampling method in Uganda. Tropical Medicine and International Health 10, 647658.Google Scholar
Brooker, S., Kabatereine, N. B., Tukahebwa, E. M. and Kazibwe, F. (2004) Spatial analysis of the distribution of intestinal nematode infections in Uganda. Epidemiology and Infection 132, 10651071.Google ScholarPubMed
Brooker, S., Miguel, E. A., Waswa, P., Namunyu, R., Moulin, S., Guyatt, H. and Bundy, D. A. P. (2001). The potential of rapid screening methods for Schistosoma mansoni in western Kenya. Annals of Tropical Medicine and Parasitology 95, 343351.Google Scholar
Brooker, S., Rowlands, M., Haller, L., Savioli, L. and Bundy, D. A. P. (2000). Towards an atlas of human helminth infection in sub-Saharan Africa: the use of geographical information systems (GIS). Parasitology Today 16, 303307.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., Seung-Hee, Frances Lee, 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 in Developing Countries, Second Edition (ed. Jamison, D., Breman, J. G., Measham, A. R., Alleyne, G., Claeson, M., Evans, D., Jha, P., Mills, A. and Musgrove, P.), pp. 10911108. The World Bank and Oxford University Press, NY, USA.Google Scholar
Chappuis, F., Rijal, S., Jha, U. K., Desjeux, P., Karki, B. M., Koirala, S., Loutan, L. and Boelaert, M. (2006). Field validity, reproducibility and feasibility of diagnostic tests for visceral leishmaniasis in rural Nepal. Tropical Medicine and International Health 11, 3140.Google Scholar
Clements, A. C. A., Barnett, A. G., Nyandindi, U., Lwambo, N. J. S., Kihamia, C. M. and Blair, J. (2008 a). Age and gender effects in self-reported urinary schistosomiasis in Tanzania. Tropical Medicine and International Health 13, 713721.Google Scholar
Clements, A. C. A., Brooker, S., Nyandindi, U., Fenwick, A. and Blair, L. (2008 b). Bayesian spatial analysis of a national urinary schistosomiasis questionnaire to assist geographic targeting of schistosomiasis control in Tanzania, East Africa. International Journal for Parasitology 38, 401415.Google Scholar
Danso-Appiah, A., Garner, P., Olliaro, P. L. and Utzinger, J. (2009). Treatment of urinary schistosomiasis: methodological issues and research needs identified through a Cochrane systematic review. Parasitology 136 (in press).Google Scholar
de Vlas, S. J. and Gryseels, B. (1992). Underestimation of Schistosoma mansoni prevalences. Parasitology Today 8, 274277.Google Scholar
Diggle, P. J., Thomson, M. C., Christensen, O. F., Rowlingson, B., Obsomer, V., Gardon, J., Wanji, S., Takougang, I., Enyong, P., Kamgno, J., Remme, J. H., Boussinesq, M. and Molyneux, D. H. (2007). Spatial modelling and the prediction of Loa loa risk: decision making under uncertainty. Annals of Tropical Medicine and Parasitology 101, 499509.Google ScholarPubMed
Doumenge, J. P., Mott, K. E., Cheung, C., Villenave, D., Chapuis, O., Perrin, M. F. and Read-Thomas, G. (1987). Atlas of the Global Distribution of Schistosomiasis. World Health Organization, Geneva.Google Scholar
Engels, D., Sinzinkayo, E. and Gryseels, B. (1996). Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. American Journal of Tropical Medicine and Hygiene 54, 319324.Google Scholar
Engels, D., Sinzinkayo, E. and Gryseels, B. (1997). Intraspecimen fecal egg count variation in Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 57, 571577.CrossRefGoogle ScholarPubMed
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
Gryseels, B. (1992). Morbidity due to infection with Schistosoma mansoni: an update. Tropical and Geographical Medicine 44, 189200.Google ScholarPubMed
Gyapong, J. O., Kyelem, D., Kleinschmidt, I., Agbo, K., Ahouandogbo, F., Gaba, J., Owusu-Banahene, G., Sanou, S., Sodahlon, Y. K., Biswas, G., Kale, O. O., Molyneux, D. H., Roungou, J. B., Thomson, M. C. and Remme, J. (2002). The use of spatial analysis in mapping the distribution of bancroftian filariasis in four West African countries. Annals of Tropical Medicine and Parasitology 96, 695705.Google Scholar
Gyapong, J. O. and Remme, J. F. H. (2001). Validation of a rapid assessment method for the distribution of Bancroftian filariasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 681686.CrossRefGoogle Scholar
Hall, A. and Fentiman, A. (1999). Blood in the urine of adolescent girls in an area of Ghana with a low prevalence of infection of Schistosoma haematobium. Transactions of the Royal Society of Tropical Medicne and Hygiene 93, 411412.Google Scholar
Hotez, P. J., Molyneux, D. H., Fenwick, A., Kumaresan, J., Ehrlich Sachs, S., Sachs, J. D. and Savioli, L. (2007). Control of neglected tropical diseases. New England Journal of Medicine 357, 10181027.CrossRefGoogle ScholarPubMed
Hutin, Y. J., Legros, D., Owini, V., Brown, V., Lee, E., Mbulamberi, D. and Paquet, C. (2004). Trypanosoma brucei gambiense trypanosomiasis in Terego county, northern Uganda, 1996: a lot quality assurance sampling survey. American Journal of Tropical Medicine and Hygiene 70, 390394.Google Scholar
Kabatereine, N. B., Brooker, S., Koukounari, A., Kazibwe, F., Tukahebwa, E. M., Fleming, F. M., Zhang, Y., 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, 9199.Google ScholarPubMed
Kabatareine, 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, 372380.CrossRefGoogle Scholar
Katabarwa, M., Onapa, A. W. and Nakileza, B. (1999). Rapid epidemiological mapping of onchocerciasis in areas of Uganda where Simulium neavei sl is the vector. East African Medical Journal 76, 440446.Google ScholarPubMed
Kolaczinski, J., Kabatereine, N. B., Onapa, A., Ndyomugyengi, R., Kakmebo, A. S. and Brooker, S. (2007). Neglected tropical diseases in Uganda: the prospect and challenge of integrated control. Trends in Parasitology 23, 485493.Google Scholar
Kurowski, C., Wyss, K., Abdulla, S. and Mills, A. (2007). Scaling up priority health interventions in Tanzania: the human resources challenge. Health Policy and Planning 22, 113127.CrossRefGoogle ScholarPubMed
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
Legesse, M. and Erko, B. (2007). Field-based evaluation of a reagent strip test for diagnosis of Schistosoma mansoni by detecting circulating cathodic antigen in urine before and after chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 668673.Google Scholar
Legesse, M. and Erko, B. (2008). Field-based evaluation of a reagent strip test for diagnosis of schistosomiasis mansoni by detecting circulating cathodic antigen (CCA) in urine in low endemic area in Ethiopia. Parasite 15, 151155.Google Scholar
Lengeler, C., de Savigny, D., Mshinda, H., Mayombana, C., Tayari, S., Hatz, C., Degrémont, A. and Tanner, M. (1991 a). Community-based questionnaires and health statistics as tools for the cost-efficient identification of communities at risk of urinary schistosomiasis. International Journal of Epidemiology 20, 796807.Google Scholar
Lengeler, C., Kilima, P., Mshinda, H., Morona, D., Hatz, C. and Tanner, M. (1991 b). Rapid, low-cost, two-step method to screen for urinary schistosomiasis at the district level: the Kilosa experience. Bulletin of the World Health Organization 69, 179189.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
Mafe, M. A. (1997). The diagnostic potential of three indirect tests for urinary schistosomiasis in Nigeria. Acta Tropica 68, 277284.CrossRefGoogle ScholarPubMed
Mafe, M. A., von Stamm, T., Utzinger, J. and N'Goran, E. K. (2000). Control of urinary schistosomiasis: an investigation into the effective use of questionnaires to identify high-risk communities and individuals in Niger State, Nigeria. Tropical Medicine and International Health 5, 5363.Google Scholar
Marx, A., Pewsner, D., Egger, M., Nüesch, R., Bucher, H. C., Genton, B., Hatz, C. and Jüni, P. (2005). Meta-analysis: accuracy of rapid tests for malaria in travelers returning from endemic areas. Annals of Internal Medicine 142, 836846.Google Scholar
Massara, C. L., Peixoto, S. V., Enk, M. J., da Silva Barros, H., dos Santos Carvalho, O., Sakurai, E. and Schall, V. (2006). Evaluation of an improved approach using residences of schistosomiasis-positive school children to identify carriers in an area of low endemicity. American Journal of Tropical Medicine and Hygiene 74, 495499.CrossRefGoogle Scholar
Mathieu, E., Deming, M., Lammie, P. J., McLaughlin, S. I., Beach, M. J., Deodat, D. J. and Addiss, D. G. (2003). Comparison of methods for estimating drug coverage for filariasis elimination, Leogane commune, Haiti. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 501505.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
Moody, A. (2002). Rapid diagnostic tests for malaria parasites. Clinical Microbiology Reviews 15, 6678.Google Scholar
Mtasiwa, D., Mayombana, C., Kilima, P. and Tanner, M. (1996). Validation of reagent sticks in diagnosing urinary schistosomiasis in an urban setting. East African Medical Journal 73, 198200.Google Scholar
Myatt, M., Limburg, H., Minassian, D. and Katyola, D. (2003). Field trial of applicability of lot quality assurance sampling survey method for rapid assessment of prevalence of active trachoma. Bulletin of the World Health Organization 81, 877885.Google Scholar
N'Goran, E. K., Utzinger, J., Traore, M., Lengeler, C. and Tanner, M. (1998). Identification rapide par questionnaire des principaux foyers de bilharziose urinaire au centre de la Côte d'Ivoire. Médecine Tropicale 58, 253260.Google Scholar
Ngoumou, P., Walsh, J. F. and Mace, J. M. (1994). A rapid mapping technique for the prevalence and distribution of onchocerciasis: a Cameroon case study. Annals of Tropical Medicine and Parasitology 88, 463474.Google Scholar
N'Guessan, N. A., Acka, C. A., Utzinger, J. and N'Goran, E. K. (2007). Identification des régions à haut risque de schistosomoses en Côte d'Ivoire. Bulletin de la Société de Pathologie Exotique 100, 119123.Google Scholar
Noma, M., Nwoke, B. E., Nutall, I., Tambala, P. A., Enyong, P., Namsenmo, A., Remme, J., Amazigo, U. V., Kale, O. O. and Sékétéli, A. (2002). Rapid epidemiological mapping of onchocerciasis (REMO): its application by the African programme for onchocerciasis control (APOC). Annals of Tropical Medicine and Parasitology 96, S29S39.Google Scholar
Onapa, A. W., Simonsen, P. E., Baehr, I. and Pedersen, E. M. (2005). Rapid assessment of the geographical distribution of lymphatic filariasis in Uganda, by screening of schoolchildren for circulating filarial antigens. Annals in Tropical Medicine and Parasitology 99, 141153.Google Scholar
Partnership for Child Development (1997). Better health, nutrition and education for the school aged child. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 12.Google Scholar
Poggensee, G., Krantz, I., Kiwelu, I. and Feldmeier, H. (2000). Screening of Tanzanian women of childbearing age for urinary schistosomiasis: validity of urine reagent strip readings and self-reported symptoms. Bulletin of the World Health Organization 78, 542548.Google Scholar
Rabarijaona, L., Rakotomanana, F., Ranaivo, L., Raharimalala, L., Modiano, D., Boisier, P., De Giorgi, F., Raveloson, N. and Jambou, R. (2001). Validity of lot quality assurance sampling to optimize falciparum malaria surveys in low-transmission areas. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 267269.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
Robertson, S. E. and Valadez, J. J. (2006). Global review of health care surveys using lot quality assurance sampling (LQAS), 1984–2004. Social Science and Medicine 63, 16481660.Google Scholar
Sherchand, J. B., Obsomer, V., Thakur, G. D. and Hommel, M. (2003). Mapping of lymphatic filariasis in Nepal. Filaria Journal 2, 7.Google Scholar
Simoonga, C., Utzinger, J., Brooker, S., Vounatsou, P., Appleton, C. C., Stensgaard, A. S., Olsen, A. and Kristensen, T. K. (2009). Remote sensing, geographical information system and spatial analysis for schistosomiasis epidemiology and ecology in Africa. Parasitology 136 (in press).Google Scholar
Srividya, A., Michael, E., Palaniyandi, M., Pani, S. P. and Das, P. K. (2002). A geostatistical analysis of the geographic distribution of lymphatic filariasis prevalence in southern India. American Journal of Tropical Medicine and Hygiene 67, 480489.Google Scholar
Stothard, J. R., Kabatereine, N. B., Tukahebwa, E. M., Kazibwe, F., Rollinson, D., Mathieson, W., Webster, J. P. and Fenwick, A. (2006). Use of circulating cathodic antigen (CCA) dipsticks for detection of intestinal and urinary schistosomiasis. Acta Tropica 97, 219228.Google Scholar
Takougang, I., Meremikwu, M., Wandji, S., Yenshu, E. V., Aripko, B., Lamlenn, S. B., Eka, B. L., Enyong, P., Meli, J., Kale, O. and Remme, J. H. (2002). Rapid assessment method for prevalence and intensity of Loa loa infection. Bulletin of the World Health Organization 80, 852858.Google Scholar
TDR (2001). Rapid Assessment Procedures for Loiasis: Report of a Multi-Centre Study. UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases, Geneva.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.CrossRefGoogle ScholarPubMed
Utzinger, J., Booth, M., N'Goran, E. K., Müller, I., Tanner, M. and Lengeler, C. (2001). Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 122, 537544.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., N'Goran, E. K., Esse Aya, C. M., Acka Adjoua, C., Lohourignon, K. L., Tanner, M. and Lengeler, C. (1998). Schistosoma mansoni, intestinal parasites and perceived morbidity indicators in schoolchildren in a rural endemic area of western Côte d'Ivoire. Tropical Medicine and International Health 3, 711720.CrossRefGoogle Scholar
Utzinger, J., N'Goran, E. K., Ossey, Y. A., Booth, M., Traoré, M., Lohourignon, K. L., Allangba, A., Ahiba, L. A., Tanner, M. and Lengeler, C. (2000). Rapid screening for Schistosoma mansoni in western Côte d'Ivoire using a simple school questionnaire. Bulletin of the World Health Organization 78, 389398.Google Scholar
van Dam, G. J., Wichers, J. H., Falcao Ferreira, T. M., Ghati, D., van Amerongen, A. and Deelder, A. M. (2004). Diagnosis of schistosomiasis by reagent strip test for detection of circulating cathodic antigen. Journal of Clinical Microbiology 42, 54585461.CrossRefGoogle ScholarPubMed
van der Werf, M. J., Borsboom, G. J. and de Vlas, S. J. (2003). No effect of recall period length on prevalence of self-reported haematuria in Schistosoma haematobium-endemic areas. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 373374.CrossRefGoogle ScholarPubMed
van Etten, L., van Lieshout, L., Mansour, M. M. and Deelder, A. M. (1997). A reagent strip antigen capture assay for the assessment of cure of schistosomiasis patients. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 154155.Google Scholar
Vanamail, P., Subramanian, S., Srividya, A., Ravi, R., Krishnamoorthy, K. and Das, P. K. (2006). Operational feasibility of lot quality assurance sampling (LQAS) as a tool in routine process monitoring of filariasis control programmes. Tropical Medicine and International Health 11, 12561263.CrossRefGoogle ScholarPubMed
Vounatsou, P., Raso, G., Tanner, M., N'Goran, E. K. and Utzinger, J. (2009). Bayesian geostatistical modelling for risk profiling of schistosomiasis: a review. Parasitology 136 (in press).Google Scholar
Wang, S. J., Lengeler, C., Smith, T. A., Vounatsou, P., Cissé, G., Diallo, D. A., Akogbeto, M., Mtasiwa, D., Teklehaimanot, A. and Tanner, M. (2005). Rapid urban malaria appraisal (RUMA) in sub-Saharan Africa. Malaria Journal 4, 40.CrossRefGoogle ScholarPubMed
Wanji, S., Tendongfor, N., Esum, M., Yundze, S. S. J., Taylor, M. J. and Enyong, P. (2005). Combined utilisation of rapid assessment procedures for loiasis (RAPLOA) and onchocerciasis (REA) in rain forest villages of Cameroon. Filaria Journal 4, 2.Google Scholar
Weil, G. J., Lammie, P. J. and Weiss, N. (1997). The ICT filariasis test: a rpid-format test for diagnosis of bancroftian filariasis. Parasitology Today 13, 401404.Google Scholar
WHO (1995). The schistosomiasis manual. Social and Economic Research Project Reports No. 3. World Health Organization, Geneva.Google Scholar
WHO (2000). Operational Guidelines for Rapid Mapping of Bancroftian filariasis in Africa. WHO/CDS/CPE/CEE/2000.9. World Health Organization, Geneva.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, 1–57.Google Scholar
WHO (2006). Preventive Chemotherapy in Human Helminthiasis: Co-ordinated Use of Anthelminthic Drugs in Control Interventions. A Manual for Health Professionals and Programme Managers. World Health Organization, Geneva.Google Scholar