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One hundred years of neglect in paediatric schistosomiasis

Published online by Cambridge University Press:  01 March 2017

AMAYA L. BUSTINDUY Open the ORCID record for AMAYA L. BUSTINDUY [Opens in a new window] ,
STEPHEN WRIGHT ,
ELIZABETH C. JOEKES ,
NARCIS B. KABATEREINE ,
JUTTA REINHARD-RUPP ,
CHARLES H. KING  and
J. RUSSELL STOTHARD
AMAYA L. BUSTINDUY*
Affiliation:
Department of Clinical Research, London School Of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
STEPHEN WRIGHT
Affiliation:
Hospital for Tropical Diseases, Mortimer Market Centre, Mortimer Market, London WC1E 6JD, UK
ELIZABETH C. JOEKES
Affiliation:
Department of Radiology, The Royal Liverpool University Hospitals NHS Trust, Liverpool L78XP, UK
NARCIS B. KABATEREINE
Affiliation:
Schistosomiasis Control Initiative, Imperial College of London, 1 Norfolk Place, Paddington, London W2 1PG, UK
JUTTA REINHARD-RUPP
Affiliation:
Global Health R&D Department (route de la Verrerie 6, 1267 Coinsins, Switzerland) being part of the Biopharma Business of Merck KGaA, Darmstadt, Germany
CHARLES H. KING
Affiliation:
Center for Global Health and Diseases, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, Ohio, 44106, USA
J. RUSSELL STOTHARD
Affiliation:
Department of Parasitology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK
*
*Corresponding author: Department of Clinical Research, London School of Hygiene & Tropical Medicine, Keppel Street, London, WC1E 7HT, UK. E-mail: [email protected]
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Summary

Early in the history of schistosomiasis research, children under 5 years of age were known to be infected. Although this problem was recognized over 100 years ago, insufficient action has been taken to address this issue. Under current policy, such infected children only receive their first antiparasitic treatment (praziquantel – PZQ) upon entry into primary school as current mass drug administration programmes typically target school-aged children. For many infected children, they will wait up to 6 years before receiving their first medication and significant schistosomiasis-related morbidity may have already established. This inequity would not be accepted for other diseases. To unveil some of the reasons behind this neglect, it is paramount to understand the intricate historical relationship between schistosomiasis and British Imperial medicine, to underline its lasting influence on today's public health priorities. This review presents a perspective on the historical neglect of paediatric schistosomiasis, focusing on important gaps that persist from the early days after discovery of this parasite. Looking to end this inequity, we address several issues that need to be overcome to move forward towards the lasting success of schistosomiasis control and elimination efforts.

Keywords

paediatricsschistosomiasisSchistosomapraziquantelintestinal schistosomiasisurogenital schistosomiasisultrasound
Type
Special Issue Review
Information
Parasitology , Volume 144 , Special Issue 12: Glasgow encounters with tropical diseases , October 2017 , pp. 1613 - 1623
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Amarir, F., El Mansouri, B., Fellah, H., Sebti, F., Mohammed, L., Handali, S., Wilkins, P., El Idrissi, A. L., Sadak, A. and Rhajaoui, M. (2011). National serologic survey of Haematobium schistosomiasis in Morocco: evidence for elimination. American Journal of Tropical Medicine and Hygiene 84, 15–19.Google Scholar
Belard, S., Tamarozzi, F., Bustinduy, A. L., Wallrauch, C., Grobusch, M. P., Kuhn, W., Brunetti, E., Joekes, E. and Heller, T. (2016). Point-of-care ultrasound assessment of tropical infectious diseases – a review of applications and perspectives. American Journal of Tropical Medicine and Hygiene 94, 8–21.CrossRefGoogle Scholar
Blair, D. M., Meeser, C. V., Loveridge, F. G., Ross, W. F. (1949). Urinary schistosomiasis treated with miracil D. Lancet 1, 344–346.CrossRefGoogle ScholarPubMed
Bosompem, K. M., Bentum, I. A., Otchere, J., Anyan, W. K., Brown, C. A., Osada, Y., Takeo, S., Kojima, S. and Ohta, N. (2004). Infant schistosomiasis in Ghana: a survey in an irrigation community. Tropical Medicine and International Health 9, 917–922.CrossRefGoogle Scholar
Bustinduy, A. L., King, C. H. (2013). Schistosomiasis. In Manson's Tropical Diseases (ed. Farrar, J., Hotez, P. J., Junghanss, T., Kang, G., Lalloo, D. and White, N. J.), pp. 698–725. Elsevier.Google Scholar
Bustinduy, A. L., Thomas, C. L., Fiutem, J. J., Parraga, I. M., Mungai, P. L., Muchiri, E. M., Mutuku, F., Kitron, U. and King, C. H. (2011). Measuring fitness of Kenyan children with polyparasitic infections using the 20-meter shuttle run test as a morbidity metric. PLoS Neglected Tropical Diseases 5, e1213.CrossRefGoogle ScholarPubMed
Bustinduy, A. L., Parraga, I. M., Thomas, C. L., Mungai, P. L., Mutuku, F., Muchiri, E. M., Kitron, U. and King, C. H. (2013). Impact of polyparasitic infections on anemia and undernutrition among Kenyan children living in a Schistosoma haematobium-endemic area. American Journal of Tropical Medicine and Hygiene 88, 433–440.CrossRefGoogle Scholar
Bustinduy, A., Waterhouse, D., de Sousa-Figueiredo, J., Roberts, S. A., Atuhaire, A., Van Dam, G. J., Corstjens, P. A., Scott, J. T., Stanton, M. C., Kabatereine, N. B., Ward, S., Hope, W. H., Stothard, J. R. (2016 a). Population pharmacokinetics and pharmacodynamics of praziquantel in Ugandan children with intestinal schistosomiasis: higher dosages are required for maximal efficacy. MBio 7, e00227–16.CrossRefGoogle ScholarPubMed
Bustinduy, A. L., Friedman, J. F., Kjetland, E. F., Ezeamama, A. E., Kabatereine, N. B., Stothard, J. R. and King, C. H. (2016 b). Expanding praziquantel (PZQ) access beyond mass drug administration programs: paving a way forward for a pediatric PZQ formulation for schistosomiasis. PLoS Neglected Tropical Diseases 10, e0004946.CrossRefGoogle ScholarPubMed
Christopherson, J. B. (1918). Intravenous injections of antimonium tartaratum in Bilharziosis. British Medical Journal 2, 652–653.CrossRefGoogle ScholarPubMed
Christopherson, J. B. (1924). Longevity of parasitic worms. The term of living existence of Schistosoma haematobium in the human body. Lancet 742–743.CrossRefGoogle Scholar
Colley, D. G., Binder, S., Campbell, C., King, C. H., Tchuem Tchuente, L. A., N'Goran, E. K., Erko, B., Karanja, D. M., Kabatereine, N. B., van Lieshout, L. and Rathbun, S. (2013). A five-country evaluation of a point-of-care circulating cathodic antigen urine assay for the prevalence of Schistosoma mansoni . American Journal of Tropical Medicine and Hygiene 88, 426–432.CrossRefGoogle ScholarPubMed
Colley, D. G., Bustinduy, A. L., Secor, W. E. and King, C. H. (2014). Human schistosomiasis. Lancet 383, 2253–2264.Google Scholar
Cook, J. A., Jordan, P., Woodstock, L. and Pilgrim, V. (1977). A controlled trial of hycanthone and placebo in Schistosomiasis mansoni in St. Lucia. Annals of Tropical Medicine and Parasitology 71, 197–202.Google Scholar
Coutinho, H. M., Acosta, L. P., McGarvey, S. T., Jarilla, B., Jiz, M., Pablo, A., Su, L., Manalo, D. L., Olveda, R. M., Kurtis, J. D. and Friedman, J. F. (2006 a). Nutritional status improves after treatment of Schistosoma japonicum-infected children and adolescents. Journal of Nutrition 136, 183–188.Google Scholar
Coutinho, H. M., Leenstra, T., Acosta, L. P., Su, L., Jarilla, B., Jiz, M. A., Langdon, G. C., Olveda, R. M., McGarvey, S. T., Kurtis, J. D. and Friedman, J. F. (2006 b). Pro-inflammatory cytokines and C-reactive protein are associated with undernutrition in the context of Schistosoma japonicum infection. American Journal of Tropical Medicine and Hygiene 75, 720–726.Google Scholar
da Silva, L. C., Sette, H. Jr., Chamone, D. A., Saez-Alquezar, A., Punskas, J. A. and Raia, S. (1975). Further clinical trials with oxamniquine (UK 4271), a new anti-schistosomal agent. Revista do Instituto de Medicina Tropical de Sao Paulo 17, 307–311.Google ScholarPubMed
Davis, A. (1966). Field trials of ambilhar in the treatment of urinary bilharziasis in schoolchildren. Bulletin of the World Health Organisation 35, 827–835.Google Scholar
Davis, A. (1968). Comparative trials of antimonial drugs in urinary schistosomiasis. Bulletin of the World Health Organisation 38, 197–227.Google ScholarPubMed
Davis, A. and Wegner, D. H. (1979). Multicentre trials of praziquantel in human schistosomiasis: design and techniques. Bulletin of the World Health Organisation 57, 767–771.Google Scholar
Davis, A., Biles, J. E. and Ulrich, A. M. (1979). Initial experiences with praziquantel in the treatment of human infections due to Schistosoma haematobium . Bulletin of the World Health Organisation 57, 773–779.Google ScholarPubMed
Doenhoff, M. J., Cioli, D. and Utzinger, J. (2008). Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Current Opinion in Infectious Diseases 21, 659–667.Google Scholar
Ezeamama, A. E., Friedman, J. F., Acosta, L. P., Bellinger, D. C., Langdon, G. C., Manalo, D. L., Olveda, R. M., Kurtis, J. D. and McGarvey, S. T. (2005 a). Helminth infection and cognitive impairment among Filipino children. American Journal of Tropical Medicine and Hygiene 72, 540–548.CrossRefGoogle ScholarPubMed
Ezeamama, A. E., Friedman, J. F., Olveda, R. M., Acosta, L. P., Kurtis, J. D., Mor, V. and McGarvey, S. T. (2005 b). Functional significance of low-intensity polyparasite helminth infections in anemia. Journal of Infectious Diseases 192, 2160–2170.CrossRefGoogle ScholarPubMed
Farley, J. (1991). Bilharzia: A History of Imperial Tropical Medicine, Cambridge University Press, Cambridge, MA.Google Scholar
Farquharson, C. and Ahmed, S. F. (2013). Inflammation and linear bone growth: the inhibitory role of SOCS2 on GH/IGF-1 signaling. Pediatric Nephrology 28, 547–556.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, 1719–1730.CrossRefGoogle ScholarPubMed
Ferrari, M. L., Coelho, P. M., Antunes, C. M., Tavares, C. A. and da Cunha, A. S. (2003). Efficacy of oxamniquine and praziquantel in the treatment of Schistosoma mansoni infection: a controlled trial. Bulletin of the World Health Organisation 81, 190–196.Google Scholar
Frank, C., Mohamed, M. K., Strickland, G. T., Lavanchy, D., Arthur, R. R., Magder, L. S., El Khoby, T., Abdel-Wahab, Y., Aly Ohn, E. S., Anwar, W. and Sallam, I. (2000). The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet 355, 887–891.Google Scholar
Friedman, J. F., Kanzaria, H. K. and McGarvey, S. T. (2005). Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends in Parasitology 21, 386–392.Google Scholar
Garba, A., Toure, S., Dembele, R., Boisier, P., Tohon, Z., Bosque-Oliva, E., Koukounari, A. and Fenwick, A. (2009). Present and future schistosomiasis control activities with support from the Schistosomiasis control initiative in West Africa. Parasitology 136, 1731–1737.CrossRefGoogle ScholarPubMed
Gelfand, M. (1967). A Clinical Study of Intestinal Bilharziasis (Schistosoma Mansoni) in Africa. Edward Arnold (Publishers) Ltd, London, UK.Google Scholar
Gryseels, B. (1989). The relevance of schistosomiasis for public health. Annals of Tropical Medicine and Parasitology 40, 134–142.Google Scholar
Gurarie, D., Wang, X., Bustinduy, A. L. and King, C. H. (2011). Modeling the effect of chronic schistosomiasis on childhood development and the potential for catch-up growth with different drug treatment strategies promoted for control of endemic schistosomiasis. American Journal of Tropical Medicine & Hygiene 84, 773–781.Google Scholar
Jordan, P. (2000). From katayama to the Dakhla Oasis: the beginning of epidemiology and control of bilharzia. Acta Tropica 77, 9–40.Google Scholar
Jukes, M. C., Nokes, C. A., Alcock, K. J., Lambo, J. K., Kihamia, C., Ngorosho, N., Mbise, A., Lorri, W., Yona, E., Mwanri, L., Baddeley, A. D., Hall, A., Bundy, D. A. and Partnership for Child, D. (2002). Heavy schistosomiasis associated with poor short-term memory and slower reaction times in Tanzanian schoolchildren. Tropical Medicine and International Health 7, 104–117.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 Organisation 85, 91–99.Google ScholarPubMed
King, C. H. (2009). Toward the elimination of schistosomiasis. New England Journal of Medicine 360, 106–109.Google Scholar
King, C. H. (2010). Parasites and poverty: the case of schistosomiasis. Acta Tropica 113, 95–104.Google Scholar
King, C. H. (2015). It's time to dispel the myth of “asymptomatic” schistosomiasis. PloS Neglected Tropical Diseases 9, e0003504.Google Scholar
King, C. H. and Dangerfield-Cha, M. (2008). The unacknowledged impact of chronic schistosomiasis. Chronic Illness 4, 65–79.Google Scholar
King, C. H. and Mahmoud, A. A. (1989). Drugs five years later: praziquantel. Annals of Internal Medicine 110, 290–296.CrossRefGoogle ScholarPubMed
King, C. H., Lombardi, G., Lombardi, C., Greenblatt, R., Hodder, S., Kinyanjui, H., Ouma, J., Odiambo, O., Bryan, P. J., Muruka, J., Magak, P., Weinert, D., Ransohoff, D., Houser, H., Koech, D., Arap Siongok, T. K. and Mahmoud, A. A. F. (1988). Chemotherapy-based control of schistosomiasis haematobia. I. Metrifonate versus praziquantel in control of intensity and prevalence of infection. American Journal of Tropical Medicine and Hygiene 39, 295–305.Google Scholar
King, C. H., Lombardi, G., Lombardi, C., Greenblatt, R., Hodder, S., Kinyanjui, H., Ouma, J., Odiambo, O., Bryan, P. J., Muruka, J. et al. (1990). Chemotherapy-based control of schistosomiasis haematobia. II. Metrifonate vs. praziquantel in control of infection-associated morbidity. American Journal of Tropical Medicine and Hygiene 42, 587–595.Google Scholar
King, C. H., Muchiri, E. M., Mungai, P., Ouma, J. H., Kadzo, H., Magak, P. and Koech, D. K. (2002). Randomized comparison of low-dose versus standard-dose praziquantel therapy in treatment of urinary tract morbidity due to Schistosoma haematobium infection. American Journal of Tropical Medicine and Hygiene 66, 725–730.CrossRefGoogle Scholar
King, C. H., Olbrych, S. K., Soon, M., Singer, M. E., Carter, J. and Colley, D. G. (2011). Utility of repeated praziquantel dosing in the treatment of schistosomiasis in high-risk communities in Africa: a systematic review. PloS Neglected Tropical Diseases 5, e1321.Google Scholar
Kjetland, E. F., Leutscher, P. D. and Ndhlovu, P. D. (2012). A review of female genital schistosomiasis. Trends in Parasitology 28, 58–65.Google Scholar
Koukounari, A., Fenwick, A., Whawell, S., Kabatereine, N. B., Kazibwe, F., Tukahebwa, E. M., Stothard, J. R., Donnelly, C. A. and Webster, J. P. (2006). Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. American Journal of Tropical Medicine and Hygiene 75, 278–286.Google Scholar
Koukounari, A., Gabrielli, A. F., Toure, S., Bosque-Oliva, E., Zhang, Y., Sellin, B., Donnelly, C. A., Fenwick, A. and Webster, J. P. (2007). Schistosoma haematobium infection and morbidity before and after large-scale administration of praziquantel in Burkina Faso. Journal of Infectious Diseases 196, 659–669.CrossRefGoogle ScholarPubMed
Latham, M. C., Stephenson, L. S., Kurz, K. M. and Kinoti, S. N. (1990). Metrifonate or praziquantel treatment improves physical fitness and appetite of Kenyan schoolboys with Schistosoma haematobium and hookworm infections. American Journal of Tropical Medicine and Hygiene 43, 170–179.Google Scholar
Leenstra, T., Coutinho, H. M., Acosta, L. P., Langdon, G. C., Su, L., Olveda, R. M., McGarvey, S. T., Kurtis, J. D. and Friedman, J. F. (2006). Schistosoma japonicum reinfection after praziquantel treatment causes anemia associated with inflammation. Infection and Immunity 74, 6398–6407.CrossRefGoogle ScholarPubMed
Lees, R. E. (1966). Lucanthone hydrochloride in the treatment of Schistosoma mansoni infection. Transactions of the Royal Society of Tropical Medicine & Hygiene 60, 233–236.Google Scholar
McGarvey, S. T., Aligui, G., Daniel, B. L., Peters, P., Olveda, R. and Olds, G. R. (1992). Child growth and schistosomiasis japonica in northeastern Leyte, the Philippines: cross-sectional results. American Journal of Tropical Medicine and Hygiene 46, 571–581.CrossRefGoogle ScholarPubMed
McGarvey, S. T., Aligui, G., Graham, K. K., Peters, P., Olds, G. R. and Olveda, R. (1996). Schistosomiasis japonica and childhood nutritional status in northeastern Leyte, the Philippines: a randomized trial of praziquantel versus placebo. American Journal of Tropical Medicine and Hygiene 54, 498–502.Google Scholar
Moore, J. A. (1972). Teratogenicity of hycanthone in mice. Nature 239, 107–109.Google Scholar
Mott, K. E. (1982). “Control of schistosomiasis”: morbidity-reduction and chemotherapy. Acta Leidensia 49, 101–111.Google Scholar
Mott, K. E. (2004). Schistosomiasis. In Global Epidemiology of Infectious Diseases (ed. Murray, C. J. L., Lopez, A. and Mathers, C. D.), pp. 341–391. World Health Organisation, Geneva, Switzerland.Google Scholar
Mott, K. E. and Cline, B. L. (1980). Advances in epidemiology survey methodology and techniques in schistosomiasis. Bulletin of the World Health Organisation 58, 639–647.Google Scholar
Mott, K. E., Dixon, H., Osei-Tutu, E., England, E. C. and Davis, A. (1985). Effect of praziquantel on hematuria and proteinuria in urinary schistosomiasis. American Journal of Tropical Medicine and Hygiene 34, 1119–1126.Google Scholar
Mupfasoni, D., Karibushi, B., Koukounari, A., Ruberanziza, E., Kaberuka, T., Kramer, M. H., Mukabayire, O., Kabera, M., Nizeyimana, V., Deville, M. A., Ruxin, J., Webster, J. P. and Fenwick, A. (2009). Polyparasite helminth infections and their association to anaemia and undernutrition in northern Rwanda. PloS Neglected Tropical Diseases 3, e517.Google Scholar
Murray, C. J. L. A. (1996). Rethinking DALYs;The Global Burden of Disease. Harvard School of Public Health/World Bank, Cambridge, MA, 1–98.Google Scholar
Mutapi, F., Rujeni, N., Bourke, C., Mitchell, K., Appleby, L., Nausch, N., Midzi, N. and Mduluza, T. (2011). Schistosoma haematobium treatment in 1–5 year old children: safety and efficacy of the antihelminthic drug praziquantel. PloS Neglected Tropical Diseases 5, e1143.Google Scholar
Newsome, J. and Halawani, A. (1950). The treatment of urinary bilharzia in Egypt by miracil D. Transactions of the Royal Society of Tropical Medicine & Hygiene 44, 67–76.CrossRefGoogle ScholarPubMed
Nicholson, N. G. and McMahon, J. E. (1966). Death following ambilhar therapy. British Medical Journal 2, 1261.Google Scholar
Nokes, C., McGarvey, S. T., Shiue, L., Wu, G., Wu, H., Bundy, D. A. and Olds, G. R. (1999). Evidence for an improvement in cognitive function following treatment of Schistosoma japonicum infection in Chinese primary schoolchildren. American Journal of Tropical Medicine and Hygiene 60, 556–565.Google Scholar
Odogwu, S. E., Ramamurthy, N. K., Kabatereine, N. B., Kazibwe, F., Tukahebwa, E., Webster, J. P., Fenwick, A. and Stothard, J. R. (2006). Schistosoma mansoni in infants (aged < 3 years) along the Ugandan shoreline of Lake Victoria. Annals of Tropical Medicine and Parasitology 100, 315–326.CrossRefGoogle ScholarPubMed
Parraga, I. M., Assis, A. M., Prado, M. S., Barreto, M. L., Reis, M. G., King, C. H. and Blanton, R. E. (1996). Gender differences in growth of school-aged children with schistosomiasis and geohelminth infection. American Journal of Tropical Medicine and Hygiene 55, 150–156.Google Scholar
Pineiro Perez, R., Santiago Garcia, B., Fernandez Llamazares, C. M., Baquero Artigao, F., Noguera Julian, A., Mellado Pena, M. J. and en representacion de p, T. (2016). [The challenge of administering anti-tuberculosis treatment in infants and pre-school children. pTBred Magistral Project]. Anales de Pediatria(Barcelona) 85, 4–12.Google ScholarPubMed
Richter, J., Botelho, M. C., Holtfreter, M. C., Akpata, R., El Scheich, T., Neumayr, A., Brunetti, E., Hatz, C., Dong, Y. and Dietrich, C. F. (2016). Ultrasound assessment of schistosomiasis. Zeitschrift für Gastroenterologie 54, 653–660.Google Scholar
Sacks, J. (2005). The End of Poverty: Economic Possibilities for our Time. Penguin Press, London.Google Scholar
Salomon, J. A., Vos, T., Hogan, D. R., Gagnon, M., Naghavi, M., Mokdad, A., Begum, N., Shah, R., Karyana, M., Kosen, S., Farje, M. R., Moncada, G., Dutta, A., Sazawal, S., Dyer, A., Seiler, J., Aboyans, V., Baker, L., Baxter, A., Benjamin, E. J., Bhalla, K., Bin Abdulhak, A., Blyth, F., Bourne, R., Braithwaite, T., Brooks, P., Brugha, T. S., Bryan-Hancock, C., Buchbinder, R., Burney, P. et al. (2012). Common values in assessing health outcomes from disease and injury: disability weights measurement study for the Global Burden of Disease Study 2010. Lancet 380, 2129–2143.Google Scholar
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, 83–92.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, 1677–1681.Google Scholar
Sousa-Figueiredo, J. C., Basanez, M. G., Mgeni, A. F., Khamis, I. S., Rollinson, D. and Stothard, J. R. (2008). A parasitological survey, in rural Zanzibar, of pre-school children and their mothers for urinary schistosomiasis, soil-transmitted helminthiases and malaria, with observations on the prevalence of anaemia. Annals of Tropical Medicine and Parasitology 102, 679–692.Google Scholar
Sousa-Figueiredo, J. C., Pleasant, J., Day, M., Betson, M., Rollinson, D., Montresor, A., Kazibwe, F., Kabatereine, N. B. and Stothard, J. R. (2010). Treatment of intestinal schistosomiasis in Ugandan preschool children: best diagnosis, treatment efficacy and side-effects, and an extended praziquantel dosing pole. International Health 2, 103–113.Google Scholar
Stephenson, L. S., Latham, M. C., Kurz, K. M., Kinoti, S. N., Oduori, M. L. and Crompton, D. W. (1985 a). Relationships of Schistosoma haematobium, hookworm and malarial infections and metrifonate treatment to growth of Kenyan school children. American Journal of Tropical Medicine and Hygiene 34, 1109–1118.Google Scholar
Stephenson, L. S., Latham, M. C., Kurz, K. M., Miller, D., Kinoti, S. N. and Oduori, M. L. (1985 b). Urinary iron loss and physical fitness of Kenyan children with urinary schistosomiasis. American Journal of Tropical Medicine and Hygiene 34, 322–330.Google Scholar
Stothard, J. R., Sousa-Figueiredo, J. C., Betson, M., Green, H. K., Seto, E. Y., Garba, A., Sacko, M., Mutapi, F., Vaz Nery, S., Amin, M. A., Mutumba-Nakalembe, M., Navaratnam, A., Fenwick, A., Kabatereine, N. B., Gabrielli, A. F. and Montresor, A. (2011). Closing the praziquantel treatment gap: new steps in epidemiological monitoring and control of schistosomiasis in African infants and preschool-aged children. Parasitology 138, 1593–1606.Google Scholar
Stothard, J. R., Sousa-Figueiredo, J. C., Betson, M., Bustinduy, A. and Reinhard-Rupp, J. (2013). Schistosomiasis in African infants and preschool children: let them now be treated! Trends in Parasitology 29, 197–205.Google Scholar
Stothard, J. R., Stanton, M. C., Bustinduy, A. L., Sousa-Figueiredo, J. C., Van Dam, G. J., Betson, M., Waterhouse, D., Ward, S., Allan, F., Hassan, A. A., Al-Helal, M. A., Memish, Z. A. and Rollinson, D. (2014). Diagnostics for schistosomiasis in Africa and Arabia: a review of present options in control and future needs for elimination. Parasitology 141, 1947–1961.Google Scholar
Stothard, J. R., Kabatereine, N. B., Archer, J., Al-Shehri, H., Tchuem-Tchuente, L. A., Gyapong, M. and Bustinduy, A. L. (2016). A centenary of Robert T. Leiper's lasting legacy on schistosomiasis and a COUNTDOWN on control of neglected tropical diseases. Parasitology 1–11. doi: 10.1017/S0031182016000998.Google Scholar
Terer, C. C., Bustinduy, A. L., Magtanong, R. V., Muhoho, N., Mungai, P. L., Muchiri, E. M., Kitron, U., King, C. H. and Mutuku, F. M. (2013). Evaluation of the health-related quality of life of children in Schistosoma haematobium-endemic communities in Kenya: a cross-sectional study. PloS Neglected Tropical Diseases 7, e2106.Google Scholar
Van Dam, G. J., Xu, J., Bergquist, R., de Dood, C. J., Utzinger, J., Qin, Z. Q., Guan, W., Feng, T., Yu, X. L., Zhou, J., Zheng, M., Zhou, X. N. and Corstjens, P. L. (2015). An ultra-sensitive assay targeting the circulating anodic antigen for the diagnosis of Schistosoma japonicum in a low-endemic area, People's Republic of China. Acta Tropica 141, 190–197.Google Scholar
Verani, J. R., Abudho, B., Montgomery, S. P., Mwinzi, P. N., Shane, H. L., Butler, S. E., Karanja, D. M. and Secor, W. E. (2011). Schistosomiasis among young children in Usoma, Kenya. American Journal of Tropical Medicine and Hygiene 84, 787–791.Google Scholar
Vos, T., Flaxman, A. D., Naghavi, M., Lozano, R., Michaud, C., Ezzati, M., Shibuya, K., Salomon, J. A., Abdalla, S., Aboyans, V., Abraham, J., Ackerman, I., Aggarwal, R., Ahn, S. Y., Ali, M. K., Alvarado, M., Anderson, H. R., Anderson, L. M., Andrews, K. G., Atkinson, C., Baddour, L. M., Bahalim, A. N., Barker-Collo, S., Barrero, L. H., Bartels, D. H., Basanez, M. G., Baxter, A., Bell, M. L., Benjamin, E. J., Bennett, D. et al. (2012). Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380, 2163–2196.CrossRefGoogle ScholarPubMed
Wamachi, A. N., Mayadev, J. S., Mungai, P. L., Magak, P. L., Ouma, J. H., Magambo, J. K., Muchiri, E. M., Koech, D. K., King, C. H. and King, C. L. (2004). Increased ratio of tumor necrosis factor-alpha to interleukin-10 production is associated with Schistosoma haematobium-induced urinary-tract morbidity. Journal of Infectious Diseases 190, 2020–2030.Google Scholar
Wang, L., Utzinger, J. and Zhou, X. N. (2008). Schistosomiasis control: experiences and lessons from China. Lancet 372, 1793–1795.Google Scholar
Wang, X., Gurarie, D., Mungai, P. L., Muchiri, E. M., Kitron, U. and King, C. H. (2012). Projecting the long-term impact of school- or community-based mass-treatment interventions for control of Schistosoma infection. PloS Neglected Tropical Diseases 6, e1903.Google Scholar
Warren, K. S., Siongok, T. K., Ouma, J. H. and Houser, H. B. (1978). Hycanthone dose-response in Schistosoma mansoni infection in Kenya. Lancet 1, 352–354.Google Scholar
Warren, K. S., Mahmoud, A. A., Muruka, J. F., Whittaker, L. R., Ouma, J. H. and Arap Siongok, T. K. (1979). Schistosomiasis haematobia in coast province Kenya. Relationship between egg output and morbidity. American Journal of Tropical Medicine and Hygiene 28, 864–870.Google Scholar
Webbe, G. (1982). The intermediate hosts and host-parasite relationships. In Schistosomiasis Epidemiology, Treatment and Control (eds. Jordan, P. and Webbe, G.), pp. 16–49. Heinemann, London.Google Scholar
World Health Organization. (2007). Integrated Management of Childhood Illnesses, World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization. (2011). Report of a Meeting to Review the Results of Studies on the Treatment of Schistosomiasis in Preschool-aged Children. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization. (2012). Accelerating Work to Overcome the Global Impact of Neglected Tropical Diseases : A Roadmap for Implementation: Executive Summary, World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization. (2016). Schistosomiasis: number of people treated worldwide in 2014. The Weekly Epidemiological Record 91, 53–60. World Health Organization, Geneva, Switzerland.Google Scholar
Xiao, S. H. (2005). Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemisinins. Acta Tropica 96, 153–167.Google Scholar