Hostname: page-component-6bf8c574d5-xtvcr Total loading time: 0 Render date: 2025-02-15T11:15:31.390Z Has data issue: false hasContentIssue false
  • English
  • Français

Treatment of urinary schistosomiasis: methodological issues and research needs identified through a Cochrane systematic review

Published online by Cambridge University Press:  03 June 2009

A. DANSO-APPIAH ,
P. GARNER ,
P. L. OLLIARO  and
J. UTZINGER
A. DANSO-APPIAH*
Affiliation:
International Health Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK Department of Public Health, Erasmus MC, University Medical Center Rotterdam, P.O. Box 2040, 3000 CA Rotterdam, The Netherlands
P. GARNER
Affiliation:
International Health Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
P. L. OLLIARO
Affiliation:
UNICEF/UNDP/World Bank/WHO Special Programme on Research and Training in Tropical Diseases, World Health Organization, 20 Avenue Appia, CH-1211 Geneva 27, Switzerland
J. UTZINGER
Affiliation:
Department of Public Health and Epidemiology, Swiss Tropical Institute, P.O. Box, CH-4002 Basel, Switzerland
*
*Corresponding author: Anthony Danso-Appiah, International Health Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Guidelines recommend praziquantel (PZQ) for the treatment and control of schistosomiasis, with no real alternative. Metrifonate was still widely used against Schistosoma haematobium in the 1990s, and then withdrawn. Experimental studies and clinical trials suggest that artemisinin compounds are active against S. haematobium. In a Cochrane systematic review assessing the efficacy and safety of drugs for treating urinary schistosomiasis, 24 randomized controlled trials (n=6315 individuals) met our inclusion criteria. These trials compared a variety of single agent and combination regimens with PZQ, metrifonate or artemisinin derivatives. The review confirmed that both the standard recommended doses of PZQ (single 40 mg/kg oral dose) and metrifonate (3×7·5–10 mg/kg oral doses administered fortnightly) are efficacious and safe in treating urinary schistosomiasis, but there is no study comparing these two regimens head-to-head. There is currently not enough evidence to evaluate artemisinin compounds. Most of the studies included in the Cochrane systematic review were insufficiently powered, lacked standardization in assessing and reporting outcomes, and had a number of methodological limitations. In this paper we discuss the implications of these findings with respect to public health and research methodology and propose priority research needs.

Keywords

schistosomiasisurinary schistosomiasisSchistosoma haematobiumsystematic reviewmeta-analysispraziquantelmetrifonateartemisinin
Type
SECTION 5 TOWARDS FUTURE USE OF PRAZIQUANTEL
Information
Parasitology , Volume 136 , Special Issue 13: Control of schistosomiasis in sub-Saharan Africa , November 2009 , pp. 1837 - 1849
Copyright
Copyright © 2009 Cambridge University Press

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

Aden Abdi, Y. and Gustafsson, L. L. (1989). Field trial of the efficacy of a simplified and standard metrifonate treatments of Schistosoma haematobium. European Journal of Clinical Pharmacology 37, 371–374.Google Scholar
Altman, D. G., Schulz, K. F., Moher, D., Egger, M., Davidoff, F., Elbourne, D., Gotzsche, P. C. and Lang, T. (2001). The revised CONSORT statement for reporting randomized trials: explanation and elaboration. Annals of Internal Medicine 134, 663–694.Google Scholar
Beasley, N. M. R., Tomkins, A. M., Hall, A., Kihamia, C. M., Lorri, W., Nduma, B., Issae, W., Nokes, C. and Bundy, D. A. P (1999). The impact of population level deworming on the haemoglobin levels of schoolchildren in Tanga, Tanzania. Tropical Medicine and International Health 4, 744–750.Google Scholar
Befidi-Mengue, R. N., Ratard, R. C., Beltran, G., D'Alessandro, A., Rice, J., Befidi-Mengue, R., Kouemeni, L. E. and Cline, B. L. (1992). The impact of Schistosoma haematobium infection and of praziquantel treatment on the growth of primary school children in Bertoua, Cameroon. Journal of Tropical Medicine and Hygiene 95, 404–409.Google Scholar
Begg, C., Cho, M., Eastwood, S., Horton, R., Moher, D., Olkin, I., Pitkin, R., Rennie, D., Schulz, K. F., Simel, D. and Stroup, D. F. (1996). Improving the quality of reporting of randomized controlled trials. The CONSORT statement. JAMA 276, 637–639.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
Booth, M., Vounatsou, P., N'Goran, E. K., Tanner, M. and Utzinger, J. (2003). The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d'Ivoire. Parasitology 127, 525–531.Google Scholar
Borrmann, S., Szlezák, N., Faucher, J.-F., Matsiegui, P.-B., Neubauer, R., Binder, R. K., Lell, B. and Kremsner, P. G. (2001). Artesunate and praziquantel for the treatment of Schistosoma haematobium infections: a double-blind, randomized, placebo-controlled study. Journal of Infectious Diseases 184, 1363–1366.Google Scholar
Boulanger, D., Dieng, Y., Cisse, B., Remoue, F., Capuano, F., Dieme, J. L., Ndiaye, T., Sokhna, C., Trape, J. F., Greenwood, B. and Simondon, F. (2007). Antischistosomal efficacy of artesunate combination therapies administered as curative treatments for malaria attacks. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 113–116.Google Scholar
Caffrey, C. R. (2007). Chemotherapy of schistosomiasis: present and future. Current Opinion in Chemical Biology 11, 433–439.Google Scholar
Castro, N., Medina, R., Sotelo, J. and Jung, H. (2000). Bioavailability of praziquantel increases with concomitant administration of food. Antimicrobial Agents and Chemotherapy 44, 2903–2904.Google Scholar
Cioli, D. (2000). Praziquantel: is there real resistance and are there alternatives? Current Opinion in Infectious Diseases 13, 659–663.Google Scholar
Cioli, D., Pica-Mattoccia, L. and Archer, S. (1995). Antischistosomal drugs: past, present … and future? Pharmacology and Therapeutics 68, 35–85.Google Scholar
Danso-Appiah, A. and de Vlas, S. J. (2002). Interpreting low praziquantel cure rates of Schistosoma mansoni infections in Senegal. Trends in Parasitology 18, 125–129.Google Scholar
Danso-Appiah, A., Utzinger, J., Liu, J. and Olliaro, P. (2008). Drugs for treating urinary schistosomiasis. Cochrane Database Systematic Reviews CD000053.Google Scholar
Davis, A., Biles, J. E., Ulrich, A. M. and Dixon, H. (1981). Tolerance and efficacy of praziquantel in phase II A and II B therapeutic trials in Zambian patients. Arzneimittelforschung 31, 568–574.Google Scholar
De Clercq, D., Vercruysse, J., Kongs, A., Verlé, P., Dompnier, J. P. and Faye, P. C. (2002). Efficacy of artesunate and praziquantel in Schistosoma haematobium infected schoolchildren. Acta Tropica 82, 61–66.Google Scholar
de Vlas, S. J. and Gryseels, B. (1992). Underestimation of Schistosoma mansoni prevalences. Parasitology Today 8, 274–277.Google Scholar
Doehring, E., Ehrich, J. H., Vester, U., Feldmeier, H., Poggensee, U. and Brodehl, J. (1985). Proteinuria, hematuria, and leukocyturia in children with mixed urinary and intestinal schistosomiasis. Kidney International 28, 520–525.Google Scholar
Doenhoff, M. J. (1998). Is schistosomicidal chemotherapy sub-curative? Implications for drug resistance. Parasitology Today 14, 434–435.Google Scholar
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
Doenhoff, M. J., Sabah, A. A., Fletcher, C., Webbe, G. and Bain, J. (1987). Evidence for an immune-dependent action of praziquantel on Schistosoma mansoni in mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 947–951.Google Scholar
Feldmeier, H. and Chitsulo, L. (1999). Therapeutic and operational profiles of metrifonate and praziquantel in Schistosoma haematobium infection. Arzneimittelforschung 49, 557–565.Google Scholar
Feldmeier, H. and Doehring, E. (1987). Clinical experience with metrifonate. Review with emphasis on its use in endemic areas. Acta Tropica 44, 357–368.Google Scholar
Feldmeier, H. and Poggensee, G. (1993). Diagnostic techniques in schistosomiasis control. A review. Acta Tropica 52, 205–220.Google Scholar
Fenwick, A., Keiser, J. and Utzinger, J. (2006). Epidemiology, burden and control of schistosomiasis with particular consideration to past and current treatment trends. Drugs of the Future 31, 413–425.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, 509–515.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
Ghandour, A. M. (1978). The development of Schistosoma haematobium in the hamster. Annals of Tropical Medicine and Parasitology 72, 219–225.Google Scholar
Higgins, J. P. T. and Green, S. (2008). Cochrane Handbook for Systematic Reviews of Interventions. Version 5.0.1. The Cochrane Collaboration, 2008 (available from www.cochrane-handbook.org).Google Scholar
Holmstedt, B., Nordgren, I., Sandoz, M. and Sundwall, A. (1978). Metrifonate. Summary of toxicological and pharmacological information available. Archives of Toxicology 41, 3–29.Google Scholar
Inyang-Etoh, P. C., Ejezie, G. C., Useh, M. F. and Inyang-Etoh, E. C. (2004). Efficacy of artesunate in the treatment of urinary schistosomiasis, in an endemic community in Nigeria. Annals of Tropical Medicine and Parasitology 98, 491–499.Google Scholar
Inyang-Etoh, P. C., Ejezie, G. C., Useh, M. F. and Inyang-Etoh, E. C. (2009). Efficacy of a combination of praziquantel and artesunate in the treatment of urinary schistosomiasis in Nigeria. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 38–44.Google Scholar
Jewsbury, J. M. and Cooke, M. J. (1976). Prophylaxis of schistosomiasis – field trial of metrifonate for the prevention of human infection. Annals of Tropical Medicine and Parasitology 70, 361–363.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, 458–465.Google Scholar
Jinabhai, C. C., Taylor, M., Coutsoudis, A., Coovadia, H. M., Tomkins, A. M. and Sullivan, K. R. (2001) Epidemiology of helminth infections: implications for parasite control programmes, a South African perspective. Public Health Nutrition 4, 1211–1219.Google Scholar
Jüni, P., Altman, D. G. and Egger, M. (2001). Systematic reviews in health care: assessing the quality of controlled clinical trials. BMJ 323, 42–46.Google Scholar
Kardaman, M. W., Fenwick, A., el Igail, A. B., el Tayeb, M., Daffalla, A. A. and Dixon, H. G. (1985). Treatment with praziquantel of schoolchildren with concurrent Schistosoma mansoni and S. haematobium infections in Gezira, Sudan. Journal of Tropical Medicine and Hygiene 88, 105–109.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., 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, 1561–1569.Google Scholar
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., Mackay, W., Ransohoff, D., Houser, H., Koech, D., Siongok, T. K. A. 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., 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.Google Scholar
King, C. H., Wiper, D. W. 3rd, De Stigter, K. V., Peters, P. A. S., Koech, D., Ouma, J. H., Arap Siongok, T. K. and Mahmoud, A. A. F. (1989). Dose-finding study for praziquantel therapy of Schistosoma haematobium in Coast Province, Kenya. American Journal of Tropical Medicine and Hygiene 40, 507–513.Google Scholar
Leopold, G., Ungethum, W., Groll, E., Diekmann, H. W., Nowak, H. and Wegner, D. H. (1978). Clinical pharmacology in normal volunteers of praziquantel, a new drug against schistosomes and cestodes. An example of a complex study covering both tolerance and pharmacokinetics. European Journal of Clinical Pharmacology 14, 281–291.Google Scholar
López-Arrieta, J. M. and Schneider, L. (2006). Metrifonate for Alzheimer's disease. Cochrane Database Systematic Reviews CD003155.Google Scholar
Mandour, M. E., el Turabi, H., Homeida, M. M., el Sadig, T., Ali, H. M., Bennett, J. L., Leahey, W. J. and Harron, D. W. (1990). Pharmacokinetics of praziquantel in healthy volunteers and patients with schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 389–393.Google Scholar
McMahon, J. E. (1983). A comparative trial of praziquantel, metrifonate and niridazole against Schistosoma haematobium. Annals of Tropical Medicine and Parasitology 77, 139–142.Google Scholar
McMahon, J. E. and Kolstrup, N. (1979). Praziquantel: a new schistosomicide against Schistosoma haematobium. British Medical Journal 2 (6202), 1396–1398.Google Scholar
Moher, D., Schulz, K. F. and Altman, D. G. (2001). The CONSORT statement: revised recommendations for improving the quality of reports of parallel-group randomized trials. Annals of Internal Medicine 134, 657–662.Google Scholar
N'Goran, E. K., Utzinger, J., Gnaka, H. N., Yapi, A., N'Guessan, N. A., Kigbafori, S. D., Lengeler, C., Chollet, J., Xiao, S. H. and Tanner, M. (2003). Randomized, double-blind, placebo-controlled trial of oral artemether for the prevention of patent Schistosoma haematobium infections. American Journal of Tropical Medicine and Hygiene 68, 24–32.Google Scholar
N'Goran, E. K., Utzinger, J., N'Guessan, A. N., Müller, I., Zamble, K., Lohourignon, K. L., Traoré, M., Sosthene, B. A., Lengeler, C. and Tanner, M. (2001). Reinfection with Schistosoma haematobium following school-based chemotherapy with praziquantel in four highly endemic villages in Côte d'Ivoire. Tropical Medicine and International Health 6, 817–825.Google Scholar
Olds, G. R., King, C., Hewlett, J., Olveda, R., Wu, G., Ouma, J., Peters, P., McGarvey, S., Odhiambo, O., Koech, D., Liu, C. Y., Aligui, G., Gachihi, G., Kombe, Y., Parraga, I., Ramirez, B., Whalen, C., Horton, R. J. and Reeve, P. (1999). Double-blind placebo-controlled study of concurrent administration of albendazole and praziquantel in schoolchildren with schistosomiasis and geohelminths. Journal of Infectious Diseases 179, 996–1003.Google Scholar
Omer, A. H. (1981). Praziquantel in the treatment of mixed S. haematobium and S. mansoni infections. Arzneimittelforschung 31, 605–608.Google Scholar
Oyediran, A. B., Kofie, B. A., Bammeke, A. O. and Bamgboye, E. A. (1981). Clinical experience with praziquantel in the treatment of Nigerian patients infected with S. haematobium. Arzneimittelforschung 31, 581–584.Google Scholar
Plestina, R., Davis, A. and Bailey, D. R. (1972). Effect of metrifonate on blood cholinesterases in children during the treatment of schistosomiasis. Bulletin of the World Health Organization 46, 747–759.Google Scholar
Pugh, R. N. H. and Teesdale, C. H. (1983). Single dose oral treatment in urinary schistosomiasis: a double blind trial. British Medical Journal 286, 429–432.Google Scholar
Raso, G., N'Goran, E. K., Toty, A., Luginbühl, A., Adjoua, C. A., Tian-Bi, N. T., Bogoch, I. I., Vounatsou, P., Tanner, M. and Utzinger, J. (2004). Efficacy and side effects of praziquantel against Schistosoma mansoni in a community of western Côte d'Ivoire. Transactions of the Royal Society of Tropical Medicine and Hygiene 98, 18–27.Google Scholar
Rey, J. L., Nouhou, H. and Sellin, B. (1984). Comparaison de trois posologies de metrifonate en chimiotherapie de masse contre Schistosoma haematobium. Médecine Tropicale 44, 57–60.Google Scholar
Rey, J. L., Sellin, B., Gazere, O., Ott, D., Reges, M. and Garrouty, P. (1983). Comparaison au Niger de l'efficacite sur Schistosoma haematobium du praziquantel (30 mg/kg et 40 mg/kg) en une prise et de l'oltipraz (35 mg/kg) en deux prises. Medecine et Maladies Infectieuses 13, 328–331.Google Scholar
Sabah, A. A., Fletcher, C., Webbe, G. and Doenhoff, M. J. (1986). Schistosoma mansoni: chemotherapy of infections of different ages. Experimental Parasitology 61, 294–303.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
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, 226–231.Google Scholar
Schulz, K. F. and Grimes, D. A. (2002). Allocation concealment in randomised trials: defending against deciphering. Lancet 359, 614–618.Google Scholar
Snellen, W. M. (1981). Therapeutic properties of metrifonate. Acta Pharmacologica et Toxicologica 49 (Suppl. 5), 114–117.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, 411–425.Google Scholar
Stephenson, L. S., Kinoti, S. N., Latham, M. C., Kurz, K. M. and Kyobe, J. (1989). Single dose metrifonate or praziquantel treatment in Kenyan children. I. Effects on Schistosoma haematobium, hookworm, hemoglobin levels, splenomegaly, and hepatomegaly. American Journal of Tropical Medicine and Hygiene 41, 436–444.Google Scholar
Stephenson, L. S., Latham, M. C., Kurz, K. M., Kinoti, S. N., Oduori, M. L. and Crompton, D. W. T. (1985). 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
Taylor, P., Murare, H. M. and Manomano, K. (1988). Efficacy of low doses of praziquantel for Schistosoma mansoni and S. haematobium. Journal of Tropical Medicine and Hygiene 91, 13–17.Google Scholar
Tchuem Tchuenté, L. A., Shaw, D. J., Polla, L., Cioli, D. and Vercruysse, J. (2004). Efficacy of praziquantel against Schistosoma haematobium infection in children. American Journal of Tropical Medicine and Hygiene 71, 778–782.Google Scholar
The Cochrane Collaboration (2003). Review Manager (RevMan) 4.2 for Windows. The Nordic Cochrane Centre, Copenhagen.Google Scholar
Utzinger, J. and Keiser, J. (2004). Schistosomiasis and soil-transmitted helminthiasis: common drugs for treatment and control. Expert Opinion on Pharmacotherapy 5, 263–285.Google Scholar
Utzinger, J., Keiser, J., Xiao, S. H., Tanner, M. and Singer, B. H. (2003). Combination chemotherapy of schistosomiasis in laboratory studies and clinical trials. Antimicrobial Agents and Chemotherapy 47, 1487–1495.Google Scholar
Utzinger, J., Xiao, S. H., Tanner, M. and Keiser, J. (2007). Artemisinins for schistosomiasis and beyond. Current Opinion in Investigational Drugs 8, 105–116.Google Scholar
WHO (2002). Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Technical Repoort Series No. 912, 1–57.Google Scholar
Wilkins, H. A. and Moore, P. J. (1987). Comparative trials of regimes for the treatment of urinary schistosomiasis in The Gambia. Journal of Tropical Medicine and Hygiene 90, 83–92.Google Scholar