Skip to main content Accessibility help
×
Home

Evaluation and application of potential schistosome-associated morbidity markers within large-scale mass chemotherapy programmes

  • J. P. WEBSTER (a1), A. KOUKOUNARI (a1), P. H. L. LAMBERTON (a1), J. R. STOTHARD (a2) and A. FENWICK (a1)...

Summary

A primary objective of schistosomiasis control programmes is to achieve, and hence also demonstrate, a quantifiable reduction in schistosome-associated morbidity as a consequence of chemotherapeutic intervention. Inherent within such an objective, it is necessary to define and validate direct and indirect indicators of schistosome-related morbidity. However, to define and thereby document such morbidity, and its reduction following treatment, may not be straightforward, particularly for intestinal schistosomiasis-induced morbidity, which is often not apparent in all but the most severe or chronic cases. Within all ‘Schistosomiasis Control Initiative’ activities, across selected sub-Saharan African countries since 2002, a range of standard and novel potential morbidity markers have been monitored and evaluated. Parasitological intensity measures, combined with haemoglobin/anaemia counts and ultrasonography, proved valuable schistosomiasis-related morbidity indicators, being both logistically practical and informative. Additional measures tested, such as albumin excretion profiles, were promising, and are subject to ongoing research, whilst some measures, such as distended stomach/umbilical circumference, anthropometrics and health questionnaires proved less reliable. These results serve to both illustrate the success of current control activities in reducing schistosome-induced morbidity, and to highlight key tools and techniques for continued application within ongoing and future mass drug administration programmes.

Copyright

Corresponding author

*Corresponding author: Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London, W2 1PG, UK. Tel: +44 (0) 20 75943636; Fax: +44 (0) 20 74023927. E-mail: joanne.webster@imperial.ac.uk

References

Hide All
Balen, J., Stothard, J. R., Kabatereine, N. B., Tukahebwa, E. M., Kazibwe, F., Whawell, S., Webster, J. P., Utzinger, J. and Fenwick, A. (2006). Morbidity due to Schistosoma mansoni: an epidemiological assessment of distended abdomen syndrome in Ugandan school children with observations before and 1-year after anthelminthic chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 10391048.
Bergquist, R., Johansen, M. V. and Utzinger, J. (2009). Diagnostic dilemmas in helminthology: what tools to use and when? Trends in Parasitology 25, 151156.
Blanton, R. E., Salam, E. A., Kariuki, H. C., Magak, P., Silva, L. K., Muchiri, E. M., Thiongo, F., Abdel-Meghid, I. E., Butterworth, A. E., Reis, M. G. and Ouma, J. H. (2002). Population-based differences in Schistosoma mansoni and hepatitis C-induced disease. Journal of Infectious Diseases 185, 16441649.
Booth, M., Mayombana, C., Machibya, H., Masanja, H., Odermatt, P., Utzinger, J. and Kilima, P. (1998). The use of morbidity questionnaires to identify communities with high prevalences of schistosome or geohelminth infections in Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 484490.
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, 525531.
Campagne, G., Garba, A., Barkire, H., Vera, C., Sidiki, A. and Chippaux, J. P. (2001). Continued ultrasonic follow-up of children infected with Schistosoma haematobium after treatment with praziquantel. Tropical Medicine and International Health 6, 2430.
Carabin, H., Balolong, E., Joseph, L., McGarvey, S. T., Johansen, M. V., Fernandez, T., Willingham, A. L. and Olveda, R. (2005). Estimating sensitivity and specificity of a faecal examination method for Schistosoma japonicum infection in cats, dogs, water buffaloes, pigs, and rats in Western Samar and Sorsogon provinces, The Philippines. International Journal for Parasitology 35, 15171524.
Clavant, S. P., Osicka, T. M. and Comper, W. D. (2007). Albuminuria: its importance in disease detection. Laboratory Medicine 38, 3538.
Doehring-Schwerdtfeger, E., Abdel-Rahim, I. M., Kardorff, R., Kaiser, C., Franke, D., Schlake, J., Richter, J., Elsheikh, M., Mohamed-Ali, Q. and Ehrich, J. H. (1992). Ultrasonographical investigation of periportal fibrosis in children with Schistosoma mansoni infection: reversibility of morbidity twenty-three months after treatment with praziquantel. American Journal of Tropical Medicine and Hygiene 46, 409415.
Feldmeier, H., Leutscher, P., Poggensee, G. and Harms, G. (1999). Male genital schistosomiasis and haemospermia. Tropical Medicine and International Health 4, 791793.
Fenwick, A. (2009). Host-parasite relations and implications for control. Advances in Parasitology 68, 247261.
Fenwick, A., Webster, J. P., Bosque-Oliva, E., Blair, L., Fleming, F., Zhang, Y., Garba, A., Stothard, J. R., Gabrielli, A. F., Clements, A. C. A., Kabatereine, N. B., Toure, S., Dembele, R., Nyandini, U., Mwansa, J and Koukounaris, A. (2009). The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002 to 2008. Parasitology 136.
Gerspacher-Lara, R., Pinto-Silva, R. A., Serufo, J. C., Rayes, A. A., Drummond, S. C. and Lambertucci, J. R. (1998). Splenic palpation for the evaluation of morbidity due to schistosomiasis mansoni. Memórias do Instituto Oswaldo Cruz 93 (Suppl. 1), 245248.
Gryseels, B. and Nkulikyinka, L. (1989). Two-year follow-up of Schistosoma mansoni infection and morbidity after treatment with different regimens of oxamniquine and praziquantel. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 219228.
Hatz, C., Savioli, L., Mayombana, C., Dhunputh, J., Kisumku, U. M. and Tanner, M. (1990). Measurement of schistosomiasis-related morbidity at community level in areas of different endemicity. Bulletin of World Health Organization 68, 777787.
Hotez, P., Ottesen, E., Fenwick, A. and Molyneux, D. (2006). The neglected tropical diseases: the ancient afflictions of stigma and poverty and the prospects for their control and elimination. Advances in Experimental Medicine and Biology 582, 2333.
Jamison, D. T., Mosley, H., Measham, A. R. and Bobadilla, J. L. (1993) Disease Control Priorities in Developing Countries, New York, Oxford University Press.
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.
Kabatereine, N. B., Tukahebwa, E., Kazibwe, F., Namwangye, H., Zaramba, S., Brooker, S., Stothard, J. R., Kamenka, C., Whawell, S., Webster, J. P. and Fenwick, A. (2006). Progress towards countrywide control of schistosomiasis and soil-transmitted helminthiasis in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 208215.
King, C. H. and Dangerfield-Cha, M. (2008). The unacknowledged impact of chronic schistosomiasis. Chronic Illness 4, 6579.
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.
King, C. L., Malhotra, I., Mungai, P., Wamachi, A., Kioko, J., Muchiri, E. and Ouma, J. H. (2001). Schistosoma haematobium-induced urinary tract morbidity correlates with increased tumour necrosis factor-alpha and diminished interleukin-10 production. Journal of Infectious Diseases 184, 11761182.
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 b). 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, 278286.
Koukounari, A., Gabrielli, A. F., Touré, S., Bosque-Oliva, E., Zhang, Y., 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, 659669.
Koukounari, A., Sacko, M., Gabrielli, A., Landouré, A., Dembelé, R., Clements, A., Whawell, S., Donnelly, C. A., Fenwick, A., Traoré, M. and Webster, J. P. (2006 a). Assessment of ultrasound morbidity indicators for schistosomiasis in the context of large-scale programmes illustrated with experiences from Malian children. American Journal of Tropical Medicine and Hygiene 75, 10421052.
Lambertucci, J. R., Cota, G. F., Pinto-Silva, R. A., Serufo, J. C., Gerspacher-Lara, R., Costa Drummond, S., Antunes, C. M., Nobre, V. and Rayes, A. (2001). Hepatosplenic schistosomiasis in field-based studies: a combined clinical and sonographic definition. Memórias do Instituto Oswaldo Cruz 96 (Suppl.), 147150.
Lengeler, C., Utzinger, J. and Tanner, M. (2002). Screening for schistosomiasis with questionnaires. Trends in Parasitology 18, 375377.
Lwambo, N. J. S., Savioli, L., Kisumku, U. M., Alawi, K. S. and Bundy, D. A. P. (1997). Control of Schistosoma haematobium morbidity on Pemba Island: validity and efficiency of indirect screening tests. Bulletin of World Health Organization 75, 247252.
Michaud, C. A., Gordon, W. S. and Reich, M. R. (2004). The global burden of disease due to schistosomiasis. Working Paper Series Harvard Center for Population and Development Studies, Harvard School of Public Health, Cambridge, MA, USA, pp. 141.
Miguel, E. and Kremer, M. (2001) Worms: Education and Health Externalities in Kenya. NBER working paper w8481, Cambridge MA.
Odogwu, S. E., Ramamurthy, N. K., Kabaterenine, 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, 315326.
Richter, J. (2003). The impact of chemotherapy on morbidity due to schistosomiasis. Acta Tropica 86, 161183.
Richter, J., Hatz, C. and Häussinger, D. (2003). Ultrasound in tropical and parasitic diseases. Lancet 79, 199206.
Ridley, R. G. (2006). Diagnostics take centre stage. Nature Reviews Microbiology 4 (Suppl.), S1.
Rollinson, D., Klinger, E. V., Mgeni, A. F., Khamis, I. S. and Stothard, J. R. (2005). Urinary schistosomiasis on Zanzibar: application of two novel assays for the detection of excreted albumin and haemoglobin in urine. Journal of Helminthology 79, 199206.
Ross, A. G. P., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y., Williams, G. M. and McManus, D. P. (2002). Schistosomiasis. New England Journal of Medicine 346, 12121220.
Salih, S. Y., Marshall, T. F. and Radalowicz, A. (1979). Morbidity in relation to the clinical forms and to intensity of infection in Schistosoma mansoni infections in the Sudan. Annals of Tropical Medicine and Parasitology 73, 439449.
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.
Stephenson, L. (1993). The impact of schistosomiasis on human nutrition. Parasitology 107, S107123.
Stoltzfus, R. J., Albonico, M., Tielsch, J. M., Chwaya, H. M. and Savioli, L. (1997). Linear growth retardation in Zanzibari school children. Journal of Nutrition 127, 10991105.
Swai, B., Poggensee, G., Mtweve, S. and Krantz, I. (2006). Female genital schistosomiasis as evidence of a neglected cause for reproductive ill-health: a retrospective histopathological study from Tanzania. BMC Infectious Diseases 6, 134.
Tohon, Z. B., Mainassara, H. B., Garba, A., Mahamane, A. E., Bosqué-Oliva, E., Maman-Laminou, I., Duchemin, J-B, Chanteau, S. and Boisier, P. (2008). Controlling schistosomiasis: significant decrease of anaemia prevalence one year after a single dose of praziquantel in Nigerien schoolchildren. PLoS Neglected Tropical Diseases 2, e241.
Touré, S., Zhang, Y., Bosque-Oliva, E., Ky, C., Ouedraogo, A., Koukounari, A., Gabrielli, A. F., Sellin, B., Webster, J. P. and Fenwick, A. (2008) Two-year impact of single praziquantel treatment in the national control programme on schistosomiasis by preventive chemotherapy in Burkina Faso. Bulletin of the World Health Organization 86, 780787.
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 World Health Organization 78, 289298.
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.
Vennervald, B. J., Kahama, A. I. and Reimert, C. M. (2000). Assessment of morbidity in Schistosoma haematobium infection: current methods and future tools. Acta Tropica 77, 8189.
WHO (1998). Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level. A guide for managers of control programmes. WHO/CTD/SIP/98.1
Wiest, P. M. (1996). The epidemiology of morbidity of schistosomiasis. Parasitology Today 12, 215220.
Williams, E. H., Hayes, R. J. and Smith, P. G. (1986). Admissions to a rural hospital in the West Nile district of Uganda over a 27 year period. Journal of Tropical Medicine and Hygiene 89, 193211.
Zhou, H., Ross, A. G. P., Hartel, G. F., Sleigh, A. C., Williams, G. M., McManus, D. P., Luo, X. S., He, Y. and Li, Y. S. (1998). Diagnosis of schistosomiasis japonica in Chinese schoolchildren by administration of a questionnaire. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 245250.

Keywords

Evaluation and application of potential schistosome-associated morbidity markers within large-scale mass chemotherapy programmes

  • J. P. WEBSTER (a1), A. KOUKOUNARI (a1), P. H. L. LAMBERTON (a1), J. R. STOTHARD (a2) and A. FENWICK (a1)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed