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

Published online by Cambridge University Press:  15 June 2009

J. P. WEBSTER ,
A. KOUKOUNARI ,
P. H. L. LAMBERTON ,
J. R. STOTHARD  and
A. FENWICK
J. P. WEBSTER*
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London, W2 1PG, UK
A. KOUKOUNARI
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London, W2 1PG, UK
P. H. L. LAMBERTON
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London, W2 1PG, UK
J. R. STOTHARD
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
A. FENWICK
Affiliation:
Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College (St Mary's Campus), Norfolk Place, London, W2 1PG, UK
*
*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: [email protected]
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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.

Keywords

SchistosomiasismorbiditydiagnosiscontrolAfrica
Type
SECTION 4 MONITORING AND EVALUATION OF INTERVENTIONS
Information
Parasitology , Volume 136 , Special Issue 13: Control of schistosomiasis in sub-Saharan Africa , November 2009 , pp. 1789 - 1799
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

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, 1039–1048.CrossRefGoogle ScholarPubMed
Bergquist, R., Johansen, M. V. and Utzinger, J. (2009). Diagnostic dilemmas in helminthology: what tools to use and when? Trends in Parasitology 25, 151–156.CrossRefGoogle ScholarPubMed
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, 1644–1649.CrossRefGoogle ScholarPubMed
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, 484–490.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 24–30.CrossRefGoogle ScholarPubMed
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, 1517–1524.CrossRefGoogle ScholarPubMed
Clavant, S. P., Osicka, T. M. and Comper, W. D. (2007). Albuminuria: its importance in disease detection. Laboratory Medicine 38, 35–38.CrossRefGoogle Scholar
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, 409–415.CrossRefGoogle ScholarPubMed
Feldmeier, H., Leutscher, P., Poggensee, G. and Harms, G. (1999). Male genital schistosomiasis and haemospermia. Tropical Medicine and International Health 4, 791–793.CrossRefGoogle ScholarPubMed
Fenwick, A. (2009). Host-parasite relations and implications for control. Advances in Parasitology 68, 247–261.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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), 245–248.CrossRefGoogle ScholarPubMed
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, 219–228.CrossRefGoogle ScholarPubMed
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, 777–787.Google ScholarPubMed
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, 23–33.CrossRefGoogle ScholarPubMed
Jamison, D. T., Mosley, H., Measham, A. R. and Bobadilla, J. L. (1993) Disease Control Priorities in Developing Countries, New York, Oxford University Press.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, 91–99.Google ScholarPubMed
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, 208–215.CrossRefGoogle ScholarPubMed
King, C. H. and Dangerfield-Cha, M. (2008). The unacknowledged impact of chronic schistosomiasis. Chronic Illness 4, 65–79.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 1176–1182.CrossRefGoogle ScholarPubMed
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, 278–286.CrossRefGoogle ScholarPubMed
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, 659–669.CrossRefGoogle ScholarPubMed
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, 1042–1052.CrossRefGoogle ScholarPubMed
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.), 147–150.CrossRefGoogle ScholarPubMed
Lengeler, C., Utzinger, J. and Tanner, M. (2002). Screening for schistosomiasis with questionnaires. Trends in Parasitology 18, 375–377.CrossRefGoogle ScholarPubMed
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, 247–252.Google ScholarPubMed
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. 1–41.Google Scholar
Miguel, E. and Kremer, M. (2001) Worms: Education and Health Externalities in Kenya. NBER working paper w8481, Cambridge MA.CrossRefGoogle Scholar
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, 315–326.CrossRefGoogle ScholarPubMed
Richter, J. (2003). The impact of chemotherapy on morbidity due to schistosomiasis. Acta Tropica 86, 161–183.CrossRefGoogle ScholarPubMed
Richter, J., Hatz, C. and Häussinger, D. (2003). Ultrasound in tropical and parasitic diseases. Lancet 79, 199–206.Google Scholar
Ridley, R. G. (2006). Diagnostics take centre stage. Nature Reviews Microbiology 4 (Suppl.), S1.CrossRefGoogle Scholar
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, 199–206.CrossRefGoogle ScholarPubMed
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, 1212–1220.CrossRefGoogle ScholarPubMed
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, 439–449.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Stephenson, L. (1993). The impact of schistosomiasis on human nutrition. Parasitology 107, S107–123.CrossRefGoogle ScholarPubMed
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, 1099–1105.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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, 780–787.CrossRefGoogle ScholarPubMed
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, 289–298.Google 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, 373–374.CrossRefGoogle ScholarPubMed
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, 81–89.CrossRefGoogle Scholar
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/98.1Google Scholar
Wiest, P. M. (1996). The epidemiology of morbidity of schistosomiasis. Parasitology Today 12, 215–220.CrossRefGoogle ScholarPubMed
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, 193–211.Google Scholar
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, 245–250.CrossRefGoogle ScholarPubMed