Volume 83, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



To control intestinal schistosomiasis at a national level in sub-Saharan Africa, there is a need for field-applicable markers to measure morbidity associated with this disease. The purpose of this study was to determine whether fecal calprotectin or fecal occult blood assays could be used as morbidity indicators for intestinal schistosomiasis. The study was carried out in Uganda with a cohort of young children (n = 1,327) and their mothers (n = 726). The prevalence of egg-patent schistosomiasis was 27.2% in children and 47.6% in mothers. No association was found between schistosomiasis infection and fecal calprotectin in children (n = 83, odds ratio [OR] = 1.08, = 0.881), although an inverse relationship (n = 58, OR = 0.17, = 0.043) was found in mothers. Fecal occult blood was strongly associated with infection in children (n = 814, OR = 2.30, < 0.0001) and mothers (n = 448, OR = 1.95, = 0.004). Fecal occult blood appears to be useful for measuring morbidity associated with intestinal schistosomiasis and could be used in assessing the impact of control programs upon disease.


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  1. Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, , 2006. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411425.[Crossref]
  2. Gryseels B, Polman K, Clerinx J, Kestens L, , 2006. Human schistosomiasis. Lancet 368: 11061118.[Crossref]
  3. van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, Habbema JD, Engels D, , 2003. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86: 125139.[Crossref]
  4. Ongom VL, Owor R, Grundy R, Bradley DJ, , 1972. The epidemiology and consequences of Schistosoma mansoni infection in West Nile, Uganda. II. Hospital investigation of a sample from the Panyagoro community. Trans R Soc Trop Med Hyg 66: 852863.[Crossref]
  5. Owor R, , 1971. Pathological aspects of schistosomiasis in Uganda with particular reference to West Nile. East Afr Med J 48: 399405.
  6. von Lichtenberg F, Rollinson D, Simpson AJG, , 1987. Consequences of infections with schistosomes. , eds. The Biology of Schistosomes. From Genes to Latrines. London: Academic Press Ltd., 185232.
  7. Montes M, White AC, Jr Kontoyiannis DP, , 2004. Symptoms of intestinal schistosomiasis presenting during treatment of large B cell lymphoma. Am J Trop Med Hyg 71: 552553.
  8. Nelson GS, , 1958. Schistosoma mansoni infection in the West Nile District of Uganda. IV. Anaemia and S. mansoni infection. East Afr Med J 35: 581586.
  9. Owor R, Madda JP, , 1977. Schistosomiasis causing tumour-like lesions. East Afr Med J 54: 137141.
  10. Ongom VL, Bradley DJ, , 1972. The epidemiology and consequences of Schistosoma mansoni infection in West Nile, Uganda. I. Field studies of a community at Panyagoro. Trans R Soc Trop Med Hyg 66: 835851.[Crossref]
  11. King CH, Dickman K, Tisch DJ, , 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 15611569.[Crossref]
  12. Lamyman MJ, Noble DJ, Narang S, Dehalvi N, , 2006. Small bowel obstruction secondary to intestinal schistosomiasis. Trans R Soc Trop Med Hyg 100: 885887.[Crossref]
  13. Pearce EJ, MacDonald AS, , 2002. The immunobiology of schistosomiasis. Nat Rev Immunol 2: 499511.[Crossref]
  14. Lambertucci JR, dos Santos Silva LC, Andrade LM, de Queiroz LC, Carvalho VT, Voieta I, Antunes CM, , 2008. Imaging techniques in the evaluation of morbidity in schistosomiasis mansoni. Acta Trop 108: 209217.[Crossref]
  15. Vennervald BJ, Dunne DW, , 2004. Morbidity in schistosomiasis: an update. Curr Opin Infect Dis 17: 439447.[Crossref]
  16. Fenwick A, Webster JP, Bosque-Oliva E, Blair L, Fleming FM, Zhang Y, Garba A, Stothard JR, Gabrielli AF, Clements AC, Kabatereine NB, Toure S, Dembele R, Nyandindi U, Mwansa J, Koukounari A, , 2009. The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology 136: 17191730.[Crossref]
  17. Bundy DA, Shaeffer S, Jukes M, Beegle K, Gillespie A, Drake L, Lee SF, Hoffman AM, Jones J, Mitchell A, Wright C, Barcelona D, Camara B, Golmar C, Savioli L, Takeuchi T, Sembene M, Breman JG, Meacham AR, Alleyne G, Claeson M, Evans D, Jha P, Mills A, Musgrove P, , 2005. School-based health and nutrition programs. , eds. Disease Control Priorities in Developing Countries. Oxford, United Kingdom: Oxford University Press, 10911108.
  18. Stothard JR, Gabrielli AF, , 2007. Schistosomiasis in African infants and preschool children: to treat or not to treat? Trends Parasitol 23: 8386.[Crossref]
  19. Sousa-Figueiredo JC, Pleasant J, Day M, Betson M, Rollinson D, Montresor A, Kazibwe F, Kabatereine NB, Stothard JR, , 2010. Treatment of intestinal schistosomiasis in Ugandan preschool children: best diagnosis, treatment efficacy and side-effects, and an extended praziquantel dosing pole. Int Health 2: 103113.[Crossref]
  20. Webster JP, Koukounari A, Lamberton PH, Stothard JR, Fenwick A, , 2009. Evaluation and application of potential schistosome-associated morbidity markers within large-scale mass chemotherapy programmes. Parasitology 136: 17891799.[Crossref]
  21. Lengeler C, Utzinger J, Tanner M, , 2002. Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa. Bull World Health Organ 80: 235242.
  22. Reimert CM, Tukahebwa EM, Kabatereine NB, Dunne DW, Vennervald BJ, , 2008. Assessment of Schistosoma mansoni induced intestinal inflammation by means of eosinophil cationic protein, eosinophil protein X and myeloperoxidase before and after treatment with praziquantel. Acta Trop 105: 253259.[Crossref]
  23. Kerkhoff C, Klempt M, Sorg C, , 1998. Novel insights into structure and function of MRP8 (S100A8) and MRP14 (S100A9). Biochim Biophys Acta 1448: 200211.[Crossref]
  24. Foell D, Wittkowski H, Roth J, , 2009. Monitoring disease activity by stool analyses: from occult blood to molecular markers of intestinal inflammation and damage. Gut 58: 859868.[Crossref]
  25. Gisbert JP, McNicholl AG, , 2009. Questions and answers on the role of faecal calprotectin as a biological marker in inflammatory bowel disease. Dig Liver Dis 41: 5666.[Crossref]
  26. Hewitson P, Glasziou P, Watson E, Towler B, Irwig L, , 2008. Cochrane systematic review of colorectal cancer screening using the fecal occult blood test (hemoccult): an update. Am J Gastroenterol 103: 15411549.[Crossref]
  27. Lehman JS, Jr Mott KE, Morrow RH, Jr Muniz TM, Boyer MH, , 1976. The intensity and effects of infection with Schistosoma mansoni in a rural community in northeast Brazil. Am J Trop Med Hyg 25: 285294.
  28. Kanzaria HK, Acosta LP, Langdon GC, Manalo DL, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, , 2005. Schistosoma japonicum and occult blood loss in endemic villages in Leyte, the Philippines. Am J Trop Med Hyg 72: 115118.
  29. Katz N, Chaves A, Pellegrino J, , 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397400.
  30. Montresor A, Crompton DW, Hall A, Bundy DA, Savioli L, , 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at the Community Level. A Guide for Managers of Control Programmes. Geneva: World Health Organization.
  31. Kirkwood BR, Sterne JA, , 2003. Essential Medical Statistics. Oxford, UK: Blackwell Science.
  32. Fisher RA, , 1922. On the interpretation of chi-square from contingency tables and the calculation of P. JR Stat Soc 85: 8794.
  33. Ansell J, Guyatt HL, , 2002. Comparative cost-effectiveness of diagnostic tests for urinary schistosomiasis and the implications for school health programmes. Ann Trop Med Parasitol 96: 145153.[Crossref]
  34. Raso G, Luginbuhl A, Adjoua CA, Tian-Bi NT, Silue KD, Matthys B, Vounatsou P, Wang Y, Dumas ME, Holmes E, Singer BH, Tanner M, N'Goran EK, Utzinger J, , 2004. Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Cote d'Ivoire. Int J Epidemiol 33: 10921102.[Crossref]
  35. Rudge JW, Stothard JR, Basanez MG, Mgeni AF, Khamis IS, Khamis AN, Rollinson D, , 2008. Micro-epidemiology of urinary schistosomiasis in Zanzibar: local risk factors associated with distribution of infections among schoolchildren and relevance for control. Acta Trop 105: 4554.[Crossref]
  36. Yang TH, Tzeng S, Cheng I, Burnett MG, Yoshizawa Y, Fukuyama K, Lee SC, Epstein WL, , 1997. Identification of the mouse calcium-binding proteins, MRP 8 and MRP 14, in Schistosoma mansoni-induced granulomas: biochemical and functional characterization. J Leukoc Biol 61: 258266.
  37. Jeffery J, Joshi S, Lewis SJ, Creanor S, Ayling RM, , 2009. Age-related faecal calprotectin, lactoferrin, and tumour M2-PK concentrations in healthy volunteers. Ann Clin Biochem 47: 259263.
  38. Campeotto F, Butel MJ, Kalach N, Derrieux S, Aubert-Jacquin C, Barbot L, Francoual C, Dupont C, Kapel N, , 2004. High faecal calprotectin concentrations in newborn infants. Arch Dis Child Fetal Neonatal Ed 89: F353F355.[Crossref]
  39. Savino F, Castagno E, Calabrese R, Viola S, Oggero R, Miniero R, , 2009. High faecal calprotectin levels in healthy, exclusively breast-fed infants. Neonatology 97: 299304.[Crossref]
  40. Damms A, Bischoff SC, , 2008. Validation and clinical significance of a new calprotectin rapid test for the diagnosis of gastrointestinal diseases. Int J Colorectal Dis 23: 985992.[Crossref]
  41. Shastri Y, Povse N, Stein J, , 2009. A prospective comparative study for new rapid bedside fecal calprotectin test with an established ELISA to assess intestinal inflammation. Clin Lab 55: 5355.
  42. Stothard JR, Pleasant J, Oguttu D, Adriko M, Galimaka R, Ruggiana A, Kazibwe F, Kabatereine NB, , 2008. Strongyloides stercoralis: a field-based survey of mothers and their preschool children using ELISA, Baermann and Koga plate methods reveals low endemicity in western Uganda. J Helminthol 82: 263269.[Crossref]
  43. Sousa-Figueiredo JC, Basanez MG, Mgeni AF, Khamis IS, Rollinson D, Stothard JR, , 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. Ann Trop Med Parasitol 102: 679692.[Crossref]
  44. Stothard JR, Webster BL, Weber T, Nyakaana S, Webster JP, Kazibwe F, Kabatereine NB, Rollinson D, , 2009. Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantial genetic diversity within Lake Albert and Lake Victoria populations. Parasitology 136: 18131824.[Crossref]
  45. Warren KS, Su DL, Xu ZY, Yuan HC, Peters PA, Cook JA, Mott KE, Houser HB, , 1983. Morbidity in schistosomiasis japonica in relation to intensity of infection. A study of two rural brigades in Anhui Province, China. N Engl J Med 309: 15331539.[Crossref]
  46. Ndamba J, Makaza N, Kaondera KC, Munjoma M, , 1991. Morbidity due to Schistosoma mansoni among sugar-cane cutters in Zimbabwe. Int J Epidemiol 20: 787795.[Crossref]
  47. Armitage P, Berry G, , 1994. Statistical Methods in Medical Research. Oxford, UK: Blackwell Scientific.

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  • Received : 30 May 2010
  • Accepted : 26 Jul 2010

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