Volume 75, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


We assessed morbidity indicators for both and infections and evaluated the appropriateness of the World Health Organization (WHO) guidelines for ultrasound in schistosomiasis in the context of large-scale control interventions. Abdominal and urinary tract ultrasonography was performed on 2,247 and 2,822 school children, respectively, from 29 randomly selected schools in Mali before the implementation of mass anthelminthic drug administration. Using two-level logistic regression models, we examined associations of potential factors with the risk of having a positive ultrasound global score (morbidity indicative of infection), abnormal image pattern scores, dilatation of the portal vein, and/or enlarged liver (morbidity indicative of infection). The WHO protocol was found useful for detection of pathology but overestimated the risk of portal vein dilatation and left liver lobe enlargement associated with infection. We conclude that ultrasonography should be included in large-scale control interventions, where logistics allow, but cautiously.


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  1. Chitsulo L, Engels D, Montresor A, Savioli L, 2000. The global status of schistosomiasis and its control. Acta Trop 77 : 41–51. [Google Scholar]
  2. Van der Werf M, de Vlas SJ, Landouré A, Bosompem KM, Habbema JD, 2004. Measuring schistosomiasis case management of the health services in Ghana and Mali. Trop Med Int Health 9 : 149–157. [Google Scholar]
  3. King CH, Dickman K, Tisch D, 2005. Reassessment of the cost of chronic helminthic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365 : 1561–1569. [Google Scholar]
  4. World Health Organization, 1985. The control of schistosomiasis: report of a WHO Expert Committee. World Health Organ Tech Rep Ser 728 : 1–113. [Google Scholar]
  5. Gryseels B, Polderman A, 1991. Morbidity due to Schistosomiasis mansoni, and its control in Subsaharan Africa. Parasitol Today 7 : 223–259. [Google Scholar]
  6. Kariuki CH, Mbugua G, Mapak P, Bailey JA, Muchiri EM, Thiongo FW, King CH, Butterworth AE, Ouma JH, Blanton RE, 2001. Prevalence and familial aggregation of schistosomal liver morbidity in Kenya: evaluation by new ultrasound criteria. J Infect Dis 183 : 960–966. [Google Scholar]
  7. Campagne G, Garba A, Barkiré H, Vera C, Sidiki A, Chippaux JP, 2001. Continued ultrasonic follow-up of children infected with Schistosoma haematobium after treatment with praziquantel. Trop Med Int Health 6 : 24–30. [Google Scholar]
  8. Richter J, Hatz C, Häussinger D, 2003. Ultrasound in tropical and parasitic diseases. Lancet 362 : 900–902. [Google Scholar]
  9. Kabatereine NB, Kemijumbi J, Ouma JH, Kariuki HC, Richter J, Kadzo H, Madsen H, Butterworth AE, Ornbjerg N, Vennervald BJ, 2004. Epidemiology and morbidity of Schistosoma mansoni infection in a fishing community along Lake Albert in Uganda. Trans R Soc Trop Med Hyg 98 : 711–718. [Google Scholar]
  10. Mongy F, Hazem T, Safwat M, Nawaytou MS, Arafa NM, 1978. The Value of Sonography in Diagnosing Schistosomal Vesical Lesions. Proceedings of the third international workshop on diagnostic ultrasound imaging. Cairo, Egypt: Al-Ahram Press, 447–456.
  11. Abdel-Wahab MF, Abdel-Latif Z, El-Kady NM, Arafa NM, 1978. The Use of Ultrasonography in Diagnosis of Different Schistosomal Syndromes. Proceedings of the Third International Workshop on Diagnostic Ultrasound Imaging. Cairo, Egypt: Al-Ahram Press, 457–475.
  12. Browning MD, Narooz SI, Strickland GT, El-Masry NA, Abdel-Wahab MF, 1984. Clinical characteristics and response to therapy in Egyptian children infected with Schistosoma haematobium. J Infect Dis 149 : 998–1004. [Google Scholar]
  13. Devidas A, Lamothe F, Develoux M, Mouchet F, Sellin B, 1989. Ultrasonographic assessment of the regression of bladder and renal lesions due to Schistosoma haematobium after treatment with praziquantel. Ann Soc Belg Med Trop 69 : 57–65. [Google Scholar]
  14. Hatz C, Jenkins JM, Meudt R, Abdel-Wahab MF, Tanner M, 1992. A review of the literature on the use of ultrasonography in schistosomiasis with special reference to its use in field studies. 1. Schistosoma haematobium. Acta Trop 51 : 1–14. [Google Scholar]
  15. Hatz C, Savioli L, Mayombana C, Dhunputh J, Kisumku U, Tanner M, 1990. Measurement of schistosomiasis-related morbidity at community level in areas of different endemicity. Bull World Health Organ 68 : 777–787. [Google Scholar]
  16. Richter J, Domingues ALC, Barata CH, Prata AR, Lambertucci JR, 2001. Report of the Second Satellite Symposium on Ultrasound in Schistosomiasis. Mem Inst Oswaldo Cruz 96 : 151–156. [Google Scholar]
  17. King CH, Magak P, Salam AE, Ouma JH, Kariuki CH, Blanton RE, 2003. Measuring morbidity in schistosomiasis mansoni: relationship between image pattern, portal vein diameter and portal branch thickness in large-scale surveys using new WHO coding guidelines for ultrasound in schistosomiasis. Trop Med Int Health 8 : 109–117. [Google Scholar]
  18. Hatz C, 2001. The use of ultrasound in schistosomiasis. Adv Parasitol 48 : 225–284. [Google Scholar]
  19. Richter J, Hatz C, Campagne G, Bergquist N, Jenkins J, 2000. Ultrasound in Schistosomiasis: A Practical Guide to the Standardized Use of Ultrasonography for the Assessment of Schistosomiasis-Related Morbidity. Geneva: World Health Organization.
  20. Coulibaly G, Diallo M, Madsen H, Dabo A, Traoré M, Keita S, 2004. Comparison of schistosome transmission in a single- and a double-cropped area in the rice irrigation scheme, ‘Office du Niger’, Mali. Acta Trop 91 : 15–25. [Google Scholar]
  21. Traoré M, Traoré HA, Kardorff R, Diarra A, Landouré A, Vester U, Doehring E, Bradley DJ, 1998. The public health significance of urinary schistosomiasis as a cause of morbidity in two districts in Mali. Am J Trop Med Hyg 59 : 407–413. [Google Scholar]
  22. Vercruysse J, De Clercq D, Sacko M, Traoré M, Southgate VR, Rollinson D, De Clercq D, Sacko M, De Bont J, Mungomba LM, 1994. Studies on transmission and schistosome interactions in Senegal, Mali and Zambia. Trop Geogr Med 46 : 220–226. [Google Scholar]
  23. Keita AD, Sangho H, Sacko M, Diarra Z, Simaga S, Traoré I, 2005. Prevalence of schistosomiasis lesions detected by ultrasonography in children, in Molodo, Mali. Gastroenterol Clin Biol 29 : 652–655. [Google Scholar]
  24. Brooker S, Whawell S, Kabatereine N, Fenwick A, Anderson RM, 2004. Evaluating the epidemiological impact of national control programs for helminths. Trends Parasitol 20 : 537–545. [Google Scholar]
  25. Feldmeier H, Poggensee G, 1993. Diagnostic techniques in schistosomiasis control. Acta Trop 52 : 205–220. [Google Scholar]
  26. Kato K, Miura M, 1954. Comparative examinations. Jpn J Parasitol 3 : 35. [Google Scholar]
  27. 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 : 397–400. [Google Scholar]
  28. Yazdanpanah Y, Thomas AK, Kardorff R, Talla I, Sow S, Niang M, Stelma FF, Decam C, Rogerie F, Gryseels B, Capron A, Doehring E, 1997. Organometric investigation of the spleen and liver by ultrasound in S. mansoni endemic and non endemic villages in Senegal. Am J Trop Med Hyg 57 : 245–249. [Google Scholar]
  29. Carpenter J, Kenward M, 2005. Missing data. London: London School of Hygiene and Tropical Medicine. Available from http://www.lshtm.ac.uk/msu/missingdata/index.html.
  30. World Health Organization, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO Expert Committee. World Health Organ Tech Rep Ser 912 : 1–57. [Google Scholar]
  31. Goldstein H, Rasbash J, 1996. Improved approximations for multilevel models with binary responses. J Roy Stat Soc A 159 : 505–513. [Google Scholar]
  32. Rasbash J, Steele F, Browne W, Prosser B, 2004. A User’s Guide to MLwin Version 2.0. London: Institute of Education, University of London.
  33. Goldstein H, Browne W, Rasbash J, 2002. Partitioning variation in multilevel models. Understanding Stat 1 : 223–231. [Google Scholar]
  34. Larsen K, Petersen JH, Jørgensen EB, Endahl L, 2000. Interpreting parameters in the logistic regression model with random effects. Biometrics 56 : 909–914. [Google Scholar]
  35. Larsen K, Merlo J, 2005. Appropriate assessment of neighborhood effects on individual health: integrating random and fixed effects in multilevel logistic regression. Am J Epidemiol 161 : 81–88. [Google Scholar]
  36. Browne WJ, Subramanian SV, Jones K, Goldstein H, 2005. Variance partitioning in multilevel logistic models that exhibit overdispersion. J Roy Stat Soc A 168 : 599–613. [Google Scholar]
  37. Snidjers T, Bosker R, 1999. Multilevel Analysis: An Introduction to Basic and Advanced Multilevel Modeling. Newcastle Upon Tune, United Kingdom: Sage Publications.
  38. Brouwer K, Munatsi A, Ndhlovu PD, Wagatsuma Y, Shiff CJ, 2004. Urinary schistosomiasis in Zimbabwean school children: predictors of morbidity. Afr Health Sci 4 : 115–118. [Google Scholar]
  39. de Celis G, Mir J, Casal J, Gómez D, 2003. 31-year-old woman with an enlarged tender liver. Lancet 346 : 1270. [Google Scholar]
  40. Lougue-Sorgho LC, Cisse R, Kagone M, Bamouni YA, Tapsoba TL, Sanou A, 2002. Radiographie et échographie dans la prise en charge des tumeurs de la vessie: à propos de 71 cas au centre hospitalier national Yalgado Ouedraogo (Burkina Faso). Bull Soc Pathol Exot 95 : 244–247. [Google Scholar]
  41. Abdel-Wahab MF, Strickland GT, 1993. Abdominal ultrasonography for assessing morbidity from schistosomiasis. 2. Hospital Studies. Trans R Soc Trop Med Hyg 87 : 135–137. [Google Scholar]
  42. Bahakim HH, Hussain S, Al Sulaimani SH, 1986. Ultrasonography of pancreatic schistosomiasis: A case report. J Trop Med Hyg 89 : 81–84. [Google Scholar]
  43. Vennervald BJ, Booth M, Butterworth AE, Kariuki HC, Kadzo H, Ireri E, Amaganga C, Kimani G, Kenty L, Mwatha J, Ouma JH, Dunne DW, 2005. Regression of hepatosplenomegaly in Kenyan school-aged children after praziquantel treatment and three years of greatly reduced exposure to Schistosoma mansoni. Trans R Soc Trop Med Hyg 99 : 150–160. [Google Scholar]
  44. Vennervald BJ, Kenty L, Butterworth AE, Kariuki CH, Kadzo H, Ireri E, Amaganga C, Kimani G, Mwatha J, Otedo A, Booth M, Ouma JH, Dunne DW, 2004. Detailed clinical and ultrasound examination of children and adolescents in a Schistosoma mansoni endemic area in Kenya: hepatosplenic disease in the absence of portal fibrosis. Trop Med Int Health 9 : 461–470. [Google Scholar]
  45. Leutscher PD, Reimert CM, Vennervald BJ, Ravaoalimalala VE, Ramarokoto CE, Serieye J, Raobelison A, Rasendramino M, Christensen NO, Esterre P, 2000. Morbidity assessment in urinary schistosomiasis infection through ultrasonography and measurement of eosinophil cationic protein (ECP) in urine. Trop Med Int Health 5 : 88–93. [Google Scholar]
  46. Friis H, Ndholvu P, Kaondera K, Franke D, Vennervald BJ, Christensen NO, Doehring E, 1996. Ultrasonographic assessment of Schistosoma mansoni and S haematobium morbidity in Zimbabwean schoolchildren. Am J Trop Med Hyg 55 : 290–294. [Google Scholar]
  47. Lengeler C, Kilima P, Mshinda H, Morona D, Hatz C, Tanner M, 1991. Rapid, low-cost, two-step method to screen for urinary schistosomiasis at the district level: the Kilosa experience. Bull World Health Organ 69 : 179–189. [Google Scholar]
  48. Utzinger J, N’Goran EK, Esse Aya CM, Acka Adjoua C, Lohourignon KL, Tanner M, Lengeler C, 1998. Schistosoma mansoni, intestinal parasites and perceived morbidity indicators in schoolchildren in a rural endemic area of western Côte d’Ivoire. Trop Med Int Health 3 : 711–720. [Google Scholar]
  49. Boisier P, Ramarokoto C-E, Ravoniarimbinina P, Rabarijaona L, Ravaolimalala VE, 2001. Geographic differences in hepatosplenic complications of schistosomiasis mansoni and explanatory factors of morbidity. Trop Med Int Health 6 : 699–706. [Google Scholar]
  50. Frenzel K, Grigull L, Odongo-Aginya E, Ndwugwa CM, Loroni-Lakwo T, Schweigmann U, Vester U, Spannbrucker N, Doehring E, 1999. Evidence of a long-term effect of a single doze of praziquantel on Schistosoma mansoni-induced hepatosplenic lessions in northern Uganda. Am J Trop Med 60 : 927–931. [Google Scholar]
  51. Kardoff R, Gabone RM, Mugashe C, Obiga D, Ramarokoto CE, Mahlert C, Spannbrucker N, Lang A, Gunzler V, Gryseels B, Ehrich JH, Doehring E, 1997. Schistosoma mansoni-related morbidity on Ukerewe Island, Tanzania: clinical, ultrasonographical and biochemical parameters. Trop Med Int Health 2 : 230–239. [Google Scholar]
  52. Vester U, Kardoff R, Traoré M, Traoré HA, Fongoro S, Juchem C, Franke D, Korte R, Gryseels B, Ehrich JH, Doehring E, 1997. Urinary tract morbidity due to Schistosoma haematobium infection in Mali. Kidney Int 52 : 478–481. [Google Scholar]
  53. Kardoff R, Stelma FF, Vocke AK, Yazdanpanah Y, Thomas AK, Mbaye A, Talla I, Niang M, Ehrich JH, Doehring E, Gryseels B, 1996. Ultrasonography in a Senegalese community recently exposed to Schistosoma mansoni infection. Am J Trop Med Hyg 54 : 586–590. [Google Scholar]
  54. Kardorff R, Traoré M, Diarra M, Sacko M, Maiga M, Franke D, Vester U, Hansen U, Traoré HA, Fongoro S, Gorgien H, Korte R, Gryseels B, Doehring-Schwerdtfeger E, Ehrich JH, 1994. Lack of ultrasonographic evidence for severe hepatosplenic morbidity in Schistosoma mansoni in Mali. Am J Trop Med Hyg 51 : 116–120. [Google Scholar]
  55. Heurtier Y, Lamothe F, Develoux M, Docquier J, Mouchet F, Sellin E, Sellin B, 1986. Urinary tract lesions due to Schistosoma haematobium infection assessed by ultrasonography in a community based study in Niger. Am J Trop Med Hyg 35 : 1163–1172. [Google Scholar]
  56. Keita AD, Dembelé M, Kane M, Fongoro S, Traoré M, Sacko M, Diallo S, Sidibe S, Traoré HA, Doumbo O, Traoré I, 2001. Aspects échographiques de la schistosomose urinaire chez les enfants du plateau Dogon et de l’office du Niger; impact du traitement par le praziquantel. Bull Soc Pathol Exot 94 : 335–338. [Google Scholar]
  57. Kabatereine NB, Kemijumbi J, Ouma JH, Kariuki HC, Richter J, Kadzo H, Madsen H, Butterworth AE, Ornbjerg N, Vennervald BJ, 2004. Epidemiology and morbidity of Schistosoma mansoni infection in a fishing community along Lake Albert in Uganda. Trans R Soc Trop Med Hyg 98 : 711–718. [Google Scholar]
  58. World Health Organization, 2005. International Travel and Health: Situation as on 1 January 2005. Geneva: World Health Organization.
  59. Odogwu SE, Ramamurthy NK, Kabatereine NB, Kazibwe F, Tukahebwa E, Webster JP, Fenwick A, Stothard JR, 2006. Schistosoma mansoni in infants (aged < 3 years) along the Ugandan shoreline of Lake Victoria. Ann Trop Med Parasitol 100 : 1–12. [Google Scholar]
  60. Hatz C, Vennervald BJ, Nkulila T, Vounatsou P, Kombe Y, Mayombana C, Mshinda H, Tanner M, 1998. Evolution of Schistosoma haematobium-related pathology over 24 months after treatment with praziquantel among schoolchildren in Southeastern Tanzania. Am J Trop Med Hyg 59 : 775–781. [Google Scholar]

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  • Received : 28 Feb 2006
  • Accepted : 22 Jun 2006

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