MORBIDITY INDICATORS OF SCHISTOSOMA MANSONI: RELATIONSHIP BETWEEN INFECTION AND ANEMIA IN UGANDAN SCHOOLCHILDREN BEFORE AND AFTER PRAZIQUANTEL AND ALBENDAZOLE CHEMOTHERAPY

ARTEMIS KOUKOUNARI Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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ALAN FENWICK Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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SARAH WHAWELL Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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NARCIS B. KABATEREINE Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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FRANCIS KAZIBWE Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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EDRIDAH M. TUKAHEBWA Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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J. RUSSELL STOTHARD Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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CHRISTL A. DONNELLY Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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JOANNE P. WEBSTER Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom; Vector Control Division, Ministry of Health, Kampala, Uganda; Department of Zoology, Natural History Museum, London, United Kingdom; Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, London, United Kingdom

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The potential relationship between Schistosoma mansoni and anemia was examined using data obtained by the Schistosomiasis Control Initiative (SCI) before (baseline) and 1 year after (follow-up) a chemotherapeutic treatment program in Uganda. Changes in hemoglobin (Hb) levels in 2,788 children in relation to their schistosomiasis and/or hookworm infection intensity category and baseline anemia status were analyzed. At baseline, significant predictors of childhood anemia were intensities of S. mansoni and hookworm infection. At follow-up, moderate or heavy hookworm as well as heavy S. mansoni infections were important. Children heavily infected with S. mansoni or hookworm had significantly lower Hb counts at baseline compared with those not infected. Among anemic children at the baseline survey, a significant increase in Hb counts of 0.834 g/dL after treatment was found. Our results suggest that anemia is associated with schistosomiasis and hookworm in Ugandan children and that such anemia shows a significant improvement after chemotherapy.

Author Notes

Reprint requests: Artemis Koukounari, Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Imperial College Faculty of Medicine, St. Mary’s Campus, Room G26, Norfolk Place, London W2 1PG, UK, E-mail: artemis.koukounari@imperial.ac.uk.
  • 1

    Crawley J, 2004. Reducing the burden of anemia in infants and young children in malaria-endemic countries of Africa: from evidence to action. Am J Trop Med Hyg 71 :25–34.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Engels D, Chitsulo L, Montresor A, Savioli L, 2002. The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Trop 82 :139–146.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Coutinho HM, McGarvey ST, Acosta LP, Manalo DL, Langdon GC, Leenstra T, Kanzaria HK, Solomon J, Wu H, Olveda RM, Kurtis JD, Friedman JF, 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. J Infect Dis 192 :528–536.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Nokes C, McGarvey ST, Shiue L, Wu G, Wu H, Bundy DA, Olds GR, 1999. Evidence for an improvement in cognitive function following treatment in Schistosoma japonicum infection in chinese primary schoolchildren. Am J Trop Med Hyg 60 :556–565.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Olsen A, Magnussen P, Ouma JH, Andreassen J, Friis H, 1998. The contribution of hookworm and other parasitic infections to haemoglobin and iron status among children and adults in western Kenya. Trans R Soc Trop Med Hyg 92 :643–649.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Stephenson LS, Holland C, 1987. The Impact of Helminth Infections on Human Nutrition. London, UK: Taylor and Frances.

    • PubMed
    • Export Citation
  • 7

    Stephenson LS, 1993. The impact of schistosomiasis on human nutrition. Parasitology 107 :107–123.

  • 8

    Preston JM, Dargie JD, 1975. Mechanisms involved in ovine schistosomal anaemia Welsh CN, ed. Nuclear Techniques in Helminthology Research. Vienna, Austria: International Atomic Energy Agency, 121–126.

    • PubMed
    • Export Citation
  • 9

    Foy H, Nelson GS, 1963. Helminths in the etiology of anaemia in the tropics, with special reference to hookworms and schistosomes. Exp Parasitol 14 :240–262.

  • 10

    Latham MC, Stephenson LS, Hall A, Wolgemuth JC, Elliot TC, Crompton DW, 1983. Parasitic infections, anaemia and nutritional status: a study of their interrelationships and the effect of prophylaxis and treatment on workers in Kwale District, Kenya. Trans R Soc Trop Med Hyg 77 :41–48.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Vennervald BJ, Dunne DW, 2004. Morbidity in Schistosomiasis: an update. Curr Opin Infect Dis 17 :439–447.

  • 12

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Brouwer KC, Ndhlovu PD, Wagatsuma Y, Munatsi A, Shiff CJ, 2003. Epidemiological assessment of Schistosoma haematobium-induced kidney and bladder pathology in rural Zimbabwe. Acta Trop 85 :339–347.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Richter J, 2003. The impact of chemotherapy on morbidity due to schistosomiasis. Acta Trop 86 :161–183.

  • 16

    Booth M, Vennervald BJ, Kabatereine NB, Kazibwe F, Ouma JH, Kariuki CH, Muchiri E, Kadzo H, Ireri E, Kimani G, Mwatha JK, Dunne DW, 2004. Hepatosplenic morbidity in two neighbouring communities in Uganda with high levels of Schistosoma mansoni infection but very different durations of residence. Trans R Soc Trop Med Hyg 98 :125–136.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Kabatereine NB, Kemijumbi J, Ouma JH, Sturrock RF, Butterworth AE, Madsen H, Ornbjerg N, Dunne DW, Vennnervald BJ, 2003. Efficacy and side effects of praziquantel treatment in a highly endemic Schistosoma mansoni focus at Lake Albert, Uganda. Trans R Soc Trop Med Hyg 97 :599–603.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Kabatereine NB, Vennervald BJ, Ouma JH, Kemijumbi J, Butterworth AE, Dunne DW, Fulford AJ, 1999. Adult resistance to schistosomiasis mansoni: age dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118 :101–105.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Brooker S, Whawell S, Kabatereine NB, Fenwick A, Anderson RM, 2004. Evaluating the epidemiological impact of national control programmes for helminths. Trends Parasitol 20 :537–545.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Stothard JR, Kabatereine NB, Tukahebwa EM, Kazibwe F, Rollinson D, Mathieson W, Webster JP, Fenwick A, 2006. Use of circulating cathodic antigen (CCA) dipsticks for detection of intestinal and urinary schistosomiasis. Acta Trop. 97 :219–228.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Kabatereine NB, Tukahebwa EM, Kazibwe F, Twa-Twa JM, Barenzi JF, Zaramba S, Stothard JR, Fenwick A, Brooker S, 2005. Soil-transmitted helminthiasis in Uganda: epidemiology and cost of control. Trop Med Int Health 10 :1187–1189.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Parker DR, Bargiota A, Cowan FG, Corrall RJ, 1997. Suspected hypoglycaemia in out patient practice: accuracy of dried blood spot analysis. Clin Endocrinol 47 :679–683.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    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 :125–139.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Mauny F, Viel JF, Handschumacher P, Sellin B, 2004. Multilevel modelling and malaria: a new method for an old disease. Int J Epidemiol 33 :1337–1344.

  • 25

    Verbeke G, Molenberghs G, 2000. Linear Mixed Models for Longitudinal Data. New York: Springer Series in Statistics.

    • PubMed
    • Export Citation
  • 26

    Gibson R, 1990. Principles of Nutritional Assessment. New York: Oxford University Press.

    • PubMed
    • Export Citation
  • 27

    Gorstein J, Sullivan K, Yip R, de Onis M, Trowbridge F, Fajans P, Clugston G, 1994. Issues in the assessment of nutrition status using anthropometry. Bull World Health Organ 72 :273–283.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    World Health Organization, 1995. Physical status: the use and interpretation of anthropometry. World Health Organ Tech Rep Ser :854.

  • 29

    Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anaemia: (the relationship and potential mechanisms. Trends Parasitol 21 :386–392.

  • 30

    Kabatereine NB, Tukahebwa E, Kazibwe F, Namwangye H, Zaramba S, Brooker S, Stothard JR, Kamenka C, Whawell S, Webster JP, Fenwick A, 2006. Progress towards countrywide control of schistosomiasis and soil-transmitted helminthiasis in Uganda. Trans R Soc Trop Med Hyg 100 :208–215.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Nullis-Kapp C, 2004. Darfur overshadows “forgotten” crisis in neighbouring Uganda. Bull World Health Organ 82 :886.

  • 32

    Taylor M, Jinabhai CC, Couper I, Kleinschmidt I, Jogessar B, 2001. The effect of different anthelmintic treatment regimens combined with iron supplementation on the nutritional status of schoolchildren in KwaZulu-Natal South Africa: a randomized control trial. Trans R Soc Trop Med Hyg 95 :211–216.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L, 1998. Effects of the Zanzibar school-based deworming program on iron status of children. Am J Clin Nutr 68 :179–186.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Beasley NMR, Tomkins AM, Hall A, Kihamia CM, Lorri W, Nduma B, Issae W, Nokes C, Bundy DAP, 1999. The impact of population level deworming on the haemoglobin level of schoolchildren in Tanga, Tanzania. Trop Med Int Health 4 :744–750.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Friis H, Mwaniki D, Omondi B, Muniu E, Thiong’o F, Ouma J, Magnussen P, Geissler PW, Michaelsen KF, 2003. Effects on haemoglobin of multi-micronutrient supplementation and multi-helminth chemotherapy: a randomized, control trial in Kenyan schoolchildren. Eur J Clin Nutr 57 :573–579.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Uganda Ministry of Health, Available at http://www.health.go.ug/blood_trans.htm.

    • PubMed
    • Export Citation
  • 37

    Kabatereine NB, Brooker S, Tukahebwa EM, Kazibwe F, Onapa AW, 2004. Epidemiology and geography of Schistosoma mansoni in Uganda: implications for planning control. Trop Med Int Health 9 :372–380.

    • PubMed
    • Search Google Scholar
    • Export Citation
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