Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T11:33:59.213Z Has data issue: false hasContentIssue false
  • English
  • Français

Anaemia in Ugandan preschool-aged children: the relative contribution of intestinal parasites and malaria

Published online by Cambridge University Press:  08 August 2011

HELEN K. GREEN ,
JOSE C. SOUSA-FIGUEIREDO ,
MARIA-GLORIA BASÁÑEZ ,
MARTHA BETSON ,
NARCIS B. KABATEREINE ,
ALAN FENWICK  and
J. RUSSELL STOTHARD
HELEN K. GREEN
Affiliation:
Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London (St Mary's Campus), Norfolk Place, London W2 1PG, UK
JOSE C. SOUSA-FIGUEIREDO
Affiliation:
WHO Collaborating Centre for Schistosomiasis, Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, London SW7 5BD, UK Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK
MARIA-GLORIA BASÁÑEZ
Affiliation:
Department of Infectious Disease Epidemiology, School of Public Health, Imperial College London (St Mary's Campus), Norfolk Place, London W2 1PG, UK
MARTHA BETSON
Affiliation:
Centre for Tropical and Infectious Diseases, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
NARCIS B. KABATEREINE
Affiliation:
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
ALAN FENWICK
Affiliation:
Schistosomiasis Control Initiative, Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College London, Norfolk Place, London W2 1PG, UK
J. RUSSELL STOTHARD*
Affiliation:
Centre for Tropical and Infectious Diseases, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
*
*Corresponding author: E-mail: jrstoth@liverpool.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Anaemia is a severe public health issue among African preschool-aged children, yet little effective progress has been made towards its amelioration, in part due to difficulties in unravelling its complex, multifactorial aetiology. To determine the current anaemia situation and assess the relative contribution of malaria, intestinal schistosomiasis and infection with soil-transmitted helminths, two separate cross-sectional epidemiological surveys were carried out in Uganda including 573 and 455 preschool-aged children (⩽6 years) living along the shores of Lake Albert and on the islands in Lake Victoria, respectively. Anaemia was found to be a severe public health problem in Lake Albert, affecting 68·9% of children (ninety-five percent confidence intervals (95% CI) 64·9–72·7%), a statistically significant higher prevalence relative to the 27·3% detected in Lake Victoria (95% CI: 23·3–31·7%). After multivariate analysis (controlling for sex and age of the child), the only factor found to be significantly associated with increased odds of anaemia in both lake systems was malaria (Lake Albert, odds ratio (OR)=2·1, 95% CI: 1·4–3·2; Lake Victoria, OR=1·9, 95% CI: 1·2–2·9). Thus intervention strategies primarily focusing on very young children and combating malaria appear to represent the most appropriate use of human and financial resources for the prevention of anaemia in this age group and area. Looking to the future, these activities could be further emphasised within the National Child Health DaysPLUS agenda.

Keywords

AnaemiamalariaSchistosoma mansonisoil-transmitted helminthsmalnutritionchild healthUganda
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 12: Symposia of the British Society for Parasitology Volume 47 , October 2011 , pp. 1534 - 1545
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Beutler, E. (1994). G6PD deficiency. Blood 84, 3613–3636.Google Scholar
Brito, L. L., Barreto, M. L., de Cassia, R., Silva, R., Assis, A. M., Reis, M. G., Parraga, I. M. and Blanton, R. E. (2006). Moderate- and low-intensity co-infections by intestinal helminths and Schistosoma mansoni, dietary iron intake, and anemia in Brazilian children. American Journal of Tropical Medicine and Hygiene 75, 939–944.Google Scholar
Brooker, S., Akhwale, W., Pullan, R., Estambale, B., Clarke, S. E., Snow, R. W. and Hotez, P. J. (2007 a). Epidemiology of Plasmodium-helminth co-infection in Africa, populations at risk, potential impact on anemia, and prospects for combining control. American Journal of Tropical Medicine and Hygiene 77 (6 Suppl.), 88–98.CrossRefGoogle ScholarPubMed
Brooker, S., Jardim-Botelho, A., Quinnell, R. J., Geiger, S. M., Caldas, I. R., Fleming, F., Hotez, P. J., Correa-Oliveira, R., Rodrigues, L. C. and Bethony, J. M. (2007 b). Age-related changes in hookworm infection, anaemia and iron deficiency in an area of high Necator americanus hookworm transmission in south-eastern Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 146–154. doi: 10.1016/j.trstmh.2006.05.012.Google Scholar
Cairns, M., Carneiro, I., Milligan, P., Owusu-Agyei, S., Awine, T., Gosling, R., Greenwood, B. and Chandramohan, D. (2008). Duration of protection against malaria and anaemia provided by intermittent preventive treatment in infants in Navrongo, Ghana. PLoS One 3, e2227. doi: 10.1371/journal.pone.0002227.CrossRefGoogle ScholarPubMed
Chizema-Kawesha, E., Miller, J. M., Steketee, R. W., Mukonka, V. M., Mukuka, C., Mohamed, A. D., Miti, S. K. and Campbell, C. C. (2010). Scaling up malaria control in Zambia, progress and impact 2005–2008. American Journal of Tropical Medicine and Hygiene 83, 480–488. doi: 10.4269/ajtmh.2010.10-0035.Google Scholar
Clark, T. D., Mmiro, F., Ndugwa, C., Perry, R. T., Jackson, J. B., Melikian, G. and Semba, R. D. (2002). Risk factors and cumulative incidence of anaemia among human immunodeficiency virus-infected children in Uganda. Annals of Tropical Paediatrics 22, 11–17.CrossRefGoogle ScholarPubMed
Crawley, J. (2004). Reducing the burden of anemia in infants and young children in malaria-endemic countries of Africa, from evidence to action. American Journal of Tropical Medicine and Hygiene 71 (2 Suppl.), 25–34.CrossRefGoogle ScholarPubMed
de Benoist, B., McLean, E., Egli, I. and Cogswell, M. (2008). Worldwide Prevalence of Anaemia 1993–2005. World Health Organization Press, Geneva.Google Scholar
de Vlas, S. J. and Gryseels, B. (1992). Underestimation of Schistosoma mansoni prevalences. Parasitology Today 8, 274–277.CrossRefGoogle ScholarPubMed
Deribew, A., Alemseged, F., Tessema, F., Sena, L., Birhanu, Z., Zeynudin, A., Sudhakar, M., Abdo, N., Deribe, K. and Biadgilign, S. (2010). Malaria and under-nutrition, a community based study among under-five children at risk of malaria, south-west Ethiopia. PLoS One 5, e10775. doi: 10.1371/journal.pone.0010775.Google Scholar
Friedman, J. F., Kanzaria, H. K. and McGarvey, S. T. (2005). Human schistosomiasis and anemia, the relationship and potential mechanisms. Trends in Parasitology 21, 386–392. doi: 10.1016/0169-4758(88)90137-8.Google Scholar
Gabrielli, A. F., Ramsan, M., Naumann, C., Tsogzolmaa, D., Bojang, B., Khoshal, M. H., Connolly, M., Stothard, J. R., Montresor, A. and Savioli, L. (2005). Soil-transmitted helminths and haemoglobin status among Afghan children in World Food Programme assisted schools. Journal of Helminthology 79, 381–384.CrossRefGoogle ScholarPubMed
Gera, T., Sachdev, H. P., Nestel, P. and Sachdev, S. S. (2007). Effect of iron supplementation on haemoglobin response in children, systematic review of randomised controlled trials. Journal of Pediatric Gastroenterology and Nutrition 44, 468–486. doi: 10.1097/01.mpg.0000243440.85452.38.CrossRefGoogle ScholarPubMed
Grantham-McGregor, S. and Ani, C. (2001). A review of studies on the effect of iron deficiency on cognitive development in children. Journal of Nutrition 131, 649S–666S.CrossRefGoogle ScholarPubMed
Griffin, J. T., Hollingsworth, T. D., Okell, L. C., Churcher, T. S., White, M., Hinsley, W., Bousema, T., Drakeley, C. J., Ferguson, N. M., Basáñez, M. G. and Ghani, A. C. (2010). Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Medicine 7, e1000324. doi: 10.1371/journal.pmed.1000324.Google Scholar
Hall, A., Bobrow, E., Brooker, S., Jukes, M., Nokes, K., Lambo, J., Guyatt, H., Bundy, D., Adjei, S., Wen, S., Subagio, H., Rafiluddin, M. Z., Miguel, T., Moulin, S., de Graft Johnson, J., Mukaka, M., Roschnik, N., Sacko, M., Zacher, A., Mahumane, B., Kihamia, C., Mwanri, L., Tatala, S., Lwambo, N., Siza, J., Nguyen Bao Khanh, L., Huy Khoi, H. and Duy Toan, N. (2001). Anaemia in schoolchildren in eight countries in Africa and Asia. Public Health 4, 749–756. doi: 10.1079/PHN2000111.Google ScholarPubMed
Hartgers, F. C. and Yazdanbakhsh, M. (2006). Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunology 28, 497–506. doi: 10.1111/j.1365-3024.2006.00901.x.CrossRefGoogle ScholarPubMed
Hoffbrand, V., Moss, P. and Pettit, J. (2006). Essential Haematology, 5th Edn. Blackwell Science, Oxford.Google Scholar
Iannotti, L. L., Tielsch, J. M., Black, M. M. and Black, R. E. (2006). Iron supplementation in early childhood: health benefits and risks. American Journal of Clinical Nutrition 84, 1261–1276.Google Scholar
Ihaka, R. and Gentleman, R. (1996). R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5, 299–314.Google Scholar
Jonkman, A., Chibwe, R. A., Khoromana, C. O., Liabunya, U. L., Chaponda, M. E., Kandiero, G. E., Molyneux, M. E. and Taylor, T. E. (1995). Cost-saving through microscopy based versus presumptive diagnosis of malaria in adult outpatients in Malawi. Bulletin of the World Health Organization 73, 223–227.Google ScholarPubMed
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. doi: 10.1590/S0042-96862007000200006. Google Scholar
Katz, N., Chavez, A. and Pellegrino, J. (1972). A simple device for quantitative stool thick smear technique in schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de São Paulo 14, 397–400.Google Scholar
Kirkwood, B. R. and Sterne, J. A. C. (2003). Essential Medical Statistics, 2nd Edn. Blackwell Science, Oxford.Google Scholar
Kolaczinski, J. H., Kabatereine, N. B., Onapa, A. W., Ndyomugyenyi, R., Kakembo, A. S. L. and Brooker, S. (2007). Neglected tropical diseases in Uganda: the prospect and challenge of integrated control. Trends in Parasitology 23, 485–493. doi: 10.1016/j.pt.2009.03.011.CrossRefGoogle ScholarPubMed
Korenromp, E. L., Armstrong-Schellenberg, J. R., Williams, B. G., Nahlen, B. L. and Snow, R. W. (2004). Impact of malaria control on childhood anaemia in Africa—a quantitative review. Tropical Medicine and International Health 9, 1050–1065.Google Scholar
Koukounari, A., Estambale, B. B. A., Kiambo Njagi, J., Cundill, B., Ajanga, A., Crudder, C., Otido, J., Jukes, M., Clarke, S. E. and Brooker, S. (2008). Relationships between anaemia and parasitic infections in Kenyan schoolchildren, a Bayesian hierarchical modelling approach. International Journal for Parasitology 38, 1663–1671. doi: 10.1016/j.ijpara.2008.05.013.Google Scholar
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). 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
Kung'u, J. K., Goodman, D., Haji, H. J., Ramsan, M., Wright, V. J., Bickle, Q. D., Tielsch, J. M., Raynes, J. G. and Stoltzfus, R. J. (2009). Early helminth infections are inversely related to anemia, malnutrition, and malaria and are not associated with inflammation in 6- to 23-month-old Zanzibari children. American Journal of Tropical Medicine and Hygiene 81, 1062–1070. doi: 10.4269/ajtmh.2009.09-0091.Google Scholar
Mazigo, H. D., Waihenya, R., Lwambo, N. J., Mnyone, L. L., Mahande, A. M., Seni, J., Zinga, M., Kapesa, A., Kweka, E. J., Mshana, S. E., Heukelbach, J. and Mkoji, G. M. (2010). Co-infections with Plasmodium falciparum, Schistosoma mansoni and intestinal helminths among schoolchildren in endemic areas of northwestern Tanzania. Parasites and Vectors 3, 44. doi: 10.1186/1756-3305-3-44.Google Scholar
McLean, E., Cogswell, M., Egli, I., Wojdyla, D. and de Benoist, B. (2009). Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutrition 12, 444–454. doi: 10.1017/S1368980008002401.CrossRefGoogle ScholarPubMed
Melo, G. C., Reyes-Lecca, R. C., Vitor-Silva, S., Monteiro, W. M., Martins, M., Benzecry, S. G., Alecrim, M. G. and Lacerda, M. V. (2010). Concurrent helminthic infection protects schoolchildren with Plasmodium vivax from anemia. PLoS One 5, e11206. doi: 10.1371/journal.pone.0011206.Google Scholar
Menendez, C., Kahigwa, E., Hirt, R., Vounatsou, P., Aponte, J. J., Font, F., Acosta, C. J., Schellenberg, D. M., Galindo, C. M., Kimario, J., Urassa, H., Brabin, B., Smith, T. A., Kitua, A. Y., Tanner, M. and Alonso, P. L. (1997). Randomised placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet 350, 844–850.CrossRefGoogle ScholarPubMed
Menendez, C., Todd, J., Alonso, P. L., Francis, N., Lulat, S., Ceesay, S., M'Boge, B. and Greenwood, B. M. (1994). The effects of iron supplementation during pregnancy, given by traditional birth attendants, on the prevalence of anaemia and malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 590–593.CrossRefGoogle ScholarPubMed
Midzi, N., Mtapuri-Zinyowera, S., Mapingure, M. P., Sangweme, D., Chirehwa, M. T., Brouwer, K. C., Mudzori, J., Hlerema, G., Mutapi, F., Kumar, N. and Mduluza, T. (2010). Consequences of polyparasitism on anaemia among primary school children in Zimbabwe. Acta Tropica 115, 103–111.Google Scholar
Miettinen, O. S. (1970). Estimation of relative risk from individually matched series. Biometrics 26, 75–86.Google Scholar
Ministry of Health Uganda and ORC Macro. (2006). Uganda HIV/AIDS Sero-behavioural Survey 2004–2005. Calverton, Maryland, USA: Ministry of Health and ORC Macro.Google Scholar
Mupfasoni, D., Karibushi, B., Koukounari, A., Ruberanziza, E., Kaberuka, T., Kramer, M. H., Mukabayire, O., Kabera, M., Nizeyimana, V., Deville, M-A., Ruxin, J., Webster, J. P. and Fenwick, A. (2009). Polyparasite helminth infections and their association to anaemia and undernutrition in Northern Rwanda. PLoS Neglected Tropical Diseases 3, e517. doi: 10.1371/journal.pntd.0000517.CrossRefGoogle ScholarPubMed
Mwanakasale, V., Siziya, S., Mwansa, J., Koukounari, A. and Fenwick, A. (2009). Impact of iron supplementation on schistosomiasis control in Zambian school children in a highly endemic area. Malawi Medical Journal 21, 12–18.Google Scholar
Mwangi, T. W., Bethony, J. M. and Brooker, S. (2006). Malaria and helminth interactions in humans: an epidemiological viewpoint. Annals of Tropical Medicine and Parasitology 100, 551–570. doi: 10.1179/136485906X118468.Google Scholar
Oguike, M. C., Betson, M., Burke, M., Nolder, D., Stothard, J. R., Kleinschmidt, I., Proietti, C., Bousema, T., Ndounga, M., Tanabe, K., Ntege, E., Culleton, R. and Sutherland, C. J. (2011). Plasmodium ovale curtisi and Plasmodium ovale wallikeri circulate simultaneously in African communities. International Journal for Parasitology 41, 677–683. doi: 10.1016/j.ijpara.2011.01.004.Google Scholar
President's Malaria Initiative, Country Profile Uganda (2009). Accessed August 2010. http://www.fightingmalaria.gov/countries/profiles/uganda_profile.pdfGoogle Scholar
Raso, G., Luginbühl, A., Adjoua, C. A., Tian-Bi, N. T., Silue, K. D., Matthys, B., Vounatsou, P., Wang, Y., Dumas, M. E., Holmes, E., Singer, B. H., Tanner, M., N'Goran, E. K. and Utzinger, J. (2004). Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Côte d'Ivoire. International Journal of Epidemiology 33, 1092–1102.Google Scholar
Rohner, F., Zimmermann, M. B., Amon, R. J., Vounatsou, P., Tschannen, A. B., N'Goran, E. K., Nindjin, C., Cacou, M-C., Té-Bonlé, M. D., Aka, H., Sess, D. E., Utzinger, J. and Hurrell, R. F. (2010). In a randomised controlled trial of iron fortification, anthelmintic treatment, and intermittent preventive treatment of malaria for anemia control in Ivorian children, only anthelmintic treatment shows modest benefit. Journal of Nutrition 140, 635–641.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. doi: 10.1079/JOH2005305.CrossRefGoogle ScholarPubMed
Ruxton, G. D. (2006). The unequal variance t-test is an underused alternative to Student's t-test and the Mann-Whitney U test. Behavioral Ecology 17, 688–690. doi: 10.1093/beheco/ark016.Google Scholar
Sazawal, S., Black, R. E., Ramsan, M., Chwaya, H. M., Stoltzfus, R. J., Dutta, A., Dhingra, U., Kabole, I., Deb, S., Othman, M. K. and Kabole, F. M. (2006). Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial. Lancet 367, 133–143.CrossRefGoogle Scholar
Schneider, J. M., Fujii, M. L., Lamp, C. L., Lonnerdal, B., Dewey, K. G. and Zidenberg-Cherr, S. (2008). The use of multiple logistic regression to identify risk factors associated with anemia and iron deficiency in a convenience sample of 12-36-mo-old children from low-income families. American Journal of Clinical Nutrition 87, 614–620.CrossRefGoogle Scholar
Schofield, L. and Grau, G. E. (2005). Immunological processes in malaria pathogenesis. Nature Reviews Immunology 5, 722–735. doi: 10.1038/nri1686.Google Scholar
Siegel, E. H., Stoltzfus, R. J., Khatry, S. K., Leclerq, S. and Tielsch, J. M. (2006). Epidemiology of anemia among 4- to 17-month children living in south central Nepal. European Journal of Clinical Nutrition 60, 228–235. doi: 10.1038/sj.ejcn.1602306.Google Scholar
Smith, J. L. and Brooker, S. (2010). Impact of hookworm infection and deworming on anaemia in non-pregnant populations, a systematic review. Tropical Medicine and International Health 15, 776–795. doi: 10.1111/j.1365-3156.2010.02542.x.Google Scholar
Sousa-Figueiredo, J. C., Basáñez, M. G., Mgeni, A. F., Khamis, I. S., Rollinson, D. and Stothard, J. R. (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. Annals of Tropical Medicine and Parasitology 102, 679–692. doi: 10.1179/136485908X337607.CrossRefGoogle ScholarPubMed
Sousa-Figueiredo, J. C., Oguttu, D., Adriko, M., Besigye, F., Nankasi, A., Arinaitwe, M., Namukuta, A., Betson, M., Kabatereine, N. B. and Stothard, J. R. (2010 a). Investigating portable fluorescent microscopy (CyScope®) as an alternative rapid diagnostic test for malaria in children and women of child-bearing age. Malaria Journal 9, 245. doi: 10.1186/1475-2875-9-245.CrossRefGoogle ScholarPubMed
Sousa-Figueiredo, J. C., Pleasant, J., Day, M., Betson, M., Rollinson, D., Montresor, A., Kazibwe, F., Kabatereine, N. B. and Stothard, J. R. (2010 b). Treatment of intestinal schistosomiasis in Ugandan pre-school children, best diagnosis, treatment efficacy and side-effects, and an extended praziquantel dosing pole. International Health 2, 103–113. doi: 10.1016/j.inhe.2010.02.003.CrossRefGoogle Scholar
Stoltzfus, R. J., Chwaya, H. M., Montresor, A., Albonico, M., Savioli, L. and Tielsch, J. M. (2000). Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0 to 5yr old Zanzibari children and these relationships change with age. Journal of Nutrition 130, 1724–1733.CrossRefGoogle Scholar
Stoltzfus, R. J., Chway, H. M., Montresor, A., Tielsch, J. M., Jape, J. K., Albonico, M. and Savioli, L. (2004). Low dose daily iron supplementation improves iron status and appetite but not anemia, whereas quarterly anthelminthic treatment improves growth, appetite and anemia in Zanzibari preschool children. Journal of Nutrition 134, 348–356.Google Scholar
Subbaraman, R., Devaleenal, B., Selvamuthu, P., Yepthomi, T., Solomon, S. S., Mayer, K. H. and Kumarasamy, N. (2009). Factors associated with anaemia in HIV-infected individuals in southern India. International Journal of STD & AIDS 20, 489–492.Google Scholar
Tohon, Z. B., Mainassara, H. B., Garba, A., Mahamane, A. E., Bosque-Oliva, E., Ibrahim, M-L., Duchemin, J-B., Chanteau, S. and Boiser, P. (2008). Controlling schistosomiasis: significant decrease of anaemia prevalence one year after a single dose of praziquantel in Nigerian schoolchildren. PLoS Neglected Tropical Diseases 2, e241. doi: 10.1371/journal.pntd.0000241.CrossRefGoogle ScholarPubMed
Uganda Ministry of Health (2010). Malaria Control Programme: Uganda Malaria Control Strategic Plan 2005/06 – 2009/10. Accessed August 2010. http://www.eac.int/health/index.php?option=com_docman&task=cat_view&gid=32&Itemid=144Google Scholar
UNAIDS and WHO (2008). Epidemiological Fact Sheets on HIV and AIDS, 2008 Update. Accessed October 2010. http://apps.who.int/globalatlas/predefinedReports/EFS2008/full/EFS2008_UG.pdfGoogle Scholar
World Health Organization (1987). Atlas of the global distribution of schistosomiasis Uganda. Accessed August 2010. http://www.who.int/wormcontrol/documents/maps/en/uganda.pdfGoogle Scholar
World Health Organization (2002). Prevention and control of schistosomiasis and soil-transmitted helminthiasis. First report of the joint WHO expert committees. WHO Technical Report Series No. 912. World Health Organization, Geneva.Google Scholar
World Health Organization (2006 a). Vitamin and Mineral Nutrition Information System, Uganda. Accessed October 2010. http://who.int/vmnis/anaemia/data/database/countries/uga_ida.pdfGoogle Scholar
World Health Organization (2006 b). Iron supplementation of young children in regions where malaria transmission is intense and infectious disease highly prevalent. Accessed November 2010. http://www.searo.who.int/LinkFiles/Nutrition_for_Health_and_Development_WHO_UNICEF_statement_malaria.pdfGoogle Scholar
WHO and UNICEF (1998). Complementary Feeding of Young Children in Developing Countries: a Review of Current Scientific Knowledge. World Health Organization: Geneva.Google Scholar
WHO and UNICEF (2004). Focusing on anaemia, towards an integrated approach for effective anaemia control. Joint statement by the World Health Organization and the United Nations Children's Fund. Geneva, World Health Organization. Accessed November 2010. http://whqlibdoc.who.int/hq/2004/anaemiastatement.pdfGoogle Scholar
Zimmermann, M. B. and Hurrell, R. F. (2007). Nutritional iron deficiency. Lancet 370, 511–520.Google Scholar