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

Parasitology

Volumn 138, Issue 12, 2011, Pages 1534-1545

  Green, Helen K ^a   Sousa Figueiredo, Jose C ^b,c   Basáñez, Maria Gloria ^a   Betson, Martha ^d   Kabatereine, Narcis B ^e   Fenwick, Alan ^f   Stothard, J Russell ^d  

^a Centre for Environment and Health   (United Kingdom)

^b Dept of Oral Medicine and Pathology   (United Kingdom)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^e MINISTRY OF HEALTH   (Uganda)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Anaemia; child health; malaria; malnutrition; Schistosoma mansoni; soil transmitted helminths; Uganda

Indexed keywords

ALBENDAZOLE; ARTEMETHER PLUS BENFLUMETOL; ARTEMISININ; PRAZIQUANTEL; QUININE;

ANEMIA; ARTICLE; ASCARIASIS; ASCARIS LUMBRICOIDES; CHILD; CHILD HEALTH; CHILD HEALTH CARE; CONFIDENCE INTERVAL; CONTROLLED STUDY; FEMALE; GROUPS BY AGE; HEALTH SURVEY; HELMINTHIASIS; HOOKWORM INFECTION; HUMAN; INFANT; ISLAND (GEOLOGICAL); MAJOR CLINICAL STUDY; MALARIA; MALARIA FALCIPARUM; MALE; MALNUTRITION; MULTIVARIATE ANALYSIS; PRESCHOOL CHILD; PRIORITY JOURNAL; PUBLIC HEALTH PROBLEM; QUESTIONNAIRE; RISK; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; STATISTICAL SIGNIFICANCE; TRICHURIASIS; TRICHURIS; UGANDA;

ANEMIA; ANIMALS; CHILD; CHILD WELFARE; CHILD, PRESCHOOL; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; LAKES; LONGITUDINAL STUDIES; MALARIA; MALE; MALNUTRITION; MATERNAL WELFARE; PREGNANCY; PREVALENCE; QUESTIONNAIRES; SCHISTOSOMIASIS MANSONI; SOIL; UGANDA;

SCHISTOSOMA MANSONI; VERMES;

EID: 84855644764     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182011001016     Document Type: Article

References (68)

1. Beutler E. G6PD deficiency Blood 1994 84 3613-3636.
2. Beutler, E. (1994). G6PD deficiency. Blood 84, 3613-3636. 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.
3. Brooker, S., Akhwale, W., Pullan, R., Estambale, B., Clarke, S. E., Snow, R.W. and Hotez, P. J. (2007a). 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.
4. 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. (2007b). 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. De Benoist, B., McLean, E., Egli, I. and Cogswell, M. (2008). Worldwide Prevalence of Anaemia 1993-2005. World Health Organization Press, Geneva.
10. de Vlas, S. J. and Gryseels, B. (1992). Underestimation of Schistosoma mansoni prevalences. Parasitology Today 8, 274-277.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. Hartgers, F. C. and Yazdanbakhsh, M. (2006). Co-infection of helminthes and malaria: modulation of the immune responses to malaria. Parasite Immunology 28, 497-506. doi: 10.1111/j.1365-3024.2006.00901.x.
19. Hoffbrand, V., Moss, P. and Pettit, J. (2006). Essential Haematology, 5th Edn. Blackwell Science, Oxford.
20. 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.
21. Ihaka, R. and Gentleman, R. (1996). R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5, 299-314.
22. 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.
23. 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.
24. 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 Säo Paulo 14, 397-400.
25. Kirkwood, B. R. and Sterne, J. A. C. (2003). Essential Medical Statistics, 2nd Edn. Blackwell Science, Oxford.
26. 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.
27. 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.
28. 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 modeling approach. International Journal for Parasitology 38, 1663-1671. doi: 10.1016/j.ijpara.2008.05.013.
29. 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.
30. 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.
31. 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 helminthes among schoolchildren in endemic areas of northwestern Tanzania. Parasites and Vectors 3, 44. doi: 10.1186/1756-3305-3-44.
32. cLean, 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.
33. 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.
34. 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 placebocontrolled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet 350, 844-850.
35. 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.
36. 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.
37. Miettinen, O. S. (1970). Estimation of relative risk from individually matched series. Biometrics 26, 75-86.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. President'sMalaria Initiative, Country Profile Uganda (2009). Accessed August 2010. http://www.fightingmalaria.gov/countries/profiles/uganda- profile.pdf
44. 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 morbidityin a community of rural Cǒte d'Ivoire. International Journal of Epidemiology 33, 1092-1102.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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 lowincome families. American Journal of Clinical Nutrition 87, 614-620.
50. Schofield, L. and Grau, G. E. (2005). Immunological processes in malaria pathogenesis. Nature Reviews Immunology 5, 722-735. doi: 10.1038/nri1686.
51. 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.
52. 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.
53. 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.
54. 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. (2010a). 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.
55. Sousa-Figueiredo, J. C., Pleasant, J., Day, M., Betson, M., Rollinson, D., Montresor, A., Kazibwe, F., Kabatereine, N. B. and Stothard, J. R. (2010b). 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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=144
61. 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.pdf
62. World Health Organization (1987). Atlas of the global distribution of schistosomiasis Uganda. Accessed August 2010. http://www.who.int/ wormcontrol/documents/maps/en/uganda.pdf
63. 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.
64. World Health Organization (2006a). Vitamin and Mineral Nutrition Information System, Uganda. Accessed October 2010. http://who.int/ vmnis/anaemia/data/database/countries/uga-ida.pdf
65. World Health Organization (2006b). 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.pdf
66. WHOand UNICEF (1998). Complementary Feeding of Young Children in Developing Countries: a Review of Current Scientific Knowledge. World Health Organization: Geneva.
67. 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.pdf
68. Zimmermann, M. B. and Hurrell, R. F. (2007). Nutritional iron deficiency. Lancet 370, 511-520.