Volume 87, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Anemia affects one-quarter of the world's population, but its etiology remains poorly understood. We determined the prevalence of anemia and studied underlying risk factors in infants (6–23 months), young school-aged children (6–8 years), and young non-pregnant women (15–25 years) in south-central Côte d'Ivoire. Blood, stool, and urine samples were subjected to standardized, quality-controlled methods. We found high prevalence of anemia, malaria, inflammation, and deficiencies of iron, riboflavin, and vitamin A but low prevalence and intensities of soil-transmitted helminth and schistosome infections. Multivariate regression analysis revealed significant associations between anemia and for infants, inflammation for school-aged children, and cellular iron deficiency for both school-aged children and non-pregnant women. Women with riboflavin deficiency had significantly lower odds of anemia. Our findings call for interventions to protect infants from malaria, improved intake of dietary iron, better access to health care, and health education.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. McLean E, Cogswell M, Egli I, Wojdyla D, de Benoist B, , 2009. Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993–2005. Public Health Nutr 12: 444454.[Crossref] [Google Scholar]
  2. Tolentino K, Friedman JF, , 2007. An update on anemia in less developed countries. Am J Trop Med Hyg 77: 4451. [Google Scholar]
  3. WHO/UNICEF/UNU, 2001. Iron Deficiency Anemia: Assessment, Prevention and Control. Geneva: World Health Organization. [Google Scholar]
  4. Rohner F, Zimmermann MB, Amon RJ, Vounatsou P, Tschannen AB, N'Goran EK, Nindjin C, Cacou MC, Te-Bonle MD, Aka H, Sess DE, Utzinger J, Hurrell RF, , 2010. In a randomized 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. J Nutr 140: 635641.[Crossref] [Google Scholar]
  5. Wegmüller R, Camara F, Zimmermann MB, Adou P, Hurrell RF, , 2006. Salt dual-fortified with iodine and micronized ground ferric pyrophosphate affects iron status but not hemoglobin in children in Côte d'Ivoire. J Nutr 136: 18141820. [Google Scholar]
  6. Staubli Asobayire F, Adou P, Davidsson L, Cook JD, Hurrell RF, , 2001. Prevalence of iron deficiency with and without concurrent anemia in population groups with high prevalences of malaria and other infections: a study in Côte d'Ivoire. Am J Clin Nutr 74: 776782. [Google Scholar]
  7. ter Kuile FO, Terlouw DJ, Kariuki SK, Phillips-Howard PA, Mirel LB, Hawley WA, Friedman JF, Shi YP, Kolczak MS, Lal AA, Vulule JM, Nahlen BL, , 2003. Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western Kenya. Am J Trop Med Hyg 68: 6877. [Google Scholar]
  8. Bonfoh B, Raso G, Koné I, Dao D, Girardin O, Cissé G, Zinsstag J, Utzinger J, Tanner M, , 2011. Research in a war zone. Nature 474: 569571.[Crossref] [Google Scholar]
  9. Becker SL, Sieto B, Silué KD, Adjossan L, Koné S, Hatz C, Kern WV, N'Goran EK, Utzinger J, , 2011. Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Negl Trop Dis 5: e1292.[Crossref] [Google Scholar]
  10. N'Goran EK, Diabate S, Utzinger J, Sellin B, , 1997. Changes in human schistosomiasis levels after the construction of two large hydroelectric dams in central Côte d'Ivoire. Bull World Health Organ 75: 541545. [Google Scholar]
  11. WHO, 1990. Adequacy of Sample Size in Health Studies. New York: John Wiley & Sons. [Google Scholar]
  12. Katz N, Chaves A, Pellegrino J, , 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop São Paulo 14: 397400. [Google Scholar]
  13. WHO, 1991. Basic Laboratory Methods in Medical Parasitology. Geneva: World Health Organization. [Google Scholar]
  14. Schneider RG, , 1974. Differentiation of electrophoretically similar hemoglobins—such as S, D, G, and P; or A2, C, E, and O—by electrophoresis of the globin chains. Clin Chem 20: 11111115. [Google Scholar]
  15. Dror Y, Stern F, Komarnitsky M, , 1994. Optimal and stable conditions for the determination of erythrocyte glutathione reductase activation coefficient to evaluate riboflavin status. Int J Vitam Nutr Res 64: 257262. [Google Scholar]
  16. Sauberlich H, , 1999. Vitamin B-2. Laboratory Tests for the Assessment of Nutritional Status, 2nd Ed. Boca Raton, FL: CRC Press, 5569. [Google Scholar]
  17. Erhardt JG, Estes JE, Pfeiffer CM, Biesalski HK, Craft NE, , 2004. Combined measurement of ferritin, soluble transferrin receptor, retinol binding protein, and C-reactive protein by an inexpensive, sensitive, and simple sandwich enzyme-linked immunosorbent assay technique. J Nutr 134: 31273132. [Google Scholar]
  18. Tanumihardjo SA, Permaesih D, Muhilal, 2004. Vitamin A status and hemoglobin concentrations are improved in Indonesian children with vitamin A and deworming interventions. Eur J Clin Nutr 58: 12231230.[Crossref] [Google Scholar]
  19. Cook JD, Skikne BS, Baynes RD, , 1993. Serum transferrin receptor. Annu Rev Med 44: 6374.[Crossref] [Google Scholar]
  20. WHO, 2011. Serum Retinol Concentrations for Determining the Prevalence of Vitamin A Deficiency in Populations. Vitamin and Mineral Nutrition Information System. Geneva: World Health Organization. [Google Scholar]
  21. Gorstein JL, Dary O, Pongtorn Shell-Duncan B, Quick T, Wasanwisut E, , 2008. Feasibility of using retinol-binding protein from capillary blood specimens to estimate serum retinol concentrations and the prevalence of vitamin A deficiency in low-resource settings. Public Health Nutr 11: 513520.[Crossref] [Google Scholar]
  22. Wang W, Knovich MA, Coffman LG, Torti FM, Torti SV, , 2010. Serum ferritin: past, present and future. Biochim Biophys Acta 1800: 760769.[Crossref] [Google Scholar]
  23. Thurnham DI, McCabe GP, Northrop-Clewes CA, Nestel P, , 2003. Effects of subclinical infection on plasma retinol concentrations and assessment of prevalence of vitamin A deficiency: meta-analysis. Lancet 362: 20522058.[Crossref] [Google Scholar]
  24. N'Goran EK, Utzinger J, N'Guessan AN, Müller I, Zamblé K, Lohourignon KL, Traoré M, Sosthène BA, Lengeler C, Tanner M, , 2001. Reinfection with Schistosoma haematobium following school-based chemotherapy with praziquantel in four highly endemic villages in Côte d'Ivoire. Trop Med Int Health 6: 817825.[Crossref] [Google Scholar]
  25. Booth M, Vounatsou P, N'Goran EK, Tanner M, Utzinger J, , 2003. The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d'Ivoire. Parasitology 127: 525531.[Crossref] [Google Scholar]
  26. WHO, 1998. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. Geneva: World Health Organization. [Google Scholar]
  27. Marti H, Koella JC, , 1993. Multiple stool examinations for ova and parasites and rate of false-negative results. J Clin Microbiol 31: 30443045. [Google Scholar]
  28. Utzinger J, Booth M, N'Goran EK, Müller I, Tanner M, Lengeler C, , 2001. Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 122: 537544.[Crossref] [Google Scholar]
  29. Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, Rollinson D, Marti H, Utzinger J, , 2008. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis 2: e331.[Crossref] [Google Scholar]
  30. Knopp S, Rinaldi L, Khamis IS, Stothard JR, Rollinson D, Maurelli MP, Steinmann P, Marti H, Cringoli G, Utzinger J, , 2009. A single FLOTAC is more sensitive than triplicate Kato-Katz for the diagnosis of low-intensity soil-transmitted helminth infections. Trans R Soc Trop Med Hyg 103: 347354.[Crossref] [Google Scholar]
  31. Magalhães RJ, Clements ACA, , 2011. Mapping the risk of anaemia in preschool-age children: the contribution of malnutrition, malaria, and helminth infections in West Africa. PLoS Med 8: e1000438.[Crossref] [Google Scholar]
  32. Noor AM, Mutheu JJ, Tatem AJ, Hay SI, Snow RW, , 2009. Insecticide-treated net coverage in Africa: mapping progress in 2000–07. Lancet 373: 5867.[Crossref] [Google Scholar]
  33. Murphy SC, Breman JG, , 2001. Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am J Trop Med Hyg 64 (1–2 Suppl): 5767. [Google Scholar]
  34. Stoltzfus RJ, , 2003. Iron deficiency: global prevalence and consequences. Food Nutr Bull 24: S99S103.[Crossref] [Google Scholar]
  35. Haider BA, Bhutta ZA, , 2011. Neonatal vitamin A supplementation for the prevention of mortality and morbidity in term neonates in developing countries. Cochrane Database Syst Rev 10: CD006980. [Google Scholar]
  36. Zimmermann MB, Biebinger R, Rohner F, Dib A, Zeder C, Hurrell RF, Chaouki N, , 2006. Vitamin A supplementation in children with poor vitamin A and iron status increases erythropoietin and hemoglobin concentrations without changing total body iron. Am J Clin Nutr 84: 580586. [Google Scholar]
  37. Scott JM, Kraemer K, Zimmermann MB, , 2007. Nutritional anemia: B-vitamins. , eds. Nutritional Anemia. Basel, Switzerland: Sight and Life Press, 111132. [Google Scholar]
  38. West KP, Jr Gernand AD, Sommer A, Kraemer K, Zimmermann MB, , 2007. Vitamin A in nutritional anemia. , eds. Nutritional Anemia. Basel, Switzerland: Sight and Life Press, 133154. [Google Scholar]
  39. Cercamondi CI, Egli IM, Ahouandjinou E, Dossa R, Zeder C, Salami L, Tjalsma H, Wiegerinck E, Tanno T, Hurrell RF, Hounhouigan J, Zimmermann MB, , 2010. Afebrile Plasmodium falciparum parasitemia decreases absorption of fortification iron but does not affect systemic iron utilization: a double stable-isotope study in young Beninese women. Am J Clin Nutr 92: 13851392.[Crossref] [Google Scholar]
  40. Roodenburg AJ, West CE, Beguin Y, Van Dijk JE, Van Eijk HG, Marx JJ, Beynen AC, , 2000. Indicators of erythrocyte formation and degradation in rats with either vitamin A or iron deficiency. J Nutr Biochem 11: 223230.[Crossref] [Google Scholar]
  41. Walter T, Dallman PR, Pizarro F, Velozo L, Pena G, Bartholmey SJ, Hertrampf E, Olivares M, Letelier A, Arredondo M, , 1993. Effectiveness of iron-fortified infant cereal in prevention of iron deficiency anemia. Pediatrics 91: 976982. [Google Scholar]
  42. Okebe JU, Yahav D, Shbita R, Paul M, , 2011. Oral iron supplements for children in malaria-endemic areas. Cochrane Database Syst Rev 10: CD006589. [Google Scholar]
  43. Faber M, Jogessar VB, Benade AJ, , 2001. Nutritional status and dietary intakes of children aged 2–5 years and their caregivers in a rural South African community. Int J Food Sci Nutr 52: 401411.[Crossref] [Google Scholar]
  44. Abrams SA, Mushi A, Hilmers DC, Griffin IJ, Davila P, Allen L, , 2003. A multinutrient-fortified beverage enhances the nutritional status of children in Botswana. J Nutr 133: 18341840. [Google Scholar]
  45. Siekmann JH, Allen LH, Bwibo NO, Demment MW, Murphy SP, Neumann CG, , 2003. Kenyan school children have multiple micronutrient deficiencies, but increased plasma vitamin B-12 is the only detectable micronutrient response to meat or milk supplementation. J Nutr 133: 3972S3980S. [Google Scholar]
  46. Rohner F, Zimmermann MB, Wegmüller R, Tschannen AB, Hurrell RF, , 2007. Mild riboflavin deficiency is highly prevalent in school-age children but does not increase risk for anaemia in Côte d'Ivoire. Br J Nutr 97: 970976.[Crossref] [Google Scholar]
  47. Powers HJ, Hill MH, Mushtaq S, Dainty JR, Majsak-Newman G, Williams EA, , 2011. Correcting a marginal riboflavin deficiency improves hematologic status in young women in the United Kingdom (RIBOFEM). Am J Clin Nutr 93: 12741284.[Crossref] [Google Scholar]
  48. Powers HJ, Bates CJ, Prentice AM, Lamb WH, Jepson M, Bowman H, , 1983. The relative effectiveness of iron and iron with riboflavin in correcting a microcytic anaemia in men and children in rural Gambia. Hum Nutr Clin Nutr 37: 413425. [Google Scholar]
  49. Kaikai P, Thurnham DI, , 1983. The influence of riboflavin deficiency on Plasmodium berghei infection in rats. Trans R Soc Trop Med Hyg 77: 680686.[Crossref] [Google Scholar]
  50. Thurnham DI, Oppenheimer SJ, Bull R, , 1983. Riboflavin status and malaria in infants in Papua New Guinea. Trans R Soc Trop Med Hyg 77: 423424.[Crossref] [Google Scholar]
  51. Yapi HF, Ahiboh H, Ago K, Ake M, Monnet D, , 2005. Protein profile and vitamin A in children of school age in Ivory Coast. Ann Biol Clin (Paris) 63: 291295. [Google Scholar]
  52. Glinz D, N'Guessan NA, Utzinger J, N'Goran EK, , 2010. High prevalence of Strongyloides stercoralis among school children in rural Côte d'Ivoire. J Parasitol 96: 431433.[Crossref] [Google Scholar]

Data & Media loading...

  • Received : 19 Dec 2011
  • Accepted : 21 Apr 2012
  • Published online : 05 Sep 2012

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error