Volume 97, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Anemia is a worldwide public health concern especially in preschool children in developing countries and iron deficiency (ID) is generally assumed to cause at least 50% of the cases. However, data on this contribution are scarce. To close this gap, we determined in 2013 the contribution of ID in the etiology of anemia and measured others factors associated to noniron deficiency anemia (NIDA) in 900 preschool children randomly selected during a two-stage cluster nutritional survey in the Miti-Murhesa health zone, in eastern Democratic Republic of the Congo. In these children, we collected sociodemographic, clinical, and biological parameters and determined the nutritional status according to the World Health Organization 2006 standards. Anemia was defined as altitude-adjusted hemoglobin < 110 g/L and ID was defined as serum ferritin < 12 μg/L or < 30 μg/L in the absence or presence of inflammation, respectively. Median (interquartile range) age was 29.4 (12–45) months. The prevalence of anemia was 46.6% (391/838) among whom only 16.5% (62/377) had ID. Among children without signs of inflammation, only 4.4% (11/251) met the ferritin-based (unadjusted) definition of ID. Logistic regression analysis identified ID, history of fever during the last 2 weeks and mid-upper arm circumference < 125 mm as the only independent factors associated to anemia. In conclusion, anemia is a severe public health problem in the Miti-Murhesa health zone, but NIDA is mostly predominant and needs to be further studied. Control of infections and prevention of acute undernutrition (wasting) are some of appropriate interventions to reduce the burden anemia in this region.


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  1. WHO, 2011. Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. Vitamin and Mineral Nutrition Information System. Geneva, Switzerland: World Health Organization (WHO/NMH/NHD/MNM/11.1). Available at: http://apps.who.int/iris/bitstream/10665/85839/3/WHO_NMH_NHD_MNM_11.1_eng.pdf?ua=1. Accessed June 16, 2016.
  2. Alvarez-Uria G, Naik PK, Midde M, Yalla PS, Pakam R, , 2014. Prevalence and severity of anaemia stratified by age and gender in rural India. Anemia 2014: 176182.[Crossref]
  3. WHO, 2005. World Health Report 2005. Geneva, Switzerland: World Health Organization.
  4. Walker SP, Wachs TD, Meeks Gardner J, Lozoff B, Wasserman GA, Pollitt E, Carter JA, , 2007. Child development: risk factors for adverse outcomes in developing countries. Lancet 369: 145157.[Crossref]
  5. Lozoff BJE, Hagen J, Mollen E, Wolf AW, , 2000. Poorer behavioral and developmental outcome more than 10 years after treatment for iron deficiency in infancy. Pediatrics 105: e51.[Crossref]
  6. Sherriff A, Emond A, Bell CJ, Golding J, ; ALSPAC Study Team, 2001. Should infants be screened for anaemia? A prospective study investigating the relation between haemoglobin at 8, 12, and 18 months and development at 18 months. Arch Dis Child 84: 480485.[Crossref]
  7. 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]
  8. Balarajan Y, Ramakrishnan U, Özaltin E, Shankar AH, Subramanian SV, , 2011. Anaemia in low-income and middle-income countries. Lancet 378: 21232135.[Crossref]
  9. Diouf S, Folquet M, Mbofung K, Ndiaye O, Brou K, Dupont C, Vuillerod M, Azais-Braesco V, Tetanye E, , 2015. Prevalence and determinants of anemia in young children in French-speaking Africa. Role of iron deficiency [in French]. Arch Pediatr 22: 11881197.[Crossref]
  10. International MoPaM, 2008. Democratic Republic of Congo Demographic and Health Survey 2007. Calverton, MD: Ministère du Plan et Macro International.
  11. Stoltzfus JR, Chwaya MH, Tielsch MJ, Schulze JK, Albonico M, Savioli L, , 1997. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. Am J Clin Nutr 65: 153159.
  12. Ezzati MLA, Rodgers AA, Murray CJL, , 2004. Comparative Quantification of Health Risks: Global and Regional Burden of Disease Attributable to Selected Major Risk Factors, Vol. 1. Geneva, Switzerland: World Health Organization.
  13. Fondu P, Hariga-Muller C, Mozes N, Neve J, Van Steirteghem A, Mandelbaum IM, , 1978. Protein-energy malnutrition and anemia in Kivu. Am J Clin Nutr 31: 4656.
  14. Mitangala PN, ., 2013. Malaria infection and nutritional status: results from a cohort survey of children from 6-59 months old in the Kivu province, Democratic Republic of the Congo. Rev Epidemiol Sante Publique 61: 111120.[Crossref]
  15. Action Against Hunger, 2012. Enquête Nutritionnelle Anthropométrique: zone de santé de Miti-Murhesa [in French]. Available at: http://www.actionagainsthunger.org/sites/default/files/publications/Enquete_Nutritionnelle_Anthropometrique_Zone_de_Sante_de_Miti-Murhesa_Province_du_Sud-Kivu_DRC_08.2011.pdf. Accessed June 16, 2016.
  16. Gorstein J, Sullivan KM, Parvanta I, Begin F, , 2007. Indicators and Methods for Cross-Sectional Surveys of Vitamin and Mineral Status of Populations. Atlanta, GA: Centers for Disease Control and Prevention
  17. SMART, 2012. Sampling Methods and Sample Size Calculation for the SMART Methodology. Available at: http://smartmethodology.org/survey-planning-tools/smart-methodology/. Accessed February 23, 2013.
  18. Cogill B, , 2003. Anthropometric Indicators Measurement Guide. Washington, DC: Food and Nutrition Technical Assistance (FANTA) Project, FHI 360.
  19. 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.
  20. de Onis M, Onyango WA, van den Broeck J, Chumlea WM, Martorell R, , 2004. Measurement and standardization protocols for anthropometry used in the construction of a new international growth reference. Food Nutr Bull 25(1 Suppl): S27S36.[Crossref]
  21. WHO, 2013. Guideline: Updates on the Management of Severe Acute Malnutrition in Infants and Children. Geneva, Switzerland: World Health Organization.
  22. Annan AR, Webb P, , Brown R , 2014. Management of Moderate Acute Malnutrition (MAM): Current Knowledge and Practice: CMAM Forum Technical Brief. Available at: http://foodaidquality.org/sites/default/files/publications/MAM-management-CMAM-Forum-Technical-Brief-Sept-2014.pdf. Accessed August 3, 2016.
  23. WHO/CDC, 2004. Technical Consultation on the Assessment of Iron Status at the Population Level. Geneva, Switzerland: World Health Organization.
  24. 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]
  25. Donnen P, Brasseur D, Dramaix M, Assimbo V, Hennart P, , 1997. Effects of cow's milk supplementation on milk output of protein deficient lactating mothers and on their infants' energy and protein status. Trop Med Int Health 2: 3846.[Crossref]
  26. Levitt DG, Levitt MD, , 2016. Human serum albumin homeostasis: a new look at the roles of synthesis, catabolism, renal and gastrointestinal excretion, and the clinical value of serum albumin measurements. Int J Gen Med 9: 229255.[Crossref]
  27. Ministry of Planning and Monitoring of the Implementation of the Revolution of Modernity (MPMIRM), Ministry of Public Health (MPH) and ICF International, 2014. Demographic and Health Survey in the Democratic Republic of Congo 2013–2014. Rockville, MD: MPMIRM, MPH and ICF International.
  28. Harvey-Leeson S, ., 2016. Anemia and micronutrient status of women of childbearing age and children 6–59 months in the Democratic Republic of the Congo. Nutrients 8: 98.[Crossref]
  29. Gahutu JB, ., 2011. Prevalence and risk factors of malaria among children in southern highland Rwanda. Malar J 10: 134.[Crossref]
  30. Ndeba PM, , 2012. Efficacy of artesunate plus amodiaquine for treatment of uncomplicated clinical Falciparum malaria in severely malnourished children aged 6–59 months, Democratic Republic of Congo. J Clin Exp Pathol. S3: 5.
  31. Bahizire E, Mitangala P, Donnen P, Balegamire S, Mulinganya G, Bahizi P, D'Alessandro U, Senterre C, Meuris S, Dramaix M, , 2016. Malaria at the first antenatal visit: prevalence and associated factors in rural area in south Kivu, eastern part of the Democratic Republic of Congo. Med Afr Noire 63: 437449.
  32. Frosch AE, Ondigo BN, Ayodo GA, Vulule JM, John CC, Cusick SE, , 2014. Decline in childhood iron deficiency after interruption of malaria transmission in highland Kenya. Am J Clin Nutr 100: 968973.[Crossref]
  33. Danquah I, Gahutu JB, Zeile I, Musemakweri A, Mockenhaupt FP, , 2014. Anaemia, iron deficiency and a common polymorphism of iron-regulation, TMPRSS6 rs855791, in Rwandan children. Trop Med Int Health 19: 117122.[Crossref]
  34. Chang Cojulun A, Bustinduy AL, Sutherland LJ, Mungai PL, Mutuku F, Muchiri E, Kitron U, King CH, , 2015. Anemia among children exposed to polyparasitism in coastal Kenya. Am J Trop Med Hyg 93: 10991105.[Crossref]
  35. Asobayire SFAP, Davidsson L, Cook DJ, Hurrell FR, , 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.
  36. Ngnie-Teta I, Sanou D, , 2012. Risk factors for anemia in preschool children in Sub-Saharan Africa, Silverberg D, ed., Anemia. Rijeka, Croatia: InThech. Available at: http://www.intechopen.com/books/anemia/risk-factors-for-anemia-in-preschool-children-in-sub-saharan-africa. Accessed August 3, 2016.
  37. Kateera F, Ingabire CM, Hakizimana E, Kalinda P, Mens PF, Grobusch MP, Mutesa L, van Vugt M, , 2015. Malaria, anaemia and under-nutrition: three frequently co-existing conditions among preschool children in rural Rwanda. Malar J 14: 440.[Crossref]
  38. Foote EM, Sullivan KM, Ruth LJ, Oremo J, Sadumah I, Williams TN, Suchdev PS, , 2013. Determinants of anemia among preschool children in rural, western Kenya. Am J Trop Med Hyg 88: 757764.[Crossref]
  39. McCuskee S, Brickley EB, Wood A, Mossialos E, , 2014. Malaria and macronutrient deficiency as correlates of anemia in young children: a systematic review of observational studies. Ann Glob Health 80: 458465.[Crossref]
  40. Wieringa FT, ., 2016. The high prevalence of anemia in Cambodian children and women cannot be satisfactorily explained by nutritional deficiencies or hemoglobin disorders. Nutrients 8: pii: E348.
  41. Osawa M, Yamaguchi T, Nakamura Y, Kaneko S, Onodera M, Sawada K, Jegalian A, Wu H, Nakauchi H, Iwama A, , 2002. Erythroid expansion mediated by the Gfi-1B zinc finger protein: role in normal hematopoiesis. Blood 100: 27692777.[Crossref]
  42. Prasad AS, , 2009. Zinc: role in immunity, oxidative stress and chronic inflammation. Curr Opin Clin Nutr Metab Care 12: 646652.[Crossref]
  43. Ganz T, , 2011. Hepcidin and iron regulation, 10 years later. Blood 117: 44254433.[Crossref]
  44. Prentice AM, Cox SE, , 2012. Iron and malaria interactions: research needs from basic science to global policy. Adv Nutr 3: 583591.[Crossref]
  45. Kasvosve I, , 2013. Effect of ferroportin polymorphism on iron homeostasis and infection. Clin Chim Acta 416: 2025.[Crossref]
  46. Burte F, ., 2013. Circulatory hepcidin is associated with the anti-inflammatory response but not with iron or anemic status in childhood malaria. Blood 121: 30163022.[Crossref]
  47. Shaw JG, Friedman JF, , 2011. Iron deficiency anemia: focus on infectious diseases in lesser developed countries. Anemia 2011: 260380.[Crossref]
  48. Elbadry MA, ., 2015. High prevalence of asymptomatic malaria infections: a cross-sectional study in rural areas in six departments in Haiti. Malar J 14: 510.[Crossref]
  49. Parr JB, ., 2016. Pfhrp2-deleted Plasmodium falciparum parasites in the Democratic Republic of the Congo: a National Cross-sectional Survey. J Infect Dis., doi: 10.1093/infdis/jiw538. https://doi.org/10.1093/infdis/jiw538
  50. Taylor-Robinson DC, Maayan N, Soares-Weiser K, Donegan S, Garner P, , 2015. Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin, and school performance. Cochrane Database Syst Rev 3: CD000371.
  51. de Gier B, Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC, van de Bor M, Ponce MC, Polman K, Wieringa FT, , 2016. Species-specific associations between soil-transmitted helminths and micronutrients in Vietnamese schoolchildren. Am J Trop Med Hyg 95: 7782.[Crossref]
  52. Gahutu JB, Musemakweri A, Harms G, Mockenhaupt FP, , 2012. Prevalence of classic erythrocyte polymorphisms among 749 children in southern highland Rwanda. Trans R Soc Trop Med Hyg 106: 6365.[Crossref]
  53. Tshilolo L, Aissi LM, Lukusa D, Kinsiama C, Wembonyama S, Gulbis B, Vertongen F, , 2009. Neonatal screening for sickle cell anaemia in the Democratic Republic of the Congo: experience from a pioneer project on 31 204 newborns. J Clin Pathol 62: 3538.[Crossref]
  54. Veenemans J, ., 2008. Alpha+-thalassemia protects against anemia associated with asymptomatic malaria: evidence from community-based surveys in Tanzania and Kenya. J Infect Dis 198: 401408.[Crossref]
  55. Calis JC, ., 2008. Severe anemia in Malawian children. N Engl J Med 358: 888899.[Crossref]
  56. Cikomola JC, Vandepoele K, Katchunga PB, Kishabongo AS, Padalko EY, Speeckaert MM, Delanghe JR, , 2016. The association between fructosamine-3 kinase 900C/G polymorphism, transferrin polymorphism and human herpesvirus-8 infection in diabetics living in South Kivu. Acta Trop 163: 1419.[Crossref]

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  • Received : 12 Jan 2017
  • Accepted : 15 Mar 2017

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