{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,17]],"date-time":"2026-04-17T17:17:02Z","timestamp":1776446222458,"version":"3.51.2"},"reference-count":46,"publisher":"MDPI AG","issue":"15","license":[{"start":{"date-parts":[[2023,8,2]],"date-time":"2023-08-02T00:00:00Z","timestamp":1690934400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Arla Food for Health"},{"name":"Danish Dairy Research Foundation"},{"name":"Augustinus Fonden"},{"name":"L\u00e6ge Sofus Carl Emil Friis og Hustru Olga Doris Friis\u2019 Legat"},{"name":"A. P. M\u00f8ller Fonden til L\u00e6gevidenskabens Fremme"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>Micronutrient deficiencies and stunting are prevalent. We assessed correlates of iron, cobalamin, folate, and vitamin A biomarkers in a cross-sectional study of stunted children aged 12\u201359 months in eastern Uganda. The biomarkers measured were serum ferritin (S-FE), soluble transferrin receptor (S-TfR), retinol binding protein (S-RBP), plasma cobalamin (P-Cob), methylmalonic acid (P-MMA), and folate (P-Fol). Using linear regression, we assessed socio-demography, stunting severity, malaria rapid test, and inflammation as correlates of micronutrient biomarkers. Of the 750 children, the mean (SD) age was 32.0 (11.7) months, and 45% were girls. Iron stores were depleted (inflammation-corrected S-FE &lt; 12 \u00b5g\/L) in 43%, and 62% had tissue iron deficiency (S-TfR &gt; 8.3 mg\/L). P-Cob was low (&lt;148 pmol\/L) and marginal (148\u2013221 pmol\/L) in 3% and 20%, and 16% had high P-MMA (&gt;0.75 \u00b5mol\/L). Inflammation-corrected S-RBP was low (&lt;0.7 \u00b5mol\/L) in 21% and P-Fol (&lt;14 nmol\/L) in 1%. Age 24\u201359 months was associated with higher S-FE and P-Fol and lower S-TfR. Breastfeeding beyond infancy was associated with lower iron status and cobalamin status, and malaria was associated with lower cobalamin status and tissue iron deficiency (higher S-TfR) despite iron sequestration in stores (higher S-FE). In conclusion, stunted children have iron, cobalamin, and vitamin A deficiencies. Interventions addressing stunting should target co-existing micronutrient deficiencies.<\/jats:p>","DOI":"10.3390\/nu15153429","type":"journal-article","created":{"date-parts":[[2023,8,2]],"date-time":"2023-08-02T10:57:33Z","timestamp":1690973853000},"page":"3429","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Correlates of Iron, Cobalamin, Folate, and Vitamin A Status among Stunted Children: A Cross-Sectional Study in Uganda"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1311-9946","authenticated-orcid":false,"given":"Rolland","family":"Mutumba","sequence":"first","affiliation":[{"name":"Department of Nutrition, Exercise and Sports, University of Copenhagen, 1958 Frederiksberg C, Denmark"},{"name":"Department of Paediatrics and Child Health, School of Medicine, College of Health Sciences, Makerere University, Kampala P.O. Box 7072, Uganda"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hannah","family":"Pesu","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Exercise and Sports, University of Copenhagen, 1958 Frederiksberg C, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7602-8008","authenticated-orcid":false,"given":"Joseph","family":"Mbabazi","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Exercise and Sports, University of Copenhagen, 1958 Frederiksberg C, Denmark"},{"name":"Department of Paediatrics and Child Health, School of Medicine, College of Health Sciences, Makerere University, Kampala P.O. Box 7072, Uganda"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eva","family":"Greibe","sequence":"additional","affiliation":[{"name":"Department of Clinical Biochemistry, Aarhus University Hospital, 8200 Aarhus N, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mette F.","family":"Olsen","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Exercise and Sports, University of Copenhagen, 1958 Frederiksberg C, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9390-8541","authenticated-orcid":false,"given":"Andr\u00e9","family":"Briend","sequence":"additional","affiliation":[{"name":"Tampere Center for Child, Adolescent and Maternal Health Research, Faculty of Medicine and Health Technology, Tampere University and Tampere University Hospital, 33520 Tampere, Finland"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christian","family":"M\u00f8lgaard","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Exercise and Sports, University of Copenhagen, 1958 Frederiksberg C, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5095-0624","authenticated-orcid":false,"given":"Christian","family":"Ritz","sequence":"additional","affiliation":[{"name":"National Institute of Public Health, University of Southern Denmark, 5230 Odense, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nicolette","family":"Nabukeera-Barungi","sequence":"additional","affiliation":[{"name":"Department of Paediatrics and Child Health, School of Medicine, College of Health Sciences, Makerere University, Kampala P.O. Box 7072, Uganda"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ezekiel","family":"Mupere","sequence":"additional","affiliation":[{"name":"Department of Paediatrics and Child Health, School of Medicine, College of Health Sciences, Makerere University, Kampala P.O. Box 7072, Uganda"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Suzanne","family":"Filteau","sequence":"additional","affiliation":[{"name":"Faculty of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London WC1E 7HT, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Henrik","family":"Friis","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Exercise and Sports, University of Copenhagen, 1958 Frederiksberg C, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Benedikte","family":"Grenov","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Exercise and Sports, University of Copenhagen, 1958 Frederiksberg C, Denmark"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,2]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization, and Food Agriculture Organization of the United Nations (2004). Vitamin and Mineral Requirements in Human Nutrition, World Health Organization. [2nd ed.]."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e1590","DOI":"10.1016\/S2214-109X(22)00367-9","article-title":"Micronutrient deficiencies among preschool-aged children and women of reproductive age worldwide: A pooled analysis of individual-level data from population-representative surveys","volume":"10","author":"Stevens","year":"2022","journal-title":"Lancet Glob. Health"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2123","DOI":"10.1016\/S0140-6736(10)62304-5","article-title":"Anaemia in low-income and middle-income countries","volume":"378","author":"Balarajan","year":"2011","journal-title":"Lancet"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"S126","DOI":"10.1177\/15648265080292S117","article-title":"Effects of Vitamin B12 and Folate Deficiency on Brain Development in Children","volume":"29","author":"Black","year":"2008","journal-title":"Food Nutr. Bull."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1093\/ajcn\/85.4.931","article-title":"An overview of evidence for a causal relation between iron deficiency during development and deficits in cognitive or behavioral function","volume":"85","author":"McCann","year":"2007","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1111\/nure.12102","article-title":"Nutrition and brain development in early life","volume":"72","author":"Prado","year":"2014","journal-title":"Nutr. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"d5094","DOI":"10.1136\/bmj.d5094","article-title":"Vitamin A supplements for preventing mortality, illness, and blindness in children aged under 5: Systematic review and meta-analysis","volume":"343","author":"Imdad","year":"2011","journal-title":"BMJ"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Muriuki, J.M., Mentzer, A.J., Webb, E.L., Morovat, A., Kimita, W., Ndungu, F.M., Macharia, A.W., Crane, R.J., Berkley, J.A., and Lule, S.A. (2020). Estimating the burden of iron deficiency among African children. BMC Med., 18.","DOI":"10.1186\/s12916-020-1502-7"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e528","DOI":"10.1016\/S2214-109X(15)00039-X","article-title":"Trends and mortality effects of vitamin A deficiency in children in 138 low-income and middle-income countries between 1991 and 2013: A pooled analysis of population-based surveys","volume":"3","author":"Stevens","year":"2015","journal-title":"Lancet Glob. Health"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1995S","DOI":"10.1093\/jn\/nxy201","article-title":"Biomarkers of Nutrition for Development (BOND): Vitamin B-12 Review","volume":"148","author":"Allen","year":"2018","journal-title":"J. Nutr."},{"key":"ref_11","unstructured":"World Health Organization, and United Nations Children\u2019s Fund (2021). The World Bank. Levels and Trends in Child Malnutrition: UNICEF\/WHO\/The World Bank Group Joint Child Malnutrition Estimates: Key Findings of the 2021 Edition, World Health Organization."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1179\/2046905514Y.0000000158","article-title":"The stunting syndrome in developing countries","volume":"34","author":"Prendergast","year":"2014","journal-title":"Paediatr. Int. Child Health"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e243","DOI":"10.1016\/S2542-5196(21)00352-1","article-title":"Global, regional, and national consumption of animal-source foods between 1990 and 2018: Findings from the Global Dietary Database","volume":"6","author":"Miller","year":"2022","journal-title":"Lancet Planet. Health"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"349","DOI":"10.3945\/an.115.010215","article-title":"Overview of the Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) Project","volume":"7","author":"Suchdev","year":"2016","journal-title":"Adv. Nutr."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Bendich, A., and Deckelbaum, R.J. (2010). Preventive Nutrition: The Comprehensive Guide for Health Professionals, Humana Press.","DOI":"10.1007\/978-1-60327-542-2"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1016\/S0140-6736(07)61692-4","article-title":"Maternal and child undernutrition: Consequences for adult health and human capital","volume":"371","author":"Victora","year":"2008","journal-title":"Lancet"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e473","DOI":"10.1542\/peds.2009-1519","article-title":"Worldwide Timing of Growth Faltering: Revisiting Implications for Interventions","volume":"125","author":"Victora","year":"2010","journal-title":"Pediatrics"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"nzab067","DOI":"10.1093\/cdn\/nzab067","article-title":"The Role of Milk Protein and Whey Permeate in Lipid-based Nutrient Supplements on the Growth and Development of Stunted Children in Uganda: A Randomized Trial Protocol (MAGNUS)","volume":"5","author":"Pesu","year":"2021","journal-title":"Curr. Dev. Nutr."},{"key":"ref_19","unstructured":"Uganda Bureau of Statistcs (UBOS) and ICF (2017). Uganda Demographic and Health Survey 2016: Key Indicators Report, Uganda Bureau of Statistics."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"3127","DOI":"10.1093\/jn\/134.11.3127","article-title":"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","volume":"134","author":"Erhardt","year":"2004","journal-title":"J. Nutr."},{"key":"ref_21","unstructured":"Centers for Disease Control and Prevention, World Health Organization, Nutrition International, and UNICEF (2020). Micronutrient Survey Manual, World Health Organization."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1258\/acb.2011.011039","article-title":"Screening for metabolic vitamin B12 deficiency by holotranscobalamin in patients suspected of vitamin B12 deficiency: A multicentre study","volume":"49","author":"Heil","year":"2012","journal-title":"Ann. Clin. Biochem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"125","DOI":"10.3945\/jn.116.240028","article-title":"Assessment of Regression Models for Adjustment of Iron Status Biomarkers for Inflammation in Children with Moderate Acute Malnutrition in Burkina Faso","volume":"147","author":"Cichon","year":"2017","journal-title":"J. Nutr."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Friis, H., Cichon, B., Fabiansen, C., Iuel-Brockdorff, A.-S., Yam\u00e9ogo, C.W., Ritz, C., Frikke-Schmidt, R., Briend, A., Michaelsen, K.F., and Christensen, V.B. (2022). Serum cobalamin in children with moderate acute malnutrition in Burkina Faso: Secondary analysis of a randomized trial. PLoS Med., 19.","DOI":"10.1371\/journal.pmed.1003943"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1093\/jn\/137.3.676","article-title":"Low Plasma Vitamin B-12 in Kenyan School Children Is Highly Prevalent and Improved by Supplemental Animal Source Foods","volume":"137","author":"McLean","year":"2007","journal-title":"J. Nutr."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1007\/s12571-020-01060-9","article-title":"Fish as a source of (micro)nutrients to combat hidden hunger in Zambia","volume":"12","author":"Genschick","year":"2020","journal-title":"Food Secur."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Ssentongo, P., Ba, D.M., Ssentongo, A.E., Fronterre, C., Whalen, A., Yang, Y., Ericson, J.E., and Chinchilli, V.M. (2020). Association of vitamin A deficiency with early childhood stunting in Uganda: A population-based cross-sectional study. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0233615"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"96","DOI":"10.11604\/pamj.2019.32.96.17221","article-title":"Programmatic implications of some vitamin A supplementation and deworming determinants among children aged 6\u201359 months in resource-poor rural Kenya","volume":"32","author":"Shadrack","year":"2019","journal-title":"Pan. Afr. Med. J."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Likoswe, B.H., Joy, E.J.M., Sandalinas, F., Filteau, S., Maleta, K., and Phuka, J.C. (2021). Re-Defining the Population-Specific Cut-Off Mark for Vitamin A Deficiency in Pre-School Children of Malawi. Nutrients, 13.","DOI":"10.3390\/nu13030849"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1097\/MPG.0000000000000206","article-title":"Iron Requirements of Infants and Toddlers","volume":"58","author":"Braegger","year":"2014","journal-title":"J. Pediatr. Gastroenterol. Nutr."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1146\/annurev-nutr-043020-011242","article-title":"Breastfeeding Beyond 12 Months: Is There Evidence for Health Impacts?","volume":"41","author":"Lackey","year":"2021","journal-title":"Annu. Rev. Nutr."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"278S","DOI":"10.1093\/advances\/nmy022","article-title":"Overview of Nutrients in Human Milk","volume":"9","author":"Dror","year":"2018","journal-title":"Adv. Nutr. Int. Rev. J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"389","DOI":"10.3945\/ajcn.113.058479","article-title":"Cobalamin and haptocorrin in human milk and cobalamin-related variables in mother and child: A 9-mo longitudinal study","volume":"98","author":"Greibe","year":"2013","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1007\/BF00931158","article-title":"Characterization of cobalamin-dependent methionine synthase purified from the human malarial parasite, Plasmodium falciparum","volume":"75","author":"Krungkrai","year":"1989","journal-title":"Parasitol. Res."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Musabyimana, J.P., Distler, U., Sassmannshausen, J., Berks, C., Manti, J., Bennink, S., Blaschke, L., Burda, P.-C., Flammersfeld, A., and Tenzer, S. (2022). Plasmodium falciparum S-Adenosylmethionine Synthetase Is Essential for Parasite Survival through a Complex Interaction Network with Cytoplasmic and Nuclear Proteins. Microorganisms, 10.","DOI":"10.3390\/microorganisms10071419"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1128\/CMR.00033-08","article-title":"Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance","volume":"22","author":"Scholz","year":"2009","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1017\/S0007114522000757","article-title":"Measuring the impact of malaria infection on indicators of iron and vitamin A status: A systematic literature review and meta-analysis","volume":"129","author":"Sandalinas","year":"2022","journal-title":"Br. J. Nutr."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1001S","DOI":"10.1093\/jn\/nxx036","article-title":"Biomarkers of Nutrition for Development (BOND)\u2014Iron Review","volume":"148","author":"Lynch","year":"2018","journal-title":"J. Nutr."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1093\/nutrit\/nuw021","article-title":"Iron and malaria: A dangerous liaison?","volume":"74","author":"Cot","year":"2016","journal-title":"Nutr. Rev."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1093\/ajcn\/nqac038","article-title":"Malaria reduction drives childhood stunting decline in Uganda: A mixed-methods country case study","volume":"115","author":"Keats","year":"2022","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"359S","DOI":"10.3945\/ajcn.116.141762","article-title":"Adjusting ferritin concentrations for inflammation: Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) project","volume":"106","author":"Namaste","year":"2017","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"372S","DOI":"10.3945\/ajcn.116.142232","article-title":"Adjusting soluble transferrin receptor concentrations for inflammation: Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) project","volume":"106","author":"Rohner","year":"2017","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Larson, L.M., Guo, J., Williams, A.M., Young, M.F., Ismaily, S., Addo, O.Y., Thurnham, D., Tanumihardjo, S.A., Suchdev, P.S., and Northrop-Clewes, C.A. (2018). Approaches to Assess Vitamin A Status in Settings of Inflammation: Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) Project. Nutrients, 10.","DOI":"10.3390\/nu10081100"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"197","DOI":"10.3945\/an.116.014167","article-title":"Metabolic Effects of Inflammation on Vitamin A and Carotenoids in Humans and Animal Models","volume":"8","author":"Rubin","year":"2017","journal-title":"Adv. Nutr. Int. Rev. J."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1093\/ajcn\/nqz303","article-title":"Interpretation of vitamin B-12 and folate concentrations in population-based surveys does not require adjustment for inflammation: Biomarkers reflecting inflammation and nutritional determinants of anemia (BRINDA) project","volume":"111","author":"Young","year":"2020","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_46","unstructured":"Ross, A.C. (2014). Modern Nutrition in Health and Disease, Wolters Kluwer Health\/Lippincott Williams & Wilkins. [11th ed.]."}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/15\/15\/3429\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:24:42Z","timestamp":1760127882000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/15\/15\/3429"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,2]]},"references-count":46,"journal-issue":{"issue":"15","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["nu15153429"],"URL":"https:\/\/doi.org\/10.3390\/nu15153429","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,2]]}}}