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Prevalence of iron deficiency and related factors in Spanish adolescents

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Abstract

Iron deficiency anaemia continues to be the world’s most important cause of years lived with disability in children and adolescents. Assessment of iron deficiency traditionally depended on laboratory parameters that may be modified by inflammation states, including obesity, which is nowadays a current condition in adolescent population of high-income countries. The present study ascertains the prevalence of iron deficiency and its related factors in adolescents, using the serum transferrin receptor and the reticulocyte haemoglobin content, in order to avoid this confusing effect of classical parameters. A cross-sectional study was conducted on a population-based representative sample for teenagers in Almería (Spain), of 405 subjects aged 12 to 16 years. Iron deficiency was present in 13.3% of adolescents, but iron deficiency anaemia only in 1.2%. Multivariate logistic regression analyses showed that being part of an immigrant family, a low iron bioavailability diet, meat consumption below four times a week and fish consumption below twice a week, were independent risk factors for iron deficiency.

Conclusion: This study provides an estimate iron deficiency prevalence of 13.3% in Spanish healthy adolescents, avoiding potential confounding factors through the use of new iron status parameters, based on a wide representative sample of adolescents from the city of Almería.

What is Known:

For children and adolescents, iron deficiency anaemia continues to be the world’s most important cause of years lived with disability.

Assessment of iron deficiency has traditionally depended on laboratory parameters that may be modified by inflammatory states, including obesity.

What is New:

• Iron deficiency prevalence and their related factors were analysed in Spanish adolescents, avoiding potential confounding factors through the use of sTfR and CHr.

• Being part of an immigrant family and consuming a low iron bioavailability diet are independent risk factors for iron deficiency.

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Abbreviations

BMI:

Body mass index

CHr:

Reticulocyte haemoglobin content

CI:

Confidence intervals

CRP:

C-reactive protein

EP:

Erythrocyte protoporphyrin

ID:

Iron deficiency

IDA:

Iron deficiency anaemia

IDE:

Iron-deficient erythropoiesis

ISD:

Iron store depletion

MCV:

Mean corpuscular volume

OR:

Odds ratio

SD:

Standard deviation

sEPO:

Serum erythropoietin

sTfR:

Serum transferrin receptor

TS:

Transferrin saturation

References

  1. Global Burden of Disease Child and Adolescent Health Collaboration, Kassebaum N, Kyu HH, Zoeckler L, Olsen HE, Thomas K, Pinho C et al (2017) Child and adolescent health from 1990 to 2015: findings from the global burden of diseases, injuries, and risk factors 2015 study. JAMA Pediatr 171(6):573–592

    Google Scholar 

  2. World Health Organization (2019) Worldwide prevalence on anaemia 1993-2005. Available at: https://www.who.int/vmnis/anaemia/prevalence/en/. Accessed on December 15th 2019

  3. More S, Shivkumar VB, Gangane N, Shende S (2013) Effects of iron deficiency on cognitive function in school going adolescent females in rural area of Central India. Anemia 2013:819136

    PubMed  PubMed Central  Google Scholar 

  4. Sharma R, Stanek JR, Koch TL, Grooms L, O'Brien SH (2016) Intravenous iron therapy in non-anemic iron-deficient menstruating adolescent females with fatigue. Am J Hematol 91(10):973–977

    CAS  PubMed  Google Scholar 

  5. Halterman JS, Kaczorowski JM, Aligne CA, Auinger P, Szilagyi PG (2001) Iron deficiency and cognitive achievement among school-aged children and adolescents in the United States. Pediatrics 107(6):1381–1386

    CAS  PubMed  Google Scholar 

  6. Jáuregui-Lobera I (2014) Iron deficiency and cognitive functions. Neuropsychiatr Dis Treat 10:2087–2095

    PubMed  PubMed Central  Google Scholar 

  7. Mattiello V, Schmugge M, Hengartner H, von der Weid N, Renella R, SPOG Pediatric Hematology Working Group (2020) Diagnosis and management of iron deficiency in children with or without anemia: consensus recommendations of the SPOG Pediatric Hematology Working Group. Eur J Pediatr 179(4):527–545

    PubMed  Google Scholar 

  8. Mesías M, Seiquer I, Navarro MP (2013) Iron nutrition in adolescence. Crit Rev Food Sci Nutr 53(11):1226–1237

    PubMed  Google Scholar 

  9. Castro De Andrade Cairo R, Rodrigues Silva L, Carneiro Bustani N, Ferreira Marques CD (2014) Iron deficiency anemia in adolescents; a literature review. Nutr Hosp 29(6):1240–1249

    Google Scholar 

  10. Hoppe M, Sjöberg A, Hallberg L, Hulthén L (2008) Iron status in Swedish teenage girls: impact of low dietary iron bioavailability. Nutrition 24(7–8):638–645

    CAS  PubMed  Google Scholar 

  11. Vandevijvere S, Michels N, Verstraete S, Ferrari M, Leclercq C, Cuenca-García M, Grammatikaki E, Manios Y, Gottrand F, Valtueña J, Kersting M, Gonzalez-Gross M, Moreno L, Mouratidou T, Stevens K, Meirhaeghe A, Dallongeville J, Sjöström M, Hallstrom L, Kafatos A, Widhalm K, Molnar D, De Henauw S, Huybrechts I, HELENA Study Group (2013) Intake and dietary sources of haem and non-haem iron among European adolescents and their association with iron status and different lifestyle and socio-economic factors. Eur J Clin Nutr 67:765–772

    CAS  PubMed  Google Scholar 

  12. Samuelson G (2000) Dietary habits and nutritional status in adolescents over Europe. An overview of current studies in the Nordic countries. Eur J Clin Nutr 54(Suppl 1):S21–S28

    PubMed  Google Scholar 

  13. Pynaert I, Matthys C, Bellemans M, De Maeyer M, De Henauw S, De Backer G (2005) Iron intake and dietary sources of iron in Flemish adolescents. Eur J Clin Nutr 59(7):826–834

    CAS  PubMed  Google Scholar 

  14. Fismen AS, Smith OR, Torsheim T, Rasmussen M, Pedersen Pagh T, Augustine L, Ojala K, Samdal O (2016) Trends in food habits and their relation to socioeconomic status among Nordic adolescents 2001/2002-2009/2010. PLoS One 11(2):e0148541

    PubMed  PubMed Central  Google Scholar 

  15. Ferrari M, Mistura L, Patterson E, Sjöström M, Díaz LE, Stehle P, Gonzalez-Gross M, Kersting M, Widhalm K, Molnár D, Gottrand F, De Henauw S, Manios Y, Kafatos A, Moreno LA, Leclercq C, HELENA Study Group (2011) Evaluation of iron status in European adolescents through biochemical iron indicators: the HELENA Study. Eur J Clin Nutr 65(3):340–349

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Centers for Disease Control and Prevention (CDC) (2002) Iron deficiency--United States, 1999-2000. MMWR Morb Mortal Wkly Rep 51(40):897–899

    Google Scholar 

  17. Gupta PM, Hamner HC, Suchdev PS, Flores-Ayala R, Mei Z (2017) Iron status of toddlers, nonpregnant females, and pregnant females in the United States. Am J Clin Nutr 106(Suppl 6):1640S–1646S

    PubMed  PubMed Central  Google Scholar 

  18. Hallberg L, Hultén L, Lindstedt G, Lundberg PA, Mark A, Purens J, Svanberg B, Swolin B (1993) Prevalence of iron deficiency in Swedish adolescents. Pediatr Res 34(5):680–687

    CAS  PubMed  Google Scholar 

  19. Eskeland B, Hunskaar S (1999) Anaemia and iron deficiency screening in adolescence: a pilot study of iron stores and haemoglobin response to iron treatment in a population of 14-15-year-olds in Norway. Acta Paediatr 88(8):815–821

    CAS  PubMed  Google Scholar 

  20. Milman N, Taylor CL, Merkel J, Brannon PM (2017) Iron status in pregnant women and women of reproductive age in Europe. Am J Clin Nutr 106(Suppl 6):1655S–1662S

    PubMed  PubMed Central  Google Scholar 

  21. Durá Travé T, Aguirre Abad P, Mauleón Rosquil C, Oteiza Flores MS, Díaz Velaz L (2002) Lack of iron in adolescents aged 10 to 14. Aten Primaria 29(2):72–77

    PubMed  Google Scholar 

  22. Hutchinson C (2016) A review on iron studies in overweight and obese children and adolescents: a double burden in the young? Eur J Nutr 55(7):2179–2197

    PubMed  Google Scholar 

  23. Nead KG, Halterman JS, Kaczorowski JM, Auinger P, Weitzman M (2004) Overweight children and adolescents: a risk group for iron deficiency. Pediatrics 114(1):104–108

    Google Scholar 

  24. Marković M, Majkić-Singh N, Ignjatović S, Singh S (2007) Reticulocyte haemoglobin content vs. soluble transferrin receptor and ferritin index in iron deficiency anaemia accompanied with inflammation. Int J Lab Hematol 29(5):341–346

    PubMed  Google Scholar 

  25. Vázquez-López MA, Ibáñez-Alcalde M, Lendínez-Molinos F, Ruíz-Sánchez AM, Galera-Martínez R, García-García E, Parrón-Carreño T, Bonillo-Perales A (2015) Reference values of serum transferrin receptor and sTfR/log ferritin index in healthy adolescents. J Pediatr Hematol Oncol 37(4):274–280

    PubMed  Google Scholar 

  26. Ibáñez-Alcalde MM, Vázquez-López MÁ, Ruíz-Sánchez AM, Lendínez-Molinos FJ, Galera-Martínez R, Bonillo-Perales A, Parrón-Carreño T (2018) Reference values of reticulocyte hemoglobin content in healthy adolescents. J Pediatr Hematol Oncol 40(4):298–303

    PubMed  Google Scholar 

  27. Vázquez-López MA, López-Ruzafa E, Ibáñez-Alcalde MM, Martín-González M, Bonillo-Perales A, Lendínez-Molinos F (2019) The usefulness of reticulocyte hemoglobin content, serum transferrin receptor and the sTfR-ferritin index to discriminate iron deficiency in healthy children aged 1-16 years. Eur J Pediatr 178(1):41–49

    PubMed  Google Scholar 

  28. Zhao L, Zhang X, Shen Y, Fang X, Wang Y, Wang F (2015) Obesity and iron deficiency: a quantitative meta-analysis. Obes Rev 16(12):1081–1093

    CAS  PubMed  Google Scholar 

  29. Ferrari M, Cuenca-García M, Valtueña J, Moreno LA, Censi L, González-Gross M, Androutsos O, Gilbert CC, Huybrechts I, Dallongeville J, Sjöström M, Molnar D, De Henauw S, Gómez-Martínez S, de Moraes AC, Kafatos A, Widhalm K, Leclercq C, HELENA Study Group (2015) Inflammation profile in overweight/obese adolescents in Europe: an analysis in relation to iron status. Eur J Clin Nutr 69(2):247–255

    CAS  PubMed  Google Scholar 

  30. Zhu Y, He B, Xiao Y, Chen Y (2019) Iron metabolism and its association with dyslipidemia risk in children and adolescents: a cross-sectional study. Lipids Health Dis 18(1):50

    PubMed  PubMed Central  Google Scholar 

  31. Serra Majem L, Ribas Barba L, Aranceta Bartrina J, Pérez Rodrigo C, Saavedra Santana P, Peña Quintana L (2003) Childhood and adolescent obesity in Spain. Results of the ENKID study (1998-2000). Med Clin (Barc) 121:725–732

    Google Scholar 

  32. Pepys MB, Hirschfield GM (2003) C-reactive protein: a critical update. J Clin Invest 111(12):1805–1812

    CAS  PubMed  PubMed Central  Google Scholar 

  33. García-García E, Vázquez-López MÁ, García-Fuentes E, Rodríguez-Sánchez FI, Muñoz FJ, Bonillo-Perales A, Soriguer F (2012) Iodine intake and prevalence of thyroid autoimmunity and autoimmune thyroiditis in children and adolescents aged between 1 and 16 years. Eur J Endocrinol 167:387–392

    PubMed  Google Scholar 

  34. Tanner JM (1962) Growth at adolescence, 2nd edn. Blackwell Scientific Publication, Oxford, p 212

    Google Scholar 

  35. Carrascosa Lezcano A, Fernández García JM, Fernández Ramos C, Ferrández Longás A, López-Siguero JP, Sánchez González E, Sobradillo Ruiz B, Yeste Fernández D, Grupo Colaborador Español (2008) Spanish cross-sectional growth study 2008. Part II. Height, weight and body mass index values from birth to adulthood. An Pediatr (Barc) 68:552–569

    CAS  Google Scholar 

  36. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320:1240–1243

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Hernán García M, Cabrera León A, Alaminos Romero F (2007) La salud en la población infantil y adolescente en Andalucía. Encuesta andaluza de Salud 2003. Marín Vega J (ed) Sevilla: Consejería de Salud; Consejería para la Igualdad y Bienestar Social

  38. Harrison E, Rose D (2006) The European socio-economic classification (ESeC) user guide. Institute for Social and Economic Research, University of Essex, Colcheser

    Google Scholar 

  39. Grupo Colaborativo de la Sociedad Española de Nutrición Comunitaria (SENC), Aranceta Bartrina J, Arija Val V, Maíz Aldalur E, Martínez de la Victoria Muñoz E, Ortega Anta RM, Pérez-Rodrigo C, Quiles Izquierdo J, Rodríguez Martín A, Román Viñas B, Salvador Castell G, Tur Marí JA, Varela Moreiras G, Serra Majem L (2016) Dietary guidelines for the Spanish population (SENC, December 2016); the new graphic icon of healthy nutrition. Nutr Hosp 33(Suppl 8):1–48

    Google Scholar 

  40. Harvey LJ, Berti C, Casgrain A, Cetin I, Collings R, Gurinovic M, Hermoso M, Hooper L, Hurst R, Koletzko B, Ngo J, Viñas BR, Vollhardt C, Vucic V, Fairweather-Tait SJ (2013) EURRECA-estimating iron requirements for deriving dietary reference values. Crit Rev Food Sci Nutr 53(10):1064–1076

    CAS  PubMed  Google Scholar 

  41. WHO (2018) Preventing and controlling anaemia through primary health care: a guide for health administrators and programme managers. WHO 1989. Available at: http://www.who.int/nutrition/publications/micronutrients/anaemia_iron_deficiency/9241542497.pdf. Accessed on August 27th, 2018

  42. Looker AC, Dallman PR, Carroll MD, Gunter EW, Johnson CL (1997) Prevalence of iron deficiency in the United States. JAMA 277(12):973–976

    CAS  PubMed  Google Scholar 

  43. Doudin A, Becker A, Rothenberger A, Meyer T (2018) Relationship between serum 25-hydroxyvitamin D and red blood cell indices in German adolescents. Eur J Pediatr 177(4):583–591

    CAS  PubMed  Google Scholar 

  44. Galicia L, Grajeda R, de Romaña DL (2016) Nutrition situation in Latin America and the Caribbean: current scenario, past trends, and data gaps. Rev Panam Salud Publica 40(2):104–113

    PubMed  Google Scholar 

  45. Hwalla N, Al Dhaheri AS, Radwan H, Alfawaz HA, Fouda MA, Al-Daghri NM, Zaghloul S, Blumberg JB (2017) The prevalence of micronutrient deficiencies and inadequacies in the Middle East and approaches to interventions. Nutrients 9(3):229

    PubMed Central  Google Scholar 

  46. Mwangi MN, Phiri KS, Abkari A, Gbané M, Bourdet-Sicard R, Braesco VA, Zimmermann MB, Prentice AM (2017) Iron for Africa-report of an expert workshop. Nutrients 9(6):576

    PubMed Central  Google Scholar 

  47. Beard JL (2000) Iron requirements in adolescent females. J Nutr 130(2S Suppl):440S–442S

    CAS  PubMed  Google Scholar 

  48. Caballo Roig N, García P, Valdemoro M, del Castillo ML, Santos Tapia M, González Vargaz A, Arias Alvarez MA, Serna Saugán C, Merino JM, García Teresa MA (1993) The prevalence of anemia in the children and adolescents of Madrid. An Esp Pediatr 39(3):219–222

    CAS  PubMed  Google Scholar 

  49. Eftekhari M, Mozaffari-Khosravi H, Shidfar F (2009) The relationship between BMI and iron status in iron-deficient adolescent Iranian girls. Public Health Nutr 12(12):2377–2381

    PubMed  Google Scholar 

  50. Ganz T (2013) Systemic iron homeostasis. Physiol Rev 93:1721–1741

    CAS  PubMed  Google Scholar 

  51. Achouri I, Aboussaleh Y, Sbaibi R, Ahami A, El Hioui M (2015) Prevalence of iron deficiency anaemia among school children in Kenitra, northwest of Morocco. Pak J Biol Sci 18(4):191–195

    CAS  PubMed  Google Scholar 

  52. El Hioui M, Ahami AO, Aboussaleh Y, Rusinek S, Dik K, Soualem A, Azzaoui FZ, Loutfi H, Elqaj M (2008) Risk factors of anaemia among rural school children in Kenitra, Morocco. East Afr J Public Health 5(2):62–66

    PubMed  Google Scholar 

  53. Beck KL, Conlon CA, Kruger R, Coad J (2014) Dietary determinants of and possible solutions to iron deficiency for young women living in industrialized countries: a review. Nutrients 6(9):3747–3776

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Gulec S, Anderson GJ, Collins JF (2014) Mechanistic and regulatory aspects of intestinal iron absorption. Am J Physiol Gastrointest Liver Physiol 307(4):G397–G409

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Sharp PA (2010) Intestinal iron absorption: regulation by dietary & systemic factors. Int J Vitam Nutr Res 80(4–5):231–242

    CAS  PubMed  Google Scholar 

  56. Samaniego-Vaesken ML, Partearroyo T, Olza J, Aranceta-Bartrina J, Gil Á, González-Gross M, Ortega RM, Serra-Majem L, Varela-Moreiras G (2017) Iron intake and dietary sources in the Spanish population: findings from the ANIBES study. Nutrients 9(3):203

    PubMed Central  Google Scholar 

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Authors

Contributions

MMIA contributed to analysis and interpretation of the data and writing of the manuscript; MAVL contributed to conception and design, analysis and interpretation of the data and writing of the manuscript; ELR contributed to the acquisition of data and drafting of the manuscript; FJLM, ABP and TPC critically revised the manuscript and contributed with their final suggestions. All the authors approved the final manuscript for publication.

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Correspondence to María Mercedes Ibáñez-Alcalde.

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The authors declare that they have no conflict of interest.

Ethical approval

The Ethics and Research Committee of Torrecárdenas Hospital (Almería) approved the study. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or National Research Committee and with the 1964 Helsinki Declaration, and its later amendments or comparable ethical standards.

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Informed written consent was obtained from parents or legal guardians as well as from the participants themselves if they were > 12 years.

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Communicated by Gregorio Paolo Milani

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Ibáñez-Alcalde, M.M., Vázquez-López, M.Á., López-Ruzafa, E. et al. Prevalence of iron deficiency and related factors in Spanish adolescents. Eur J Pediatr 179, 1587–1595 (2020). https://doi.org/10.1007/s00431-020-03651-2

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