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Epidemiology and Population Health

Changes in obesity and iron deficiency between 4 and 9 years of age. Longitudinal study of childhood obesity (ELOIN)

Abstract

Background

Recent studies revealed that children who are overweight have a higher risk of iron deficiency, although the etiology of this relationship remains unclear. The aim of the study was to evaluate the association between changes in obesity status between 4 and 9 years of age and iron deficiency.

Subjects

This population-based cohort study included 1347 children from the ELOIN study, conducted in Madrid, Spain. Follow-up with physical examinations and a computer-assisted telephone interview were carried out at 4, 6 and 9 years of age, and a blood test was performed at 9 years.

Methods

Changes in obesity were estimated based on body mass index and waist circumference, according to the persistence or variation in obesity rates at 4, 6 and 9 years and were classified as follows: (1) Stable without obesity; (2) Remitting obesity at 9 years; (3) Incident obesity or relapse at 9 years; and (4) Stable with obesity. Iron deficiency was defined as transferrin saturation value below 16%. Odds ratios (ORs) for iron deficiency were estimated according to obesity status using logistic regression and adjusted for confounding variables, including C-reactive protein (CRP).

Results

The prevalence of iron deficiency in the stable general obesity (GO) and abdominal obesity (AO) groups was 38.2% and 41.2%, versus 23.6% and 23.4% in the stable without obesity groups, respectively. The ORs for iron deficiency were 1.85 (95% CI: 1.03–3.32) in the stable GO group and 2.34 (95% CI: 1.29–4.24) in the stable AO group. This association disappeared when CRP was included in the analysis.

Conclusions

An extended state of obesity during the first stages of life is associated with iron deficiency, and this association may be mediated by CRP. Prevention and early detection of obesity in children should be a priority to avoid a double burden of malnutrition.

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References

  1. Saloojee H, Pettifor JM. Iron deficiency and impaired child development: The relation may be causal, but it may not be a priority for intervention. BMJ. 2001;323:1377–8. https://doi.org/10.1136/bmj.323.7326.1377.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. WHO. The global prevalence of anaemia in 2011. Geneva: World Health Organization; 2015.

  3. López-Ruzafa E, Vázquez-López MA, Galera-Martínez R, Lendínez-Molinos F, Gómez-Bueno S, Martín-González M. Prevalence and associated factors of iron deficiency in Spanish children aged 1 to 11 years. Eur J Pediatr. 2021. https://doi.org/10.1007/s00431-021-04037-8.

  4. Waldvogel-Abramowski S, Waeber G, Gassner C, Buser A, Frey BM, Favrat B, et al. Physiology of iron metabolism. Transfus Med Hemother. 2014;41:213–21. https://doi.org/10.1159/000362888.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Abbaspour N, Hurrell R, Kelishadi R. Review on iron and its importance for human health. J Res Med Sci. 2014;19:164–74.

    PubMed  PubMed Central  Google Scholar 

  6. Jáuregui-Lobera I. Iron deficiency and cognitive functions. Neuropsychiatr Dis Treat. 2014;10:2087–95. https://doi.org/10.2147/NDT.S72491.

    Article  PubMed  PubMed Central  Google Scholar 

  7. World Health Organization (WHO). Obesity and overweight [Internet]. [Accessed 3 may 2021]. https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight.

  8. Agencia Española de Seguridad Alimentaria y Nutrición. Ministerio de Consumo. Estudio ALADINO 2019: Estudio sobre Alimentación, Actividad Física, Desarrollo Infantil y Obesidad en España 2019. 2020. https://www.aesan.gob.es/AECOSAN/docs/documentos/nutricion/observatorio/Informe_Breve_ALADINO2019_NAOS.pdf.

  9. Wenzel BJ, Stults HB, Mayer J. Hypoferraemia in obese adolescents. Lancet. 1962;2:327–8. https://doi.org/10.1016/s0140-6736(62)90110-1.

    Article  CAS  PubMed  Google Scholar 

  10. Seltzer CC, Mayer J. Serum iron and iron-binding capacity in adolescents: II. Comparison of obese and nonobese subjects. Am J Clin Nutr. 1963;13:354–61. https://doi.org/10.1093/ajcn/13.6.354.

    Article  CAS  PubMed  Google Scholar 

  11. Zhao L, Zhang X, Shen Y, Fang X, Wang Y, Wang F. Obesity and iron deficiency: a quantitative meta-analysis. Obes Rev. 2015;16:1081–93. https://doi.org/10.1111/obr.12323.

    Article  CAS  PubMed  Google Scholar 

  12. Tussing-Humphreys L, Pustacioglu C, Nemeth E, Braunschweig C. Rethinking iron regulation and assessment in iron deficiency, anemia of chronic disease, and obesity: introducing hepcidin. J Acad Nutr Diet. 2012;112:391–400. https://doi.org/10.1016/j.jada.2011.08.038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Haidari F, Abiri B, Haghighizadeh M-H, Kayedani GA, Birgani NK. Association of hematological parameters with obesity- induced inflammation among young females in Ahvaz, South-West of Iran. Int J Prev Med. 2020;11:55. https://doi.org/10.4103/ijpvm.IJPVM_35_18.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Khan A, Khan WM, Ayub M, Humayun M, Haroon M. Ferritin is a marker of inflammation rather than iron deficiency in overweight and obese people. J Obes. 2016;1937320. https://doi.org/10.1155/2016/1937320.

  15. Shattnawi KK, Alomari MA, Al-Sheyab N, Bani Salameh A. The relationship between plasma ferritin levels and body mass index among adolescents. Sci Rep. 2018;8:15307. https://doi.org/10.1038/s41598-018-33534-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Andrews Guzmán M, Arredondo Olguín M. Association between ferritin, high sensitivity c-reactive protein (hsCRP) and relative abundance of Hepcidin mRNA with the risk of type 2 diabetes in obese subjects. Nutrición Hospitalaria. 2014;30:577–84. https://doi.org/10.3305/nh.2014.30.3.7647.

    Article  PubMed  Google Scholar 

  17. del Giudice EM, Santoro N, Amato A, Brienza C, Calabrò P, Wiegerinck ET, et al. Hepcidin in obese children as a potential mediator of the association between obesity and iron deficiency. J Clin Endocrinol Metab. 2009;94:5102–7. https://doi.org/10.1210/jc.2009-1361.

    Article  PubMed  Google Scholar 

  18. Grote Beverborg N, Klip IJT, Meijers WC, Voors AA, Vegter EL, van der Wal HH, et al. Definition of iron deficiency based on the gold standard of bone marrow iron staining in heart failure patients. Circ Heart Fail. 2018;11:004519. https://doi.org/10.1161/CIRCHEARTFAILURE.117.004519.

    Article  Google Scholar 

  19. Dignass A, Farrag K, Stein J. Limitations of serum Ferritin in diagnosing iron deficiency in inflammatory conditions. Int J Chronic Dis. 2018;9394060. https://doi.org/10.1155/2018/9394060.

  20. Miller JL. Iron deficiency anemia: a common and curable disease. Cold Spring Harb Perspect Med. 2013;3:a011866. https://doi.org/10.1101/cshperspect.a011866.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Zafon C, Lecube A, Simó R. Iron in obesity. An ancient micronutrient for a modern disease. Obes Rev. 2010;11:322–8. https://doi.org/10.1111/j.1467-789X.2009.00638.x.

    Article  CAS  PubMed  Google Scholar 

  22. Sproston NR, Ashworth JJ. Role of C-reactive protein at sites of inflammation and infection. Front Immunol. 2018;9:754. https://doi.org/10.3389/fimmu.2018.00754.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Aronson D, Bartha P, Zinder O, Kerner A, Markiewicz W, Avizohar O, et al. Obesity is the major determinant of elevated C-reactive protein in subjects with the metabolic syndrome. Int J Obes. 2004;28:674–9. https://doi.org/10.1038/sj.ijo.0802609.

    Article  CAS  Google Scholar 

  24. Ortiz-Marrón H, Cuadrado-Gamarra JI, Esteban-Vasallo M, Cortés-Rico O, Sánchez-Díaz J, Galán-Labaca I. Estudio Longitudinal de Obesidad Infantil (ELOIN): diseño, participación y características de la muestra. Rev Esp Cardiol. 2016;69:521–3. https://doi.org/10.1016/j.recesp.2016.01.018.

    Article  PubMed  Google Scholar 

  25. de Onis M, Onyango A, Borghi E, Siyam A, Blössner M, Lutter C, et al. Worldwide implementation of the WHO Child Growth Standards. Public Health Nutr. 2012;15:1603–10. https://doi.org/10.1017/S136898001200105.

    Article  PubMed  Google Scholar 

  26. de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85:660–7.

    Article  Google Scholar 

  27. Zimmet P, Alberti KGM, Kaufman F, Tajima N, Silink M, Arslanian S, et al. The metabolic syndrome in children and adolescents - an IDF consensus report. Pediatr Diabetes. 2007;8:299–306.

    Article  Google Scholar 

  28. Koerper MA, Dallman PR. Serum iron concentration and transferrin saturation in the diagnosis of iron deficiency in children: normal developmental changes. J Pediatr. 1977;91:870–4. https://doi.org/10.1016/s0022-3476(77)80879-2.

    Article  CAS  PubMed  Google Scholar 

  29. Manios Y, Moschonis G, Chrousos GP, Lionis C, Mougios V, Kantilafti M, et al. The double burden of obesity and iron deficiency on children and adolescents in Greece: the Healthy Growth Study. J Hum Nutr Diet. 2013;26:470–8. https://doi.org/10.1111/jhn.12025.

    Article  CAS  PubMed  Google Scholar 

  30. UNICEF/UNU/WHO. Iron deficiency anaemia: assessment, prevention and control, a guide for programme managers. Geneva, World Health Organization, 2001. https://apps.who.int/nutrition/publications/micronutrients/anaemia_iron_deficiency/WHO_NHD_01.3/en/index.html.

  31. Torsheim T, Cavallo F, Levin KA, Schnohr C, Mazur J, Niclasen B, et al. Psychometric validation of the revised family affluence scale: a latent variable approach. Child Indic Res. 2016;9:771–84. https://doi.org/10.1007/s12187-015-9339-x.

    Article  PubMed  Google Scholar 

  32. Manchola-González J, Bagur-Calafat CY, Girabent-Farrés M. Reliability Spanish version of questionnaire of physical activity PAQ-C. Rev Int Med Cienc Act Fís Deporte. 2017;17:139–52. https://doi.org/10.15366/rimcafd2017.65.010.

    Article  Google Scholar 

  33. Hutchinson C. A review of iron studies in overweight and obese children and adolescents: a double burden in the young? Eur J Nutr. 2016;55:2179–97. https://doi.org/10.1007/s00394-016-1155-7.

    Article  PubMed  Google Scholar 

  34. Moschonis G, Chrousos GP, Lionis C, Mougios V, Manios Y, Healthy Growth Study group. Association of total body and visceral fat mass with iron deficiency in preadolescents: the Healthy Growth Study. Br J Nutr. 2012;108:710–9. https://doi.org/10.1017/S0007114511005952.

    Article  CAS  PubMed  Google Scholar 

  35. Błażewicz A, Klatka M, Astel A, Partyka M, Kocjan R. Differences in trace metal concentrations (Co, Cu, Fe, Mn, Zn, Cd, And Ni) in whole blood, plasma, and urine of obese and nonobese children. Biol Trace Elem Res. 2013;155:190–200. https://doi.org/10.1007/s12011-013-9783-8.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Nead KG, Halterman JS, Kaczorowski JM, Auinger P, Weitzman M. Overweight children and adolescents: a risk group for iron deficiency. Pediatrics. 2004;114:104–8. https://doi.org/10.1542/peds.114.1.104.

    Article  PubMed  Google Scholar 

  37. Pinhas-Hamiel O, Newfield RS, Koren I, Agmon A, Lilos P, Phillip M. Greater prevalence of iron deficiency in overweight and obese children and adolescents. Int J Obes Relat Metab Disord. 2003;27:416–8. https://doi.org/10.1038/sj.ijo.0802224.

    Article  CAS  PubMed  Google Scholar 

  38. Aeberli I, Hurrell RF, Zimmermann MB. Overweight children have higher circulating hepcidin concentrations and lower iron status but have dietary iron intakes and bioavailability comparable with normal weight children. Int J Obes. 2009;33:1111–7. https://doi.org/10.1038/ijo.2009.146.

    Article  CAS  Google Scholar 

  39. Azab SFA, Saleh SH, Elsaeed WF, Elshafie MA, Sherief LM, Esh AMH. Serum trace elements in obese Egyptian children: a case-control study. Ital J Pediatr. 2014;40:20 https://doi.org/10.1186/1824-7288-40-20.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Sharma AP, McKenna AM, Lepage N, Nieuwenhuys E, Filler G. Relationships among serum iron, inflammation, and body mass index in children. Adv Pediatr. 2009;56:135–44. https://doi.org/10.1016/j.yapd.2009.08.014.

    Article  PubMed  Google Scholar 

  41. Evensen E, Wilsgaard T, Furberg AS, Skeie G. Tracking of overweight and obesity from early childhood to adolescence in a population-based cohort - the Tromsø Study, Fit Futures. BMC Pediatr. 2016;16:64. https://doi.org/10.1186/s12887-016-0599-5.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wheaton N, Millar L, Allender S, Nichols M. The stability of weight status through the early to middle childhood years in Australia: a longitudinal study. BMJ Open. 2015;5:e006963–e006963. https://doi.org/10.1136/bmjopen-2014-006963.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Teng IC, Tseng SH, Aulia B, Shih CK, Bai CH, Chang JS. Can diet-induced weight loss improve iron homoeostasis in patients with obesity: a systematic review and meta-analysis. Obes Rev. 2020;21:e13080. https://doi.org/10.1111/obr.13080.

    Article  PubMed  Google Scholar 

  44. Dobashi K. Evaluation of obesity in school-age children. J Atheroscler Thromb. 2016;23:32–8. https://doi.org/10.5551/jat.29397.

    Article  PubMed  Google Scholar 

  45. Esteban-Vasallo MD, Galán I, Ortiz-Pinto MA, Astray San Martín A, Cabrero López EM, Morales San José MT, et al. Accuracy of anthropometric measurements and weight status perceptions reported by parents of 4-year-old children. Public Health Nutr. 2019;23:589–98. https://doi.org/10.1017/S1368980019003008.

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank all of the health care professionals for their assistance with the study and all of the families who were willing to collaborate and participate in the cohort. We thank the Fundación para la Investigación e Innovación Biosanitaria de Atención Primaria (FIIBAP) for funding.

Funding

This work was supported by the General Directorate of Public Health of Ministry of Health (Community of Madrid).

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GC, IG and HOM conceptualized and designed the study, developed the initial manuscript with tables and figures, and checked and revised the final manuscript. GC, IG, HOM and MAOP designed the instruments for data collection, data collection, and initial analysis. AGG, PCT, EDN and MOG participated in the data collection and critically reviewed the manuscript by making important contributions to its content. All authors gave their approval to the final manuscript and agreed and assume responsibility for all aspects of the work.

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Correspondence to Honorato Ortiz-Marrón.

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Cabañas Pujadas, G., Ortiz-Marrón, H., Ortiz-Pinto, M.A. et al. Changes in obesity and iron deficiency between 4 and 9 years of age. Longitudinal study of childhood obesity (ELOIN). Int J Obes 46, 1992–1999 (2022). https://doi.org/10.1038/s41366-022-01196-y

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