Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Adiposity in women and children from transition countries predicts decreased iron absorption, iron deficiency and a reduced response to iron fortification

International Journal of Obesity volume 32, pages 1098–1104 (2008)Cite this article

Abstract

Background:

Overweight is increasing in transition countries, while iron deficiency remains common. In industrialized countries, greater adiposity increases risk of iron deficiency. Higher hepcidin levels in obesity may reduce dietary iron absorption. Therefore, we investigated the association between body mass index (BMI) and iron absorption, iron status and the response to iron fortification in populations from three transition countries (Thailand, Morocco and India).

Methods:

In Thai women (n=92), we examined the relationship between BMI and iron absorption from a reference meal containing ∼4 mg of isotopically labeled fortification iron. We analyzed data from baseline (n=1688) and intervention (n=727) studies in children in Morocco and India to look for associations between BMI Z-scores and baseline hemoglobin, serum ferritin and transferrin receptor, whole blood zinc protoporphyrin and body iron stores, and changes in these measures after provision of iron.

Results:

In the Thai women, 20% were iron deficient and 22% were overweight. Independent of iron status, a higher BMI Z-score was associated with decreased iron absorption (P=0.030). In the Indian and Moroccan children, 42% were iron deficient and 6.3% were overweight. A higher BMI Z-score predicted poorer iron status at baseline (P<0.001) and less improvement in iron status during the interventions (P<0.001).

Conclusions:

Adiposity in young women predicts lower iron absorption, and pediatric adiposity predicts iron deficiency and a reduced response to iron fortification. These data suggest the current surge in overweight in transition countries may impair efforts to control iron deficiency in these target groups. Interactions of the ‘double burden’ of malnutrition during the nutrition transition may have adverse consequences.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Popkin B . The nutrition transition: an overview of world patterns of change. Nutr Rev 2004; 62: S140–S143.

    Article  Google Scholar 

  2. Doak CM, Adair LS, Bentley M, Monteiro C, Popkin BM . The dual burden household and the nutrition transition paradox. Int J Obesity 2005; 29: 129–136.

    Article  CAS  Google Scholar 

  3. Kosulwat V . The nutrition and health transition in Thailand. Public Health Nutr 2002; 5: 183–189.

    Article  Google Scholar 

  4. Benjelloun S . Nutrition transition in Morocco. Public Health Nutr 2002; 5: 135–140.

    Article  Google Scholar 

  5. Shetty PS . Nutrition transition in India. Public Health Nutr 2002; 5: 175–182.

    Article  Google Scholar 

  6. Kantachuvessiri A . Obesity in Thailand. J Med Assoc Thai 2005; 88: 554–562.

    PubMed  Google Scholar 

  7. Zimmermann MB, Winichagoon P, Gowachirapant S, Hess SY, Harrington M, Chavasit V et al. Comparison of the efficacy of wheat-based snacks fortified with ferrous sulfate, electrolytic iron, or hydrogen-reduced elemental iron: randomized, double-blind, controlled trial in Thai women. Am J Clin Nutr 2005; 82: 1276–1282.

    Article  CAS  Google Scholar 

  8. Aboussaleh Y, Ahami AO, Alaoui L, Delisle H . Prevalence of anemia among schoolchildren in the province of Kenitra in Morocco (in French). Sante 2004; 14: 37–42.

    PubMed  Google Scholar 

  9. Moroccan Ministry of Health. Demographic and Health Survey (DHS). Enquête nationale sur la planification familiale, la fécondité et la santé de la population au Maroc. Rapport national (ENPS II). 1992.

  10. Rguibi M, Belahsen R . Prevalence of obesity in Morocco. Obes Rev 2007; 8: 11–13.

    Article  CAS  Google Scholar 

  11. Srihari G, Eilander A, Muthayya S, Kurpad AV, Seshadri S . Nutritional status of affluent Indian school children: what and how much do we know? Indian Pediatr 2007; 44: 204–213.

    CAS  PubMed  Google Scholar 

  12. Popkin BM . An overview on the nutrition transition and its health implications: the Bellagio meeting. Public Health Nutr 2002; 5: 93–103.

    PubMed  Google Scholar 

  13. Wenzel BJ, Stults HB, Mayer J . Hypoferraemia in obese adolescents. Lancet 1962; 2: 327–328.

    Article  CAS  Google Scholar 

  14. Seltzer CC, Mayer J . Serum iron and iron-binding capacity in adolescents. Comparison of obese and nonobese subjects. Am J Clin Nutr 1963; 13: 354–361.

    Article  CAS  Google Scholar 

  15. Scheer JC, Guthrie HA . Hemoglobin criteria with respect to obesity. Am J Clin Nutr 1981; 34: 2748–2751.

    Article  CAS  Google Scholar 

  16. 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: 416–418.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  18. Brotanek JM, Gosz J, Weitzman M, Flores G . Iron deficiency in early childhood in the United States: risk factors and racial/ethnic disparities. Pediatrics 2007; 120: 568–575.

    Article  Google Scholar 

  19. Micozzi MS, Albanes D, Stevens RG . Relation of body size and composition to clinical biochemical and hematologic indices in US men and women. Am J Clin Nutr 1989; 50: 1276–1281.

    Article  CAS  Google Scholar 

  20. Whitfield JB, Treloar S, Zhu G, Powell LW, Martin NG . Relative importance of female-specific and non-female-specific effects on variation in iron stores between women. Br J Haematol 2003; 120: 860–866.

    Article  Google Scholar 

  21. Rossi E, Bulsara MK, Olynyk JK, Cullen DJ, Summerville L, Powell LW . Effect of hemochromatosis genotype and lifestyle factors on iron and red cell indices in a community population. Clin Chem 2001; 47: 202–208.

    CAS  PubMed  Google Scholar 

  22. Lecube A, Carrera A, Losada E, Hernandez C, Simo R, Mesa J . Iron deficiency in obese postmenopausal women. Obesity (Silver Spring) 2006; 14: 1724–1730.

    Article  CAS  Google Scholar 

  23. Yanoff LB, Menzie CM, Denkinger B, Sebring NG, McHugh T, Remaley AT et al. Inflammation and iron deficiency in the hypoferremia of obesity. Int J Obes (Lond) 2007; 31: 1412–1419.

    Article  CAS  Google Scholar 

  24. Chung B, Matak P, McKie AT, Sharp P . Leptin increases the expression of the iron regulatory hormone hepcidin in HuH7 human hepatoma cells. J Nutr 2007; 137: 2366–2370.

    Article  CAS  Google Scholar 

  25. Bekri S, Gual P, Anty R, Luciani N, Dahman M, Ramesh B et al. Increased adipose tissue expression of hepcidin in severe obesity is independent from diabetes and NASH. Gastroenterology 2006; 131: 788–796.

    Article  CAS  Google Scholar 

  26. Laftah AH, Ramesh B, Simpson RJ, Solanky N, Bahram S, Schumann K et al. Effect of hepcidin on intestinal iron absorption in mice. Blood 2004; 103: 3940–3944.

    Article  CAS  Google Scholar 

  27. Sachdev H, Gera T, Nestel P . Effect of iron supplementation on mental and motor development in children: systematic review of randomised controlled trials. Public Health Nutr 2005; 8: 117–132.

    Article  Google Scholar 

  28. Zimmermann MB, Hurrell RF . Nutritional iron deficiency. Lancet 2007; 370: 511–520.

    Article  CAS  Google Scholar 

  29. Walczyk T, Tuntipopipat S, Zeder C, Sirichakwal P, Wasantwisut E, Hurrell RF . Iron absorption by human subjects from different iron fortification compounds added to Thai fish sauce. Eur J Clin Nutr 2005; 59: 668–674.

    Article  CAS  Google Scholar 

  30. Tuntipopipat S, Judprasong K, Zeder C, Wasantwisut E, Winichagoon P, Charoenkiatkul S et al. Chili, but not turmeric, inhibits iron absorption in young women from an iron-fortified composite meal. J Nutr 2006; 136: 2970–2974.

    Article  CAS  Google Scholar 

  31. World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 1995; 854: 1–452.

    Google Scholar 

  32. WHO/UNICEF/UNU. Iron Deficiency Anemia Assessment, Prevention, and Control. World Health Organization: Geneva, 2001.

  33. Walczyk T, Davidsson L, Zavaleta N, Hurrell RF . Stable isotope labels as a tool to determine iron absorption by Peruvian school children from a breakfast meal. Fresenius J Anal Chem 1997; 359: 445–449.

    Article  CAS  Google Scholar 

  34. Zimmermann MB, Zeder C, Chaouki N, Saad A, Torresani T, Hurrell RF . Dual fortification of salt with iodine and microencapsulated iron: a randomized, double-blind, controlled trial in Moroccan schoolchildren. Am J Clin Nutr 2003; 77: 425–432.

    Article  CAS  Google Scholar 

  35. Zimmermann MB, Wegmueller R, Zeder C, Chaouki N, Rohner F, Saïssi M et al. Dual fortification of salt with iodine and micronized ferric pyrophosphate: a randomized, double-blind, controlled trial. Am J Clin Nutr 2004; 80: 952–959.

    Article  CAS  Google Scholar 

  36. Moretti D, Zimmermann MB, Muthayya S, Thankachan P, Lee TC, Kurpad AV et al. Extruded rice fortified with micronized ground ferric pyrophosphate reduces iron deficiency in Indian schoolchildren: a double-blind randomized controlled trial. Am J Clin Nutr 2006; 84: 822–829.

    Article  CAS  Google Scholar 

  37. Zimmermann MB, Molinari L, Staubli F, Hess S, Chaouki N, Adou P et al. Serum transferrin receptor and zinc protoporphyrin as indicators of iron status in African children. Am J Clin Nutr 2005; 81: 615–623.

    Article  CAS  Google Scholar 

  38. Skikne BS, Flowers CH, Cook JD . Serum transferrin receptor: a quantitative measure of tissue iron deficiency. Blood 1990; 75: 1870–1876.

    CAS  PubMed  Google Scholar 

  39. Cook JD, Flowers CH, Skikne BS . The quantitative assessment of body iron. Blood 2003; 101: 3359–3363.

    Article  CAS  Google Scholar 

  40. Cook JD, Dassenko SA, Lynch SR . Assessment of the role of nonheme-iron availability in iron balance. Am J Clin Nutr 1991; 54: 717–722.

    Article  CAS  Google Scholar 

  41. Thaikruea L, Seetamanotch W, Seetamanotch S . Appropriate cut-off level of BMI for screening in Thai adults. J Med Assoc Thai 2006; 89: 2123–2128.

    PubMed  Google Scholar 

  42. 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: 660–667.

    Article  Google Scholar 

  43. Aeberli I, Kaspar M, Zimmermann MB . Dietary intake and physical activity of normal weight and overweight 6–14 year old Swiss children. Swiss Med Wkly 2007; 137: 424–430.

    CAS  Google Scholar 

  44. Anonymous. Iron. In: Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc. National Academy Press: Washington, DC, 2001, pp 290–393.

  45. Kaplowitz PB, Slora EJ, Wasserman RC, Pedlow SE, Herman-Giddens ME . Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics 2001; 108: 347–353.

    Article  CAS  Google Scholar 

  46. Nemeth E, Valore EV, Territo M, Schiller G, Lichtenstein A, Ganz T . Hepcidin, a putative mediator of anemia of inflammation, is a type II acute-phase protein. Blood 2003; 101: 2461–2463.

    Article  CAS  Google Scholar 

  47. Knutson MD, Oukka M, Koss LM, Aydemir F, Wessling-Resnick M . Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and downregulated by hepcidin. Proc Natl Acad Sci USA 2005; 102: 1324–1328.

    Article  CAS  Google Scholar 

  48. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996; 334: 292–295.

    Article  CAS  Google Scholar 

  49. Smith KD . Iron metabolism at the host pathogen interface: lipocalin 2 and the pathogen-associated iroA gene cluster. Int J Biochem Cell Biol 2007; 39: 1776–1780.

    Article  CAS  Google Scholar 

  50. Wang Y, Lam KS, Kraegen EW, Sweeney G, Zhang J, Tso AW et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem 2007; 53: 34–41.

    Article  CAS  Google Scholar 

  51. Kennedy ML, Failla ML, Smith JC . Influence of genetic obesity on tissue concentrations of zinc, copper, manganese and iron in mice. J Nutr 1986; 116: 1432–1441.

    Article  CAS  Google Scholar 

  52. Failla ML, Kennedy ML, Chen ML . Iron metabolism in genetically obese (ob/ob) mice. J Nutr 1988; 118: 46–51.

    Article  CAS  Google Scholar 

  53. Gillum RF . Association of serum ferritin and indices of body fat distribution and obesity in Mexican American men—the Third National Health and Nutrition Examination Survey. Int J Obes Relat Metab Disord 2001; 25: 639–645.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the participating women and children, as well as the local health care staff in Thailand, Morocco and India for their assistance on the project. We thank M Andersson (Zürich, Switzerland), D Moretti (Vlaardingen, The Netherlands), T Walcyzk (Singapore), P Thankachan and A Kurpad (Bangalore, India), S Tuntipopipat (Bangkok, Thailand), and A Saad (Rabat, Morocco). MZ, CZ, SM, PW, NC did the field work, MZ wrote the first draft of the manuscript, all authors contributed to the writing and editing of the manuscript. None of the authors has a conflict of interest relating to this paper. This study was supported by the Thrasher Foundation (Salt Lake City, USA) the Micronutrient Initiative (Ottawa, Canada); the Nestlé Foundation (Lausanne, Switzerland); the Foundation for Micronutrients in Medicine (Rapperswil, Switzerland) and the Swiss Federal Institute of Technology (Zürich, Switzerland).

Author information

Authors and Affiliations

  1. Human Nutrition Laboratory, Swiss Federal Institute of Technology, Zürich, Switzerland

    M B Zimmermann, C Zeder, I Aeberli & R F Hurrell

  2. Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands

    M B Zimmermann

  3. Institute of Population Health and Clinical Research, St John's National Academy of Health Sciences, Bangalore, India

    S Muthayya

  4. Institute of Nutrition, Mahidol University, Salaya, Nakhon Pathom, Thailand

    P Winichagoon

  5. The Ministry of Health, Rabat, Morocco

    N Chaouki

Authors
  1. M B Zimmermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C Zeder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S Muthayya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P Winichagoon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N Chaouki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. I Aeberli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R F Hurrell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M B Zimmermann.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Zimmermann, M., Zeder, C., Muthayya, S. et al. Adiposity in women and children from transition countries predicts decreased iron absorption, iron deficiency and a reduced response to iron fortification. Int J Obes 32, 1098–1104 (2008). https://doi.org/10.1038/ijo.2008.43

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2008.43

Keywords

This article is cited by

Search

Advanced search

Quick links