Dietary iron intake, iron status, and gestational diabetes

Cuilin Zhang, Shristi Rawal, Cuilin Zhang, Shristi Rawal

Abstract

Pregnant women are particularly vulnerable to iron deficiency and related adverse pregnancy outcomes and, as such, are routinely recommended for iron supplementation. Emerging evidence from both animal and population-based studies, however, has raised potential concerns because significant associations have been observed between greater iron stores and disturbances in glucose metabolism, including increased risk of type 2 diabetes among nonpregnant individuals. Yet, the evidence is uncertain regarding the role of iron in the development of gestational diabetes mellitus (GDM), a common pregnancy complication which has short-term and long-term adverse health ramifications for both women and their children. In this review, we critically and systematically evaluate available data examining the risk of GDM associated with dietary iron, iron supplementation, and iron status as measured by blood concentrations of several indicators. We also discuss major methodologic concerns regarding the available epidemiologic studies on iron and GDM.

Keywords: dietary iron; gestational diabetes mellitus; iron status; iron supplementation; pregnancy.

© 2017 American Society for Nutrition.

References

    1. Hansen JB, Moen IW, Mandrup-Poulsen T. Iron: the hard player in diabetes pathophysiology. Acta Physiol (Oxf) 2014;210:717–32.
    1. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans 2008;36:343–7.
    1. Cooksey RC, Jouihan HA, Ajioka RS, Hazel MW, Jones DL, Kushner JP, McClain DA. Oxidative stress, beta-cell apoptosis, and decreased insulin secretory capacity in mouse models of hemochromatosis. Endocrinology 2004;145:5305–12.
    1. Rajpathak SN, Crandall JP, Wylie-Rosett J, Kabat GC, Rohan TE, Hu FB. The role of iron in type 2 diabetes in humans. Biochim Biophys Acta 2009;1790:671–81.
    1. Fernández-Real JM, McClain D, Manco M. Mechanisms linking glucose homeostasis and iron metabolism toward the onset and progression of type 2 diabetes. Diabetes Care 2015;38:2169–76.
    1. Green A, Basile R, Rumberger JM. Transferrin and iron induce insulin resistance of glucose transport in adipocytes. Metabolism 2006;55:1042–5.
    1. Huang J, Jones D, Luo B, Sanderson M, Soto J, Abel ED, Cooksey RC, McClain DA. Iron overload and diabetes risk: a shift from glucose to fatty acid oxidation and increased hepatic glucose production in a mouse model of hereditary hemochromatosis. Diabetes 2011;60:80–7.
    1. Andrews NC. Forging a field: the golden age of iron biology. Blood 2008;112:219–30.
    1. Cao C, Thomas CE, Insogna KL, O’Brien KO. Duodenal absorption and tissue utilization of dietary heme and nonheme iron differ in rats. J Nutr 2014;144:1710–7.
    1. Anderson GJ, Frazer DM. Current understanding of iron homeostasis. Am J Clin Nutr 2017;106(Suppl):1559S–66S.
    1. Nemeth E, Ganz T. Regulation of iron metabolism by hepcidin. Annu Rev Nutr 2006;26:323–42.
    1. Han O. Molecular mechanism of intestinal iron absorption. Metallomics 2011;3:103–9.
    1. Mastrogiannaki M, Matak P, Peyssonnaux C. The gut in iron homeostasis: role of HIF-2 under normal and pathological conditions. Blood 2013;122:885–92.
    1. Dupic F, Fruchon S, Bensaid M, Loreal O, Brissot P, Borot N, Roth MP, Coppin H. Duodenal mRNA expression of iron related genes in response to iron loading and iron deficiency in four strains of mice. Gut 2002;51:648–53.
    1. Wessling-Resnick M. Iron homeostasis and the inflammatory response. Annu Rev Nutr 2010;30:105–22.
    1. Rohner F, Namaste SM, Larson LM, Addo OY, Mei Z, Suchdev PS, Williams AM, Sakr Ashour FA, Rawat R, Raiten DJ, et al. . Adjusting soluble transferrin receptor concentrations for inflammation: Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) project. Am J Clin Nutr 2017;106:372S–82S.
    1. Knowles J, Thurnham DI, Phengdy B, Houamboun K, Philavong K, Keomoungkhone I, Keovilay K. Impact of inflammation on the biomarkers of iron status in a cross-sectional survey of Lao women and children. Br J Nutr 2013;110:2285–97.
    1. American College of Obstetricians and Gynecologists. ACOG Practice Bulletin No. 95: anemia in pregnancy. Obstet Gynecol 2008;112:201–7.
    1. Montonen J, Boeing H, Steffen A, Lehmann R, Fritsche A, Joost HG, Schulze MB, Pischon T. Body iron stores and risk of type 2 diabetes: results from the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam study. Diabetologia 2012;55:2613–21.
    1. Zhao Z, Li S, Liu G, Yan F, Ma X, Huang Z, Tian H. Body iron stores and heme-iron intake in relation to risk of type 2 diabetes: a systematic review and meta-analysis. PLoS One 2012;7:e41641.
    1. Ford ES, Cogswell ME. Diabetes and serum ferritin concentration among U.S. adults. Diabetes Care 1999;22:1978–83.
    1. Forouhi NG, Harding AH, Allison M, Sandhu MS, Welch A, Luben R, Bingham S, Khaw KT, Wareham NJ. Elevated serum ferritin levels predict new-onset type 2 diabetes: results from the EPIC-Norfolk prospective study. Diabetologia 2007;50:949–56.
    1. Sun L, Franco OH, Hu FB, Cai L, Yu Z, Li H, Ye X, Qi Q, Wang J, Pan A, et al. . Ferritin concentrations, metabolic syndrome, and type 2 diabetes in middle-aged and elderly chinese. J Clin Endocrinol Metab 2008;93:4690–6.
    1. Kim CH, Kim HK, Bae SJ, Park JY, Lee KU. Association of elevated serum ferritin concentration with insulin resistance and impaired glucose metabolism in Korean men and women. Metabolism 2011;60:414–20.
    1. Zein S, Rachidi S, Hininger-Favier I. Is oxidative stress induced by iron status associated with gestational diabetes mellitus? J Trace Elem Med Biol 2014;28:65–9.
    1. Zhang C, Rawal S, Chong YS. Risk factors for gestational diabetes: is prevention possible? Diabetologia 2016;59:1385–90.
    1. Bowers K, Yeung E, Williams MA, Qi L, Tobias DK, Hu FB, Zhang C. A prospective study of prepregnancy dietary iron intake and risk for gestational diabetes mellitus. Diabetes Care 2011;34:1557–63.
    1. Qiu C, Zhang C, Gelaye B, Enquobahrie DA, Frederick IO, Williams MA. Gestational diabetes mellitus in relation to maternal dietary heme iron and nonheme iron intake. Diabetes Care 2011;34:1564–9.
    1. Darling AM, Mitchell AA, Werler MM. Preconceptional iron intake and gestational diabetes mellitus. Int J Environ Res Public Health 2016;13:E525.
    1. Helin A, Kinnunen TI, Raitanen J, Ahonen S, Virtanen SM, Luoto R. Iron intake, haemoglobin and risk of gestational diabetes: a prospective cohort study. BMJ Open 2012;2:e001730.
    1. Behboudi-Gandevani S, Safary K, Moghaddam-Banaem L, Lamyian M, Goshtasebi A, Alian-Moghaddam N. The relationship between maternal serum iron and zinc levels and their nutritional intakes in early pregnancy with gestational diabetes. Biol Trace Elem Res 2013;154:7–13.
    1. Palma S, Perez-Iglesias R, Prieto D, Pardo R, Llorca J, Delgado-Rodriguez M. Iron but not folic acid supplementation reduces the risk of low birthweight in pregnant women without anaemia: a case-control study. J Epidemiol Community Health 2008;62:120–4.
    1. Bo S, Menato G, Villois P, Gambino R, Cassader M, Cotrino I, Cavallo-Perin P. Iron supplementation and gestational diabetes in midpregnancy. Am J Obstet Gynecol 2009;201:158.e1–6.
    1. Chan KK, Chan BC, Lam KF, Tam S, Lao TT. Iron supplement in pregnancy and development of gestational diabetes–a randomised placebo-controlled trial. BJOG 2009;116:789–97, discussion 797–8.
    1. Ouladsahebmadarek E, Sayyah-Melli M, Taghavi S, Abbasalizadeh S, Seyedhejazie M. The effect of supplemental iron elimination on pregnancy outcome. Pak J Med Sci 2011;27:641–5.
    1. Kinnunen TI, Luoto R, Helin A, Hemminki E. Supplemental iron intake and the risk of glucose intolerance in pregnancy: re-analysis of a randomised controlled trial in Finland. Matern Child Nutr 2016;12:74–84.
    1. Fu S, Li F, Zhou J, Liu Z. The relationship between body iron status, iron intake and gestational diabetes: a systematic review and meta-analysis. Medicine (Baltimore) 2016;95:e2383.
    1. Bowers K, Tobias DK, Yeung E, Hu FB, Zhang C. A prospective study of prepregnancy dietary fat intake and risk of gestational diabetes. Am J Clin Nutr 2012;95:446–53.
    1. Zhang C, Schulze MB, Solomon CG, Hu FB. A prospective study of dietary patterns, meat intake and the risk of gestational diabetes mellitus. Diabetologia 2006;49:2604–13.
    1. Manoguerra AS, Erdman AR, Booze LL, Christianson G, Wax PM, Scharman EJ, Woolf AD, Chyka PA, Keyes DC, Olson KR, et al. . Iron ingestion: an evidence-based consensus guideline for out-of-hospital management. Clin Toxicol (Phila) 2005;43:553–70.
    1. Lao TT, Chan PL, Tam KF. Gestational diabetes mellitus in the last trimester - a feature of maternal iron excess? Diabet Med 2001;18:218–23.
    1. Tarim E, Kilicdag E, Bagis T, Ergin T. High maternal hemoglobin and ferritin values as risk factors for gestational diabetes. Int J Gynaecol Obstet 2004;84:259–61.
    1. Chen X, Scholl TO, Stein TP. Association of elevated serum ferritin levels and the risk of gestational diabetes mellitus in pregnant women: the Camden study. Diabetes Care 2006;29:1077–82.
    1. Amiri FN, Basirat Z, Omidvar S, Sharbatdaran M, Tilaki KH, Pouramir M. Comparison of the serum iron, ferritin levels and total iron-binding capacity between pregnant women with and without gestational diabetes. J Nat Sci Biol Med 2013;4:302–5.
    1. Afkhami-Ardekani M, Rashidi M. Iron status in women with and without gestational diabetes mellitus. J Diabetes Complications 2009;23:194–8.
    1. Soubasi V, Petridou S, Sarafidis K, Tsantali C, Diamanti E, Buonocore G, Drossou-Agakidou V. Association of increased maternal ferritin levels with gestational diabetes and intra-uterine growth retardation. Diabetes Metab 2010;36:58–63.
    1. Derbent AU, Simavli SA, Kaygusuz I, Gumus II, Yilmaz S, Yildirim M, Uysal S. Serum hepcidin is associated with parameters of glucose metabolism in women with gestational diabetes mellitus. J Matern Fetal Neonatal Med 2013;26:1112–5.
    1. Khambalia AZ, Aimone A, Nagubandi P, Roberts CL, McElduff A, Morris JM, Powell KL, Tasevski V, Nassar N. High maternal iron status, dietary iron intake and iron supplement use in pregnancy and risk of gestational diabetes mellitus: a prospective study and systematic review. Diabet Med 2016;33:1211–21.
    1. Khambalia AZ, Collins CE, Roberts CL, Morris JM, Powell KL, Tasevski V, Nassar N. Iron deficiency in early pregnancy using serum ferritin and soluble transferrin receptor concentrations are associated with pregnancy and birth outcomes. Eur J Clin Nutr 2016;70:358–63.
    1. Sharifi F, Ziaee A, Feizi A, Mousavinasab N, Anjomshoaa A, Mokhtari P. Serum ferritin concentration in gestational diabetes mellitus and risk of subsequent development of early postpartum diabetes mellitus. Diabetes Metab Syndr Obes 2010;3:413–9.
    1. Javadian P, Alimohamadi S, Gharedaghi MH, Hantoushzadeh S. Gestational diabetes mellitus and iron supplement; effects on pregnancy outcome. Acta Med Iran 2014;52:385–9.
    1. Kaygusuz I, Gumus II, Yilmaz S, Simavli S, Uysal S, Derbent AU, Gozdemir E, Kafali H. Serum levels of visfatin and possible interaction with iron parameters in gestational diabetes mellitus. Gynecol Obstet Invest 2013;75:203–9.
    1. Cauza E, Hanusch-Enserer U, Bischof M, Spak M, Kostner K, Tammaa A, Dunky A, Ferenci P. Increased C282Y heterozygosity in gestational diabetes. Fetal Diagn Ther 2005;20:349–54.
    1. Bowers KA, Olsen SF, Bao W, Halldorsson TI, Strom M, Zhang C. Plasma concentrations of ferritin in early pregnancy are associated with risk of gestational diabetes mellitus in women in the Danish National Birth Cohort. J Nutr 2016;146:1756–61.
    1. Rawal S, Hinkle SN, Bao W, Zhu Y, Grewal J, Albert PS, Weir NL, Tsai MY, Zhang C. A longitudinal study of iron status during pregnancy and the risk of gestational diabetes: findings from a prospective, multiracial cohort. Diabetologia 2017;60:249–57.
    1. Gungor ES, Danisman N, Mollamahmutoglu L. Maternal serum ferritin and hemoglobin values in patients with gestational diabetes mellitus. Saudi Med J 2007;28:478–80.
    1. Zein S, Rachidi S, Awada S, Osman M, Al-Hajje A, Shami N, Sharara I, Cheikh-Ali K, Salameh P, Hininger-Favier I. High iron level in early pregnancy increased glucose intolerance. J Trace Elem Med Biol 2015;30:220–5.
    1. Maitland RA, Seed PT, Briley AL, Homsy M, Thomas S, Pasupathy D, Robson SC, Nelson SM, Sattar N, Poston L; UPBEAT trial consortium. Prediction of gestational diabetes in obese pregnant women from the UK Pregnancies Better Eating and Activity (UPBEAT) pilot trial. Diabet Med 2014;31:963–70.
    1. Yeniel AÖ, Ergenoglu AM, Sanhal CY, Sahin C, Ulukus M, Oztekin K. Does high maternal first trimester iron status have an effect on the 50 g oral glucose test? J Obstet Gynaecol 2012;32:332–4.
    1. Harms K, Kaiser T. Beyond soluble transferrin receptor: old challenges and new horizons. Best Pract Res Clin Endocrinol Metab 2015;29:799–810.
    1. Lao TT, Chan LY, Tam KF, Ho LF. Maternal hemoglobin and risk of gestational diabetes mellitus in Chinese women. Obstet Gynecol 2002;99:807–12.
    1. Tan PC, Chai JN, Ling LP, Omar SZ. Maternal hemoglobin level and red cell indices as predictors of gestational diabetes in a multi-ethnic Asian population. Clin Exp Obstet Gynecol 2011;38:150–4.
    1. Skikne BS, Flowers CH, Cook JD. Serum transferrin receptor: a quantitative measure of tissue iron deficiency. Blood 1990;75:1870–6.
    1. Skikne BS. Circulating transferrin receptor assay–coming of age. Clin Chem 1998;44:7–9.
    1. Cao C, O’Brien KO. Pregnancy and iron homeostasis: an update. Nutr Rev 2013;71:35–51.
    1. Ganz T, Nemeth E. Hepcidin and iron homeostasis. Biochim Biophys Acta 2012;1823:1434–43.
    1. Lao TT, Ho LF. Impact of iron deficiency anemia on prevalence of gestational diabetes mellitus. Diabetes Care 2004;27:650–6.
    1. Akhlaghi F, Bagheri SM, Rajabi O. A comparative study of relationship between micronutrients and gestational diabetes. ISRN Obstet Gynecol 2012;2012:470419.
    1. Wang Y, Tan M, Huang Z, Sheng L, Ge Y, Zhang H, Jiang M, Zhang G. Elemental contents in serum of pregnant women with gestational diabetes mellitus. Biol Trace Elem Res 2002;88:113–8.
    1. Al-Saleh E, Nandakumaran M, Al-Shammari M, Al-Harouny A. Maternal-fetal status of copper, iron, molybdenum, selenium and zinc in patients with gestational diabetes. J Matern Fetal Neonatal Med 2004;16:15–21.
    1. Lao TT, Tam KF. Maternal serum ferritin and gestational impaired glucose tolerance. Diabetes Care 1997;20:1368–9.
    1. Portha B, Giroix MH, Cros JC, Picon L. Diabetogenic effect of N-nitrosomethylurea and N-nitrosomethylurethane in the adult rat. Ann Nutr Aliment 1980;34:1143–51.
    1. McGrowder D, Ragoobirsingh D, Dasgupta T. Effects of S-nitroso-N-acetyl-penicillamine administration on glucose tolerance and plasma levels of insulin and glucagon in the dog. Nitric Oxide 2001;5:402–12.
    1. Ottum MS, Mistry AM. Advanced glycation end-products: modifiable environmental factors profoundly mediate insulin resistance. J Clin Biochem Nutr 2015;57:1–12.
    1. Bao W, Chavarro JE, Tobias DK, Bowers K, Li S, Hu FB, Zhang C. Long-term risk of type 2 diabetes in relation to habitual iron intake in women with a history of gestational diabetes: a prospective cohort study. Am J Clin Nutr 2016;103:375–81.
    1. Rajpathak S, Ma J, Manson J, Willett WC, Hu FB. Iron intake and the risk of type 2 diabetes in women: a prospective cohort study. Diabetes Care 2006;29:1370–6.
    1. Raiten DJ, Sakr Ashour FA, Ross AC, Meydani SN, Dawson HD, Stephensen CB, Brabin BJ, Suchdev PS, van Ommen B; INSPIRE Consultative Group. Inflammation and Nutritional Science for Programs/Policies and Interpretation of Research Evidence (INSPIRE). J Nutr 2015;145:1039S–108S.
    1. Thurnham DI, McCabe LD, Haldar S, Wieringa FT, Northrop-Clewes CA, McCabe GP. Adjusting plasma ferritin concentrations to remove the effects of subclinical inflammation in the assessment of iron deficiency: a meta-analysis. Am J Clin Nutr 2010;92:546–55.
    1. Wallace DF. The regulation of iron absorption and homeostasis. Clin Biochem Rev 2016;37:51–62.
    1. Siu AL, Force USPST. Screening for iron deficiency anemia and iron supplementation in pregnant women to improve maternal health and birth outcomes: U.S. Preventive Services Task Force Recommendation Statement. Ann Intern Med 2015;163:529–36.

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