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Body Iron Stores and Heme-Iron Intake in Relation to Risk of Type 2 Diabetes: A Systematic Review and Meta-Analysis
Open accessAbstract
BACKGROUND AND OBJECTIVE: Emerging evidence from biological and epidemiological studies has suggested that body iron stores and heme-iron intake may be related to the risk of type 2 diabetes (T2D). We aimed to examine the association of body iron stores and heme-iron intake with T2D risk by conducting a systematic review and meta-analysis of previously published studies. RESEARCH DESIGN AND METHODS: Systematic review and subsequent meta-analysis were conducted by searching MEDLINE database up to June 22, 2012 to identify studies that analyzed the association of body iron stores or dietary heme-iron intake with T2D risk. The meta-analysis was performed using the effect estimates and 95% confidence intervals (CIs) to calculate the pooled risk estimates, while the heterogeneity among studies was examined using the I(2) and Q statistic. RESULTS: The meta-analysis included 16 high-quality studies: 12 studies analyzed ferritin levels (4,366 T2D patients and 41,091 controls) and 4 measured heme-iron intake (9,246 T2D patients and 179,689 controls). The combined relative risk (RR) comparing the highest and lowest category of ferritin levels was 1.66 (95% CI: 1.15-2.39) for prospective studies, 2.29 (95% CI: 1.48-3.54) for cross-sectional studies with heterogeneity (Q = 14.84, p = 0.01, I(2) = 66.3%; Q = 44.16, p<0.001, I(2) = 88.7%). The combined RR comparing the highest and lowest category of heme-iron intake was 1.31 (95% CI: 1.21-1.43) with heterogeneity (Q = 1.39, p = 0.71, I(2) = 0%). No publication bias was found. Additional 15 studies that were of good quality, had significant results, and analyzed the association between body iron stores and T2D risk were qualitatively included in the systematic review. CONCLUSIONS: The meta-analysis and systematic review suggest that increased ferritin levels and heme-iron intake are both associated with higher risk of T2D.
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Citations
Cites
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139
Quantifying heterogeneity in a meta‐analysis
Higgins, J. P. T., & Thompson, S. G. (2002) · Statistics in Medicine · doi:10.1002/sim.1186 · Cited by 36,763
Meta-analysis of Observational Studies in Epidemiology<SUBTITLE>A Proposal for Reporting</SUBTITLE>
Stroup, D. F. (2000) · JAMA · doi:10.1001/jama.283.15.2008 · Cited by 20,623
(2014) · Medical Entomology and Zoology · Cited by 17,633
[1] Role of free radicals and catalytic metal ions in human disease: An overview
Halliwell, B., & Gutteridge, J. M. C. (1990) · Methods in Enzymology · doi:10.1016/0076-6879(90)86093-b · Cited by 4,994
Andrews, N. C. (1999) · New England Journal of Medicine · doi:10.1056/nejm199912233412607 · Cited by 2,130
Tiedge, M., Lortz, S., Drinkgern, J., & Lenzen, S. (1997) · Diabetes · doi:10.2337/diab.46.11.1733 · Cited by 1,211
Systematic Review: Why sources of heterogeneity in meta-analysis should be investigated
Thompson, S. G. (1994) · BMJ · doi:10.1136/bmj.309.6965.1351 · Cited by 1,017
Hemochromatosis and Iron-Overload Screening in a Racially Diverse Population
Adams, P. C., Reboussin, D. M., Barton, J. C., McLaren, C. E., Eckfeldt, J. H., McLaren, G. D., Dawkins, F. W., Acton, R. T., Harris, E. L., Gordeuk, V. R., et al. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa041534 · Cited by 770
A note on graphical presentation of estimated odds ratios from several clinical trials
Galbraith, R. F. (1988) · Statistics in Medicine · doi:10.1002/sim.4780070807 · Cited by 663
Diabetes mellitus and free radicals
Wolff, S. P. (1993) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a072637 · Cited by 660
Body Iron Stores in Relation to Risk of Type 2 Diabetes in Apparently Healthy Women
Jiang, R. (2004) · JAMA · doi:10.1001/jama.291.6.711 · Cited by 598
Insulin resistance–associated hepatic iron overload
Mendler, M.-H., Turlin, B., Moirand, R., Jouanolle, A., Sapey, T., Guyader, D., Gall, J. L., Brissot, P., David, V., & Deugnier, Y. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70401-4 · Cited by 494
The Role of Iron in Diabetes and Its Complications
Swaminathan, S., Fonseca, V. A., Alam, M. G., & Shah, S. V. (2007) · Diabetes Care · doi:10.2337/dc06-2625 · Cited by 423
Diabetes and serum ferritin concentration among U.S. adults.
Ford, E. S., & Cogswell, M. E. (1999) · Diabetes Care · doi:10.2337/diacare.22.12.1978 · Cited by 419
A Prospective Study of Red Meat Consumption and Type 2 Diabetes in Middle-Aged and Elderly Women
Song, Y., Manson, J. E., Buring, J. E., & Liu, S. (2004) · Diabetes Care · doi:10.2337/diacare.27.9.2108 · Cited by 368
The role of iron in type 2 diabetes in humans
Rajpathak, S. N., Crandall, J. P., Wylie-Rosett, J., Kabat, G. C., Rohan, T. E., & Hu, F. B. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2008.04.005 · Cited by 363
Swiglo, B. A., Murad, M. H., Schünemann, H. J., Kunz, R., Vigersky, R. A., Guyatt, G. H., & Montori, V. M. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-1907 · Cited by 302
Forouhi, N. G., Harding, A.-H., Allison, M., Sandhu, M. S., Welch, A. A., Luben, R., Bingham, S. A., Khaw, K., & Wareham, N. J. (2007) · Diabetologia · doi:10.1007/s00125-007-0604-5 · Cited by 269
Cooksey, R. C., Jouihan, H. A., Ajioka, R. S., Hazel, M. W., Jones, D. L., Kushner, J. P., & McClain, D. A. (2004) · Endocrinology · doi:10.1210/en.2004-0392 · Cited by 255
Relation between iron stores and non-insulin dependent diabetes in men: case-control study
Salonen, J. T., Tuomainen, T.-P., Nyyssönen, K., Lakka, H.-M., & Punnonen, K. (1998) · BMJ · doi:10.1136/bmj.317.7160.727 · Cited by 242
Ferritin Concentrations, Metabolic Syndrome, and Type 2 Diabetes in Middle-Aged and Elderly Chinese
Sun, L. D., Franco, O. H., Hu, F. B., Cai, L., Yu, Z., Li, H., Ye, X., Qi, Q., Wang, J., Pan, A., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1159 · Cited by 202
Blood Donations and Risk of Coronary Heart Disease in Men
Ascherio, A., Rimm, E. B., Giovannucci, E. L., Willett, W. C., & Stampfer, M. J. (2001) · Circulation · doi:10.1161/01.cir.103.1.52 · Cited by 192
Potential Role of Increased Iron Stores in Diabetes
Wilson, J. G., Maher, J. F., Lindquist, J. H., Grambow, S. C., & Crook, E. D. (2003) · The American Journal of the Medical Sciences · doi:10.1097/00000441-200306000-00004 · Cited by 176 · cited 2×
“Researchers hypothesized that increased iron deposition in tissues initially induces insulin resistance, and the resulting hyperinsulinemia ultimately causes pancreatic islet apoptosis and the progression of T2D [48].”
BackgroundJiang, R., Ma, J., Ascherio, A., Stampfer, M. J., Willett, W. C., & Hu, F. B. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/79.1.70 · Cited by 173
Thirty-One Novel Biomarkers as Predictors for Clinically Incident Diabetes
Salomaa, V. V., Havulinna, A. S., Saarela, O., Zeller, T., Jousilahti, P., Jula, A. M., Münzel, T. F., Aromaa, A., Evans, A., Kuulasmaa, K., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010100 · Cited by 167
Insulin resistance, iron, and the liver
Ferrannini, E. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02397-7 · Cited by 165
Development of a Type 2 Diabetes Risk Model From a Panel of Serum Biomarkers From the Inter99 Cohort
Kolberg, J. A., Jørgensen, T., Gerwien, R. W., Hamren, S., McKenna, M. P., Moler, E. J., Rowe, M. W., Urdea, M. S., Xu, X. M., Hansen, T. F., et al. (2009) · Diabetes Care · doi:10.2337/dc08-1935 · Cited by 164
Kim, C., Kim, H., Bae, S. J., Park, J., & Lee, K.-U. (2010) · Metabolism · doi:10.1016/j.metabol.2010.03.007 · Cited by 151
Iron Intake and the Risk of Type 2 Diabetes in Women
Rajpathak, S. N., Ma, J., Manson, J. E., Willett, W. C., & Hu, F. B. (2006) · Diabetes Care · doi:10.2337/dc06-0119 · Cited by 151
Lee, D.-H., Folsom, A. R., & Jacobs, D. R. (2004) · Diabetologia · doi:10.1007/s00125-003-1307-1 · Cited by 143
Fumeron, F., Péan, F., Driss, F., Balkau, B., Tichet, J., Marre, M., Grandchamp, B., & for the DESIR Study Group (2006) · Diabetes Care · doi:10.2337/dc06-0093 · Cited by 137
Jehn, M. L., Guallar, E., Clark, J. M., Couper, D., Duncan, B. B., Ballantyne, C. M., Hoogeveen, R. C., Harris, Z. L., & Pankow, J. S. (2007) · American Journal of Epidemiology · doi:10.1093/aje/kwk093 · Cited by 136
Hardikar, P. S., Joshi, S. M., Bhat, D., RAUT, D. A., Katre, P. A., Lubree, H., Jere, A., Pandit, A. N., Fall, C. H. D., & Yajnik, C. S. (2012) · Diabetes Care · doi:10.2337/dc11-1321 · Cited by 123
Transferrin and iron induce insulin resistance of glucose transport in adipocytes
Green, A., Basile, R., & Rumberger, J. M. (2006) · Metabolism · doi:10.1016/j.metabol.2006.03.015 · Cited by 111
Shi, Z., Hu, X., Yuan, B., Pan, X., Meyer, H. E., & Holmboe‐Ottesen, G. (2006) · Diabetes Care · doi:10.2337/dc06-0327 · Cited by 108
Lee, B.-K., Kim, Y., & Kim, Y.-I. (2011) · Metabolism · doi:10.1016/j.metabol.2011.02.008 · Cited by 105
Body Iron Stores and Dietary Iron Intake in Relation to Diabetes in Adults in North China
Luan, D. C., Li, H., Li, S. J., Zhao, Z., Li, X., & Liu, Z. M. (2008) · Diabetes Care · doi:10.2337/dc07-0921 · Cited by 86
Self-citationBiomarkers of body iron stores and risk of developing type 2 diabetes
Rajpathak, S. N., Wylie‐Rosett, J., Gunter, M. J., Negassa, A., Kabat, G. C., Rohan, T. E., & Crandall, J. P. (2009) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2008.00985.x · Cited by 85
Hepcidin expression and iron parameters change in Type 2 diabetic patients
Jiang, F., Sun, Z., Tang, Y., Xu, C., & Jiao, X. (2011) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2011.03.028 · Cited by 80
Elevated Transferrin Saturation and Risk of Diabetes
Ellervik, C., Mandrup-Poulsen, T. R., Andersen, H. U., Tybjærg‐Hansen, A., Frandsen, M., Birgens, H., & Nordestgaard, B. G. (2011) · Diabetes Care · doi:10.2337/dc11-0416 · Cited by 68
Soluble transferrin receptors and ferritin in Type 2 diabetic patients
Hernández, C., Lecube, A., Carrera, A., & Simó, R. (2004) · Diabetic Medicine · doi:10.1111/j.1464-5491.2004.01331.x · Cited by 49
Aso, Y., Takebayashi, K., Wakabayashi, S., Momobayashi, A., Sugawara, N., Terasawa, T., Naruse, R., Hara, K., Suetsugu, M., Morita, K., et al. (2010) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2010.09.008 · Cited by 41
Serum ferritin in healthy subjects and type 2 diabetic patients
Kim, N. H., Oh, J. H., Choi, K. M., Kim, Y. H., Baik, S. H., Choi, D. S., & Kim, S. J. (2000) · Yonsei Medical Journal · doi:10.3349/ymj.2000.41.3.387 · Cited by 38
Ren, Y., Tian, H., Li, X., Liang, J., & Guizhi, Z. (2004) · Diabetes Care · doi:10.2337/diacare.27.2.622 · Cited by 31
Self-citationAshourpour, M., Djalali, M., Djazayery, A., Eshraghian, M. R., Taghdir, M., & Saedisomeolia, A. (2010) · International Journal of Food Sciences and Nutrition · doi:10.3109/09637480903555150 · Cited by 30
Le, T. D., Bae, S., Hsu, C. E., Singh, K. P., Blair, S. N., & Shang, N. (2008) · The Review of Diabetic Studies · doi:10.1900/rds.2008.5.245 · Cited by 27
Kim, C., Cheng, Y. J., & Beckles, G. L. (2008) · Diabetes Care · doi:10.2337/dc07-2362 · Cited by 25
Wu, H., Yu, Z., Qi, Q., Li, H., Sun, Q., & Lin, X. (2011) · BMJ Open · doi:10.1136/bmjopen-2011-000191 · Cited by 18
Is an elevated serum transferrin saturation associated with the development of diabetes?
Mainous, A. G., King, D. E., Pearson, W. S., & Garr, D. R. (2002) · PubMed · Cited by 16
Rowe, M. W., Bergman, R. N., Wagenknecht, L. E., & Kolberg, J. A. (2012) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2305 · Cited by 15
Freixenet, N., Vilardell, C., Llauradó, G., Giménez‐Palop, O., Berlanga, E., Gutiérrez, C., Caixàs, A., Vendrell, J. J., & González-Clemente, J. M. (2010) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2010.10.003 · Cited by 12
Body Iron Stores and Dietary Iron Intake in Relation to Diabetes in Adults in North China
Shi, Z., & Pan, X. (2008) · Diabetes Care · doi:10.2337/dc07-2048 · Cited by 6
Body Iron Stores and Dietary Iron Intake in Relation to Diabetes in Adults in North China
Luan, D. C., Li, H., Li, S. J., Zhao, Z., Li, X., & Liu, Z. M. (2008) · Diabetes Care · doi:10.2337/dc07-2122 · Cited by 5
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Mozaffarian, D. (2016) · Circulation · doi:10.1161/circulationaha.115.018585 · Cited by 2,216
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Ley, S. H., Hamdy, O., Mohan, V., & Hu, F. B. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60613-9 · Cited by 1,301
Myelin and iron concentration in the human brain: a quantitative study of MRI contrast
Stüber, C., Morawski, M., Schäfer, A., Labadie, C., Wähnert, M., Leuze, C., Streicher, M., Barapatre, N., Reimann, K., Geyer, S., et al. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.02.026 · Cited by 635
Kell, D. B., & Pretorius, E. (2014) · Metallomics · doi:10.1039/c3mt00347g · Cited by 667
Metadata
- Authors
- Zhao, Z., Li, S., Liu, G., Yan, F., Ma, X., Huang, Z., & Tian, H.
- Affiliations
- Sichuan University (CN)
- Corresponding author
- Tian, Haoming
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-07-26
- Volume
- 7
- Issue
- 7
- Pages
- e41641
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3406072
- OpenAlex
- W2124636230
- Cited by
- 227
- References
- 54
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 8 · 2023: 8 · 2022: 16 · 2021: 19 · 2020: 24 · 2019: 18 · 2018: 14 · 2017: 27 · 2016: 21 · 2015: 12 · 2014: 26 · 2013: 19 · 2012: 2
- FWCI
- 3.00
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Keywords
- type 2 diabetes, iron stores, ferritin, iron metabolism, dietary iron
- MeSH terms
- Animals, Biological Transport, Diabetes Mellitus, Type 2, Heme, Humans, Iron, Risk
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