European Journal of Nutrition

, Volume 57, Issue 3, pp 939–949 | Cite as

Association between pre-pregnancy consumption of meat, iron intake, and the risk of gestational diabetes: the SUN project

  • Amelia Marí-Sanchis
  • Ginette Díaz-Jurado
  • F. Javier Basterra-Gortari
  • Carmen de la Fuente-Arrillaga
  • Miguel A. Martínez-González
  • Maira Bes-RastrolloEmail author
Original Contribution



We assessed the association of total meat, processed, and unprocessed red meat and iron intake with the risk of developing gestational diabetes mellitus (GDM) in pregnant women.


We conducted a prospective study among 3298 disease-free Spanish women participants of the SUN cohort who reported at least one pregnancy between December 1999 and March 2012. Meat consumption and iron intake were assessed at baseline through a validated, 136-item semi-quantitative, food frequency questionnaire. We categorized total, red, and processed meat consumption and iron intake into quartiles. Logistic regression models were used to adjust for potential confounders.


We identified 172 incident cases of GDM. In the fully adjusted analysis, total meat consumption was significantly associated with a higher risk of GDM [OR = 1.67 (95% CI 1.06–2.63, p-trend 0.010)] for the highest versus the lowest quartile of consumption. The observed associations were particularly strong for red meat consumption [OR = 2.37 (95% CI 1.49–3.78, p-trend < 0.001)] and processed meat consumption [OR = 2.01 (95% CI 1.26–3.21, p-trend 0.003)]. Heme iron intake was also directly associated with GDM [OR = 2.21 (95% CI 1.37–3.58, p-trend 0.003)], although the association was attenuated and lost its statistical significance when we adjusted for red meat consumption [OR = 1.57 (95% CI 0.91–2.70, p-trend 0.213)]. No association was observed for non-heme and total iron intake, including supplements.


Our overall findings suggest that higher pre-pregnancy consumption of total meat, especially red and processed meat, and heme iron intake, are significantly associated with an increased GDM risk in a Mediterranean cohort of university graduates.


Gestational diabetes mellitus Total meat Red and processed meat Heme iron intake Mediterranean population 



We are thankful to Mark Sullivan for the revision of English spelling, grammar, and writing. The SUN Project has received funding from the Spanish Government-Instituto de Salud Carlos III, and the European Regional Development Fund (FEDER) (RD 06/0045, CIBER-OBN, Grants PI10/02658, PI10/02293, PI13/00615, PI14/01668, PI14/01798, PI14/01764, and G03/140), the Navarra Regional Government (45/2011, 122/2014), and the University of Navarra.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.


  1. 1.
    Metzger BE, Coustan DR, the Organizing Committee (1998) Summary and recommendations of the Fourth International Workshop-Conference on gestational diabetes mellitus. Diabetes Care 21(Suppl. 2):161–167Google Scholar
  2. 2.
    Kim C, Newton KM, Knopp RH (2002) Gestational diabetes and the incidence of type 2 diabetes: a systematic review. Diabetes Care 25:1862–1868CrossRefGoogle Scholar
  3. 3.
    Bellamy L, Casas JP, Hingorani AD, Williams D (2009) Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. The Lancet 373:1773–1779CrossRefGoogle Scholar
  4. 4.
    Boney CM, Verma A, Tucker R, Vohr BR (2005) Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 115:e290–e296CrossRefGoogle Scholar
  5. 5.
    Silverman BL, Metzger BE, Cho NH, Loeb CA (1995) Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care 18:611–617CrossRefGoogle Scholar
  6. 6.
    Landon MB, Spong CY, Thom E, Carpenter MW, Ramin SM, Casey B, Wapner RJ, Varner MW, Rouse DJ, Thorp JM et al (2009) A multicenter, randomized trial of treatment for mild gestational diabetes. N Engl J Med 361:1339–1348CrossRefGoogle Scholar
  7. 7.
    Reece EA, Leguizamón G, Wiznitzer A (2009) Gestational diabetes: the need for a common ground. Lancet 373:1789–1797CrossRefGoogle Scholar
  8. 8.
    American Diabetes Association (2009) Standards of medical care in diabetes. Diabetes Care 32(Suppl 1):S13–S61CrossRefGoogle Scholar
  9. 9.
    Buckley BS, Harreiter J, Damm P, Corcoy R, Chico A, Simmons D, Vellinga A, Dunne F; DALI Core Investigator Group (2012) Gestational diabetes mellitus in Europe: prevalence, current screening practice and barriers to screening. A review. Diabet Med 29:844–854CrossRefGoogle Scholar
  10. 10.
    Zhang C, Schulze MB, Solomon CG, Hu FB (2006) A prospective study of dietary patterns, meat intake and the risk of gestational diabetes mellitus. Diabetologia 49:2604–2613CrossRefGoogle Scholar
  11. 11.
    Schoenaker DA, Mishra GD, Callway LK, Soedamah-Muthu SS (2016) The role of energy, nutrients, foods and dietary patterns in the development of gestational diabetes mellitus: a systematic review of observational studies. Diabetes Care 39:16–23CrossRefGoogle Scholar
  12. 12.
    Bao W, Bowers K, Tobias DK, Hu FB, Zhang C (2013) Prepregnancy dietary protein intake, major dietary protein sources, and the risk of gestational diabetes mellitus: a prospective cohort study. Diabetes Care 36:2001–2008CrossRefGoogle Scholar
  13. 13.
    Schoenaker DA, Soedamah-Muthu SS, Callway LK, Mishra GD (2015) Pre-pregnancy dietary patterns and risk of gestational diabetes mellitus: results from an Australian population-based prospective cohort study. Diabetologia 58:2726–2735CrossRefGoogle Scholar
  14. 14.
    Dominguez LJ, Martínez-González MA, Basterra-Gortari FJ, Gea A, Barbagallo M, Bes-Rastrollo M (2014) Fast food consumption and gestational diabetes incidence in the SUN project. PLoS One 9:e106627CrossRefGoogle Scholar
  15. 15.
    Martínez-González MA, Sánchez-Villegas A, De Irala J, Marti A, Martínez JA (2002) Mediterranean diet and stroke: objectives and design of the SUN project. Seguimiento Universidad de Navarra. Nutr Neurosci 5:65–73CrossRefGoogle Scholar
  16. 16.
    Seguí-Gómez M, de la Fuente C, Vázquez Z, de Irala J, Martínez-González MA (2006) Cohort profile: the ‘Seguimiento Universidad de Navarra’ (SUN) study. Int J Epidemiol 35:1417–1422CrossRefGoogle Scholar
  17. 17.
    Martin-Moreno JM, Boyle P, Gorgojo L, Maisonneuve P, Fernández-Rodríguez JC, Salvini S, Willett WC (1993) Development and validation of a food frequency questionnaire in Spain. Int J Epidemiol 22:512–519CrossRefGoogle Scholar
  18. 18.
    De la Fuente-Arrillaga C, Ruiz ZV, Bes-Rastrollo M, Sampson L, Martinez-Gonzalez MA (2010) Reproducibility of an FFQ validated in Spain. Public Health Nutr 13:1364–1372CrossRefGoogle Scholar
  19. 19.
    Fernandez-Ballart JD, Pinol JL, Zazpe I, Corella D, Carrasco P, Toledo E, Pérez-Bauer M, Martínez-González MA, Salas-Salvadó J, Martín-Moreno JM (2010) Relative validity of a semi-quantitative food-frequency questionnaire in an elderly mediterranean population of Spain. Br J Nutr 103:1808–1816CrossRefGoogle Scholar
  20. 20.
    Trichopoulou A, Costacou T, Bamia C, Trichopoulos D (2003) Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348:2599–2608CrossRefGoogle Scholar
  21. 21.
    Moreiras O (2009) Tablas de composición de alimentos (Food Composition Tables), 16th edn. Ediciones Pirámide, MadridGoogle Scholar
  22. 22.
    Mataix J (2003) Tablas de composición de alimentos (Food Composition Tables), 5th edn. GranadaGoogle Scholar
  23. 23.
    National Diabetes Data Group (1979) Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 28:1039–1057CrossRefGoogle Scholar
  24. 24.
    American Diabetes Association (2010) Diagnosis and classification of diabetes mellitus. Diabetes Care 33(Suppl 1):S62–S69CrossRefGoogle Scholar
  25. 25.
    Bes-Rastrollo M, Pérez-Valdivieso J, Sánchez-Villegas A, Alonso A, Martínez-González MA (2005) Validación del peso e índices de masa corporal auto-declarados de los participantes de una cohorte de graduados universitarios (Validation weight and self-reported body mass index of participants in a cohort of university graduates). Rev Esp Obes 3:183–189Google Scholar
  26. 26.
    Martínez-González MA, López-Fontana C, Varo JJ, Sánchez-Villegas A, Martínez JA (2005) Validation of the Spanish version of the physical activity questionnaire used in the Nurses’ Health Study and the Health Professionals’ Follow-up Study. Public Health Nutr 8:920–927CrossRefGoogle Scholar
  27. 27.
    Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, O’Brien WL, Bassett DR Jr, Schmitz KH, Emplaincourt PO et al (2000) Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc 32(Suppl 9):S498–S504CrossRefGoogle Scholar
  28. 28.
    van Dam RM, Willet WC, Rimm EB, Stampfer MJ, Hu FB (2002) Dietary fat and meat intake in relation to risk of type 2 diabetes in men. Diabetes Care 25:417–424CrossRefGoogle Scholar
  29. 29.
    Pan A, Sun Q, Bernstein AM, Schulze MB, Manson JE, Willett WC, Hu FB (2011) Red meat consumption and risk of type 2 diabetes: 3 cohort of US adults and an updated metaanalysis. Am J Clin Nutr 94:1088–1096CrossRefGoogle Scholar
  30. 30.
    Tobias DK, Zhang C, Chavarro J, Bowers K, Rich-Edwards J, Rosner B, Mozaffarian D, Hu FB (2002) Prepregnancy adherence to dietary patterns and lowers risk of gestational diabetes mellitus. Am J Clin Nutr 96:289–295CrossRefGoogle Scholar
  31. 31.
    Bowers K, Yeung E, Williams MA, Qi L, Tobias DK, Hu FB, Zhang C (2011) A prospective study of prepregnancy dietary iron intake and risk for gestational diabetes mellitus. Diabetes Care 34:1557–1563CrossRefGoogle Scholar
  32. 32.
    Qiu C, Zhang C, Gelaye B, Enquobahrie DA, Frederick IO, Williams MA (2011) Gestational diabetes mellitus in relation to maternal dietary heme iron and nonheme iron intake. Diabetes Care 34:1564–1569CrossRefGoogle Scholar
  33. 33.
    Fernandez-Cao JC, Arija V, Aranda N, Bullo M, Basora J, Martínez-González MA, Díez-Espino J, Salas-Salvadó J (2013) Heme iron intake and risk of new-onset diabetes in a Mediterranean population at high risk of cardiovascular disease: an observational cohort analysis. BMC Public Health 13:1042CrossRefGoogle Scholar
  34. 34.
    Chan KK, Chan BC, Lam KF, Tam S, Lao TT (2009) Iron supplement in pregnancy and development of gestational diabetes—a randomised placebo-controlled trial. BJOG 116:789–798CrossRefGoogle Scholar
  35. 35.
    Bo S, Menato G, Villois P, Gambino R, Cassader M, Cotrino I, Cavallo-Perin P (2009) Iron supplementation and gestational diabetes in midpregnancy. Am J Obstet Gynecol 201(158):e1–e158.e6Google Scholar
  36. 36.
    Zhang C (2010) Risk factors for gestational diabetes-from an epidemiological standpoint. In: Kim C, Ferrara A (eds) Gestational diabetes during and after pregnancy. Springer-Verlag London Limites, London, pp 71–81CrossRefGoogle Scholar
  37. 37.
    Lao TT, Ho LF (2004) Impact of iron deficiency anemia on prevalence of gestational diabetes mellitus. Diabetes Care 27:650–656CrossRefGoogle Scholar
  38. 38.
    Swaminathan S, Fonseca VA, Alam MG, Shah SV (2007) The role of iron in diabetes and its complications. Diabetes Care 30:1926–1933CrossRefGoogle Scholar
  39. 39.
    Kim Y, Keogh J, Clifton P (2015) A review of potential metabolic etiologies of the observed association between red meat consumption and development of type 2 diabetes mellitus. Metabolism 64:768–779CrossRefGoogle Scholar
  40. 40.
    Willett WC, Colditz GA (1998) Approaches for conducting large cohort studies. Epidemiol Rev 20:91–99CrossRefGoogle Scholar
  41. 41.
    Alonso A, Seguí-Gómez M, de Irala J, Sánchez-Villegas A, Beunza JJ, Martínez-González MA (2006) Predictors of follow-up and assessment of selection bias from dropouts using inverse probability weighting in a cohort of university graduates. Eur J Epidemiol 21:351–358CrossRefGoogle Scholar
  42. 42.
    Rothman KJ, Greenland S, Lash TL (2008) Validity in epidemiologic studies. In Modern Epidemiology. 3 th ed. Rothman KJ, Greenland S, Lash TL. Philadelphia, Lippincott Williams & Wilkins, p146–147Google Scholar
  43. 43.
    Food Standards Australia New Zealand (2011) Pregnancy and healthy eating.
  44. 44.
    Williamson CS (2006) Nutrition in pregnancy. Br Nutr Found Nutr Bull 31:28–59CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Amelia Marí-Sanchis
    • 1
    • 2
  • Ginette Díaz-Jurado
    • 1
  • F. Javier Basterra-Gortari
    • 1
    • 3
  • Carmen de la Fuente-Arrillaga
    • 1
    • 4
    • 5
  • Miguel A. Martínez-González
    • 1
    • 4
    • 5
  • Maira Bes-Rastrollo
    • 1
    • 4
    • 5
    Email author
  1. 1.Department of Preventive Medicine and Public Health, School of MedicineUniversity of NavarraPamplonaSpain
  2. 2.Division of Nutrition, Department of Endocrinology and NutritionHospital de NavarraPamplonaSpain
  3. 3.Department of Internal Medicine (Endocrinology)Hospital Reina SofiaTudelaSpain
  4. 4.Navarra Institute for Health Research (IDISNA)PamplonaSpain
  5. 5.Biomedical Research Center Network on Physiopathology of Obesity and Nutrition (CIBERobn)Institute of Health Carlos IIIMadridSpain

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