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

Abstract

Purpose

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.

Methods

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.

Results

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.

Conclusions

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.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  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):161–167

    Google Scholar 

  2. 2.

    Kim C, Newton KM, Knopp RH (2002) Gestational diabetes and the incidence of type 2 diabetes: a systematic review. Diabetes Care 25:1862–1868

    Article  Google 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 373:1773–1779

    CAS  Article  Google 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–e296

    Article  Google 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 18:611–617

    CAS  Article  Google 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 361:1339–1348

    CAS  Article  Google Scholar 

  7. 7.

    Reece EA, Leguizamón G, Wiznitzer A (2009) Gestational diabetes: the need for a common ground. Lancet 373:1789–1797

    Article  Google Scholar 

  8. 8.

    American Diabetes Association (2009) Standards of medical care in diabetes. Diabetes Care 32(Suppl 1):S13–S61

    Article  Google 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 29:844–854

    CAS  Article  Google 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 49:2604–2613

    CAS  Article  Google 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 39:16–23

    Article  Google 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 36:2001–2008

    CAS  Article  Google 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 58:2726–2735

    CAS  Article  Google 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:e106627

    Article  Google 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 5:65–73

    Article  Google 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 35:1417–1422

    Article  Google 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 22:512–519

    CAS  Article  Google 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 13:1364–1372

    Article  Google 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 103:1808–1816

    CAS  Article  Google 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 348:2599–2608

    Article  Google Scholar 

  21. 21.

    Moreiras O (2009) Tablas de composición de alimentos (Food Composition Tables), 16th edn. Ediciones Pirámide, Madrid

  22. 22.

    Mataix J (2003) Tablas de composición de alimentos (Food Composition Tables), 5th edn. Granada

  23. 23.

    National Diabetes Data Group (1979) Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 28:1039–1057

    Article  Google Scholar 

  24. 24.

    American Diabetes Association (2010) Diagnosis and classification of diabetes mellitus. Diabetes Care 33(Suppl 1):S62–S69

    Article  Google 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 3:183–189

    Google 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 8:920–927

    Article  Google 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–S504

    CAS  Article  Google 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 25:417–424

    Article  Google 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 94:1088–1096

    CAS  Article  Google 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 96:289–295

    Article  Google 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 34:1557–1563

    Article  Google 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 34:1564–1569

    CAS  Article  Google 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 13:1042

    Article  Google 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 116:789–798

    CAS  Article  Google 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.e6

    Google 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 71–81

    Google Scholar 

  37. 37.

    Lao TT, Ho LF (2004) Impact of iron deficiency anemia on prevalence of gestational diabetes mellitus. Diabetes Care 27:650–656

    Article  Google Scholar 

  38. 38.

    Swaminathan S, Fonseca VA, Alam MG, Shah SV (2007) The role of iron in diabetes and its complications. Diabetes Care 30:1926–1933

    CAS  Article  Google 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 64:768–779

    CAS  Article  Google Scholar 

  40. 40.

    Willett WC, Colditz GA (1998) Approaches for conducting large cohort studies. Epidemiol Rev 20:91–99

    CAS  Article  Google 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 21:351–358

    Article  Google 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, p146–147

    Google Scholar 

  43. 43.

    Food Standards Australia New Zealand (2011) Pregnancy and healthy eating. http://www.foodstandards.gov.au/consumer/generalissues/pregnancy/pages/default.aspx

  44. 44.

    Williamson CS (2006) Nutrition in pregnancy. Br Nutr Found Nutr Bull 31:28–59

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Maira Bes-Rastrollo.

Ethics declarations

Conflict of interest

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Marí-Sanchis, A., Díaz-Jurado, G., Basterra-Gortari, F.J. et al. Association between pre-pregnancy consumption of meat, iron intake, and the risk of gestational diabetes: the SUN project. Eur J Nutr 57, 939–949 (2018). https://doi.org/10.1007/s00394-017-1377-3

Download citation

Keywords

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