, Volume 62, Issue 12, pp 2222–2232 | Cite as

Dietary inflammatory index and type 2 diabetes risk in a prospective cohort of 70,991 women followed for 20 years: the mediating role of BMI

  • Nasser Laouali
  • Francesca Romana Mancini
  • Mariem Hajji-Louati
  • Douae El Fatouhi
  • Beverley Balkau
  • Marie-Christine Boutron-Ruault
  • Fabrice Bonnet
  • Guy FagherazziEmail author



Diet is one of the main lifestyle-related factors that can modulate the inflammatory process. Surprisingly the dietary inflammatory index (DII) has been little investigated in relation to type 2 diabetes, and the role of BMI in this relationship is not well established. We studied this association and the role of BMI in the inflammatory process in a large population-based observational study.


A total of 70,991 women from the E3N (Etude Epidémiologique auprès de femmes de la Mutuelle Générale de l’Education Nationale) cohort study were followed for 20 years. Incident type 2 diabetes cases were identified using diabetes-specific questionnaires and drug reimbursement insurance databases, and 3292 incident cases were validated. The DII was derived from a validated food frequency questionnaire. Multivariable Cox regression models estimated HRs and 95% CIs between DII and incident type 2 diabetes. Interactions were tested between DII and BMI on incident type 2 diabetes and a mediation analysis of BMI was performed.


Higher DII scores, corresponding to a higher anti-inflammatory potential of the diet, were associated with a lower risk of type 2 diabetes. Compared with the 1st quintile group, women from the 2nd quintile group (HR 0.85 [95% CI 0.77, 0.94]) up to the 5th quintile group (HR 0.77 [95% CI 0.69, 0.85]) had a lower risk of type 2 diabetes before adjustment for BMI. There was an interaction between DII and BMI on type 2 diabetes risk (pInteraction < 0.0001). The overall association was partly mediated by BMI (58%).


Our findings suggest that a higher anti-inflammatory potential of the diet is associated with a lower risk of type 2 diabetes, and the association may be mediated by BMI. These results may improve our understanding of the mechanisms underlying the role of diet-related anti-inflammation in the pathogenesis of type 2 diabetes in women. Further studies are warranted to validate our results and evaluate whether the results are similar in men.


BMI, Body mass index Cohort Diet inflammation Mediation analysis Prevention Risk Type 2 diabetes 



Adapted dietary inflammatory index


Controlled direct effect


Dietary inflammatory index


Etude Epidémiologique auprès de femmes de la Mutuelle Générale de l’Education Nationale


Natural direct effect


Natural indirect effect



The authors are indebted to all participants for their continued participation. They are also grateful to all members of the E3N study group.

Contribution statement

NL, FRM and GF conceived and designed the study. NL and GF performed the statistical analysis. NL and FRM drafted the original manuscript. All authors contributed to the interpretation of data discussed in the manuscript, revised the manuscript and approved its final version to be published. GF is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.


This work was supported by a grant for the E4N study project by the Agence Nationale de Recherche (ANR-10-COHO-0006 grant) and by a grant for the Nutriperso Project (IDEX Paris Saclay).

Duality of interest

The authors declare that there is no duality of interest associated with this manuscript.

Supplementary material

125_2019_4972_MOESM1_ESM.pdf (297 kb)
ESM (PDF 297 kb)


  1. 1.
    International Diabetes Federation (2015) IDF Diabetes Atlas, 7th edn. Brussels, Belgium, IDFGoogle Scholar
  2. 2.
    Cho NH, Shaw JE, Karuranga S et al (2018) IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281. CrossRefPubMedGoogle Scholar
  3. 3.
    Hu FB, Meigs JB, Li TY, Rifai N, Manson JE (2004) Inflammatory markers and risk of developing type 2 diabetes in women. Diabetes 53(3):693–700. CrossRefPubMedGoogle Scholar
  4. 4.
    Shoelson SE, Lee J, Goldfine AB (2006) Inflammation and insulin resistance. J Clin Invest 116(7):1793–1801. CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Duncan BB, Schmidt MI, Pankow JS et al (2003) Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes 52(7):1799–1805. CrossRefPubMedGoogle Scholar
  6. 6.
    Kang D-H, Rice M, Park N-J, Turner-Henson A, Downs C (2010) Stress and inflammation: a biobehavioral approach for nursing research. West J Nurs Res 32(6):730–760. CrossRefPubMedGoogle Scholar
  7. 7.
    Smidowicz A, Regula J (2015) Effect of nutritional status and dietary patterns on human serum C-reactive protein and interleukin-6 concentrations. Adv Nutr 6(6):738–747. CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Minihane AM, Vinoy S, Russell WR et al (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114(7):999–1012. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Nowlin SY, Hammer MJ, Melkus GD (2012) Diet, inflammation, and glycemic control in type 2 diabetes: an integrative review of the literature. J Nutr Metab 2012:1–21. CrossRefGoogle Scholar
  10. 10.
    Cavicchia PP, Steck SE, Hurley TG et al (2009) A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr 139(12):2365–2372. CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Shivappa N, Steck SE, Hurley TG, Hussey JR, Hébert JR (2014) Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr 17(8):1689–1696. CrossRefPubMedGoogle Scholar
  12. 12.
    van Woudenbergh GJ, Theofylaktopoulou D, Kuijsten A et al (2013) Adapted dietary inflammatory index and its association with a summary score for low-grade inflammation and markers of glucose metabolism: the Cohort study on Diabetes and Atherosclerosis Maastricht (CODAM) and the Hoorn study. Am J Clin Nutr 98(6):1533–1542. CrossRefPubMedGoogle Scholar
  13. 13.
    Vahid F, Shivappa N, Karamati M, Naeini AJ, Hebert JR, Davoodi SH (2017) Association between Dietary Inflammatory Index (DII) and risk of prediabetes: a case-control study. Appl Physiol Nutr Metab 42(4):399–404. CrossRefPubMedGoogle Scholar
  14. 14.
    Moslehi N, Ehsani B, Mirmiran P et al (2016) Inflammatory properties of diet and glucose-insulin homeostasis in a cohort of Iranian adults. Nutrients 8(11):735. CrossRefPubMedCentralGoogle Scholar
  15. 15.
    Denova-Gutiérrez E, Muñoz-Aguirre P, Shivappa N et al (2018) Dietary inflammatory index and type 2 diabetes mellitus in adults: the Diabetes Mellitus Survey of Mexico City. Nutrients 10(4). CrossRefGoogle Scholar
  16. 16.
    Clavel-Chapelon F, for the E3N Study Group (2014) Cohort profile: the French E3N Cohort Study. Int J Epidemiol 44(3):801–809CrossRefGoogle Scholar
  17. 17.
    van Liere MJ, Lucas F, Clavel F, Slimani N, Villeminot S (1997) Relative validity and reproducibility of a French dietary history questionnaire. Int J Epidemiol 26(Suppl 1):S128–S136. CrossRefPubMedGoogle Scholar
  18. 18.
    de Securite Sanitaire (ANSES) AN (2013) Table de composition nutritionnelle des aliments Ciqual. Accessed 12 Dec 2016
  19. 19.
    Fagherazzi G, Vilier A, Lajous M et al (2014) Wine consumption throughout life is inversely associated with type 2 diabetes risk, but only in overweight individuals: results from a large female French cohort study. Eur J Epidemiol 29(11):831–839. CrossRefPubMedGoogle Scholar
  20. 20.
    Mancini FR, Rajaobelina K, Praud D et al (2018) Nonlinear associations between dietary exposures to perfluorooctanoic acid (PFOA) or perfluorooctane sulfonate (PFOS) and type 2 diabetes risk in women: findings from the E3N cohort study. Int J Hyg Environ Health 221(7):1054–1060. CrossRefPubMedGoogle Scholar
  21. 21.
    Mancini FR, Affret A, Dow C et al (2018) Dietary antioxidant capacity and risk of type 2 diabetes in the large prospective E3N-EPIC cohort. Diabetologia 61(2):308–316. CrossRefPubMedGoogle Scholar
  22. 22.
    Mancini FR, Dow C, Affret A et al (2018) Micronutrient dietary patterns associated with type 2 diabetes mellitus among women of the E3N-EPIC (Etude Epidémiologique auprès de femmes de l’Education Nationale) cohort study. J Diabetes 10(8):665–674. CrossRefPubMedGoogle Scholar
  23. 23.
    Harrell FE (2013) Regression modeling strategies: with applications to linear models, logistic regression, and survival analysis. Springer Science & Business Media, New YorkGoogle Scholar
  24. 24.
    Valeri L, Vanderweele TJ (2013) Mediation analysis allowing for exposure-mediator interactions and causal interpretation: theoretical assumptions and implementation with SAS and SPSS macros. Psychol Methods 18(2):137–150. CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Ikram MA, Arfan Ikram M, VanderWeele TJ (2015) A proposed clinical and biological interpretation of mediated interaction. Eur J Epidemiol 30(10):1115–1118. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Valeri L, VanderWeele TJ (2015) SAS macro for causal mediation analysis with survival data. Epidemiology 26(2):e23–e24. CrossRefPubMedGoogle Scholar
  27. 27.
    VanderWeele T (2015) Explanation in causal inference: methods for mediation and interaction. Oxford University Press, New YorkGoogle Scholar
  28. 28.
    Trichopoulou A, Naska A, DAFNE III Group (2003) European food availability databank based on household budget surveys: the Data Food Networking initiative. Eur J Pub Health 13(3 Suppl):24–28. CrossRefGoogle Scholar
  29. 29.
    Neufcourt L, Assmann KE, Fezeu LK et al (2016) Prospective Association Between the Dietary Inflammatory Index and Cardiovascular Diseases in the SUpplémentation en VItamines et Minéraux AntioXydants (SU.VI.MAX) Cohort. J Am Heart Assoc 5(3):e002735CrossRefGoogle Scholar
  30. 30.
    Ma Y, Hébert JR, Li W et al (2008) Association between dietary fiber and markers of systemic inflammation in the Women’s Health Initiative Observational Study. Nutrition 24(10):941–949. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Liu S, Stampfer MJ, Hu FB et al (1999) Whole-grain consumption and risk of coronary heart disease: results from the Nurses’ Health Study. Am J Clin Nutr 70(3):412–419. CrossRefPubMedGoogle Scholar
  32. 32.
    InterAct Consortium, Romaguera D, Guevara M et al (2011) Mediterranean diet and type 2 diabetes risk in the European Prospective Investigation into Cancer and Nutrition (EPIC) study: the InterAct project. Diabetes Care 34(9):1913–1918. CrossRefGoogle Scholar
  33. 33.
    Phillips CM, Shivappa N, Hébert JR, Perry IJ (2018) Dietary inflammatory index and biomarkers of lipoprotein metabolism, inflammation and glucose homeostasis in adults. Nutrients 10(8). CrossRefGoogle Scholar
  34. 34.
    Kim Y, Chen J, Wirth MD, Shivappa N, Hebert JR (2018) Lower dietary inflammatory index scores are associated with lower glycemic index scores among college students. Nutrients 10(2). CrossRefGoogle Scholar
  35. 35.
    Farhangi MA, Najafi M (2018) Dietary inflammatory index: a potent association with cardiovascular risk factors among patients candidate for coronary artery bypass grafting (CABG) surgery. Nutr J 17(1).
  36. 36.
    Schulze MB, Hoffmann K, Manson JE et al (2005) Dietary pattern, inflammation, and incidence of type 2 diabetes in women. Am J Clin Nutr 82(3):675–684; quiz 714–5. CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Alkerwi A‘a, Shivappa N, Crichton G, Hébert JR (2014) No significant independent relationships with cardiometabolic biomarkers were detected in the Observation of Cardiovascular Risk Factors in Luxembourg study population. Nutr Res 34(12):1058–1065. CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Pollack RM, Donath MY, Leroith D, Leibowitz G (2016) Anti-inflammatory agents in the treatment of diabetes and its vascular complications. Diabetes Care 39(Supplement 2):S244–S252. CrossRefPubMedGoogle Scholar
  39. 39.
    Bouche C, Rizkalla SW, Luo J et al (2002) Five-week, low-glycemic index diet decreases total fat mass and improves plasma lipid profile in moderately overweight nondiabetic men. Diabetes Care 25(5):822–828. CrossRefPubMedGoogle Scholar
  40. 40.
    Neuhouser ML, Schwarz Y, Wang C et al (2011) A low-glycemic load diet reduces serum C-reactive protein and modestly increases adiponectin in overweight and obese adults. J Nutr 142(2):369–374. CrossRefGoogle Scholar
  41. 41.
    Joslowski G, Halim J, Goletzke J et al (2015) Dietary glycemic load, insulin load, and weight loss in obese, insulin resistant adolescents: RESIST study. Clin Nutr 34(1):89–94. CrossRefPubMedGoogle Scholar
  42. 42.
    Kern PA, Saghizadeh M, Ong JM, Bosch RJ, Deem R, Simsolo RB (1995) The expression of tumor necrosis factor in human adipose tissue. Regulation by obesity, weight loss, and relationship to lipoprotein lipase. J Clin Investig 95(5):2111–2119. CrossRefPubMedGoogle Scholar
  43. 43.
    Awad AB, Bradford PG (2009) Adipose tissue and inflammation. CRC Press Taylor & Francis Group, Boca Raton. CrossRefGoogle Scholar
  44. 44.
    Pahlavani M, Ramalho T, Koboziev I et al (2017) Adipose tissue inflammation in insulin resistance: review of mechanisms mediating anti-inflammatory effects of omega-3 polyunsaturated fatty acids. J Investig Med 65(7):1021–1027. CrossRefPubMedGoogle Scholar
  45. 45.
    Jayarathne S, Koboziev I, Park O-H, Oldewage-Theron W, Shen C-L, Moustaid-Moussa N (2017) Anti-inflammatory and anti-obesity properties of food bioactive components : effects on adipose tissue. Prev Nutr Food Sci 22(4):251–262. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Nasser Laouali
    • 1
    • 2
  • Francesca Romana Mancini
    • 1
    • 2
  • Mariem Hajji-Louati
    • 1
    • 2
  • Douae El Fatouhi
    • 1
    • 2
  • Beverley Balkau
    • 1
    • 2
  • Marie-Christine Boutron-Ruault
    • 1
    • 2
  • Fabrice Bonnet
    • 3
  • Guy Fagherazzi
    • 1
    • 2
    • 4
    Email author
  1. 1.Centre for Research in Epidemiology and Population Health (CESP), Inserm (Institut National de la Santé et de la Recherche Médicale) U1018, Generations and Health Across GenerationsGustave Roussy InstituteVillejuif CedexFrance
  2. 2.Faculte de MedecineUPS-UVSQ-Paris-Saclay UniversityLe Kremlin-BicêtreFrance
  3. 3.Service d’EndocrinologieGroupe Hospitalier Paris St-JosephParisFrance
  4. 4.Department of Population HealthLuxembourg Institute of Health (LIH)StrassenLuxembourg

Personalised recommendations