Dietary antioxidant capacity and risk of type 2 diabetes in the large prospective E3N-EPIC cohort

  • Francesca Romana Mancini
  • Aurélie Affret
  • Courtney Dow
  • Beverley Balkau
  • Fabrice Bonnet
  • Marie-Christine Boutron-Ruault
  • Guy Fagherazzi
Article

Abstract

Aims/hypothesis

Recent evidence suggests that oxidative stress may contribute to the pathogenesis of type 2 diabetes. The diet, and especially fruit and vegetables, contains a variety of compounds with antioxidant activity, which may have cumulative/synergistic antioxidant effects. The total antioxidant capacity, an index derived from dietary intake, is a single estimate of antioxidant capacity from all dietary antioxidants. The main aim of this study was to investigate the relationship between total antioxidant capacity and risk of type 2 diabetes.

Methods

Among 64,223 women (mean age 52 ± 7 years) from the French E3N-European Prospective Investigation into Cancer and Nutrition (EPIC) cohort, 1751 women had validated type 2 diabetes during 15 years of follow-up. The total antioxidant capacity was estimated with the ferric ion-reducing antioxidant power (FRAP) method. Adjusted Cox proportional hazards regression models were used to calculate HRs and 95% CIs for the associations between total antioxidant capacity and type 2 diabetes risk, adjusted for potential confounders.

Results

In multivariable models, higher levels of total antioxidant capacity were associated with a lower risk of type 2 diabetes. Compared with women in the lowest quintile, women in the third, fourth and fifth quintiles for total antioxidant capacity had HRs of 0.74 (95% CI 0.63, 0.86), 0.70 (95% CI 0.59, 0.83) and 0.73 (95% CI 0.60, 0.89), respectively. The inverse association between total antioxidant capacity and risk of type 2 diabetes was linear up to values of 15 mmol/day, after which the effect reached a plateau.

Conclusions/interpretation

Our findings suggest that the total antioxidant capacity may play an important role in reducing the risk of type 2 diabetes in middle-aged women. More studies are warranted to better understand the biological mechanisms underlying this inverse association.

Keywords

Diet E3N cohort FRAP (ferric ion-reducing antioxidant potential) Risk Total antioxidant capacity Type 2 diabetes 

Abbreviations

EPIC

European Prospective Investigation into Cancer and Nutrition

FRAP

Ferric ion-reducing antioxidant power

MET

Metabolic equivalents

TRAP

Total radical-trapping antioxidant parameter

Supplementary material

125_2017_4489_MOESM1_ESM.pdf (138 kb)
ESM Table 1(PDF 137 kb)

References

  1. 1.
    American Diabetes Association (2009) Diagnosis and classification of diabetes mellitus. Diabetes Care 32(Suppl 1):S62–S67CrossRefPubMedCentralGoogle Scholar
  2. 2.
    Ardisson Korat AV, Willett WC, Hu FB (2014) Diet, lifestyle, and genetic risk factors for type 2 diabetes: a review from the Nurses’ Health Study, Nurses’ Health Study 2, and Health Professionals’ Follow-up Study. Curr Nutr Rep 3:345–354CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Maritim AC, Sanders RA, Watkins JB 3rd (2003) Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol 17:24–38CrossRefPubMedGoogle Scholar
  4. 4.
    Asmat U, Abad K, Ismail K (2016) Diabetes mellitus and oxidative stress—a concise review. Saudi Pharm J 24:547–553CrossRefPubMedGoogle Scholar
  5. 5.
    Ceriello A (2000) Oxidative stress and glycemic regulation. Metabolism 49(Suppl 1):27–29CrossRefPubMedGoogle Scholar
  6. 6.
    Dakhale GN, Chaudhari HV, Shrivastava M (2016) Supplementation of vitamin C reduces blood glucose and improves glycosylated hemoglobin in type 2 diabetes mellitus: a randomized, double-blind study. Saudi Pharm J 24:547–553CrossRefGoogle Scholar
  7. 7.
    Manning PJ, Sutherland WH, Walker RJ et al (2004) Effect of high-dose vitamin E on insulin resistance and associated parameters in overweight subjects. Diabetes Care 27:2166–2171CrossRefPubMedGoogle Scholar
  8. 8.
    Rani AJ, Mythili SV (2014) Status in relation to oxidative stress in type 2 diabetes mellitus. J Clin Diagn Res 8:108–110CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Qureshi SA, Lund AC, Veierød MB et al (2014) Food items contributing most to variation in antioxidant intake; a cross-sectional study among Norwegian women. BMC Public Health 14:45CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Urquiza-Martínez MV, Fenton NB (2016) Antioxidant capacity of food. Free Radicals Antioxid 6:1CrossRefGoogle Scholar
  11. 11.
    Carlsen M, Halvorsen BL, Holte K et al (2010) The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J 9:3CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Brighenti F, Valtuena S, Pellegrini N et al (2005) Total antioxidant capacity of the diet is inversely and independently related to plasma concentration of high-sensitivity C-reactive protein in adult Italian subjects. Br J Nutr 93:619–625CrossRefPubMedGoogle Scholar
  13. 13.
    Serafini M, Bellocco R, Wolk A, Ekström AM (2002) Total antioxidant potential of fruit and vegetables and risk of gastric cancer. Gastroenterology 123:985–991CrossRefPubMedGoogle Scholar
  14. 14.
    Del Rio D, Agnoli C, Pellegrini N et al (2011) Total antioxidant capacity of the diet is associated with lower risk of ischemic stroke in a large Italian cohort. J Nutr 141:118–123CrossRefPubMedGoogle Scholar
  15. 15.
    Bastide N, Dartois L, Dyevre V et al (2016) Dietary antioxidant capacity and all-cause and cause-specific mortality in the E3N-EPIC/EPIC cohort study. Eur J Nutr 56:1233–1243CrossRefPubMedGoogle Scholar
  16. 16.
    Kim K, Vance TM, Chun OK (2016) Greater Total antioxidant capacity from diet and supplements is associated with a less atherogenic blood profile in U.S. adults. Nutrients 8:15CrossRefPubMedCentralGoogle Scholar
  17. 17.
    Rautiainen S, Lindblad BE, Morgenstern R, Wolk A (2014) Total antioxidant capacity of the diet and risk of age-related cataract: a population-based prospective cohort of women. JAMA Ophthalmol 132:247–252CrossRefPubMedGoogle Scholar
  18. 18.
    Clavel-Chapelon F, van Liere MJ, Giubout C et al (1997) E3N-EPIC, a French cohort study on cancer risk factors. E3N-EPIC Group. Etude Epidemiologique aupres de femmes de l’Education Nationale. Eur J Cancer Prev 6:473–478CrossRefPubMedGoogle Scholar
  19. 19.
    Clavel-Chapelon F, E3N Study Group (2015 Jun) Cohort profile: the French E3N cohort study. Int J Epidemiol 44:801–809CrossRefPubMedGoogle Scholar
  20. 20.
    Consortium IA, Langenberg C, Sharp S et al (2011) Design and cohort description of the InterAct Project: an examination of the interaction of genetic and lifestyle factors on the incidence of type 2 diabetes in the EPIC Study. Diabetologia 54:2272–2282CrossRefGoogle Scholar
  21. 21.
    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–S136CrossRefPubMedGoogle Scholar
  22. 22.
    Agence Nationale de Securit_e Sanitaire (ANSES) [Internet]. Table de composition nutritionnelle des aliments Ciqual; 2013. Available from: www.ansespro.fr/TableCIQUAL/. Accessed 12 December 2016
  23. 23.
    Pellegrini N, Serafini M, Salvatore S, Del RD, Bianchi M, Brighenti F (2006) Total antioxidant capacity of spices, dried fruits, nuts, pulses, cereals and sweets consumed in Italy assessed by three different in vitro assays. Mol Nutr Food Res 50:1030–1038CrossRefPubMedGoogle Scholar
  24. 24.
    Pellegrini N, Serafini M, Colombi B et al (2003) Total antioxidant capacity of plant foods, beverages and oils consumed in Italy assessed by three different in vitro assays. J Nutr 133:2812–2819PubMedGoogle Scholar
  25. 25.
    Serafini M, Jakszyn P, Luján-Barroso L et al (2012) Dietary total antioxidant capacity and gastric cancer risk in the European prospective investigation into cancer and nutrition study. Int J Cancer 15:131:E544-554Google Scholar
  26. 26.
    Priftis A, Stagos D, Konstantinopoulos K et al (2015) Comparison of antioxidant activity between green and roasted coffee beans using molecular methods. Mol Med Rep 12:7293–7302CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Thorpe MG, Milte CM, Crawford D, McNaughton SA (2016) A comparison of the dietary patterns derived by principal component analysis and cluster analysis in older Australians. Int J Behav Nutr Phys Act 13:30CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Bahadoran Z, Golzarand M, Mirmiran P, Shiva N, Azizi F (2012) Dietary total antioxidant capacity and the occurrence of metabolic syndrome and its components after a 3-year follow-up in adults: Tehran Lipid and Glucose Study. Nutr Metab (Lond) 9:70CrossRefGoogle Scholar
  29. 29.
    Hermsdorff HH, Puchau B, Volp AC et al (2011) Dietary total antioxidant capacity is inversely related to central adiposity as well as to metabolic and oxidative stress markers in healthy young adults. Nutr Metab (Lond) 8:59CrossRefGoogle Scholar
  30. 30.
    Montonen J, Knekt P, Jarvinen R, Reunanen A (2004) Dietary antioxidant intake and risk of type 2 diabetes. Diabetes Care 27:362–366CrossRefPubMedGoogle Scholar
  31. 31.
    Song Y, Manson JE, Buring JE, Sesso HD, Liu S (2005) Associations of dietary flavonoids with risk of type 2 diabetes, and markers of insulin resistance and systemic inflammation in women: a prospective study and cross-sectional analysis. J Am Coll Nutr 24:376–384CrossRefPubMedGoogle Scholar
  32. 32.
    Nettleton JA, Harnack LJ, Scrafford CG, Mink PJ, Barraj LM, Jacobs DR Jr (2006) Dietary flavonoids and flavonoid-rich foods are not associated with risk of type 2 diabetes in postmenopausal women. J Nutr 136:3039–3045PubMedPubMedCentralGoogle Scholar
  33. 33.
    Knekt P, Kumpulainen J, Jarvinen R et al (2002) Flavonoid intake and risk of chronic diseases. Am J Clin Nutr 76:560–568PubMedGoogle Scholar
  34. 34.
    Wang L, Liu S, Manson JE, Gaziano JM, Buring JE, Sesso HD (2006) The consumption of lycopene and tomato-based food products is not associated with the risk of type 2 diabetes in women. J Nutr 136:620–625PubMedGoogle Scholar
  35. 35.
    Li M, Fan Y, Zhang X, Hou W, Tang Z (2014) Fruit and vegetable intake and risk of type 2 diabetes mellitus: meta-analysis of prospective cohort studies. BMJ Open 4:e005497CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Yang WS, Wang WY, Fan WY, Deng Q, Wang X (2014) Tea consumption and risk of type 2 diabetes: a dose-response meta-analysis of cohort studies. Br J Nutr 111:1329–1339CrossRefPubMedGoogle Scholar
  37. 37.
    Carlsson S, Hammar N, Grill V (2005) Alcohol consumption and type 2 diabetes meta-analysis of epidemiological studies indicates a U-shaped relationship. Diabetologia 48:1051–1054CrossRefPubMedGoogle Scholar
  38. 38.
    Zenebe W, Pechánová O, Bernátová I (2001) Protective effects of red wine polyphenolic compounds on the cardiovascular system. Exp Clin Cardiol 6:153–158PubMedPubMedCentralGoogle Scholar
  39. 39.
    Arranz S, Chiva-Blanch G, Valderas-Martínez P, Medina-Remón A, Lamuela-Raventós RM, Estruch R (2012) Wine, beer, alcohol and polyphenols on cardiovascular disease and cancer. Nutrients 4:759–781CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Howard AA, Arnsten JH, Gourevitch MN (2004) Effect of alcohol consumption on diabetes mellitus: a systematic review. Ann Intern Med 140:211–219CrossRefPubMedGoogle Scholar
  41. 41.
    Hodge AM, English DR, O’Dea K, Giles GG (2006) Alcohol intake, consumption pattern and beverage type, and the risk of type 2 diabetes. Diabet Med 23:690–697CrossRefPubMedGoogle Scholar
  42. 42.
    Sartorelli DS, Fagherazzi G, Balkau B et al (2010) Differential effects of coffee on the risk of type 2 diabetes according to meal consumption in a French cohort of women: the E3N-EPIC/EPIC cohort study. Am J Clin Nutr 91:1002–1012CrossRefPubMedGoogle Scholar
  43. 43.
    van Dam RM, Willett WC, Manson JE, Hu FB (2006) Coffee, caffeine, and risk of type 2 diabetes: a prospective cohort study in younger and middle-aged U.S. women. Diabetes Care 29:398–403CrossRefPubMedGoogle Scholar
  44. 44.
    Cao G, Booth SL, Sadowski JA, Prior RL (1998) Increases in human plasma antioxidant capacity after consumption of controlled diets high in fruit and vegetables. Am J Clin Nutr 68:1081–1087PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Francesca Romana Mancini
    • 1
  • Aurélie Affret
    • 1
  • Courtney Dow
    • 1
  • Beverley Balkau
    • 2
  • Fabrice Bonnet
    • 1
    • 3
  • Marie-Christine Boutron-Ruault
    • 1
  • Guy Fagherazzi
    • 1
  1. 1.Inserm U1018, Centre for Research in Epidemiology and Population Health (CESP) ‘Health across Generations’ Team, University Paris-Saclay, University Paris-Sud, Gustave Roussy, Espace Maurice TubianaVillejuif CedexFrance
  2. 2.Inserm U1018, Centre for Research in Epidemiology and Population Health (CESP) ‘Renal and cardiovascular Epidemiology’ Team, University Versailles, Saint Quentin, University Paris-SudVillejuifFrance
  3. 3.CHU Rennes, Université de Rennes 1, Department of Endocrinology, Diabetology and NutritionRennesFrance

Personalised recommendations