Skip to main content

Dietary antioxidant capacity and all-cause and cause-specific mortality in the E3N/EPIC cohort study

European Journal of Nutrition volume 56, pages 1233–1243 (2017)Cite this article

Abstract

Purpose

The cellular oxidative stress (balance between pro-oxidant and antioxidant) may be a major risk factor for chronic diseases. Antioxidant capacity of human diet can be globally assessed through the dietary non-enzymatic antioxidant capacity (NEAC). Our aim was to investigate the relationship between the NEAC and all-cause and cause-specific mortality, and to test potential interactions with smoking status, a well-known pro-oxidant factor.

Methods

Among the French women of the E3N prospective cohort study initiated in 1990, including 4619 deaths among 1,199,011 persons-years of follow-up. A validated dietary history questionnaire assessed usual food intake; NEAC intake was estimated using a food composition table from two different methods: ferric ion reducing antioxidant power (FRAP) and total radical-trapping antioxidant parameter (TRAP). Hazard ratio (HR) estimates and 95 % confidence intervals (CI) were derived from Cox proportional hazards regression models.

Results

In multivariate analyses, FRAP dietary equivalent intake was inversely associated with mortality from all-causes (HR for the fourth vs. the first quartile: HR4 = 0.75, 95 % CI 0.67, 0.83, p trend < 0.0001), cancer, and cardiovascular diseases. Similar results were obtained with TRAP. There was an interaction between NEAC dietary equivalent intake and smoking status for all-cause and cardiovascular disease mortality, but not cancer mortality (respectively, for FRAP, p inter = 0.002; 0.013; 0.113, results were similar with TRAP), and the association was the strongest among current smokers.

Conclusion

This prospective cohort study highlights the importance of antioxidant consumption for mortality prevention, especially among current smokers.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1

Abbreviations

NEAC:

Non-enzymatic antioxidant capacity

FRAP:

Ferric ion reducing antioxidant power

HAT:

Hydrogen atom transfer

SET:

Single electron transfer

TRAP:

Total radical-trapping antioxidant parameter

References

  1. Wang X, Ouyang Y, Liu J, Zhu M, Zhao G, Bao W et al (2014) Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies. BMJ 349:g4490

    Article  Google Scholar 

  2. Leenders M, Sluijs I, Ros MM, Boshuizen HC, Siersema PD, Ferrari P et al (2013) Fruit and vegetable consumption and mortality: European prospective investigation into cancer and nutrition. Am J Epidemiol 178(4):590–602

    Article  Google Scholar 

  3. Pellegrini N, Serafini M, Colombi B, Del RD, Salvatore S, Bianchi M 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(9):2812–2819

    CAS  Google Scholar 

  4. 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(11):1030–1038

    Article  CAS  Google Scholar 

  5. Serafini M, Del RD (2004) Understanding the association between dietary antioxidants, redox status and disease: is the total antioxidant capacity the right tool? Redox Rep 9(3):145–152

    Article  CAS  Google Scholar 

  6. Serafini M, Villano D, Spera G, Pellegrini N (2006) Redox molecules and cancer prevention: the importance of understanding the role of the antioxidant network. Nutr Cancer 56(2):232–240

    Article  CAS  Google Scholar 

  7. Rautiainen S, Serafini M, Morgenstern R, Prior RL, Wolk A (2008) The validity and reproducibility of food-frequency questionnaire-based total antioxidant capacity estimates in Swedish women. Am J Clin Nutr 87(5):1247–1253

    CAS  Google Scholar 

  8. Gulcin I (2012) Antioxidant activity of food constituents: an overview. Arch Toxicol 86(3):345–391

    Article  Google Scholar 

  9. Magalhaes LM, Segundo MA, Reis S, Lima JL (2008) Methodological aspects about in vitro evaluation of antioxidant properties. Anal Chim Acta 613(1):1–19

    Article  CAS  Google Scholar 

  10. Pantavos A, Ruiter R, Feskens EF, de Keyser CE, Hofman A, Stricker BH et al (2015) Total dietary antioxidant capacity, individual antioxidant intake and breast cancer risk: the Rotterdam study. Int J Cancer 136(9):2178–2186

    Article  CAS  Google Scholar 

  11. Serafini M, Bellocco R, Wolk A, Ekstrom AM (2002) Total antioxidant potential of fruit and vegetables and risk of gastric cancer. Gastroenterology 123(4):985–991

    Article  CAS  Google Scholar 

  12. Serafini M, Jakszyn P, Lujan-Barroso L, Agudo A, Bas Bueno-de-Mesquita H, van Duijnhoven FJ et al (2012) Dietary total antioxidant capacity and gastric cancer risk in the European prospective investigation into cancer and nutrition study. Int J Cancer 131(4):E544–E554

    Article  CAS  Google Scholar 

  13. La Vecchia C, Decarli A, Serafini M, Parpinel M, Bellocco R, Galeone C et al (2013) Dietary total antioxidant capacity and colorectal cancer: a large case-control study in Italy. Int J Cancer 133(6):1447–1451

    Article  CAS  Google Scholar 

  14. Mekary RA, Wu K, Giovannucci E, Sampson L, Fuchs C, Spiegelman D et al (2010) Total antioxidant capacity intake and colorectal cancer risk in the Health Professionals Follow-up Study. Cancer Causes Control 21(8):1315–1321

    Article  Google Scholar 

  15. Zamora-Ros R, Fedirko V, Trichopoulou A, Gonzalez CA, Bamia C, Trepo E et al (2013) Dietary flavonoid, lignan and antioxidant capacity and risk of hepatocellular carcinoma in the European prospective investigation into cancer and nutrition study. Int J Cancer 133(10):2429–2443

    Article  CAS  Google Scholar 

  16. Praud D, Parpinel M, Serafini M, Bellocco R, Tavani A, Lagiou P et al (2015) Non-enzymatic antioxidant capacity and risk of gastric cancer. Cancer Epidemiol 39(3):340–345

    Article  Google Scholar 

  17. Del RD, Agnoli C, Pellegrini N, Krogh V, Brighenti F, Mazzeo T 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(1):118–123

    Article  Google Scholar 

  18. Rautiainen S, Larsson S, Virtamo J, Wolk A (2012) Total antioxidant capacity of diet and risk of stroke: a population-based prospective cohort of women. Stroke 43(2):335–340

    Article  CAS  Google Scholar 

  19. Rautiainen S, Levitan EB, Orsini N, Akesson A, Morgenstern R, Mittleman MA et al (2012) Total antioxidant capacity from diet and risk of myocardial infarction: a prospective cohort of women. Am J Med 125(10):974–980

    Article  CAS  Google Scholar 

  20. Rautiainen S, Levitan EB, Mittleman MA, Wolk A (2013) Total antioxidant capacity of diet and risk of heart failure: a population-based prospective cohort of women. Am J Med 126(6):494–500

    Article  Google Scholar 

  21. Agudo A, Cabrera L, Amiano P, Ardanaz E, Barricarte A, Berenguer T et al (2007) Fruit and vegetable intakes, dietary antioxidant nutrients, and total mortality in Spanish adults: findings from the Spanish cohort of the European Prospective Investigation into Cancer and Nutrition (EPIC-Spain). Am J Clin Nutr 85(6):1634–1642

    CAS  Google Scholar 

  22. Henriquez-Sanchez P, Sanchez-Villegas A, Ruano-Rodriguez C, Gea A, Lamuela-Raventos RM, Estruch R et al (2015) Dietary total antioxidant capacity and mortality in the PREDIMED study. Eur J Nutr 55(1):227–236

    Article  Google Scholar 

  23. Csordas A, Wick G, Laufer G, Bernhard D (2008) An evaluation of the clinical evidence on the role of inflammation and oxidative stress in smoking-mediated cardiovascular disease. Biomark Insights 3:127–139

    CAS  Google Scholar 

  24. Pappas RS (2011) Toxic elements in tobacco and in cigarette smoke: inflammation and sensitization. Metallomics 3(11):1181–1198

    Article  CAS  Google Scholar 

  25. Clavel-Chapelon F, van Liere MJ, Giubout C, Niravong MY, Goulard H, Le CC et al (1997) E3N, a French cohort study on cancer risk factors. E3N Group. Etude Epidemiologique aupres de femmes de l’Education Nationale. Eur J Cancer Prev 6(5):473–478

    Article  CAS  Google Scholar 

  26. Lucas F, Niravong M, Villeminot S, Kaaks R, Clavel-Chapelon F (1995) Estimation of food portion size using photographs: validity, strengths, weaknesses and recommendations. J Hum Nutr Diet 8(1):65–74

    Article  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. Freedman ND, Park Y, Abnet CC, Hollenbeck AR, Sinha R (2012) Association of coffee drinking with total and cause-specific mortality. N Engl J Med 366(20):1891–1904

    Article  CAS  Google Scholar 

  29. FAO/WHO/ONU (2001) Expert consultation. Food and nutrition technical report series. Human enegrgy requirements

Ref type: report

  1. Putter H, Fiocco M, Geskus RB (2007) Tutorial in biostatistics: competing risks and multi-state models. Stat Med 26(11):2389–2430

    Article  CAS  Google Scholar 

  2. Devore EE, Kang JH, Stampfer MJ, Grodstein F (2010) Total antioxidant capacity of diet in relation to cognitive function and decline. Am J Clin Nutr 92(5):1157–1164

    Article  CAS  Google Scholar 

  3. Devore EE, Feskens E, Ikram MA, den Tom HT, Vernooij M, van der Lijn F et al (2013) Total antioxidant capacity of the diet and major neurologic outcomes in older adults. Neurology 80(10):904–910

    Article  CAS  Google Scholar 

  4. Delgado-Andrade C, Morales FJ (2005) Unraveling the contribution of melanoidins to the antioxidant activity of coffee brews. J Agric Food Chem 53(5):1403–1407

    Article  CAS  Google Scholar 

  5. Morales FJ, Somoza V, Fogliano V (2012) Physiological relevance of dietary melanoidins. Amino Acids 42(4):1097–1109

    Article  CAS  Google Scholar 

  6. Holtan SG, O’Connor HM, Fredericksen ZS, Liebow M, Thompson CA, Macon WR et al (2012) Food-frequency questionnaire-based estimates of total antioxidant capacity and risk of non-Hodgkin lymphoma. Int J Cancer 131(5):1158–1168

    Article  CAS  Google Scholar 

  7. Valtuena S, Pellegrini N, Franzini L, Bianchi MA, Ardigo D, Del RD et al (2008) Food selection based on total antioxidant capacity can modify antioxidant intake, systemic inflammation, and liver function without altering markers of oxidative stress. Am J Clin Nutr 87(5):1290–1297

    CAS  Google Scholar 

  8. Stone WL, Krishnan K, Campbell SE, Palau VE (2014) The role of antioxidants and pro-oxidants in colon cancer. World J Gastrointest Oncol 6(3):55–66

    Google Scholar 

  9. Al-Awaida W, Akash M, Aburubaiha Z, Talib WH, Shehadeh H (2014) Chinese green tea consumption reduces oxidative stress, inflammation and tissues damage in smoke exposed rats. Iran J Basic Med Sci 17(10):740–746

    Google Scholar 

  10. Das A, Dey N, Ghosh A, Das S, Chattopadhyay DJ, Chatterjee IB (2012) Molecular and cellular mechanisms of cigarette smoke-induced myocardial injury: prevention by vitamin C. PLoS One 7(9):e44151

    Article  CAS  Google Scholar 

  11. Ambrose JA, Barua RS (2004) The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 43(10):1731–1737

    Article  CAS  Google Scholar 

  12. Del BC, Porrini M, Fracassetti D, Campolo J, Klimis-Zacas D, Riso P (2014) A single serving of blueberry (V. corymbosum) modulates peripheral arterial dysfunction induced by acute cigarette smoking in young volunteers: a randomized-controlled trial. Food Funct 5(12):3107–3116

    Article  Google Scholar 

  13. Karatzi K, Papamichael C, Karatzis E, Papaioannou TG, Voidonikola PT, Lekakis J et al (2007) Acute smoking induces endothelial dysfunction in healthy smokers. Is this reversible by red wine’s antioxidant constituents? J Am Coll Nutr 26(1):10–15

    Article  Google Scholar 

  14. Carlsen MH, Halvorsen BL, Holte K, Bohn SK, Dragland S, Sampson L et al (2010) The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J 9:3

    Article  Google Scholar 

Download references

Acknowledgments

The authors are indebted to all participants for providing the data used in the E3N Study and to practitioners for providing pathology reports. They are grateful to M. Fangon, L. Hoang and M. Niravong for their technical assistance, to S. Kangas for her assistance in the construction of non-enzymatic total antioxidant capacity data, to Jessica Pontary for data management of the mortality table, and to the E3N group. The references have been checked for accuracy and completeness by NB. MCBR will act as guarantor for the paper. This material has not been published previously in a substantively similar form. The authors declare that they have no conflict of interest.

Authors contribution

N.B. and M.C.B.R. designed research; N.B., V.D., and M.C.B.R. conducted research; V.D., L.Da., and M.S. contributed to construction of dietary and medical data; N.B., V.D., L.Da., and M.C.B.R. analyzed data; N.B. and M.C.B.R. wrote the paper; M.C.B.R. had primary responsibility for final content; V.D., L.Da., L.Do., G.F., and M.S. revised the article critically. All authors read and approved the final manuscript.

Grant support

The E3N cohort is being carried out with the financial support of the “Mutuelle Générale de l’Education Nationale” (MGEN); European Community; French League against Cancer (LNCC); Gustave Roussy Institute (IGR); French Institute of Health and Medical Research (INSERM). Nadia Bastide was supported by a Fondation de France post-doctoral fellowship.

Author information

Authors and Affiliations

  1. CESP, Team 9, UMR-S 1018: INSERM, Gustave Roussy, Université Paris-Sud, Espace Maurice Tubiana, 114 rue Edouard Vaillant, 94805, Villejuif Cedex, France

    Nadia Bastide, Laureen Dartois, Valérie Dyevre, Laure Dossus, Guy Fagherazzi & Marie-Christine Boutron-Ruault

  2. Functional Foods and Metabolic Stress Prevention Laboratory, Center of Nutrition, Council for Agricultural Research and Economics, Center of Food and Nutrition, Rome, Italy

    Mauro Serafini

Authors
  1. Nadia Bastide
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laureen Dartois
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valérie Dyevre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laure Dossus
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guy Fagherazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mauro Serafini
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marie-Christine Boutron-Ruault
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marie-Christine Boutron-Ruault.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflicts of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bastide, N., Dartois, L., Dyevre, V. et al. Dietary antioxidant capacity and all-cause and cause-specific mortality in the E3N/EPIC cohort study. Eur J Nutr 56, 1233–1243 (2017). https://doi.org/10.1007/s00394-016-1172-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-016-1172-6

Keywords

  • Non-enzymatic antioxidant capacity
  • FRAP
  • TRAP
  • All-cause and cause-specific mortality
  • E3N study