Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Carbohydrates, glycemic index and diabetes mellitus

The evaluation of inflammatory and oxidative stress biomarkers on coffee–diabetes association: results from the 10-year follow-up of the ATTICA Study (2002–2012)

European Journal of Clinical Nutrition volume 69, pages 1220–1225 (2015)Cite this article

Subjects

Abstract

Background/Objectives:

The purpose of this work was to investigate the association between coffee drinking and diabetes development and potential mediation by oxidative stress and inflammatory biomarkers.

Subjects/Methods:

In 2001–2002, a random sample of 1514 men (18–87 years old) and 1528 women (18–89 years old) were selected to participate in the ATTICA study (Athens metropolitan area, Greece). A validated food-frequency questionnaire was used to assess coffee drinking (abstention, casual, habitual) and other lifestyle and dietary factors. Evaluation of oxidative stress and inflammatory markers was also performed. During 2011–2012, the 10-year follow-up of the ATTICA study was carried out. The outcome of interest in this work was incidence of type 2 diabetes, defined according to American Diabetes Association criteria.

Results:

During follow-up, 191 incident cases of diabetes were documented (incidence 13.4% in men and 12.4% in women). After various adjustments, individuals who consumed ⩾250 ml of coffee (≈1.5cup) had 54% lower odds of developing diabetes (95% confidence interval: 0.24, 0.90), as compared with abstainers. A dose-response linear trend between coffee drinking and diabetes incidence was also observed (P for trend=0.017). When controlling for several oxidative stress and inflammatory biomarkers, the inverse association between habitual coffee drinking and diabetes was found to be mediated by serum amyloid-A levels.

Conclusions:

This work highlights the significance of long-term habitual coffee drinking against diabetes onset. The anti-inflammatory effect of several coffee components may be responsible for this protection.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

References

  1. International Diabetes FederationIDF Diabetes Atlas, 6th edn. Brussels 2013.

  2. Mursu J, Virtanen JK, Tuomainen TP, Nurmi T, Voutilainen S . Intake of fruit, berries, and vegetables and risk of type 2 diabetes in Finnish men: the Kuopio Ischaemic Heart Disease Risk Factor Study. Am J Clin Nutr 2014; 99: 328–333.

    Article  CAS  Google Scholar 

  3. Panagiotakos DB, Pitsavos C, Chrysohoou C, Kokkinos P, Toutouzas P, Stefanadis C . The J-shaped effect of coffee consumption on the risk of developing acute coronary syndromes: the CARDIO2000 case-control study. J Nutr 2003; 133: 3228–3232.

    Article  CAS  Google Scholar 

  4. Vlachopoulos C, Panagiotakos D, Ioakeimidis N, Dima I, Stefanadis C . Chronic coffee consumption has a detrimental effect on aortic stiffness and wave reflections. Am J Clin Nutr 2005; 81: 1307–1312.

    Article  CAS  Google Scholar 

  5. van Dam RM, Feskens EJ . Coffee consumption and risk of type 2 diabetes mellitus. Lancet 2002; 360: 1477–1478.

    Article  Google Scholar 

  6. Boggs DA, Rosenberg L, Ruiz-Narvaez EA, Palmer JR . Coffee, tea, and alcohol intake in relation to risk of type 2 diabetes in African American women. Am J Clin Nutr 2010; 92: 960–966.

    Article  CAS  Google Scholar 

  7. Saremi A, Tulloch-Reid M, Knowler WC . Coffee consumption and the incidence of type 2 diabetes. Diabetes Care 2003; 26: 2211–2212.

    Article  Google Scholar 

  8. Reunanen A, Heliovaara M, Aho K . Coffee consumption and risk of type 2 diabetes mellitus. Lancet 2003; 361: 702–703.

    Article  Google Scholar 

  9. van Dam RM, Hu FB . Coffee consumption and risk of type 2 diabetes: a systematic review. JAMA 2005; 294: 97–104.

    Article  CAS  Google Scholar 

  10. Jiang X, Zhang D, Jiang W . Coffee and caffeine intake and incidence of type 2 diabetes mellitus: a meta-analysis of prospective studies. Eur J Nutr 2013; 53: 25–38.

    Article  Google Scholar 

  11. Akash MS, Rehman K, Chen S . Effects of coffee on type 2 diabetes mellitus. Nutrition 2014; 30: 755–763.

    Article  CAS  Google Scholar 

  12. Evans JL, Goldfine ID, Maddux BA, Grodsky GM . Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction? Diabetes 2003; 52: 1–8.

    Article  CAS  Google Scholar 

  13. Anderson RA, Roussel AM, Zouari N, Mahjoub S, Matheau JM, Kerkeni A . Potential antioxidant effects of zinc and chromium supplementation in people with type 2 diabetes mellitus. J Am Coll Nutr 2001; 20: 212–218.

    Article  CAS  Google Scholar 

  14. Donath MY, Shoelson SE . Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 2011; 11: 98–107.

    Article  CAS  Google Scholar 

  15. Donath MY, Mandrup-Poulsen T . The use of interleukin-1-receptor antagonists in the treatment of diabetes mellitus. Nat Clin Pract Endocrinol Metab 2008; 4: 240–241.

    Article  CAS  Google Scholar 

  16. Natella F, Nardini M, Giannetti I, Dattilo C, Scaccini C . Coffee drinking influences plasma antioxidant capacity in humans. J Agric Food Chem 2002; 50: 6211–6216.

    Article  CAS  Google Scholar 

  17. Kempf K, Herder C, Erlund I, Kolb H, Martin S, Carstensen M et al. Effects of coffee consumption on subclinical inflammation and other risk factors for type 2 diabetes: a clinical trial. Am J Clin Nutr 2010; 91: 950–957.

    Article  CAS  Google Scholar 

  18. Jacobs S, Kroger J, Floegel A, Boeing H, Drogan D, Pischon T et al. Evaluation of various biomarkers as potential mediators of the association between coffee consumption and incident type 2 diabetes in the EPIC-Potsdam Study. Am J Clin Nutr 2014; 100: 891–900.

    Article  CAS  Google Scholar 

  19. Pitsavos C, Panagiotakos DB, Chrysohoou C, Stefanadis C . Epidemiology of cardiovascular risk factors in Greece: aims, design and baseline characteristics of the ATTICA study. BMC Public Health 2003; 3: 32.

    Article  Google Scholar 

  20. Papathanasiou G, Georgoudis G, Papandreou M, Spyropoulos P, Georgakopoulos D, Kalfakakou V et al. Reliability measures of the short International Physical Activity Questionnaire (IPAQ) in Greek young adults. Hellenic J Cardiol 2009; 50: 283–294.

    Google Scholar 

  21. Katsouyanni K, Rimm EB, Gnardellis C, Trichopoulos D, Polychronopoulos E, Trichopoulou A . Reproducibility and relative validity of an extensive semi-quantitative food frequency questionnaire using dietary records and biochemical markers among Greek schoolteachers. Int J Epidemiol 1997; 26 (Suppl 1), S118–S127.

    Article  Google Scholar 

  22. Panagiotakos DB, Pitsavos C, Stefanadis C . Dietary patterns: a Mediterranean diet score and its relation to clinical and biological markers of cardiovascular disease risk. Nutr Metab Cardiovasc Dis 2006; 16: 559–568.

    Article  Google Scholar 

  23. Bunker ML, McWilliams M . Caffeine content of common beverages. J Am Diet Assoc 1979; 74: 28–32.

    CAS  PubMed  Google Scholar 

  24. American Diabetes Association. Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 1997; 20: 1183–1197.

    Article  Google Scholar 

  25. Koloverou E, Panagiotakos D, Pitsavos C, Chrysohoou C, Georgousopoulou E, Pitaraki E et al. 10-year incidence of diabetes and associated risk factors in Greece: the ATTICA study (2002-2012). Rev Diabet Stud 2014; 11: 181–189.

    Article  Google Scholar 

  26. Carlsson S, Hammar N, Grill V, Kaprio J . Coffee consumption and risk of type 2 diabetes in Finnish twins. Int J Epidemiol 2004; 33: 616–617.

    Article  Google Scholar 

  27. Kotani K, Tsuzaki K, Sano Y, Maekawa M, Fujiwara S, Hamada T et al. The relationship between usual coffee consumption and serum C-reactive protein level in a Japanese female population. Clin Chem Lab Med 2008; 46: 1434–1437.

    CAS  Google Scholar 

  28. Lopez-Garcia E, van Dam RM, Qi L, Hu FB . Coffee consumption and markers of inflammation and endothelial dysfunction in healthy and diabetic women. Am J Clin Nutr 2006; 84: 888–893.

    Article  CAS  Google Scholar 

  29. Yamashita K, Yatsuya H, Muramatsu T, Toyoshima H, Murohara T, Tamakoshi K . Association of coffee consumption with serum adiponectin, leptin, inflammation and metabolic markers in Japanese workers: a cross-sectional study. Nutr Diabetes 2012; 2: e33.

    Article  CAS  Google Scholar 

  30. Pham NM, Wang Z, Morita M, Ohnaka K, Adachi M, Kawate H et al. Combined effects of coffee consumption and serum gamma-glutamyltransferase on serum C-reactive protein in middle-aged and elderly Japanese men and women. Clin Chem Lab Med 2011; 49: 1661–1667.

    Article  CAS  Google Scholar 

  31. Marzi C, Huth C, Herder C, Baumert J, Thorand B, Rathmann W et al. Acute-phase serum amyloid A protein and its implication in the development of type 2 diabetes in the KORA S4/F4 study. Diabetes Care 2013; 36: 1321–1326.

    Article  CAS  Google Scholar 

  32. Montonen J, Knekt P, Jarvinen R, Reunanen A . Dietary antioxidant intake and risk of type 2 diabetes. Diabetes Care 2004; 27: 362–366.

    Article  CAS  Google Scholar 

  33. Bohlscheid-Thomas S, Hoting I, Boeing H, Wahrendorf J . Reproducibility and relative validity of food group intake in a food frequency questionnaire developed for the German part of the EPIC project. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol 1997; 26 (Suppl 1), S59–S70.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the ATTICA study group of investigators Yannis Skoumas, Natassa Katinioti, Labros Papadimitriou, Constantina Masoura, Spiros Vellas, Yannis Lentzas, Manolis Kambaxis, Konstadina Palliou, Vassiliki Metaxa, Agathi Ntzouvani, Dimitris Mpougatsas, Nikolaos Skourlis, Christina Papanikolaou, Georgia-Maria Kouli, Aimilia Christou, Adella Zana, Maria Ntertimani, Aikaterini Kalogeropoulou, Evangelia Pitaraki, Alexandros Laskaris, Mihail Hatzigeorgiou and Athanasios Grekas for their assistance in the initial physical examination and follow-up evaluation; Efi Tsetsekou for her assistance in psychological evaluation; as well as the laboratory team Carmen Vassiliadou and George Dedoussis (genetic analysis), Marina Toutouza-Giotsa, Constadina Tselika and Sia Poulopoulou (biochemical analysis) and Maria Toutouza for the database management.

Author information

Authors and Affiliations

  1. Department of Nutrition and Dietetics, School of Health Science and Education, Harokopio University, Athens, Greece

    E Koloverou, D B Panagiotakos, E N Georgousopoulou & A Laskaris

  2. First Cardiology Clinic, School of Medicine, University of Athens, Athens, Greece

    C Pitsavos, C Chrysohoou & C Stefanadis

Authors
  1. E Koloverou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D B Panagiotakos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C Pitsavos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C Chrysohoou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E N Georgousopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A Laskaris
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C Stefanadis
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

The ATTICA Study group

Corresponding author

Correspondence to D B Panagiotakos.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koloverou, E., Panagiotakos, D., Pitsavos, C. et al. The evaluation of inflammatory and oxidative stress biomarkers on coffee–diabetes association: results from the 10-year follow-up of the ATTICA Study (2002–2012). Eur J Clin Nutr 69, 1220–1225 (2015). https://doi.org/10.1038/ejcn.2015.98

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2015.98

This article is cited by

Search

Advanced search

Quick links