Skip to main content
Top
Published in: European Journal of Epidemiology 9/2019

Open Access 01-09-2019 | Insulins | DIABETES MELLITUS

Dietary antioxidant capacity and risk of type 2 diabetes mellitus, prediabetes and insulin resistance: the Rotterdam Study

Authors: Niels van der Schaft, Josje D. Schoufour, Jana Nano, Jessica C. Kiefte-de Jong, Taulant Muka, Eric J. G. Sijbrands, M. Arfan Ikram, Oscar H. Franco, Trudy Voortman

Published in: European Journal of Epidemiology | Issue 9/2019

Login to get access

Abstract

Intake of individual antioxidants has been related to a lower risk of type 2 diabetes. However, the overall diet may contain many antioxidants with additive or synergistic effects. Therefore, we aimed to determine associations between total dietary antioxidant capacity and risk of type 2 diabetes, prediabetes and insulin resistance. We estimated the dietary antioxidant capacity for 5796 participants of the Rotterdam Study using a ferric reducing ability of plasma (FRAP) score. Of these participants, 4957 had normoglycaemia and 839 had prediabetes at baseline. We used covariate-adjusted proportional hazards models to estimate associations between FRAP and risk of type 2 diabetes, risk of type 2 diabetes among participants with prediabetes, and risk of prediabetes. We used linear regression models to determine the association between FRAP score and insulin resistance (HOMA-IR). We observed 532 cases of incident type 2 diabetes, of which 259 among participants with prediabetes, and 794 cases of incident prediabetes during up to 15 years of follow-up. A higher FRAP score was associated with a lower risk of type 2 diabetes among the total population (HR per SD FRAP 0.84, 95% CI 0.75; 0.95) and among participants with prediabetes (HR 0.85, 95% CI 0.73; 0.99), but was not associated with risk of prediabetes. Dietary FRAP was also inversely associated with HOMA-IR (β − 0.04, 95% CI − 0.06; − 0.03). Effect estimates were generally similar between sexes. The findings of this population-based study emphasize the putative beneficial effects of a diet rich in antioxidants on insulin resistance and risk of type 2 diabetes.
Appendix
Available only for authorised users
Literature
1.
go back to reference Maritim AC, Sanders RA, Watkins JB. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol. 2003;17(1):24–38.CrossRef Maritim AC, Sanders RA, Watkins JB. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol. 2003;17(1):24–38.CrossRef
2.
go back to reference Benzie IFF, Choi S-W. Antioxidants in Food. Adv Food Nutr Res. 2014;1(71):1–53. Benzie IFF, Choi S-W. Antioxidants in Food. Adv Food Nutr Res. 2014;1(71):1–53.
3.
go back to reference Linnane AW, Kios M, Vitetta L. Healthy aging: regulation of the metabolome by cellular redox modulation and prooxidant signaling systems: the essential roles of superoxide anion and hydrogen peroxide. Biogerontology. 2007;8(5):445–67.CrossRef Linnane AW, Kios M, Vitetta L. Healthy aging: regulation of the metabolome by cellular redox modulation and prooxidant signaling systems: the essential roles of superoxide anion and hydrogen peroxide. Biogerontology. 2007;8(5):445–67.CrossRef
4.
go back to reference Bouayed J, Bohn T. Exogenous antioxidants—double-edged swords in cellular redox state. Oxid Med Cell Longev. 2010;3(4):228–37.CrossRef Bouayed J, Bohn T. Exogenous antioxidants—double-edged swords in cellular redox state. Oxid Med Cell Longev. 2010;3(4):228–37.CrossRef
5.
go back to reference Montonen J, Knekt P, Järvinen R, Reunanen A. Dietary antioxidant intake and risk of type 2 diabetes. Diabetes Care. 2004;27(2):362–6.CrossRef Montonen J, Knekt P, Järvinen R, Reunanen A. Dietary antioxidant intake and risk of type 2 diabetes. Diabetes Care. 2004;27(2):362–6.CrossRef
6.
go back to reference Sluijs I, Cadier E, Beulens JWJ, van der A DL, Spijkerman AMW, van der Schouw YT. Dietary intake of carotenoids and risk of type 2 diabetes. Nutr Metab Cardiovasc Dis NMCD. 2015;25(4):376–81.CrossRef Sluijs I, Cadier E, Beulens JWJ, van der A DL, Spijkerman AMW, van der Schouw YT. Dietary intake of carotenoids and risk of type 2 diabetes. Nutr Metab Cardiovasc Dis NMCD. 2015;25(4):376–81.CrossRef
7.
go back to reference Psaltopoulou T, Panagiotakos DB, Pitsavos C, Chrysochoou C, Detopoulou P, Skoumas J, et al. Dietary antioxidant capacity is inversely associated with diabetes biomarkers: the ATTICA study. Nutr Metab Cardiovasc Dis NMCD. 2011;21(8):561–7.CrossRef Psaltopoulou T, Panagiotakos DB, Pitsavos C, Chrysochoou C, Detopoulou P, Skoumas J, et al. Dietary antioxidant capacity is inversely associated with diabetes biomarkers: the ATTICA study. Nutr Metab Cardiovasc Dis NMCD. 2011;21(8):561–7.CrossRef
8.
go back to reference Okubo H, Syddall HE, Phillips DIW, Sayer AA, Dennison EM, Cooper C, et al. Dietary total antioxidant capacity is related to glucose tolerance in older people: the Hertfordshire cohort study. Nutr Metab Cardiovasc Dis NMCD. 2014;24(3):301–8.CrossRef Okubo H, Syddall HE, Phillips DIW, Sayer AA, Dennison EM, Cooper C, et al. Dietary total antioxidant capacity is related to glucose tolerance in older people: the Hertfordshire cohort study. Nutr Metab Cardiovasc Dis NMCD. 2014;24(3):301–8.CrossRef
9.
go back to reference Pellegrini N, Salvatore S, Valtueña S, Bedogni G, Porrini M, Pala V, et al. Development and validation of a food frequency questionnaire for the assessment of dietary total antioxidant capacity. J Nutr. 2007;137(1):93–8.CrossRef Pellegrini N, Salvatore S, Valtueña S, Bedogni G, Porrini M, Pala V, et al. Development and validation of a food frequency questionnaire for the assessment of dietary total antioxidant capacity. J Nutr. 2007;137(1):93–8.CrossRef
10.
go back to reference Carlsen MH, Halvorsen BL, Holte K, Bøhn SK, Dragland S, Sampson L, et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J. 2010;22(9):3.CrossRef Carlsen MH, Halvorsen BL, Holte K, Bøhn SK, Dragland S, Sampson L, et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr J. 2010;22(9):3.CrossRef
11.
go back to reference Harasym J, Oledzki R. Effect of fruit and vegetable antioxidants on total antioxidant capacity of blood plasma. Nutrition. 2014;30(5):511–7.CrossRef Harasym J, Oledzki R. Effect of fruit and vegetable antioxidants on total antioxidant capacity of blood plasma. Nutrition. 2014;30(5):511–7.CrossRef
12.
go back to reference Qureshi SA, Lund AC, Veierød MB, Carlsen MH, Blomhoff R, Andersen LF, et al. Food items contributing most to variation in antioxidant intake; a cross-sectional study among Norwegian women. BMC Public Health. 2014;16(14):45.CrossRef Qureshi SA, Lund AC, Veierød MB, Carlsen MH, Blomhoff R, Andersen LF, et al. Food items contributing most to variation in antioxidant intake; a cross-sectional study among Norwegian women. BMC Public Health. 2014;16(14):45.CrossRef
13.
go back to reference Mancini FR, Affret A, Dow C, Balkau B, Bonnet F, Boutron-Ruault M-C, et al. Dietary antioxidant capacity and risk of type 2 diabetes in the large prospective E3N-EPIC cohort. Diabetologia. 2017;61:308–16.CrossRef Mancini FR, Affret A, Dow C, Balkau B, Bonnet F, Boutron-Ruault M-C, et al. Dietary antioxidant capacity and risk of type 2 diabetes in the large prospective E3N-EPIC cohort. Diabetologia. 2017;61:308–16.CrossRef
14.
go back to reference Hofman A, Grobbee DE, de Jong PT, van den Ouweland FA. Determinants of disease and disability in the elderly: the Rotterdam elderly study. Eur J Epidemiol. 1991;7(4):403–22.CrossRef Hofman A, Grobbee DE, de Jong PT, van den Ouweland FA. Determinants of disease and disability in the elderly: the Rotterdam elderly study. Eur J Epidemiol. 1991;7(4):403–22.CrossRef
15.
go back to reference Voortman T, Jong JCK, Ikram MA, Stricker BH, van Rooij FJA, Lahousse L, et al. Adherence to the 2015 Dutch dietary guidelines and risk of non-communicable diseases and mortality in the Rotterdam study. Eur J Epidemiol. 2017;19:1–13. Voortman T, Jong JCK, Ikram MA, Stricker BH, van Rooij FJA, Lahousse L, et al. Adherence to the 2015 Dutch dietary guidelines and risk of non-communicable diseases and mortality in the Rotterdam study. Eur J Epidemiol. 2017;19:1–13.
16.
go back to reference Klipstein-Grobusch K, den Breeijen JH, Goldbohm RA, Geleijnse JM, Hofman A, Grobbee DE, et al. Dietary assessment in the elderly: validation of a semiquantitative food frequency questionnaire. Eur J Clin Nutr. 1998;52(8):588–96.CrossRef Klipstein-Grobusch K, den Breeijen JH, Goldbohm RA, Geleijnse JM, Hofman A, Grobbee DE, et al. Dietary assessment in the elderly: validation of a semiquantitative food frequency questionnaire. Eur J Clin Nutr. 1998;52(8):588–96.CrossRef
17.
go back to reference Goldbohm RA, van den Brandt PA, Brants HA, van’t Veer P, Al M, Sturmans F, et al. Validation of a dietary questionnaire used in a large-scale prospective cohort study on diet and cancer. Eur J Clin Nutr. 1994;48(4):253–65.PubMed Goldbohm RA, van den Brandt PA, Brants HA, van’t Veer P, Al M, Sturmans F, et al. Validation of a dietary questionnaire used in a large-scale prospective cohort study on diet and cancer. Eur J Clin Nutr. 1994;48(4):253–65.PubMed
18.
go back to reference Feunekes GI, Van Staveren WA, De Vries JH, Burema J, Hautvast JG. Relative and biomarker-based validity of a food-frequency questionnaire estimating intake of fats and cholesterol. Am J Clin Nutr. 1993;58(4):489–96.CrossRef Feunekes GI, Van Staveren WA, De Vries JH, Burema J, Hautvast JG. Relative and biomarker-based validity of a food-frequency questionnaire estimating intake of fats and cholesterol. Am J Clin Nutr. 1993;58(4):489–96.CrossRef
19.
go back to reference Benzie IFF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996;239(1):70–6.CrossRef Benzie IFF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996;239(1):70–6.CrossRef
20.
go back to reference Neeley WE. Simple automated determination of serum or plasma glucose by a hexokinase-glucose-6-phosphate dehydrogenase method. Clin Chem. 1972;18(6):509–15.PubMed Neeley WE. Simple automated determination of serum or plasma glucose by a hexokinase-glucose-6-phosphate dehydrogenase method. Clin Chem. 1972;18(6):509–15.PubMed
21.
go back to reference World Health Organization. Definition and diagnosis of diabetes mellitus and intermediate hyperglycaemia: report of a WHO/IDF Consultation. Geneva; 2006. p. 1–50. World Health Organization. Definition and diagnosis of diabetes mellitus and intermediate hyperglycaemia: report of a WHO/IDF Consultation. Geneva; 2006. p. 1–50.
22.
go back to reference Ligthart S, van Herpt TT, Leening MJ, Kavousi M, Hofman A, Stricker BH, et al. Lifetime risk of developing impaired glucose metabolism and eventual progression from prediabetes to type 2 diabetes: a prospective cohort study. Lancet Diabetes Endocrinol. 2016;4(1):44–51.CrossRef Ligthart S, van Herpt TT, Leening MJ, Kavousi M, Hofman A, Stricker BH, et al. Lifetime risk of developing impaired glucose metabolism and eventual progression from prediabetes to type 2 diabetes: a prospective cohort study. Lancet Diabetes Endocrinol. 2016;4(1):44–51.CrossRef
23.
go back to reference Vitezova A, Voortman T, Zillikens MC, Jansen PW, Hofman A, Uitterlinden AG, et al. Bidirectional associations between circulating vitamin D and cholesterol levels: the Rotterdam study. Maturitas. 2015;82(4):411–7.CrossRef Vitezova A, Voortman T, Zillikens MC, Jansen PW, Hofman A, Uitterlinden AG, et al. Bidirectional associations between circulating vitamin D and cholesterol levels: the Rotterdam study. Maturitas. 2015;82(4):411–7.CrossRef
24.
go back to reference Hofman A, Brusselle GG, Darwish Murad S, van Duijn CM, Franco OH, Goedegebure A, et al. The Rotterdam study: 2016 objectives and design update. Eur J Epidemiol. 2015;30(8):661–708.CrossRef Hofman A, Brusselle GG, Darwish Murad S, van Duijn CM, Franco OH, Goedegebure A, et al. The Rotterdam study: 2016 objectives and design update. Eur J Epidemiol. 2015;30(8):661–708.CrossRef
25.
go back to reference Salonen JT, Nyyssönen K, Tuomainen TP, Mäenpää PH, Korpela H, Kaplan GA, et al. Increased risk of non-insulin dependent diabetes mellitus at low plasma vitamin E concentrations: a four year follow up study in men. BMJ. 1995;311(7013):1124–7.CrossRef Salonen JT, Nyyssönen K, Tuomainen TP, Mäenpää PH, Korpela H, Kaplan GA, et al. Increased risk of non-insulin dependent diabetes mellitus at low plasma vitamin E concentrations: a four year follow up study in men. BMJ. 1995;311(7013):1124–7.CrossRef
26.
go back to reference 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):1–8.CrossRef 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):1–8.CrossRef
27.
go back to reference Newsholme P, Haber EP, Hirabara SM, Rebelato ELO, Procopio J, Morgan D, et al. Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J Physiol. 2007;583(Pt 1):9–24.CrossRef Newsholme P, Haber EP, Hirabara SM, Rebelato ELO, Procopio J, Morgan D, et al. Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J Physiol. 2007;583(Pt 1):9–24.CrossRef
28.
go back to reference Kaneto H, Kajimoto Y, Miyagawa J, Matsuoka T, Fujitani Y, Umayahara Y, et al. Beneficial effects of antioxidants in diabetes: possible protection of pancreatic beta-cells against glucose toxicity. Diabetes. 1999;48(12):2398–406.CrossRef Kaneto H, Kajimoto Y, Miyagawa J, Matsuoka T, Fujitani Y, Umayahara Y, et al. Beneficial effects of antioxidants in diabetes: possible protection of pancreatic beta-cells against glucose toxicity. Diabetes. 1999;48(12):2398–406.CrossRef
29.
go back to reference Prentki M, Nolan CJ. Islet β cell failure in type 2 diabetes. J Clin Investig. 2006;116(7):1802–12.CrossRef Prentki M, Nolan CJ. Islet β cell failure in type 2 diabetes. J Clin Investig. 2006;116(7):1802–12.CrossRef
30.
go back to reference Blaak E. Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care. 2001;4(6):499–502.CrossRef Blaak E. Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care. 2001;4(6):499–502.CrossRef
31.
go back to reference Fujita K, Nishizawa H, Funahashi T, Shimomura I, Shimabukuro M. Systemic oxidative stress is associated with visceral fat accumulation and the metabolic syndrome. Circ J. 2006;70(11):1437–42.CrossRef Fujita K, Nishizawa H, Funahashi T, Shimomura I, Shimabukuro M. Systemic oxidative stress is associated with visceral fat accumulation and the metabolic syndrome. Circ J. 2006;70(11):1437–42.CrossRef
32.
go back to reference Mirmiran P, Carlström M, Bahadoran Z, Azizi F. Long-term effects of coffee and caffeine intake on the risk of pre-diabetes and type 2 diabetes: findings from a population with low coffee consumption. Nutr Metab Cardiovasc Dis NMCD. 2018;28(12):1261–6.CrossRef Mirmiran P, Carlström M, Bahadoran Z, Azizi F. Long-term effects of coffee and caffeine intake on the risk of pre-diabetes and type 2 diabetes: findings from a population with low coffee consumption. Nutr Metab Cardiovasc Dis NMCD. 2018;28(12):1261–6.CrossRef
33.
go back to reference Bhupathiraju SN, Pan A, Manson JE, Willett WC, van Dam RM, Hu FB. Changes in coffee intake and subsequent risk of type 2 diabetes: three large cohorts of US men and women. Diabetologia. 2014;57(7):1346–54.CrossRef Bhupathiraju SN, Pan A, Manson JE, Willett WC, van Dam RM, Hu FB. Changes in coffee intake and subsequent risk of type 2 diabetes: three large cohorts of US men and women. Diabetologia. 2014;57(7):1346–54.CrossRef
34.
go back to reference Gao F, Zhang Y, Ge S, Lu H, Chen R, Fang P, et al. Coffee consumption is positively related to insulin secretion in the Shanghai high-risk diabetic screen (SHiDS) study. Nutr Metab. 2018;15:84.CrossRef Gao F, Zhang Y, Ge S, Lu H, Chen R, Fang P, et al. Coffee consumption is positively related to insulin secretion in the Shanghai high-risk diabetic screen (SHiDS) study. Nutr Metab. 2018;15:84.CrossRef
35.
go back to reference Li M, Fan Y, Zhang X, Hou W, Tang Z. Fruit and vegetable intake and risk of type 2 diabetes mellitus: meta-analysis of prospective cohort studies. BMJ Open. 2014;4(11):e005497.CrossRef Li M, Fan Y, Zhang X, Hou W, Tang Z. Fruit and vegetable intake and risk of type 2 diabetes mellitus: meta-analysis of prospective cohort studies. BMJ Open. 2014;4(11):e005497.CrossRef
36.
go back to reference Jing Y, Han G, Hu Y, Bi Y, Li L, Zhu D. Tea consumption and risk of type 2 diabetes: a meta-analysis of cohort studies. J Gen Intern Med. 2009;24(5):557–62.CrossRef Jing Y, Han G, Hu Y, Bi Y, Li L, Zhu D. Tea consumption and risk of type 2 diabetes: a meta-analysis of cohort studies. J Gen Intern Med. 2009;24(5):557–62.CrossRef
37.
go back to reference Yuan S, Li X, Jin Y, Lu J. Chocolate consumption and risk of coronary heart disease, stroke, and diabetes: a meta-analysis of prospective studies. Nutrients. 2017;9(7):688.CrossRef Yuan S, Li X, Jin Y, Lu J. Chocolate consumption and risk of coronary heart disease, stroke, and diabetes: a meta-analysis of prospective studies. Nutrients. 2017;9(7):688.CrossRef
Metadata
Title
Dietary antioxidant capacity and risk of type 2 diabetes mellitus, prediabetes and insulin resistance: the Rotterdam Study
Authors
Niels van der Schaft
Josje D. Schoufour
Jana Nano
Jessica C. Kiefte-de Jong
Taulant Muka
Eric J. G. Sijbrands
M. Arfan Ikram
Oscar H. Franco
Trudy Voortman
Publication date
01-09-2019
Publisher
Springer Netherlands
Published in
European Journal of Epidemiology / Issue 9/2019
Print ISSN: 0393-2990
Electronic ISSN: 1573-7284
DOI
https://doi.org/10.1007/s10654-019-00548-9

Other articles of this Issue 9/2019

European Journal of Epidemiology 9/2019 Go to the issue