Intake of whole grain foods and risk of type 2 diabetes: results from three prospective cohort studies

Yang Hu, Ming Ding, Laura Sampson, Walter C Willett, JoAnn E Manson, Molin Wang, Bernard Rosner, Frank B Hu, Qi Sun, Yang Hu, Ming Ding, Laura Sampson, Walter C Willett, JoAnn E Manson, Molin Wang, Bernard Rosner, Frank B Hu, Qi Sun

Abstract

Objective: To examine the associations between the intake of total and individual whole grain foods and the risk of type 2 diabetes.

Design: Prospective cohort studies.

Setting: Nurses' Health Study (1984-2014), Nurses' Health Study II (1991-2017), and Health Professionals Follow-Up Study (1986-2016), United States.

Participants: 158 259 women and 36 525 men who did not have type 2 diabetes, cardiovascular disease, or cancer at baseline.

Main outcome measures: Self-reports of incident type 2 diabetes by participants identified through follow-up questionnaires and confirmed by a validated supplementary questionnaire.

Results: During 4 618 796 person years of follow-up, 18 629 participants with type 2 diabetes were identified. Total whole grain consumption was categorized into five equal groups of servings a day for the three cohorts. After adjusting for lifestyle and dietary risk factors for diabetes, participants in the highest category for total whole grain consumption had a 29% (95% confidence interval 26% to 33%) lower rate of type 2 diabetes compared with those in the lowest category. For individual whole grain foods, pooled hazard ratios (95% confidence intervals) for type 2 diabetes in participants consuming one or more servings a day compared with those consuming less than one serving a month were 0.81 (0.77 to 0.86) for whole grain cold breakfast cereal, 0.79 (0.75 to 0.83) for dark bread, and 1.08 (1.00 to 1.17) for popcorn. For other individual whole grains with lower average intake levels, comparing consumption of two or more servings a week with less than one serving a month, the pooled hazard ratios (95% confidence intervals) were 0.79 (0.75 to 0.83) for oatmeal, 0.88 (0.82 to 0.94) for brown rice, 0.85 (0.80 to 0.90) for added bran, and 0.88 (0.78 to 0.98) for wheat germ. Spline regression showed a non-linear dose-response association between total whole grain intake and the risk of type 2 diabetes where the rate reduction slightly plateaued at more than two servings a day (P<0.001 for curvature). For whole grain cold breakfast cereal and dark bread, the rate reduction plateaued at about 0.5 servings a day. For consumption of popcorn, a J shaped association was found where the rate of type 2 diabetes was not significantly raised until consumption exceeded about one serving a day. The association between higher total whole grain intake and lower risk of type 2 diabetes was stronger in individuals who were lean than in those who were overweight or obese (P=0.003 for interaction), and the associations did not vary significantly across levels of physical activity, family history of diabetes, or smoking status.

Conclusion: Higher consumption of total whole grains and several commonly eaten whole grain foods, including whole grain breakfast cereal, oatmeal, dark bread, brown rice, added bran, and wheat germ, was significantly associated with a lower risk of type 2 diabetes. These findings provide further support for the current recommendations of increasing whole grain consumption as part of a healthy diet for the prevention of type 2 diabetes.

Conflict of interest statement

Competing interests: All authors have completed the ICMJE uniform disclosure form at www.icmje.org/coi_disclosure.pdf and declare: support from the National Institutes of Health for the submitted work. QS reports receiving consulting fees from Emavant Solutions GmbH, outside the submitted work. FBH reports grants from California Walnut Commission, personal fees from Metagenics, personal fees from Standard Process, and personal fees from Diet Quality Photo Navigation, outside the submitted work. The remaining authors report no other relationships or activities that could appear to have influenced the submitted work.

© Author(s) (or their employer(s)) 2019. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

Figures

Fig 1
Fig 1
Multivariable adjusted, pooled, dose-response associations between total whole grain intake and risk of type 2 diabetes in the Nurses’ Health Study (1984-2014), Nurses’ Health Study II (1991-2017), and Health Professionals Follow-up Study (1986-2016). Data from three cohorts were combined and truncated at the 0.5th and 99.5th centiles. (A) Consumption of total whole grains, 0.03-5.0 servings/day, (B) consumption of total whole grains excluding popcorn, 0-4.8 servings/day, (C) consumption of whole grain cold breakfast cereal, 0-1.65 servings/day, (D) consumption of dark bread, 0-4.3 servings/day, and (E) consumption of popcorn, 0-1.8 servings/day. Hazard ratios were adjusted for age (years), ethnicity (white, African American, Asian, others), body mass index (

References

    1. Slavin J. Whole grains and human health. Nutr Res Rev 2004;17:99-110. 10.1079/NRR200374
    1. Karl JP, Meydani M, Barnett JB, et al. Substituting whole grains for refined grains in a 6-wk randomized trial favorably affects energy-balance metrics in healthy men and postmenopausal women. Am J Clin Nutr 2017;105:589-99. 10.3945/ajcn.116.139683
    1. Vanegas SM, Meydani M, Barnett JB, et al. Substituting whole grains for refined grains in a 6-wk randomized trial has a modest effect on gut microbiota and immune and inflammatory markers of healthy adults. Am J Clin Nutr 2017;105:635-50. 10.3945/ajcn.116.146928
    1. Kirwan JP, Malin SK, Scelsi AR, et al. A whole-grain diet reduces cardiovascular risk factors in overweight and obese adults: a randomized controlled trial. J Nutr 2016;146:2244-51. 10.3945/jn.116.230508
    1. Kristensen M, Toubro S, Jensen MG, et al. Whole grain compared with refined wheat decreases the percentage of body fat following a 12-week, energy-restricted dietary intervention in postmenopausal women. J Nutr 2012;142:710-6. 10.3945/jn.111.142315
    1. Maki KC, Beiseigel JM, Jonnalagadda SS, et al. Whole-grain ready-to-eat oat cereal, as part of a dietary program for weight loss, reduces low-density lipoprotein cholesterol in adults with overweight and obesity more than a dietary program including low-fiber control foods. J Am Diet Assoc 2010;110:205-14. 10.1016/j.jada.2009.10.037
    1. Tighe P, Duthie G, Vaughan N, et al. Effect of increased consumption of whole-grain foods on blood pressure and other cardiovascular risk markers in healthy middle-aged persons: a randomized controlled trial. Am J Clin Nutr 2010;92:733-40. 10.3945/ajcn.2010.29417
    1. Pereira MA, Jacobs DR, Jr, Pins JJ, et al. Effect of whole grains on insulin sensitivity in overweight hyperinsulinemic adults. Am J Clin Nutr 2002;75:848-55. 10.1093/ajcn/75.5.848
    1. Katcher HI, Legro RS, Kunselman AR, et al. The effects of a whole grain-enriched hypocaloric diet on cardiovascular disease risk factors in men and women with metabolic syndrome. Am J Clin Nutr 2008;87:79-90. 10.1093/ajcn/87.1.79
    1. Mellen PB, Walsh TF, Herrington DM. Whole grain intake and cardiovascular disease: a meta-analysis. Nutr Metab Cardiovasc Dis 2008;18:283-90. 10.1016/j.numecd.2006.12.008
    1. de Munter JSL, Hu FB, Spiegelman D, Franz M, van Dam RM. Whole grain, bran, and germ intake and risk of type 2 diabetes: a prospective cohort study and systematic review. PLoS Med 2007;4:e261. 10.1371/journal.pmed.0040261
    1. Aune D, Chan DSM, Lau R, et al. Dietary fibre, whole grains, and risk of colorectal cancer: systematic review and dose-response meta-analysis of prospective studies. BMJ 2011;343:d6617. 10.1136/bmj.d6617
    1. Franz M, Sampson L. Challenges in developing a whole grain database: Definitions, methods and quantification. J Food Compos Anal 2006;19 10.1016/j.jfca.2005.12.010.
    1. Jacobs DR, Jr, Gallaher DD. Whole grain intake and cardiovascular disease: a review. Curr Atheroscler Rep 2004;6:415-23. 10.1007/s11883-004-0081-y
    1. Kamal-Eldin A, Lærke HN, Knudsen K-EB, et al. Physical, microscopic and chemical characterisation of industrial rye and wheat brans from the Nordic countries. Food Nutr Res 2009;53:1912. 10.3402/fnr.v53i0.1912
    1. Slavin JL. Mechanisms for the impact of whole grain foods on cancer risk. J Am Coll Nutr 2000;19(Suppl):300S-7S. 10.1080/07315724.2000.10718964
    1. Slavin J. Why whole grains are protective: biological mechanisms. Proc Nutr Soc 2003;62:129-34. 10.1079/PNS2002221
    1. Cho SS, Qi L, Fahey GC, Jr, Klurfeld DM. Consumption of cereal fiber, mixtures of whole grains and bran, and whole grains and risk reduction in type 2 diabetes, obesity, and cardiovascular disease. Am J Clin Nutr 2013;98:594-619. 10.3945/ajcn.113.067629
    1. Kochar J, Djoussé L, Gaziano JM. Breakfast cereals and risk of type 2 diabetes in the Physicians’ Health Study I. Obesity (Silver Spring) 2007;15:3039-44. 10.1038/oby.2007.362
    1. Sun Q, Spiegelman D, van Dam RM, et al. White rice, brown rice, and risk of type 2 diabetes in US men and women. Arch Intern Med 2010;170:961-9. 10.1001/archinternmed.2010.109
    1. Schulze MB, Manson JE, Ludwig DS, et al. Sugar-sweetened beverages, weight gain, and incidence of type 2 diabetes in young and middle-aged women. JAMA 2004;292:927-34. 10.1001/jama.292.8.927
    1. Fung TT, Malik V, Rexrode KM, Manson JE, Willett WC, Hu FB. Sweetened beverage consumption and risk of coronary heart disease in women. Am J Clin Nutr 2009;89:1037-42. 10.3945/ajcn.2008.27140
    1. Jensen MK, Koh-Banerjee P, Hu FB, et al. Intakes of whole grains, bran, and germ and the risk of coronary heart disease in men. Am J Clin Nutr 2004;80:1492-9. 10.1093/ajcn/80.6.1492
    1. Koh-Banerjee P, Franz M, Sampson L, et al. Changes in whole-grain, bran, and cereal fiber consumption in relation to 8-y weight gain among men. Am J Clin Nutr 2004;80:1237-45. 10.1093/ajcn/80.5.1237
    1. Salvini S, Hunter DJ, Sampson L, et al. Food-based validation of a dietary questionnaire: the effects of week-to-week variation in food consumption. Int J Epidemiol 1989;18:858-67. 10.1093/ije/18.4.858
    1. Sun Q, Townsend MK, Okereke OI, Franco OH, Hu FB, Grodstein F. Physical activity at midlife in relation to successful survival in women at age 70 years or older. Arch Intern Med 2010;170:194-201. 10.1001/archinternmed.2009.503
    1. Wolf AM, Hunter DJ, Colditz GA, et al. Reproducibility and validity of a self-administered physical activity questionnaire. Int J Epidemiol 1994;23:991-9. 10.1093/ije/23.5.991
    1. Willett W, Stampfer MJ, Bain C, et al. Cigarette smoking, relative weight, and menopause. Am J Epidemiol 1983;117:651-8. 10.1093/oxfordjournals.aje.a113598
    1. Rimm EB, Stampfer MJ, Colditz GA, Chute CG, Litin LB, Willett WC. Validity of self-reported waist and hip circumferences in men and women. Epidemiology 1990;1:466-73. 10.1097/00001648-199011000-00009
    1. Giovannucci E, Colditz G, Stampfer MJ, et al. The assessment of alcohol consumption by a simple self-administered questionnaire. Am J Epidemiol 1991;133:810-7. 10.1093/oxfordjournals.aje.a115960
    1. Colditz GA, Martin P, Stampfer MJ, et al. Validation of questionnaire information on risk factors and disease outcomes in a prospective cohort study of women. Am J Epidemiol 1986;123:894-900. 10.1093/oxfordjournals.aje.a114319
    1. Chiuve SE, Fung TT, Rimm EB, et al. Alternative dietary indices both strongly predict risk of chronic disease. J Nutr 2012;142:1009-18. 10.3945/jn.111.157222
    1. National Diabetes Data Group Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 1979;28:1039-57. 10.2337/diab.28.12.1039
    1. American Diabetes Association Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 1997;20(suppl 1):1183-97. 10.2337/diacare.20.7.1183
    1. American Diabetes Association Standards of medical care in diabetes—2010 [correction in: Diabetes Care 2010;33:692]. Diabetes Care 2010;33(Suppl 1):S11-61. 10.2337/dc10-S011
    1. Manson JE, Rimm EB, Stampfer MJ, et al. Physical activity and incidence of non-insulin-dependent diabetes mellitus in women. Lancet 1991;338:774-8. 10.1016/0140-6736(91)90664-B
    1. Hu FB, Leitzmann MF, Stampfer MJ, Colditz GA, Willett WC, Rimm EB. Physical activity and television watching in relation to risk for type 2 diabetes mellitus in men. Arch Intern Med 2001;161:1542-8. 10.1001/archinte.161.12.1542
    1. Rich-Edwards JW, Corsano KA, Stampfer MJ. Test of the National Death Index and Equifax Nationwide Death Search. Am J Epidemiol 1994;140:1016-9. 10.1093/oxfordjournals.aje.a117191
    1. Hu FB, Stampfer MJ, Rimm E, et al. Dietary fat and coronary heart disease: a comparison of approaches for adjusting for total energy intake and modeling repeated dietary measurements. Am J Epidemiol 1999;149:531-40. 10.1093/oxfordjournals.aje.a009849
    1. Bernstein AM, Rosner BA, Willett WC. Cereal fiber and coronary heart disease: a comparison of modeling approaches for repeated dietary measurements, intermediate outcomes, and long follow-up. Eur J Epidemiol 2011;26:877-86. 10.1007/s10654-011-9626-x
    1. Liu GF, Wang J, Liu K, Snavely DB. Confidence intervals for an exposure adjusted incidence rate difference with applications to clinical trials. Stat Med 2006;25:1275-86. 10.1002/sim.2335
    1. Rubin DB. Multiple imputation for nonresponse in surveys. Wiley, 1987. 10.1002/9780470316696.
    1. Aune D, Norat T, Romundstad P, Vatten LJ. Whole grain and refined grain consumption and the risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies. Eur J Epidemiol 2013;28:845-58. 10.1007/s10654-013-9852-5
    1. Schulze MB, Schulz M, Heidemann C, Schienkiewitz A, Hoffmann K, Boeing H. Fiber and magnesium intake and incidence of type 2 diabetes: a prospective study and meta-analysis. Arch Intern Med 2007;167:956-65. 10.1001/archinte.167.9.956
    1. FoodData Central. USDA Food Agricultural Research Service. 2019.
    1. Bhupathiraju SN, Tobias DK, Malik VS, et al. Glycemic index, glycemic load, and risk of type 2 diabetes: results from 3 large US cohorts and an updated meta-analysis. Am J Clin Nutr 2014;100:218-32. 10.3945/ajcn.113.079533
    1. Foster-Powell K, Holt SHA, Brand-Miller JC. International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr 2002;76:5-56. 10.1093/ajcn/76.1.5
    1. Popcorn Board. Industry Facts. .
    1. Holt SHA, Miller JC, Petocz P, Farmakalidis E. A satiety index of common foods. Eur J Clin Nutr 1995;49:675-90.
    1. Nguyen V, Cooper L, Lowndes J, et al. Popcorn is more satiating than potato chips in normal-weight adults. Nutr J 2012;11:71. 10.1186/1475-2891-11-71
    1. NOVA. Butter Lovers - ACT II - 12 bags * 78 g. .
    1. NOVA. Jolly Time Microwave Pop Corn - 300 g. .
    1. NOVA. Butter flavored Popcorn - Jiffy pop - 4.5 oz. .
    1. Otite FO, Jacobson MF, Dahmubed A, Mozaffarian D. Trends in trans fatty acids reformulations of US supermarket and brand-name foods from 2007 through 2011. Prev Chronic Dis 2013;10:E85. 10.5888/pcd10.120198
    1. Wang Q, Imamura F, Ma W, et al. Circulating and dietary trans fatty acids and incident type 2 diabetes in older adults: the Cardiovascular Health Study. Diabetes Care 2015;38:1099-107. 10.2337/dc14-2101
    1. Moreta C, Tena MT. Determination of perfluorinated alkyl acids in corn, popcorn and popcorn bags before and after cooking by focused ultrasound solid-liquid extraction, liquid chromatography and quadrupole-time of flight mass spectrometry. J Chromatogr A 2014;1355:211-8. 10.1016/j.chroma.2014.06.018
    1. Martínez-Moral MP, Tena MT. Determination of perfluorocompounds in popcorn packaging by pressurised liquid extraction and ultra-performance liquid chromatography-tandem mass spectrometry. Talanta 2012;101:104-9. 10.1016/j.talanta.2012.09.007
    1. Lind PM, Salihovic S, van Bavel B, Lind L. Circulating levels of perfluoroalkyl substances (PFASs) and carotid artery atherosclerosis. Environ Res 2017;152:157-64. 10.1016/j.envres.2016.10.002
    1. Lind L, Zethelius B, Salihovic S, van Bavel B, Lind PM. Circulating levels of perfluoroalkyl substances and prevalent diabetes in the elderly. Diabetologia 2014;57:473-9. 10.1007/s00125-013-3126-3
    1. Liu G, Dhana K, Furtado JD, et al. Perfluoroalkyl substances and changes in body weight and resting metabolic rate in response to weight-loss diets: A prospective study. PLoS Med 2018;15:e1002502. 10.1371/journal.pmed.1002502
    1. Sun Q, Zong G, Valvi D, Nielsen F, Coull B, Grandjean P. Plasma concentrations of perfluoroalkyl substances and risk of type 2 diabetes: A prospective investigation among U.S. women. Environ Health Perspect 2018;126:037001. 10.1289/EHP2619
    1. Bes-Rastrollo M, Sanchez-Villegas A, Basterra-Gortari FJ, Nunez-Cordoba JM, Toledo E, Serrano-Martinez M. Prospective study of self-reported usual snacking and weight gain in a Mediterranean cohort: the SUN project. Clin Nutr 2010;29:323-30. 10.1016/j.clnu.2009.08.017
    1. Mekary RA, Giovannucci E, Willett WC, van Dam RM, Hu FB. Eating patterns and type 2 diabetes risk in men: breakfast omission, eating frequency, and snacking. Am J Clin Nutr 2012;95:1182-9. 10.3945/ajcn.111.028209

Source: PubMed

3
購読する