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Carbohydrates, glycemic index and diabetes mellitus

Association of diet and lifestyle with glycated haemoglobin in type 1 diabetes participants in the EURODIAB prospective complications study

European Journal of Clinical Nutrition volume 70, pages 229–236 (2016)Cite this article

Subjects

Abstract

Background/Objectives:

Diet and lifestyle advice for type 1 diabetes (T1DM) patients is based on little evidence and putative effects on glycaemic control. Therefore, we investigated the longitudinal relation between dietary and lifestyle variables and HbA1c levels in patients with type 1 diabetes.

Subjects/Methods:

A 7-year prospective cohort analysis was performed in 1659 T1DM patients (52% males, mean age 32.5 years) participating in the EURODIAB Prospective Complications Study. Baseline dietary intake was assessed by 3- day records and physical activity, smoking status and alcohol intake by questionnaires. HbA1c during follow-up was centrally assessed by immunoassay. Analysis of variance (ANOVA) and restricted cubic spline regression analyses were performed to assess dose–response associations between diet and lifestyle variables and HbA1c levels, adjusted for age, sex, lifestyle and body composition measures, baseline HbA1c, medication use and severe hypoglycaemic attacks.

Results:

Mean follow-up of our study population was 6.8 (s.d. 0.6) years. Mean HbA1c level was 8.25% (s.d. 1.85) (or 66.6 mmol/mol) at baseline and 8.27% (s.d. 1.44) at follow-up. Physical activity, smoking status and alcohol intake were not associated with HbA1c at follow-up in multivariable ANOVA models. Baseline intake below the median of vegetable protein (<29 g/day) and dietary fibre (<18 g/day) was associated with higher HbA1c levels. Restricted cubic splines showed nonlinear associations with HbA1c levels for vegetable protein (P (nonlinear)=0.008) and total dietary fibre (P (nonlinear)=0.0009).

Conclusions:

This study suggests that low intake of vegetable protein and dietary fibre are associated with worse glycaemic control in type 1 diabetes.

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References

  1. Tamayo T, Rosenbauer J, Wild SH, Spijkerman AM, Baan C, Forouhi NG et al. Diabetes in Europe: an update. Diabetes Res Clin Pract 2014; 103: 206–217.

    Article  CAS  PubMed  Google Scholar 

  2. Livingstone SJ, Looker HC, Hothersall EJ, Wild SH, Lindsay RS, Chalmers J et al. Risk of cardiovascular disease and total mortality in adults with type 1 diabetes: Scottish registry linkage study. PLoS Med 2012; 9: e1001321.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Soedamah-Muthu SS, Fuller JH, Mulnier HE, Raleigh VS, Lawrenson RA, Colhoun HM . High risk of cardiovascular disease in patients with type 1 diabetes in the UK: a cohort study using the General Practice Research Database. Diabetes Care 2006; 29: 798–804.

    Article  PubMed  Google Scholar 

  4. Eeg-Olofsson K, Cederholm J, Nilsson PM, Zethelius B, Svensson AM, Gudbjornsdottir S et al. Glycemic control and cardiovascular disease in 7,454 patients with type 1 diabetes: an observational study from the Swedish National Diabetes Register (NDR). Diabetes Care 2010; 33: 1640–1646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Waden J, Forsblom C, Thorn LM, Gordin D, Saraheimo M, Groop PH et al. A1C variability predicts incident cardiovascular events, microalbuminuria, and overt diabetic nephropathy in patients with type 1 diabetes. Diabetes 2009; 58: 2649–2655.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Stampfer MJ, Hu FB, Manson JE, Rimm EB, Willett WC . Primary prevention of coronary heart disease in women through diet and lifestyle. N Engl J Med 2000; 343: 16–22.

    Article  CAS  PubMed  Google Scholar 

  7. Folsom AR, Yatsuya H, Nettleton JA, Lutsey PL, Cushman M, Rosamond WD et al. Community prevalence of ideal cardiovascular health, by the American Heart Association definition, and relationship with cardiovascular disease incidence. J Am Coll Cardiol 2011; 57: 1690–1696.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Delahanty LM, Halford BN . The role of diet behaviors in achieving improved glycemic control in intensively treated patients in the Diabetes Control and Complications Trial. Diabetes Care 1993; 16: 1453–1458.

    Article  CAS  PubMed  Google Scholar 

  9. Buyken AE, Toeller M, Heitkamp G, Irsigler K, Holler C, Santeusanio F et al. Carbohydrate sources and glycaemic control in Type 1 diabetes mellitus. EURODIAB IDDM Complications Study Group. Diabet Med 2000; 17: 351–359.

    Article  CAS  PubMed  Google Scholar 

  10. Buyken AE, Toeller M, Heitkamp G, Karamanos B, Rottiers R, Muggeo M et al. Glycemic index in the diet of European outpatients with type 1 diabetes: relations to glycated hemoglobin and serum lipids. Am J Clin Nutr 2001; 73: 574–581.

    Article  CAS  PubMed  Google Scholar 

  11. Buyken AE, Toeller M, Heitkamp G, Vitelli F, Stehle P, Scherbaum WA et al. Relation of fibre intake to HbA1c and the prevalence of severe ketoacidosis and severe hypoglycaemia. EURODIAB IDDM Complications Study Group. Diabetologia 1998; 41: 882–890.

    Article  CAS  PubMed  Google Scholar 

  12. Katz ML, Mehta S, Nansel T, Quinn H, Lipsky LM, Laffel LM . Associations of nutrient intake with glycemic control in youth with type 1 diabetes: differences by insulin regimen. Diabetes Technol Ther 2014; 16: 512–518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Delahanty LM, Nathan DM, Lachin JM, Hu FB, Cleary PA, Ziegler GK et al. Association of diet with glycated hemoglobin during intensive treatment of type 1 diabetes in the Diabetes Control and Complications Trial. Am J Clin Nutr 2009; 89: 518–524.

    Article  CAS  PubMed  Google Scholar 

  14. Waden J, Tikkanen H, Forsblom C, Fagerudd J, Pettersson-Fernholm K, Lakka T et al. Leisure time physical activity is associated with poor glycemic control in type 1 diabetic women: the FinnDiane study. Diabetes Care 2005; 28: 777–782.

    Article  PubMed  Google Scholar 

  15. Melin EO, Thunander M, Svensson R, Landin-Olsson M, Thulesius HO . Depression, obesity, and smoking were independently associated with inadequate glycemic control in patients with type 1 diabetes. Eur J Endocrinol 2013; 168: 861–869.

    Article  CAS  PubMed  Google Scholar 

  16. Chaturvedi N, Stephenson JM, Fuller JH . The relationship between smoking and microvascular complications in the EURODIAB IDDM Complications Study. Diabetes Care 1995; 18: 785–792.

    Article  CAS  PubMed  Google Scholar 

  17. Nilsson PM, Gudbjornsdottir S, Eliasson B, Cederholm J . Steering Committee of the Swedish National Diabetes R. Smoking is associated with increased HbA1c values and microalbuminuria in patients with diabetes—data from the National Diabetes Register in Sweden. Diabetes Metab 2004; 30: 261–268.

    Article  CAS  PubMed  Google Scholar 

  18. Hofer SE, Rosenbauer J, Grulich-Henn J, Naeke A, Frohlich-Reiterer E, Holl RW et al. Smoking and metabolic control in adolescents with type 1 diabetes. J Pediatr 2009; 154: e21.

    Article  Google Scholar 

  19. Lundman BM, Asplund K, Norberg A . Smoking and metabolic control in patients with insulin-dependent diabetes mellitus. J Intern Med 1990; 227: 101–106.

    Article  CAS  PubMed  Google Scholar 

  20. Gerber PA, Locher R, Schmid B, Spinas GA, Lehmann R . Smoking is associated with impaired long-term glucose metabolism in patients with type 1 diabetes mellitus. Nutr Metab Cardiovasc Dis 2013; 23: 102–108.

    Article  CAS  PubMed  Google Scholar 

  21. Ahmed AT, Karter AJ, Warton EM, Doan JU, Weisner CM . The relationship between alcohol consumption and glycemic control among patients with diabetes: the Kaiser Permanente Northern California Diabetes Registry. J Gen Intern Med 2008; 23: 275–282.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Franz MJ, Powers MA, Leontos C, Holzmeister LA, Kulkarni K, Monk A et al. The evidence for medical nutrition therapy for type 1 and type 2 diabetes in adults. J Am Diet Assoc 2010; 110: 1852–1889.

    Article  PubMed  Google Scholar 

  23. Stephenson J, Fuller JH, EICS Group. Microvascular and acute complications in IDDM patients: the EURODIAB IDDM Complications Study. Diabetologia 1994; 37: 278–285.

    Article  Google Scholar 

  24. Toeller M, Buyken A, Heitkamp G, Milne R, Klischan A, Gries FA . Repeatability of three-day dietary records in the EURODIAB IDDM Complications Study. Eur J Clin Nutr 1997; 51: 74–80.

    Article  CAS  PubMed  Google Scholar 

  25. Toeller M, Klischan A, Heitkamp G, Schumacher W, Milne R, Buyken A et al. Nutritional intake of 2868 IDDM patients from 30 centres in Europe. EURODIAB IDDM Complications Study Group. Diabetologia 1996; 39: 929–939.

    Article  CAS  PubMed  Google Scholar 

  26. Atwater WO, Bryant AP . The availability and fuel value of food materials. Twelfth Annual Report of the Storrs Agricultural Experiment Station 1899: Storrs Agricultural Experiment Station: Middletown, CT, USA. 1900 73–110.

    Google Scholar 

  27. Soedamah-Muthu SS, Chaturvedi N, Fuller JH, Toeller M, Group EPCS. Do European people with type 1 diabetes consume a high atherogenic diet? 7-year follow-up of the EURODIAB Prospective Complications Study. Eur J Nutr 2013; 52: 1701–1710.

    Article  CAS  PubMed  Google Scholar 

  28. Tielemans SM, Soedamah-Muthu SS, De Neve M, Toeller M, Chaturvedi N, Fuller JH et al. Association of physical activity with all-cause mortality and incident and prevalent cardiovascular disease among patients with type 1 diabetes: the EURODIAB Prospective Complications Study. Diabetologia 2012; 56: 82–91.

    Article  PubMed  Google Scholar 

  29. Toeller M, Buyken AE, Heitkamp G, Cathelineau G, Ferriss B, Michel G et al. Nutrient intakes as predictors of body weight in European people with type 1 diabetes. Int J Obes Relat Metab Disord 2001; 25: 1815–1822.

    Article  CAS  PubMed  Google Scholar 

  30. Chaturvedi N, Bandinelli S, Mangili R, Penno G, Rottiers RE, Fuller JH . Microalbuminuria in type 1 diabetes: rates, risk factors and glycemic threshold. Kidney Int 2001; 60: 219–227.

    Article  CAS  PubMed  Google Scholar 

  31. Hanas R, John G, International HBAcCC. 2010 consensus statement on the worldwide standardization of the hemoglobin A1C measurement. Diabetes Care 2010; 33: 1903–1904.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Friedewald WT, Levy RI, Fredrickson DS . Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18: 499–502.

    CAS  PubMed  Google Scholar 

  33. Desquilbet L, Mariotti F . Dose-response analyses using restricted cubic spline functions in public health research. Stat Med 2010; 29: 1037–1057.

    PubMed  Google Scholar 

  34. Harrell FE . Regression Modeling Strategies: with Applications to Linear Models, Logistic Regression, and Survival Analysis. Springer-Varlag: New York, 2001.

    Book  Google Scholar 

  35. Heinzl H, Kaider A . Manual for the SAS-Macro RCS. http://cemsiis.meduniwien.ac.at/kb/wf/software/statistische-software/rcs/SAS Institute Inc, 2007.

    Google Scholar 

  36. Boeing H, Weisgerber UM, Jeckel A, Rose HJ, Kroke A . Association between glycated hemoglobin and diet and other lifestyle factors in a nondiabetic population: cross-sectional evaluation of data from the Potsdam cohort of the European Prospective Investigation into Cancer and Nutrition Study. Am J Clin Nutr 2000; 71: 1115–1122.

    Article  CAS  PubMed  Google Scholar 

  37. Prynne CJ, Mander A, Wadsworth ME, Stephen AM . Diet and glycosylated haemoglobin in the 1946 British birth cohort. Eur J Clin Nutr 2009; 63: 1084–1090.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Altorf-van der Kuil W, Engberink MF, Ijpma I, Verberne LD, Toeller M, Chaturvedi N et al. Protein intake in relation to risk of hypertension and microalbuminuria in patients with type 1 diabetes: the EURODIAB Prospective Complications Study. J Hypertens 2013; 31: 1151–1159.

    Article  CAS  PubMed  Google Scholar 

  39. Mollsten AV, Dahlquist GG, Stattin EL, Rudberg S . Higher intakes of fish protein are related to a lower risk of microalbuminuria in young Swedish type 1 diabetic patients. Diabetes Care 2001; 24: 805–810.

    Article  CAS  PubMed  Google Scholar 

  40. American Diabetes Association. Executive summary: Standards of medical care in diabetes—2013. Diabetes Care 2013; 36: S4–10.

  41. Authors/Task Force Members, Ryden L, Grant PJ, Anker SD, Berne C, Cosentino F et al. ESC Guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD: the Task Force on diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and developed in collaboration with the European Association for the Study of Diabetes (EASD). Eur Heart J 2013; 34: 3035–3087.

    Article  Google Scholar 

  42. Schoenaker DA, Toeller M, Chaturvedi N, Fuller JH, Soedamah-Muthu SS Group EPCS. Dietary saturated fat and fibre and risk of cardiovascular disease and all-cause mortality among type 1 diabetic patients: the EURODIAB Prospective Complications Study. Diabetologia 2012; 55: 2132–2141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wallstrom P, Sonestedt E, Hlebowicz J, Ericson U, Drake I, Persson M et al. Dietary fiber and saturated fat intake associations with cardiovascular disease differ by sex in the Malmo Diet and Cancer Cohort: a prospective study. PloS One 2012; 7: e31637.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Diabetes Control and Complications Trial Research Group. Implementation of treatment protocols in the Diabetes Control and Complications Trial. Diabetes Care 1995; 18: 361–376.

  45. Post RE, Mainous AG 3rd, King DE, Simpson KN . Dietary fiber for the treatment of type 2 diabetes mellitus: a meta-analysis. J Am Board Fam Med 2012; 25: 16–23.

    Article  PubMed  Google Scholar 

  46. Lamichhane AP, Crandell JL, Jaacks LM, Couch SC, Lawrence JM, Mayer-Davis EJ . Longitudinal associations of nutritional factors with glycated hemoglobin in youth with type 1 diabetes: the SEARCH Nutrition Ancillary Study. Am J Clin Nutr 2015; 101: 1278–1285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Snell-Bergeon JK, Chartier-Logan C, Maahs DM, Ogden LG, Hokanson JE, Kinney GL et al. Adults with type 1 diabetes eat a high-fat atherogenic diet that is associated with coronary artery calcium. Diabetologia 2009; 52: 801–809.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Maffeis C, Morandi A, Ventura E, Sabbion A, Contreas G, Tomasselli F et al. Diet, physical, and biochemical characteristics of children and adolescents with type 1 diabetes: relationship between dietary fat and glucose control. Pediatr Diabetes 2012; 13: 137–146.

    Article  CAS  PubMed  Google Scholar 

  49. Snell-Bergeon JK, Wadwa RP . Hypoglycemia, diabetes, and cardiovascular disease. Diabetes Technol Ther 2012; 14: S51–S58.

    Article  CAS  PubMed  Google Scholar 

  50. Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 1993; 329: 977–986.

    Article  Google Scholar 

  51. Kromhout D, Geleijnse JM, Menotti A, Jacobs DR Jr. . The confusion about dietary fatty acids recommendations for CHD prevention. Br J Nutr 2011; 106: 627–632.

    Article  CAS  PubMed  Google Scholar 

  52. Beulens JW, Kruidhof JS, Grobbee DE, Chaturvedi N, Fuller JH, Soedamah-Muthu SS . Alcohol consumption and risk of microvascular complications in type 1 diabetes patients: the EURODIAB Prospective Complications Study. Diabetologia 2008; 51: 1631–1638.

    Article  CAS  PubMed  Google Scholar 

  53. Jaacks LM, Crandell J, Mendez MA, Lamichhane AP, Liu W, Ji L et al. Dietary patterns associated with HbA1c and LDL cholesterol among individuals with type 1 diabetes in China. J Diabetes Complications 2015; 29: 343–349.

    Article  PubMed  Google Scholar 

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Acknowledgements

The EURODIAB Prospective Complications Study was supported by grants from the Wellcome Trust, the European Community and Diabetes UK. Additional financial support was received from Gesellschaft der Freunde und Foerderer of Heinrich-Heine-University Duesseldorf, Germany, to the Nutrition Co-ordinating Centre (MT). Sponsors had no influence on the design, the performance of the study, analysis and interpretation of the results.

Author Contributions

SNB and SSS-M were responsible for conception and design. SNB was responsible for drafting of the manuscript. SNB, DAJMS and SSS-M contributed to the analysis and interpretation of the data. DAJMS, GDM, MT, NC, JHF and SSS-M contributed to critical revision of the manuscript for important intellectual content. All authors approved the final version.

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Author notes

  1. S N Balk, D A J M Schoenaker, G D Mishra, M Toeller, N Chaturvedi, J H Fuller and S S Soedamah-Muthu: See Electronic Supplementary Material for a complete list of the members of the EURODIAB Prospective Complications Study Group.

Authors and Affiliations

  1. Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands

    S N Balk & S S Soedamah-Muthu

  2. School of Public Health, University of Queensland, Brisbane, Queensland, Australia

    D A J M Schoenaker & G D Mishra

  3. Diabetes Research Institute, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany

    M Toeller

  4. Department of Epidemiology and Public-Health, University College London, London, UK

    N Chaturvedi & J H Fuller

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  1. S N Balk
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Correspondence to S S Soedamah-Muthu.

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Balk, S., Schoenaker, D., Mishra, G. et al. Association of diet and lifestyle with glycated haemoglobin in type 1 diabetes participants in the EURODIAB prospective complications study. Eur J Clin Nutr 70, 229–236 (2016). https://doi.org/10.1038/ejcn.2015.110

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