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Published in: Cardiovascular Diabetology 1/2015

Open Access 01-12-2015 | Original investigation

Isocaloric substitution of carbohydrates with protein: the association with weight change and mortality among patients with type 2 diabetes

Authors: Marjo JE Campmans-Kuijpers, Ivonne Sluijs, Ute Nöthlings, Heinz Freisling, Kim Overvad, Elisabete Weiderpass, Guy Fagherazzi, Tilman Kühn, Verena A Katzke, Amalia Mattiello, Emily Sonestedt, Giovanna Masala, Claudia Agnoli, Rosario Tumino, Annemieke MW Spijkerman, Aurelio Barricarte, Fulvio Ricceri, Saioa Chamosa, Ingegerd Johansson, Anna Winkvist, Anne Tjønneland, Diewertje Sluik, Heiner Boeing, Joline WJ Beulens

Published in: Cardiovascular Diabetology | Issue 1/2015

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Abstract

Background

The health impact of dietary replacement of carbohydrates with protein for patients with type 2 diabetes is still debated. This study aimed to investigate the association between dietary substitution of carbohydrates with (animal and plant) protein and 5-year weight change, and all-cause and cardiovascular (CVD) mortality risk in patients with type 2 diabetes.

Methods

The study included 6,107 diabetes patients from 15 European cohorts. Patients with type 1 diabetes were excluded. At recruitment, validated country-specific food-frequency questionnaires were used to estimate dietary intake. Multivariable adjusted linear regression was used to examine the associations between dietary carbohydrate substitution with protein and 5-year weight change, and Cox regression to estimate hazard ratios (HRs) for (CVD) mortality.

Results

Annual weight loss of patients with type 2 diabetes was 0.17 (SD 1.24) kg. After a mean follow-up of 9.2 (SD 2.3)y, 787 (13%) participants had died, of which 266 (4%) deaths were due to CVD. Substitution of 10 gram dietary carbohydrate with total (ß = 187 [75;299]g) and animal (ß = 196 [137;254]g) protein was associated with mean 5-year weight gain. Substitution for plant protein was not significantly associated with weight change (β = 82 [−421;584]g). Substitution with plant protein was associated with lower all-cause mortality risk (HR = 0.79 [0.64;0.97]), whereas substitution with total or animal protein was not associated with (CVD) mortality risk.

Conclusions

In diabetes patients, substitution with plant protein was beneficial with respect to weight change and all-cause mortality as opposed to substitution with animal protein. Therefore, future research is needed whether dietary guidelines should not actively promote substitution of carbohydrates by total protein, but rather focus on substitution of carbohydrates with plant protein.
Literature
1.
go back to reference Aucott L, Poobalan A, Smith WC, Avenell A, Jung R, Broom J, et al. Weight loss in obese diabetic and non-diabetic individuals and long-term diabetes outcomes–a systematic review. Diab Obes Metab. 2004;6(2):85–94.CrossRef Aucott L, Poobalan A, Smith WC, Avenell A, Jung R, Broom J, et al. Weight loss in obese diabetic and non-diabetic individuals and long-term diabetes outcomes–a systematic review. Diab Obes Metab. 2004;6(2):85–94.CrossRef
2.
go back to reference Health Council of the Netherlands. Guidelines for a healthy diet 2006. publication no. 2006/21. The Hague: Health Council of the Netherlands; 2006. Health Council of the Netherlands. Guidelines for a healthy diet 2006. publication no. 2006/21. The Hague: Health Council of the Netherlands; 2006.
3.
go back to reference Food and Nutrition Board. Dietary reference intakes for energy, carbohydrate, fiber, Fat, fatty acids, cholesterol, protein, and amino acids (macronutrients). Washington, D.C: The National Academies Press. A Report of the Panel on Macronutrients, Subcommittees on Upper Reference Levels of Nutrients and Interpretation and Uses of Dietary Reference Intakes, and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. 26-4-2013; 2013. Food and Nutrition Board. Dietary reference intakes for energy, carbohydrate, fiber, Fat, fatty acids, cholesterol, protein, and amino acids (macronutrients). Washington, D.C: The National Academies Press. A Report of the Panel on Macronutrients, Subcommittees on Upper Reference Levels of Nutrients and Interpretation and Uses of Dietary Reference Intakes, and the Standing Committee on the Scientific Evaluation of Dietary Reference Intakes. 26-4-2013; 2013.
4.
go back to reference The Diabetes and Nutrition Study Group (DNSG) of the European Association for the Study of Diabetes (EASD). Recommendations for the nutritional management of patients with diabetes mellitus. Eur J Clin Nutr. 2000;54(4):353–5.CrossRef The Diabetes and Nutrition Study Group (DNSG) of the European Association for the Study of Diabetes (EASD). Recommendations for the nutritional management of patients with diabetes mellitus. Eur J Clin Nutr. 2000;54(4):353–5.CrossRef
5.
go back to reference Dyson PA, Kelly T, Deakin T, Duncan A, Frost G, Harrison Z, et al. Diabetes UK evidence-based nutrition guidelines for the prevention and management of diabetes. Diabet Med. 2011;28(11):1282–8.CrossRefPubMed Dyson PA, Kelly T, Deakin T, Duncan A, Frost G, Harrison Z, et al. Diabetes UK evidence-based nutrition guidelines for the prevention and management of diabetes. Diabet Med. 2011;28(11):1282–8.CrossRefPubMed
6.
go back to reference Allen FM, Stilman E, Fitz R. Total dietary regulation in the treatment of diabetes. Monograph No.11. New York: The Rockefeller Institute for Medical Research; 1919. Allen FM, Stilman E, Fitz R. Total dietary regulation in the treatment of diabetes. Monograph No.11. New York: The Rockefeller Institute for Medical Research; 1919.
7.
go back to reference Kennedy RL, Chokkalingam K, Farshchi HR. Nutrition in patients with Type 2 diabetes: are low-carbohydrate diets effective, safe or desirable? Diabet Med. 2005;22(7):821–32.CrossRefPubMed Kennedy RL, Chokkalingam K, Farshchi HR. Nutrition in patients with Type 2 diabetes: are low-carbohydrate diets effective, safe or desirable? Diabet Med. 2005;22(7):821–32.CrossRefPubMed
8.
go back to reference Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, et al. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr. 2005;82(1):41–8.PubMed Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, et al. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr. 2005;82(1):41–8.PubMed
9.
go back to reference Larsen TM, Dalskov SM, van Baak M, Jebb SA, Papadaki A, Pfeiffer AF, et al. Diets with high or low protein content and glycemic index for weight-loss maintenance. N Engl J Med. 2010;363(22):2102–13.CrossRefPubMedCentralPubMed Larsen TM, Dalskov SM, van Baak M, Jebb SA, Papadaki A, Pfeiffer AF, et al. Diets with high or low protein content and glycemic index for weight-loss maintenance. N Engl J Med. 2010;363(22):2102–13.CrossRefPubMedCentralPubMed
10.
go back to reference Ankarfeldt MZ, Gottliebsen K, Angquist L, Astrup A, Heitmann BL, Sorensen TI. Dietary protein and urinary nitrogen in relation to 6-year changes in fat mass and fat-free mass. Int J Obes (Lond). 2015;39(1):162–8.CrossRef Ankarfeldt MZ, Gottliebsen K, Angquist L, Astrup A, Heitmann BL, Sorensen TI. Dietary protein and urinary nitrogen in relation to 6-year changes in fat mass and fat-free mass. Int J Obes (Lond). 2015;39(1):162–8.CrossRef
11.
go back to reference Westerterp-Plantenga MS, Nieuwenhuizen A, Tome D, Soenen S, Westerterp KR. Dietary protein, weight loss, and weight maintenance. Annu Rev Nutr. 2009;29:21–41.CrossRefPubMed Westerterp-Plantenga MS, Nieuwenhuizen A, Tome D, Soenen S, Westerterp KR. Dietary protein, weight loss, and weight maintenance. Annu Rev Nutr. 2009;29:21–41.CrossRefPubMed
12.
go back to reference Pedersen AN, Kondrup J, Borsheim E. Health effects of protein intake in healthy adults: a systematic literature review. Food Nutr Res. 2013;57:1–29.CrossRef Pedersen AN, Kondrup J, Borsheim E. Health effects of protein intake in healthy adults: a systematic literature review. Food Nutr Res. 2013;57:1–29.CrossRef
13.
go back to reference Vergnaud AC, Norat T, Mouw T, Romaguera, May AM, Bueno-De-Mesquita HB, et al. Macronutrient composition of the diet and prospective weight change in participants of the EPIC-PANACEA study. PLoS One. 2013;8(3), e57300.CrossRefPubMedCentralPubMed Vergnaud AC, Norat T, Mouw T, Romaguera, May AM, Bueno-De-Mesquita HB, et al. Macronutrient composition of the diet and prospective weight change in participants of the EPIC-PANACEA study. PLoS One. 2013;8(3), e57300.CrossRefPubMedCentralPubMed
14.
go back to reference Bujnowski D, Xun P, Daviglus ML, Van Horn L, He K, Stamler J. Longitudinal association between animal and vegetable protein intake and obesity among men in the United States: the Chicago Western Electric Study. J Am Diet Assoc. 2011;111(8):1150–5.CrossRefPubMedCentralPubMed Bujnowski D, Xun P, Daviglus ML, Van Horn L, He K, Stamler J. Longitudinal association between animal and vegetable protein intake and obesity among men in the United States: the Chicago Western Electric Study. J Am Diet Assoc. 2011;111(8):1150–5.CrossRefPubMedCentralPubMed
15.
go back to reference Larsen RN, Mann NJ, Maclean E, Shaw JE. The effect of high-protein, low-carbohydrate diets in the treatment of type 2 diabetes: a 12 month randomised controlled trial. Diabetologia. 2011;54(4):731–40.CrossRefPubMed Larsen RN, Mann NJ, Maclean E, Shaw JE. The effect of high-protein, low-carbohydrate diets in the treatment of type 2 diabetes: a 12 month randomised controlled trial. Diabetologia. 2011;54(4):731–40.CrossRefPubMed
16.
go back to reference Krebs JD, Elley CR, Parry-Strong A, Lunt H, Drury PL, Bell DA, et al. The Diabetes Excess Weight Loss (DEWL) Trial: a randomised controlled trial of high-protein versus high-carbohydrate diets over 2 years in type 2 diabetes. Diabetologia. 2012;55(4):905–14.CrossRefPubMed Krebs JD, Elley CR, Parry-Strong A, Lunt H, Drury PL, Bell DA, et al. The Diabetes Excess Weight Loss (DEWL) Trial: a randomised controlled trial of high-protein versus high-carbohydrate diets over 2 years in type 2 diabetes. Diabetologia. 2012;55(4):905–14.CrossRefPubMed
17.
go back to reference Parker B, Noakes M, Luscombe N, Clifton P. Effect of a high-protein, high-monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes Care. 2002;25(3):425–30.CrossRefPubMed Parker B, Noakes M, Luscombe N, Clifton P. Effect of a high-protein, high-monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes Care. 2002;25(3):425–30.CrossRefPubMed
18.
go back to reference Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5(6B):1113–24.CrossRefPubMed Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5(6B):1113–24.CrossRefPubMed
19.
go back to reference Nothlings U, Boeing H, Maskarinec G, Sluik D, Teucher B, Kaaks R, et al. Food intake of individuals with and without diabetes across different countries and ethnic groups. Eur J Clin Nutr. 2011;65(5):635–41.CrossRefPubMedCentralPubMed Nothlings U, Boeing H, Maskarinec G, Sluik D, Teucher B, Kaaks R, et al. Food intake of individuals with and without diabetes across different countries and ethnic groups. Eur J Clin Nutr. 2011;65(5):635–41.CrossRefPubMedCentralPubMed
20.
go back to reference Sluik D, Boeing H, Montonen J, Pischon T, Kaaks R, Teucher B, et al. Associations between general and abdominal adiposity and mortality in individuals with diabetes mellitus. Am J Epidemiol. 2011;174(1):22–34.CrossRefPubMed Sluik D, Boeing H, Montonen J, Pischon T, Kaaks R, Teucher B, et al. Associations between general and abdominal adiposity and mortality in individuals with diabetes mellitus. Am J Epidemiol. 2011;174(1):22–34.CrossRefPubMed
21.
go back to reference Margetts BM, Pietinen P. European prospective investigation into cancer and nutrition: validity studies on dietary assessment methods. Int J Epidemiol. 1997;26 Suppl 1:S1–5.CrossRefPubMed Margetts BM, Pietinen P. European prospective investigation into cancer and nutrition: validity studies on dietary assessment methods. Int J Epidemiol. 1997;26 Suppl 1:S1–5.CrossRefPubMed
22.
go back to reference Schofield C. An annotated bibliography of source material for basal metabolic rate data. Hum Nutr Clin Nutr. 1985;39 Suppl 1:42–91.PubMed Schofield C. An annotated bibliography of source material for basal metabolic rate data. Hum Nutr Clin Nutr. 1985;39 Suppl 1:42–91.PubMed
23.
go back to reference Goldberg GR, Black AE, Jebb SA, Cole TJ, Murgatryd PR, Coward WA, et al. Critical evaluation of energy intake data using fundamental principles of energy physiology: 1. Derivation of cut-off limits to identify under-recording. Eur J Clin Nutr. 1991;45(12):569–81.PubMed Goldberg GR, Black AE, Jebb SA, Cole TJ, Murgatryd PR, Coward WA, et al. Critical evaluation of energy intake data using fundamental principles of energy physiology: 1. Derivation of cut-off limits to identify under-recording. Eur J Clin Nutr. 1991;45(12):569–81.PubMed
24.
go back to reference van Bakel MM, Kaaks R, Feskens EJ, Rohrmann S, Welch AA, Pala V, et al. Dietary glycaemic index and glycaemic load in the European Prospective Investigation into Cancer and Nutrition. Eur J Clin Nutr. 2009;63 Suppl 4:S188–205.CrossRefPubMed van Bakel MM, Kaaks R, Feskens EJ, Rohrmann S, Welch AA, Pala V, et al. Dietary glycaemic index and glycaemic load in the European Prospective Investigation into Cancer and Nutrition. Eur J Clin Nutr. 2009;63 Suppl 4:S188–205.CrossRefPubMed
25.
go back to reference Foster-Powell K, Holt SH, Brand-Miller JC. International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr. 2002;76(1):5–56.PubMed Foster-Powell K, Holt SH, Brand-Miller JC. International table of glycemic index and glycemic load values: 2002. Am J Clin Nutr. 2002;76(1):5–56.PubMed
26.
go back to reference Henry CJ, Lightowler HJ, Strik CM, Storey M. Glycaemic index values for commercially available potatoes in Great Britain. Br J Nutr. 2005;94(6):917–21.CrossRefPubMed Henry CJ, Lightowler HJ, Strik CM, Storey M. Glycaemic index values for commercially available potatoes in Great Britain. Br J Nutr. 2005;94(6):917–21.CrossRefPubMed
27.
go back to reference Atkinson FS, Foster-Powell K, Brand-Miller JC. International tables of glycemic index and glycemic load values: 2008. Diabetes Care. 2008;31(12):2281–3.CrossRefPubMedCentralPubMed Atkinson FS, Foster-Powell K, Brand-Miller JC. International tables of glycemic index and glycemic load values: 2008. Diabetes Care. 2008;31(12):2281–3.CrossRefPubMedCentralPubMed
28.
go back to reference Haftenberger M, Lahmann PH, Panico S, Gonzalez CA, Seidell JC, Boeing H, et al. Overweight, obesity and fat distribution in 50- to 64-year-old participants in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2002;5(6B):1147–62.CrossRefPubMed Haftenberger M, Lahmann PH, Panico S, Gonzalez CA, Seidell JC, Boeing H, et al. Overweight, obesity and fat distribution in 50- to 64-year-old participants in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2002;5(6B):1147–62.CrossRefPubMed
29.
go back to reference Wareham NJ, Jakes RW, Rennie KL, Schuit J, Mitchell J, Hennings S, et al. Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr. 2003;6(4):407–13.CrossRefPubMed Wareham NJ, Jakes RW, Rennie KL, Schuit J, Mitchell J, Hennings S, et al. Validity and repeatability of a simple index derived from the short physical activity questionnaire used in the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr. 2003;6(4):407–13.CrossRefPubMed
30.
go back to reference Interact Consortium, Peters T, Brage S, Westgate K, Franks PW, Gradmark A, et al. Validity of a short questionnaire to assess physical activity in 10 European countries. Eur J Epidemiol. 2012;27(1):15–25.CrossRef Interact Consortium, Peters T, Brage S, Westgate K, Franks PW, Gradmark A, et al. Validity of a short questionnaire to assess physical activity in 10 European countries. Eur J Epidemiol. 2012;27(1):15–25.CrossRef
31.
go back to reference Marshall A, Altman DG, Holder RL, Royston P. Combining estimates of interest in prognostic modelling studies after multiple imputation: current practice and guidelines. BMC Med Res Methodol. 2009;9:57.CrossRefPubMedCentralPubMed Marshall A, Altman DG, Holder RL, Royston P. Combining estimates of interest in prognostic modelling studies after multiple imputation: current practice and guidelines. BMC Med Res Methodol. 2009;9:57.CrossRefPubMedCentralPubMed
32.
go back to reference Willett WC, Howe GR, Kushi LH. Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr. 1997;65(4 Suppl):1220S–8.PubMed Willett WC, Howe GR, Kushi LH. Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr. 1997;65(4 Suppl):1220S–8.PubMed
33.
go back to reference Ankarfeldt MZ, Angquist L, Jakobsen MU, Overvad K, Tjonneland A, Halkjaer J, et al. Interactions of dietary protein and adiposity measures in relation to subsequent changes in body weight and waist circumference. Obesity (Silver Spring). 2014;22(9):2097–103.CrossRef Ankarfeldt MZ, Angquist L, Jakobsen MU, Overvad K, Tjonneland A, Halkjaer J, et al. Interactions of dietary protein and adiposity measures in relation to subsequent changes in body weight and waist circumference. Obesity (Silver Spring). 2014;22(9):2097–103.CrossRef
34.
go back to reference May AM, Barnes DR, Forouhi NG, Luben R, Khaw KT, Wareham NJ, et al. Prediction of measured weight from self-reported weight was not improved after stratification by body mass index. Obesity (Silver Spring). 2013;21(1):E137–42.CrossRef May AM, Barnes DR, Forouhi NG, Luben R, Khaw KT, Wareham NJ, et al. Prediction of measured weight from self-reported weight was not improved after stratification by body mass index. Obesity (Silver Spring). 2013;21(1):E137–42.CrossRef
35.
go back to reference Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudrreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009;32(11):1993–7.CrossRefPubMedCentralPubMed Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudrreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care. 2009;32(11):1993–7.CrossRefPubMedCentralPubMed
36.
go back to reference Daniels JA, Mulligan C, McCance D, Woodside JV, Patterdon C, Young IS, et al. A randomised controlled trial of increasing fruit and vegetable intake and how this influences the carotenoid concentration and activities of PON-1 and LCAT in HDL from subjects with type 2 diabetes. Cardiovasc Diabetol. 2014;13:16.CrossRefPubMedCentralPubMed Daniels JA, Mulligan C, McCance D, Woodside JV, Patterdon C, Young IS, et al. A randomised controlled trial of increasing fruit and vegetable intake and how this influences the carotenoid concentration and activities of PON-1 and LCAT in HDL from subjects with type 2 diabetes. Cardiovasc Diabetol. 2014;13:16.CrossRefPubMedCentralPubMed
37.
go back to reference Ceriello A, Esposito K, La Sala L, Pujadas G, De Nigris V, Testa R, et al. The protective effect of the Mediterranean diet on endothelial resistance to GLP-1 in type 2 diabetes: a preliminary report. Cardiovasc Diabetol. 2014;13(1):140.CrossRefPubMedCentralPubMed Ceriello A, Esposito K, La Sala L, Pujadas G, De Nigris V, Testa R, et al. The protective effect of the Mediterranean diet on endothelial resistance to GLP-1 in type 2 diabetes: a preliminary report. Cardiovasc Diabetol. 2014;13(1):140.CrossRefPubMedCentralPubMed
38.
go back to reference Mirrahimi A, Chiavaroli L, Srichaikul K, Augustin LS, Sievenpiper JL, Kendall CW, et al. The role of glycemic index and glycemic load in cardiovascular disease and its risk factors: a review of the recent literature. Curr Atheroscler Rep. 2014;16(1):381.CrossRefPubMed Mirrahimi A, Chiavaroli L, Srichaikul K, Augustin LS, Sievenpiper JL, Kendall CW, et al. The role of glycemic index and glycemic load in cardiovascular disease and its risk factors: a review of the recent literature. Curr Atheroscler Rep. 2014;16(1):381.CrossRefPubMed
39.
go back to reference Burger KN, Beulens JW, van der Schouw YT, Sluijs I, Spijkerman AM, Sluik D, et al. Dietary fiber, carbohydrate quality and quantity, and mortality risk of individuals with diabetes mellitus. PLoS One. 2012;7(8), e43127.CrossRefPubMedCentralPubMed Burger KN, Beulens JW, van der Schouw YT, Sluijs I, Spijkerman AM, Sluik D, et al. Dietary fiber, carbohydrate quality and quantity, and mortality risk of individuals with diabetes mellitus. PLoS One. 2012;7(8), e43127.CrossRefPubMedCentralPubMed
40.
go back to reference Nagel G, Zoller D, Ruf T, Rohrmann S, Linseisen J. Long-term reproducibility of a food-frequency questionnaire and dietary changes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heidelberg cohort. Br J Nutr. 2007;98(1):194–200.CrossRefPubMed Nagel G, Zoller D, Ruf T, Rohrmann S, Linseisen J. Long-term reproducibility of a food-frequency questionnaire and dietary changes in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Heidelberg cohort. Br J Nutr. 2007;98(1):194–200.CrossRefPubMed
41.
go back to reference Johansson I, Nilsson LM, Stegmayr B, Boman K, Hallmans G, Winkvist A. Associations among 25-year trends in diet, cholesterol and BMI from 140,000 observations in men and women in Northern Sweden. Nutr J. 2012;11:40.CrossRefPubMedCentralPubMed Johansson I, Nilsson LM, Stegmayr B, Boman K, Hallmans G, Winkvist A. Associations among 25-year trends in diet, cholesterol and BMI from 140,000 observations in men and women in Northern Sweden. Nutr J. 2012;11:40.CrossRefPubMedCentralPubMed
42.
go back to reference Heitmann BL, Lissner L, Osler M. Do we eat less fat, or just report so? Int J Obes Relat Metab Disord. 2000;24(4):435–42.CrossRefPubMed Heitmann BL, Lissner L, Osler M. Do we eat less fat, or just report so? Int J Obes Relat Metab Disord. 2000;24(4):435–42.CrossRefPubMed
43.
go back to reference Freisling H, van Bakel MM, Biessy C, May AM, Byrnes G, Norat T, et al. Dietary reporting errors on 24 h recalls and dietary questionnaires are associated with BMI across six European countries as evaluated with recovery biomarkers for protein and potassium intake. Br J Nutr. 2012;107(6):910–20.CrossRefPubMed Freisling H, van Bakel MM, Biessy C, May AM, Byrnes G, Norat T, et al. Dietary reporting errors on 24 h recalls and dietary questionnaires are associated with BMI across six European countries as evaluated with recovery biomarkers for protein and potassium intake. Br J Nutr. 2012;107(6):910–20.CrossRefPubMed
Metadata
Title
Isocaloric substitution of carbohydrates with protein: the association with weight change and mortality among patients with type 2 diabetes
Authors
Marjo JE Campmans-Kuijpers
Ivonne Sluijs
Ute Nöthlings
Heinz Freisling
Kim Overvad
Elisabete Weiderpass
Guy Fagherazzi
Tilman Kühn
Verena A Katzke
Amalia Mattiello
Emily Sonestedt
Giovanna Masala
Claudia Agnoli
Rosario Tumino
Annemieke MW Spijkerman
Aurelio Barricarte
Fulvio Ricceri
Saioa Chamosa
Ingegerd Johansson
Anna Winkvist
Anne Tjønneland
Diewertje Sluik
Heiner Boeing
Joline WJ Beulens
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2015
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-015-0202-7

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