Skip to main content
Top
Published in: Diabetologia 8/2018

Open Access 01-08-2018 | Article

Nuts as a replacement for carbohydrates in the diabetic diet: a reanalysis of a randomised controlled trial

Authors: David J. A. Jenkins, Cyril W. C. Kendall, Benoît Lamarche, Monica S. Banach, Korbua Srichaikul, Edward Vidgen, Sandy Mitchell, Tina Parker, Stephanie Nishi, Balachandran Bashyam, Russell J. de Souza, Christopher Ireland, Sathish C. Pichika, Joseph Beyene, John L. Sievenpiper, Robert G. Josse

Published in: Diabetologia | Issue 8/2018

Login to get access

Abstract

Aims/hypothesis

In line with current advice, we assessed the effect of replacing carbohydrate consumption with mixed nut consumption, as a source of unsaturated fat, on cardiovascular risk factors and HbA1c in type 2 diabetes. The data presented here are from a paper that was retracted at the authors’ request (https://​doi.​org/​10.​2337/​dc16-rt02) owing to lack of adjustment for repeated measures in the same individual. Our aim, therefore, was to fix the error and add new complementary data of interest, including information on clotting factors and LDL particle size.

Methods

A total of 117 men and postmenopausal women with type 2 diabetes who were taking oral glucose-lowering agents and with HbA1c between 47.5 and 63.9 mmol/mol (6.5–8.0%) were randomised after stratification by sex and baseline HbA1c in a parallel design to one of three diets for 3 months: (1) ‘full-dose nut diet’ (n = 40): a diet with 2.0 MJ (477 kcal) per 8.4 MJ (2000 kcal) energy provided as mixed nuts (75 g/day); (2) ‘full-dose muffin diet’ (n = 39): a diet with 1.97 MJ (471 kcal) per 8.4 MJ (2000 kcal) energy provided as three whole-wheat muffins (188 g/day), with a similar protein content to the nuts, and the same carbohydrate-derived energy content as the monounsaturated fatty acid-derived energy content in the nuts; or (3) ‘half-dose nut diet’ (n = 38): a diet with 1.98 MJ (474 kcal) per 8.4 MJ (2000 kcal) energy provided as half portions of both the nuts and muffins. The primary outcome was change in HbA1c. The study was carried out in a hospital clinical research centre and concluded in 2008. Only the statistician, study physicians and analytical technicians could be blinded to the group assessment.

Results

A total of 108 participants had post-intervention data available for analysis (full-dose nut group, n = 40; full-dose muffin group, n = 35; half-dose nut group, n = 33). Compared with the full-dose muffin diet, the full-dose nut diet provided 9.2% (95% CI 7.1, 11.3) greater total energy intake from monounsaturated fat. The full-dose nut diet (median intake, 75 g/day) also reduced HbA1c compared with the full-dose muffin diet by −2.0 mmol/mol (95% CI −3.8, −0.3 mmol/mol) (−0.19% [95% CI −0.35%, −0.02%]), (p = 0.026). Estimated cholesterol levels in LDL particles with a diameter <255 ångström [LDL-c<255Å]) and apolipoprotein B were also significantly decreased after the full-dose nut diet compared with the full-dose muffin diet. According to the dose response, the full-dose nut diet is predicted to reduce HbA1c (−2.0 mmol/mol [−0.18%]; p = 0.044), cholesterol (−0.25 mmol/l; p = 0.022), LDL-cholesterol (−0.23 mmol/l; p = 0.019), non-HDL-cholesterol (−0.26 mmol/l; p = 0.020), apolipoprotein B (−0.06 g/l, p = 0.013) and LDL-c<255Å (−0.42 mmol/l; p < 0.001). No serious study-related adverse events occurred, but one participant on the half-dose nut diet was hospitalised for atrial fibrillation after shovelling snow.

Conclusions/interpretation

Nut intake as a replacement for carbohydrate consumption improves glycaemic control and lipid risk factors in individuals with type 2 diabetes.

Trial registration

Funding

The study was funded by the International Tree Nut Council Nutrition Research and Education Foundation, the Peanut Institute, Loblaw Companies and the Canada Research Chairs Program of the Government of Canada
Appendix
Available only for authorised users
Literature
1.
go back to reference Halton TL, Liu S, Manson JE, Hu FB (2008) Low-carbohydrate-diet score and risk of type 2 diabetes in women. Am J Clin Nutr 87:339–346CrossRef Halton TL, Liu S, Manson JE, Hu FB (2008) Low-carbohydrate-diet score and risk of type 2 diabetes in women. Am J Clin Nutr 87:339–346CrossRef
2.
go back to reference Pan A, Sun Q, Manson JE, Willett WC, Hu FB (2013) Walnut consumption is associated with lower risk of type 2 diabetes in women. J Nutr 143:512–518CrossRef Pan A, Sun Q, Manson JE, Willett WC, Hu FB (2013) Walnut consumption is associated with lower risk of type 2 diabetes in women. J Nutr 143:512–518CrossRef
3.
go back to reference Bao Y, Han J, Hu FB et al (2013) Association of nut consumption with total and cause-specific mortality. N Engl J Med 369:2001–2011CrossRef Bao Y, Han J, Hu FB et al (2013) Association of nut consumption with total and cause-specific mortality. N Engl J Med 369:2001–2011CrossRef
4.
go back to reference Mayhew AJ, de Souza RJ, Meyre D, Anand SS, Mente A (2016) A systematic review and meta-analysis of nut consumption and incident risk of CVD and all-cause mortality. Br J Nutr 115:212–225CrossRef Mayhew AJ, de Souza RJ, Meyre D, Anand SS, Mente A (2016) A systematic review and meta-analysis of nut consumption and incident risk of CVD and all-cause mortality. Br J Nutr 115:212–225CrossRef
5.
go back to reference Estruch R, Ros E, Salas-Salvado J et al (2013) Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med 368:1279–1290CrossRef Estruch R, Ros E, Salas-Salvado J et al (2013) Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med 368:1279–1290CrossRef
6.
go back to reference Salas-Salvado J, Bullo M, Babio N et al (2011) Reduction in the incidence of type 2 diabetes with the Mediterranean diet: results of the PREDIMED-Reus nutrition intervention randomized trial. Diabetes Care 34:14–19CrossRef Salas-Salvado J, Bullo M, Babio N et al (2011) Reduction in the incidence of type 2 diabetes with the Mediterranean diet: results of the PREDIMED-Reus nutrition intervention randomized trial. Diabetes Care 34:14–19CrossRef
7.
go back to reference Sabate J, Oda K, Ros E (2010) Nut consumption and blood lipid levels: a pooled analysis of 25 intervention trials. Arch Intern Med 170:821–827CrossRef Sabate J, Oda K, Ros E (2010) Nut consumption and blood lipid levels: a pooled analysis of 25 intervention trials. Arch Intern Med 170:821–827CrossRef
8.
go back to reference Sauder KA, McCrea CE, Ulbrecht JS, Kris-Etherton PM, West SG (2015) Effects of pistachios on the lipid/lipoprotein profile, glycaemic control, inflammation, and endothelial function in type 2 diabetes: a randomized trial. Metab Clin Exp 64:1521–1529CrossRef Sauder KA, McCrea CE, Ulbrecht JS, Kris-Etherton PM, West SG (2015) Effects of pistachios on the lipid/lipoprotein profile, glycaemic control, inflammation, and endothelial function in type 2 diabetes: a randomized trial. Metab Clin Exp 64:1521–1529CrossRef
9.
go back to reference Josse AR, Kendall CW, Augustin LS, Ellis PR, Jenkins DJ (2007) Almonds and postprandial glycemia—a dose-response study. Metab Clin Exp 56:400–404CrossRef Josse AR, Kendall CW, Augustin LS, Ellis PR, Jenkins DJ (2007) Almonds and postprandial glycemia—a dose-response study. Metab Clin Exp 56:400–404CrossRef
10.
go back to reference Doménech M, Roman P, Lapetra J, García de la Corte FJ, Sala-Vila A (2014) Mediterranean diet reduces 24-hour ambulatory blood pressure, blood glucose, and lipids: one-year randomized, clinical trial. Hypertension 64:69–76CrossRef Doménech M, Roman P, Lapetra J, García de la Corte FJ, Sala-Vila A (2014) Mediterranean diet reduces 24-hour ambulatory blood pressure, blood glucose, and lipids: one-year randomized, clinical trial. Hypertension 64:69–76CrossRef
11.
go back to reference Salas-Salvado J, Guasch-Ferre M, Bullo M, Sabate J (2014) Nuts in the prevention and treatment of metabolic syndrome. Am J Clin Nutr 100(Suppl 1):S399–S407CrossRef Salas-Salvado J, Guasch-Ferre M, Bullo M, Sabate J (2014) Nuts in the prevention and treatment of metabolic syndrome. Am J Clin Nutr 100(Suppl 1):S399–S407CrossRef
12.
go back to reference Sala-Vila A, Romero-Mamani ES, Gilabert R et al (2014) Changes in ultrasound-assessed carotid intima-media thickness and plaque with a Mediterranean diet: a substudy of the PREDIMED trial. Arterioscler Thromb Vasc Biol 34:439–445CrossRef Sala-Vila A, Romero-Mamani ES, Gilabert R et al (2014) Changes in ultrasound-assessed carotid intima-media thickness and plaque with a Mediterranean diet: a substudy of the PREDIMED trial. Arterioscler Thromb Vasc Biol 34:439–445CrossRef
14.
go back to reference Canadian Diabetes Association Clinical Practice Guidelines Expert Committee (2013) Canadian Diabetes Association 2013 clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes 37(suppl 1):S1–S212 Canadian Diabetes Association Clinical Practice Guidelines Expert Committee (2013) Canadian Diabetes Association 2013 clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes 37(suppl 1):S1–S212
15.
go back to reference Anderson TJ, Gregoire J, Hegele RA et al (2013) 2012 update of the Canadian Cardiovascular Society guidelines for the diagnosis and treatment of dyslipidemia for the prevention of cardiovascular disease in the adult. Can J Cardiol 29:151–167CrossRef Anderson TJ, Gregoire J, Hegele RA et al (2013) 2012 update of the Canadian Cardiovascular Society guidelines for the diagnosis and treatment of dyslipidemia for the prevention of cardiovascular disease in the adult. Can J Cardiol 29:151–167CrossRef
16.
go back to reference Stroes ES, Thompson PD, Corsini A et al (2015) Statin-associated muscle symptoms: impact on statin therapy—European Atherosclerosis Society Consensus Panel Statement on Assessment, Aetiology and Management. Eur Heart J 36:1012–1022CrossRef Stroes ES, Thompson PD, Corsini A et al (2015) Statin-associated muscle symptoms: impact on statin therapy—European Atherosclerosis Society Consensus Panel Statement on Assessment, Aetiology and Management. Eur Heart J 36:1012–1022CrossRef
17.
go back to reference Mann JI, De Leeuw I, Hermansen K et al (2004) Evidence-based nutritional approaches to the treatment and prevention of diabetes mellitus. Nutr Metab Cardiovasc Dis 14:373–394CrossRef Mann JI, De Leeuw I, Hermansen K et al (2004) Evidence-based nutritional approaches to the treatment and prevention of diabetes mellitus. Nutr Metab Cardiovasc Dis 14:373–394CrossRef
19.
go back to reference Jenkins DJ, Kendall CW, Banach MS et al (2011) Nuts as a replacement for carbohydrates in the diabetic diet. Diabetes Care 34:1706–1711CrossRef Jenkins DJ, Kendall CW, Banach MS et al (2011) Nuts as a replacement for carbohydrates in the diabetic diet. Diabetes Care 34:1706–1711CrossRef
20.
go back to reference Jenkins DJ, Chiavaroli L, Wong JM, et al. Adding monounsaturated fatty acids to a dietary portfolio of cholesterol-lowering foods in hypercholesterolemia. CMAJ 182:1961–1967 Jenkins DJ, Chiavaroli L, Wong JM, et al. Adding monounsaturated fatty acids to a dietary portfolio of cholesterol-lowering foods in hypercholesterolemia. CMAJ 182:1961–1967
21.
go back to reference Hu ML (1994) Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol 233:380–385CrossRef Hu ML (1994) Measurement of protein thiol groups and glutathione in plasma. Methods Enzymol 233:380–385CrossRef
22.
go back to reference St-Pierre AC, Ruel IL, Cantin B et al (2001) Comparison of various electrophoretic characteristics of LDL particles and their relationship to the risk of ischemic heart disease. Circulation 104:2295–2299CrossRef St-Pierre AC, Ruel IL, Cantin B et al (2001) Comparison of various electrophoretic characteristics of LDL particles and their relationship to the risk of ischemic heart disease. Circulation 104:2295–2299CrossRef
23.
go back to reference Rapaport SI, Aas K, Owren PA (1955) The effect of glass upon the activity of the various plasma clotting factors. J Clin Invest 34(1):9–19CrossRef Rapaport SI, Aas K, Owren PA (1955) The effect of glass upon the activity of the various plasma clotting factors. J Clin Invest 34(1):9–19CrossRef
24.
go back to reference Quick AJ, Stanley-Brown M, Bancroft FW (1935) A study of the coagulation defect in hemophilia and in jaundice. Am J Med Sci 190:501–510CrossRef Quick AJ, Stanley-Brown M, Bancroft FW (1935) A study of the coagulation defect in hemophilia and in jaundice. Am J Med Sci 190:501–510CrossRef
25.
go back to reference Clauss A (1957) Rapid physiological coagulation method in determination of fibrinogen [article in German]. Acta Haematol 17:237–246CrossRef Clauss A (1957) Rapid physiological coagulation method in determination of fibrinogen [article in German]. Acta Haematol 17:237–246CrossRef
26.
go back to reference Declerck PJ, Alessi MC, Verstreken M, Kruithof EK, Juhan-Vague I, Collen D (1988) Measurement of plasminogen activator inhibitor 1 in biologic fluids with a murine monoclonal antibody-based enzyme-linked immunosorbent assay. Blood 71:220–225PubMed Declerck PJ, Alessi MC, Verstreken M, Kruithof EK, Juhan-Vague I, Collen D (1988) Measurement of plasminogen activator inhibitor 1 in biologic fluids with a murine monoclonal antibody-based enzyme-linked immunosorbent assay. Blood 71:220–225PubMed
28.
go back to reference Atkinson FS, Foster-Powell K, Brand-Miller JC (2008) International tables of glycaemic index and glycaemic load values: 2008. Diabetes Care 31:2281–2283CrossRef Atkinson FS, Foster-Powell K, Brand-Miller JC (2008) International tables of glycaemic index and glycaemic load values: 2008. Diabetes Care 31:2281–2283CrossRef
29.
go back to reference Coniff RF, Shapiro JA, Seaton TB, Hoogwerf BJ, Hunt JA (1995) A double-blind placebo-controlled trial evaluating the safety and efficacy of acarbose for the treatment of patients with insulin-requiring type II diabetes. Diabetes Care 18:928–932CrossRef Coniff RF, Shapiro JA, Seaton TB, Hoogwerf BJ, Hunt JA (1995) A double-blind placebo-controlled trial evaluating the safety and efficacy of acarbose for the treatment of patients with insulin-requiring type II diabetes. Diabetes Care 18:928–932CrossRef
30.
go back to reference Jenkins DJ, Kendall CW, McKeown-Eyssen G et al (2008) Effect of a low-glycaemic index or a high-cereal fiber diet on type 2 diabetes: a randomized trial. JAMA 300:2742–2753CrossRef Jenkins DJ, Kendall CW, McKeown-Eyssen G et al (2008) Effect of a low-glycaemic index or a high-cereal fiber diet on type 2 diabetes: a randomized trial. JAMA 300:2742–2753CrossRef
31.
go back to reference Franz MJ, Horton ES Sr, Bantle JP et al (1994) Nutrition principles for the management of diabetes and related complications. Diabetes Care 17:490–518CrossRef Franz MJ, Horton ES Sr, Bantle JP et al (1994) Nutrition principles for the management of diabetes and related complications. Diabetes Care 17:490–518CrossRef
32.
go back to reference Vessby B, Uusitupa M, Hermansen K et al (2001) Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU study. Diabetologia 44:312–319CrossRef Vessby B, Uusitupa M, Hermansen K et al (2001) Substituting dietary saturated for monounsaturated fat impairs insulin sensitivity in healthy men and women: the KANWU study. Diabetologia 44:312–319CrossRef
33.
go back to reference Ellis PR, Kendall CW, Ren Y et al (2004) Role of cell walls in the bioaccessibility of lipids in almond seeds. Am J Clin Nutr 80:604–613CrossRef Ellis PR, Kendall CW, Ren Y et al (2004) Role of cell walls in the bioaccessibility of lipids in almond seeds. Am J Clin Nutr 80:604–613CrossRef
34.
go back to reference Halton TL, Willett WC, Liu S et al (2006) Low-carbohydrate-diet score and the risk of coronary heart disease in women. N Engl J Med 355:1991–2002CrossRef Halton TL, Willett WC, Liu S et al (2006) Low-carbohydrate-diet score and the risk of coronary heart disease in women. N Engl J Med 355:1991–2002CrossRef
35.
go back to reference Halton TL, Willett WC, Liu S, Manson JE, Stampfer MJ, Hu FB (2006) Potato and french fry consumption and risk of type 2 diabetes in women. Am J Clin Nutr 83:284–290CrossRef Halton TL, Willett WC, Liu S, Manson JE, Stampfer MJ, Hu FB (2006) Potato and french fry consumption and risk of type 2 diabetes in women. Am J Clin Nutr 83:284–290CrossRef
36.
go back to reference Aune D, Keum N, Giovannucci E et al (2016) Nut consumption and risk of cardiovascular disease, total cancer, all-cause and cause-specific mortality: a systematic review and dose-response meta-analysis of prospective studies. BMC Med 14:207CrossRef Aune D, Keum N, Giovannucci E et al (2016) Nut consumption and risk of cardiovascular disease, total cancer, all-cause and cause-specific mortality: a systematic review and dose-response meta-analysis of prospective studies. BMC Med 14:207CrossRef
38.
go back to reference Lamarche B, Tchernof A, Moorjani S et al (1997) Small, dense low-density lipoprotein particles as a predictor of the risk of ischemic heart disease in men. Prospective results from the Quebec Cardiovascular Study. Circulation 95:69–75CrossRef Lamarche B, Tchernof A, Moorjani S et al (1997) Small, dense low-density lipoprotein particles as a predictor of the risk of ischemic heart disease in men. Prospective results from the Quebec Cardiovascular Study. Circulation 95:69–75CrossRef
39.
go back to reference Desroches S, Lamarche B (2004) Diet and low-density lipoprotein particle size. Curr Atheroscler Rep 6:453–460CrossRef Desroches S, Lamarche B (2004) Diet and low-density lipoprotein particle size. Curr Atheroscler Rep 6:453–460CrossRef
40.
go back to reference Archer WR, Lamarche B, St-Pierre AC et al (2003) High carbohydrate and high monounsaturated fatty acid diets similarly affect LDL electrophoretic characteristics in men who are losing weight. J Nutr 133:3124–3129CrossRef Archer WR, Lamarche B, St-Pierre AC et al (2003) High carbohydrate and high monounsaturated fatty acid diets similarly affect LDL electrophoretic characteristics in men who are losing weight. J Nutr 133:3124–3129CrossRef
41.
go back to reference Kris-Etherton PM, Zhao G, Binkoski AE, Coval SM, Etherton TD (2001) The effects of nuts on coronary heart disease risk. Nutr Rev 59:103–111CrossRef Kris-Etherton PM, Zhao G, Binkoski AE, Coval SM, Etherton TD (2001) The effects of nuts on coronary heart disease risk. Nutr Rev 59:103–111CrossRef
42.
go back to reference Mellows S, Brozovic M, Miller GJ, Chakrabarti RR, North WR (1986) Haemostatic function and ischaemic heart disease: principal results of the Northwick Park Heart Study. Lancet 2:533–537PubMed Mellows S, Brozovic M, Miller GJ, Chakrabarti RR, North WR (1986) Haemostatic function and ischaemic heart disease: principal results of the Northwick Park Heart Study. Lancet 2:533–537PubMed
43.
go back to reference Junker R, Heinrich J, Schulte H, van de Loo J, Assmann G (1997) Coagulation factor VII and the risk of coronary heart disease in healthy men. Arterioscler Thromb Vasc Biol 17:1539–1544CrossRef Junker R, Heinrich J, Schulte H, van de Loo J, Assmann G (1997) Coagulation factor VII and the risk of coronary heart disease in healthy men. Arterioscler Thromb Vasc Biol 17:1539–1544CrossRef
Metadata
Title
Nuts as a replacement for carbohydrates in the diabetic diet: a reanalysis of a randomised controlled trial
Authors
David J. A. Jenkins
Cyril W. C. Kendall
Benoît Lamarche
Monica S. Banach
Korbua Srichaikul
Edward Vidgen
Sandy Mitchell
Tina Parker
Stephanie Nishi
Balachandran Bashyam
Russell J. de Souza
Christopher Ireland
Sathish C. Pichika
Joseph Beyene
John L. Sievenpiper
Robert G. Josse
Publication date
01-08-2018
Publisher
Springer Berlin Heidelberg
Published in
Diabetologia / Issue 8/2018
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-018-4628-9

Other articles of this Issue 8/2018

Diabetologia 8/2018 Go to the issue