The effect of nut consumption on markers of inflammation and endothelial function: A systematic review and meta-analysis of randomised controlled trials

BMJ Open

Volumn 7, Issue 11, 2017, Pages

  Neale, Elizabeth P ^a   Tapsell, Linda C ^a   Guan, Vivienne ^a   Batterham, Marijka J ^a  

^a UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; BIOLOGICAL MARKER; C REACTIVE PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1; CYTOKINE;

ARTICLE; DIET; FOOD INTAKE; HUMAN; INFLAMMATION; META ANALYSIS; NUT; PROTEIN BLOOD LEVEL; SYSTEMATIC REVIEW; VASCULAR ENDOTHELIUM; VASODILATATION; BLOOD FLOW VELOCITY; BRACHIAL ARTERY; METABOLISM; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC);

BIOMARKERS; BLOOD FLOW VELOCITY; BRACHIAL ARTERY; C-REACTIVE PROTEIN; CYTOKINES; DIET; HUMANS; INFLAMMATION; NUTS; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 85048241909     PISSN: None     EISSN: 20446055     Source Type: Journal    
DOI: 10.1136/bmjopen-2017-016863     Document Type: Article

References (77)

1. Esser N, Legrand-Poels S, Piette J, et al. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract 2014;105:141–50.
2. Libby P, Ridker PM, Maseri A, et al. Inflammation and atherosclerosis. Circulation 2002;105:1135–43.
3. Silva D, Pais de Lacerda A. [High-sensitivity C-reactive protein as a biomarker of risk in coronary artery disease]. Rev Port Cardiol 2012;31:733–45.
4. Ruan H, Lodish HF. Insulin resistance in adipose tissue: direct and indirect effects of tumor necrosis factor-alpha. Cytokine Growth Factor Rev 2003;14:447–55.
5. Gabay C. Interleukin-6 and chronic inflammation. Arthritis Res Ther 2006;8 Suppl 2:S3.
6. Stoner L, Lucero AA, Palmer BR, et al. Inflammatory biomarkers for predicting cardiovascular disease. Clin Biochem 2013;46:1353–71.
7. Robinson K, Prins J, Venkatesh B. Clinical review: adiponectin biology and its role in inflammation and critical illness. Crit Care 2011;15:221.
8. Inaba Y, Chen JA, Bergmann SR. Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a meta-analysis. Int J Cardiovasc Imaging 2010;26:631–40.
9. Casas-Agustench P, Bulló M, Salas-Salvadó J. Nuts, inflammation and insulin resistance. Asia Pac J Clin Nutr 2010;19:124–30.
10. Luo C, Zhang Y, Ding Y, et al. Nut consumption and risk of type 2 diabetes, cardiovascular disease, and all-cause mortality: a systematic review and meta-analysis. Am J Clin Nutr 2014;100:256–69.
11. Ibarrola-Jurado N, Bulló M, Guasch-Ferré M, et al. Cross-sectional assessment of nut consumption and obesity, metabolic syndrome and other cardiometabolic risk factors: the PREDIMED study. PLoS One 2013;8:e57367.
12. Afshin A, Micha R, Khatibzadeh S, et al. Consumption of nuts and legumes and risk of incident ischemic heart disease, stroke, and diabetes: a systematic review and meta-analysis. Am J Clin Nutr 2014;100:278–88.
13. Tey SL, Gray AR, Chisholm AW, et al. The dose of hazelnuts influences acceptance and diet quality but not inflammatory markers and body composition in overweight and obese individuals. J Nutr 2013;143:1254–62.
14. Sauder KA, McCrea CE, Ulbrecht JS, et al. Effects of pistachios on the lipid/lipoprotein profile, glycemic control, inflammation, and endothelial function in type 2 diabetes: A randomized trial. Metabolism 2015;64:1521–9.
15. Lee YJ, Nam GE, Seo JA, et al. Nut consumption has favorable effects on lipid profiles of Korean women with metabolic syndrome. Nutr Res 2014;34:814–20.
16. Casas-Agustench P, López-Uriarte P, Bulló M, et al. Effects of one serving of mixed nuts on serum lipids, insulin resistance and inflammatory markers in patients with the metabolic syndrome. Nutr Metab Cardiovasc Dis 2011;21:126–35.
17. Katz DL, Davidhi A, Ma Y, et al. Effects of walnuts on endothelial function in overweight adults with visceral obesity: a randomized, controlled, crossover trial. J Am Coll Nutr 2012;31:415–23.
18. Ros E, Núñez I, Pérez-Heras A, et al. A walnut diet improves endothelial function in hypercholesterolemic subjects: a randomized crossover trial. Circulation 2004;109:1609–14.
19. Gulati S, Misra A, Pandey RM, et al. Effects of pistachio nuts on body composition, metabolic, inflammatory and oxidative stress parameters in Asian Indians with metabolic syndrome: a 24-wk, randomized control trial. Nutrition 2014;30:192–7.
20. Hernández-Alonso P, Salas-Salvadó J, Baldrich-Mora M, et al. Beneficial effect of pistachio consumption on glucose metabolism, insulin resistance, inflammation, and related metabolic risk markers: a randomized clinical trial. Diabetes Care 2014;37:3098–105.
21. Liu JF, Liu YH, Chen CM, et al. The effect of almonds on inflammation and oxidative stress in Chinese patients with type 2 diabetes mellitus: a randomized crossover controlled feeding trial. Eur J Nutr 2013;52:927–35.
22. Ma Y, Njike VY, Millet J, et al. Effects of walnut consumption on endothelial function in type 2 diabetic subjects: a randomized controlled crossover trial. Diabetes Care 2010;33:227–32.
23. Mazidi M, Rezaie P, Ferns GA, et al. Impact of different types of tree nut, peanut, and soy nut consumption on serum C-reactive protein (CRP): A systematic review and meta-analysis of randomized controlled clinical trials. Medicine 2016;95:e5165.
24. Estruch R, Ros E, Salas-Salvadó J, et al. Primary prevention of cardiovascular disease with a Mediterranean diet. N Engl J Med 2013;368:1279–90.
25. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009;6:e1000097.
26. Rosen L, Suhami R. The art and science of study identification: a comparative analysis of two systematic reviews. BMC Med Res Methodol 2016;16:24.
27. Schwingshackl L, Christoph M, Hoffmann G. Effects of olive oil on markers of inflammation and endothelial function: a systematic review and meta-analysis. Nutrients 2015;7:7651–75.
28. Schwingshackl L, Hoffmann G. Mediterranean dietary pattern, inflammation and endothelial function: a systematic review and meta-analysis of intervention trials. Nutr Metab Cardiovasc Dis 2014;24:929–39.
29. Blanco Mejia S, Kendall CW, Viguiliouk E, et al. Effect of tree nuts on metabolic syndrome criteria: a systematic review and meta-analysis of randomised controlled trials. BMJ Open 2014;4:e004660.
30. Viguiliouk E, Kendall CW, Blanco Mejia S, et al. Effect of tree nuts on glycemic control in diabetes: a systematic review and meta-analysis of randomized controlled dietary trials. PLoS One 2014;9:e103376.
31. Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration 2011.
32. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ 2003;327:557–60.
33. Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629–34.
34. Duval S, Tweedie R. Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000;56:455–63.
35. Mukuddem-Petersen J, Stonehouse Oosthuizen W, Jerling JC, et al. Effects of a high walnut and high cashew nut diet on selected markers of the metabolic syndrome: a controlled feeding trial. Br J Nutr 2007;97:1144.
36. Damasceno NR, Pérez-Heras A, Serra M, et al. Crossover study of diets enriched with virgin olive oil, walnuts or almonds. Effects on lipids and other cardiovascular risk markers. Nutr Metab Cardiovasc Dis 2011;21:S14–20.
37. Guyatt GH, Oxman AD, Vist GE, et al; GRADE: an emerging consensus on rating quality of evidence and strength of recommendations, 2008.
38. López-Uriarte P, Nogués R, Saez G, et al. Effect of nut consumption on oxidative stress and the endothelial function in metabolic syndrome. Clin Nutr 2010;29:373–80.
39. Djoussé L, Lu B, Gaziano JM. Effects of walnut consumption on endothelial function in people with type 2 diabetes: a randomized pilot trial. Curr Nutr Rep 2016;5:1–8.
40. Kasliwal RR, Bansal M, Mehrotra R, et al. Effect of pistachio nut consumption on endothelial function and arterial stiffness. Nutrition 2015;31:678–85.
41. Kurlandsky SB, Stote KS. Cardioprotective effects of chocolate and almond consumption in healthy women. Nutr Res 2006;26:509–16.
42. Moreira Alves RD, Boroni Moreira AP, Macedo VS, et al. High-oleic peanuts: new perspective to attenuate glucose homeostasis disruption and inflammation related obesity. Obesity 2014;22:1981–8.
43. Casas R, Sacanella E, Urpí-Sardà M, et al. The effects of the mediterranean diet on biomarkers of vascular wall inflammation and plaque vulnerability in subjects with high risk for cardiovascular disease. A randomized trial. PLoS One 2014;9:e100084.
44. Casas R, Sacanella E, Urpí-Sardà M, et al. Long-term immunomodulatory effects of a mediterranean diet in adults at high risk of cardiovascular disease in the PREvención con DIeta MEDiterránea (PREDIMED) Randomized Controlled Trial. J Nutr 2016;146:1684–93.
45. Lasa A, Miranda J, Bulló M, et al. Comparative effect of two Mediterranean diets versus a low-fat diet on glycaemic control in individuals with type 2 diabetes. Eur J Clin Nutr 2014;68:767–72.
46. Urpi-Sarda M, Casas R, Chiva-Blanch G, et al. The Mediterranean diet pattern and its main components are associated with lower plasma concentrations of tumor necrosis factor receptor 60 in patients at high risk for cardiovascular disease. J Nutr 2012;142:1019–25.
47. Solà R, Valls RM, Godàs G, et al. Cocoa, hazelnuts, sterols and soluble fiber cream reduces lipids and inflammation biomarkers in hypertensive patients: a randomized controlled trial. PLoS One 2012;7:e31103.
48. Sweazea KL, Johnston CS, Ricklefs KD, et al. Almond supplementation in the absence of dietary advice significantly reduces C-reactive protein in subjects with type 2 diabetes. J Funct Foods 2014;10:252–9.
49. Hu Y, McIntosh GH, Le Leu RK, et al. Supplementation with Brazil nuts and green tea extract regulates targeted biomarkers related to colorectal cancer risk in humans. Br J Nutr 2016;116:1901–11.
50. Rock CL, Flatt SW, Pakiz B, et al. Effects of diet composition on weight loss, metabolic factors and biomarkers in a 1-year weight loss intervention in obese women examined by baseline insulin resistance status. Metabolism 2016;65:1605–13.
51. Barbour JA, Howe PR, Buckley JD, et al. Effect of 12 weeks high oleic peanut consumption on cardio-metabolic risk factors and body composition. Nutrients 2015;7:7381–98.
52. Burns-Whitmore B, Haddad E, Sabaté J, et al. Effects of supplementing n-3 fatty acid enriched eggs and walnuts on cardiovascular disease risk markers in healthy free-living lacto-ovo-vegetarians: a randomized, crossover, free-living intervention study. Nutr J 2014;13:29.
53. Canales A, Sánchez-Muniz FJ, Bastida S, et al. Effect of walnut-enriched meat on the relationship between VCAM, ICAM, and LTB4 levels and PON-1 activity in ApoA4 360 and PON-1 allele carriers at increased cardiovascular risk. Eur J Clin Nutr 2011;65:703–10.
54. Chen CY, Holbrook M, Duess MA, et al. Effect of almond consumption on vascular function in patients with coronary artery disease: a randomized, controlled, cross-over trial. Nutr J 2015;14:61.
55. Chiang YL, Haddad E, Rajaram S, et al. The effect of dietary walnuts compared to fatty fish on eicosanoids, cytokines, soluble endothelial adhesion molecules and lymphocyte subsets: a randomized, controlled crossover trial. Prostaglandins Leukot Essent Fatty Acids 2012;87:111–7.
56. Jenkins DJ, Kendall CW, Marchie A, et al. Dose response of almonds on coronary heart disease risk factors: blood lipids, oxidized low-density lipoproteins, lipoprotein(a), homocysteine, and pulmonary nitric oxide: a randomized, controlled, crossover trial. Circulation 2002;106:1327–32.
57. Parham M, Heidari S, Khorramirad A, et al. Effects of pistachio nut supplementation on blood glucose in patients with type 2 diabetes: a randomized crossover trial. Rev Diabet Stud 2014;11:190–6.
58. Rajaram S, Connell KM, Sabaté J. Effect of almond-enriched high-monounsaturated fat diet on selected markers of inflammation: a randomised, controlled, crossover study. Br J Nutr 2010;103:907.
59. West SG, Gebauer SK, Kay CD, et al. Diets containing pistachios reduce systolic blood pressure and peripheral vascular responses to stress in adults with dyslipidemia. Hypertension 2012;60:58–63.
60. Wu L, Piotrowski K, Rau T, et al. Walnut-enriched diet reduces fasting non-HDL-cholesterol and apolipoprotein B in healthy Caucasian subjects: a randomized controlled cross-over clinical trial. Metabolism 2014;63:382–91.
61. Njike VY, Ayettey R, Petraro P, et al. Walnut ingestion in adults at risk for diabetes: effects on body composition, diet quality, and cardiac risk measures. BMJ Open Diabetes Res Care 2015;3:e000115.
62. EFSA Panel on Dietetic Products N, Allergies. Scientific opinion on the substantiation of health claims related to walnuts and maintenance of normal blood LDL-cholesterol concentrations (ID 1156, 1158) and improvement of endothelium-dependent vasodilation (ID 1155, 1157) pursuant to Article 13(1) of Regulation (EC) No 1924/2006. EFSA Journal 2011;9:2074.
63. Thijssen DH, Black MA, Pyke KE, et al. Assessment of flow-mediated dilation in humans: a methodological and physiological guideline. Am J Physiol Heart Circ Physiol 2011;300:H2–H12.
64. Liao JK. Linking endothelial dysfunction with endothelial cell activation. J Clin Invest 2013;123:540–1.
65. Brufau G, Boatella J, Rafecas M. Nuts: source of energy and macronutrients. Br J Nutr 2006;96:S24–8.
66. Lorin J, Zeller M, Guilland JC, et al. Arginine and nitric oxide synthase: regulatory mechanisms and cardiovascular aspects. Mol Nutr Food Res 2014;58:101–16.
67. Cortés B, Núñez I, Cofán M, et al. Acute effects of high-fat meals enriched with walnuts or olive oil on postprandial endothelial function. J Am Coll Cardiol 2006;48:1666–71.
68. Barbaresko J, Koch M, Schulze MB, et al. Dietary pattern analysis and biomarkers of low-grade inflammation: a systematic literature review. Nutr Rev 2013;71:511–27.
69. Ridker PM, Buring JE, Cook NR, et al. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14 719 initially healthy American women. Circulation 2003;107:391–7.
70. Del Gobbo LC, Falk MC, Feldman R, et al. Effects of tree nuts on blood lipids, apolipoproteins, and blood pressure: systematic review, meta-analysis, and dose-response of 61 controlled intervention trials. Am J Clin Nutr 2015;102:1347–56.
71. Tapsell LC, Dunning A, Warensjo E, et al. Effects of vegetable consumption on weight loss: a review of the evidence with implications for design of randomized controlled trials. Crit Rev Food Sci Nutr 2014;54:1529–38.
72. Ravussin E, Redman LM, Rochon J, et al. A 2-year randomized controlled trial of human caloric restriction: feasibility and effects on predictors of health span and longevity. J Gerontol A Biol Sci Med Sci 2015;70:1097–104.
73. Dawson JA, Kaiser KA, Affuso O, et al. Rigorous control conditions diminish treatment effects in weight loss-randomized controlled trials. Int J Obes 2016;40:895–8.
74. Barbour JA, Howe PR, Buckley JD, et al. Nut consumption for vascular health and cognitive function. Nutr Res Rev 2014;27:131–58.
75. Neale EP, Batterham MJ, Tapsell LC. Consumption of a healthy dietary pattern results in significant reductions in C-reactive protein levels in adults: a meta-analysis. Nutr Res 2016;36:391–401.
76. Mills EJ, Chan AW, Wu P, et al. Design, analysis, and presentation of crossover trials. Trials 2009;10:27.
77. Estruch R, Martínez-González MA, Corella D, et al. Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomize trial. Ann Intern Med 2006;145:1–11.