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The effect of almonds on inflammation and oxidative stress in Chinese patients with type 2 diabetes mellitus: a randomized crossover controlled feeding trial

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Abstract

Purpose

Almond consumption is associated with ameliorations in obesity, hyperlipidemia, hypertension, and hyperglycemia. The hypothesis of this 12-week randomized, crossover, controlled feeding trial was that almond consumption would ameliorate inflammation and oxidative stress in Chinese patients with type 2 diabetes mellitus (T2DM) (9 M, 11 F; 58 years; BMI: 26 kg/m2) with mild hyperlipidemia.

Methods

After a 2-week run-in period, the patients were assigned to either a control NCEP step II diet (control diet) or almond diet for 4 weeks with a 2-week washout period between alternative diets. Almonds approximately at 56 g/day were added to the control diet to replace 20 % of total daily calorie intake.

Results

As compared to the control diet, the almond diet decreased IL-6 by a median 10.3 % (95 % confidence intervals 5.2, 12.6 %), CRP by a median 10.3 % (−24.1, 40.5), and TNF-α by a median 15.7 % (−0.3, 29.9). The almond diet also decreased plasma protein carbonyl by a median 28.2 % (4.7, 38.2) as compared to the C diet but did not alter plasma malondialdehyde. The A diet enhanced the resistance of LDL against Cu2+-induced oxidation by a median 16.3 % (7.4, 44.3) as compared to the C diet. Serum intercellular adhesion molecule-1 and vascular adhesion molecule-1 were not changed by both diets.

Conclusions

Our results suggested that incorporation of almonds into a healthy diet could ameliorate inflammation and oxidative stress in patients with T2DM.

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Abbreviations

T2DM:

Type 2 diabetes mellitus

CVD:

Cardiovascular disease

MDA:

Malondialdehyde

CRP:

C-reactive protein

IL-6:

Interleukin-6

TNF-α:

Tumor necrosis factor-α

LDL:

Low density protein

ICAM-1:

Soluble intra-cellular adhesion molecule-1

VCAM-1:

Soluble vascular adhesion molecule-1

FRAP:

Ferric reducing antioxidant power assay

References

  1. Grundy SM, Benjamin IJ, Burke GL, Chait A, Eckel RH, Howard BV, Mitch W, Smith SC Jr, Sowers JR (1999) Diabetes and cardiovascular disease: a statement for healthcare professionals from the American Heart Association. Circulation 100:1134–1146

    Article  CAS  Google Scholar 

  2. Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M (1998) Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339:229–234

    Article  CAS  Google Scholar 

  3. Rutter MK, Meigs JB, Sullivan LM, D’Agostino RB Sr, Wilson PW (2004) C-reactive protein, the metabolic syndrome, and prediction of cardiovascular events in the Framingham Offspring Study. Circulation 110:380–385

    Article  CAS  Google Scholar 

  4. Verma S, Szmitko PE, Ridker PM (2005) C-reactive protein comes of age. Nat Clin Pract Cardiovasc Med 2:29–36

    Article  CAS  Google Scholar 

  5. van den Oever IA, Raterman HG, Nurmohamed MT, Simsek S (2010) Endothelial dysfunction, inflammation, and apoptosis in diabetes mellitus. Mediat Inflamm 2010:792393

    Google Scholar 

  6. Giacco F, Brownlee M (2010) Oxidative stress and diabetic complications. Circ Res 107:1058–1070

    Article  CAS  Google Scholar 

  7. Magkos F, Yannakoulia M, Chan JL, Mantzoros CS (2009) Management of the metabolic syndrome and type 2 diabetes through lifestyle modification. Annu Rev Nutr 29:223–256

    Article  CAS  Google Scholar 

  8. Kendall CW, Esfahani A, Truan J, Srichaikul K, Jenkins DJ (2010) Health benefits of nuts in prevention and management of diabetes. Asia Pac J Clin Nutr 19:110–116

    CAS  Google Scholar 

  9. Chen C-Y, Lapsley K, Blumberg JB (2006) A nutrition and health perspective on almonds. J Sci Food Agric 86:2245–2250

    Article  CAS  Google Scholar 

  10. Sabaté J, Ang Y (2009) Nuts and health outcomes: new epidemiologic evidence. Am J Clin Nutr 89:1643S–1648S

    Article  Google Scholar 

  11. Chen C-Y, Blumberg JB (2008) Phytonutrient composition of nuts. Asian Pac J Clin Nutr 17:329–332

    CAS  Google Scholar 

  12. Jenkins DJ, Hu FB, Tapsell LC, Josse AR, Kendall CW (2008) Possible benefit of nuts in type 2 diabetes. J Nutr 138:1752S–1756S

    CAS  Google Scholar 

  13. Bantle JP, Wylie-Rosett J, Albright AL, Apovian CM, Clark NG, Franz MJ, Hoogwerf BJ, Lichtenstein AH, Mayer-Davis E, Mooradian AD, Wheeler ML (2008) Nutrition recommendations and interventions for diabetes: a position statement of the American Diabetes Association. Diabetes Care 31:S61–S78

    Article  CAS  Google Scholar 

  14. Mori AM, Considine RV, Mattes RD (2011) Acute and second-meal effects of almond form in impaired glucose tolerant adults: a randomized crossover trial. Nutr Metab (Lond) 8:6

    Article  CAS  Google Scholar 

  15. Li N, Jia X, Chen CY, Blumberg JB, Song Y, Zhang W, Zhang X, Ma G, Chen J (2007) Almond consumption reduces oxidative DNA damage and lipid peroxidation in male smokers. J Nutr 137:2717–2722

    CAS  Google Scholar 

  16. Li SC, Liu YH, Liu JF, Chang WH, Chen CM, Chen CY (2011) Almond consumption improved glycemic control and lipid profiles in patients with type 2 diabetes mellitus. Metabolism 60:474–479

    Article  CAS  Google Scholar 

  17. Cohen AE, Johnston CS (2011) Almond ingestion at mealtime reduces postprandial glycemia and chronic ingestion reduces hemoglobin A(1c) in individuals with well-controlled type 2 diabetes mellitus. Metabolism 60:1312–1317

    Article  CAS  Google Scholar 

  18. National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) (2002) Third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) final report. Circulation 106:3143–3421

    Google Scholar 

  19. Jenkins DJ, Kendall CW, Josse AR, Salvatore S, Brighenti F, Augustin LS, Ellis PR, Vidgen E, Rao AV (2006) Almonds decrease postprandial glycemia, insulinemia, and oxidative damage in healthy individuals. J Nutr 136:2987–2992

    CAS  Google Scholar 

  20. Chen CY, Milbury PE, Lapsley K, Blumberg JB (2005) Flavonoids from almond skins are bioavailable and act synergistically with vitamins C and E to enhance hamster and human LDL resistance to oxidation. J Nutr 135:1366–1373

    CAS  Google Scholar 

  21. Volpi N, Tarugi P (1998) Improvement in the high-performance liquid chromatography malondialdehyde level determination in normal human plasma. J Chromatogr B Biomed Sci Appl 713:433–437

    Article  CAS  Google Scholar 

  22. Reznick AZ, Cross CE, Hu ML, Suzuki YJ, Khwaja S, Safadi A, Motchnik PA, Packer L, Halliwell B (1992) Modification of plasma proteins by cigarette smoke as measured by protein carbonyl formation. Biochem J 286:607–611

    CAS  Google Scholar 

  23. Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Methods Enzymol 299:152–178

    Article  CAS  Google Scholar 

  24. Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76

    Article  CAS  Google Scholar 

  25. Srikanth S, Deedwania P (2011) Primary and secondary prevention strategy for cardiovascular disease in diabetes mellitus. Cardiol Clin 29:47–70

    Article  Google Scholar 

  26. Rajaram S, Connell KM, Sabaté J (2010) Effect of almond-enriched high-monounsaturated fat diet on selected markers of inflammation: a randomised, controlled, crossover study. Br J Nutr 103:907–912

    Article  CAS  Google Scholar 

  27. Kim JA, Montagnani M, Koh KK, Quon MJ (2006) Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113:1888–1904

    Article  Google Scholar 

  28. Zhao Y, Wang R, Ma X, Yan X, Zhang Z, He X, He J (2010) Distribution of C-reactive protein and its association with cardiovascular risk factors in a population-based sample of Chinese. Dis Markers 28:333–342

    Google Scholar 

  29. Jenkins DJ, Kendall CW, Marchie A, Parker TL, Connelly PW, Qian W, Haight JS, Faulkner D, Vidgen E, Lapsley KG, Spiller GA (2002) 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 106:1327–1332

    Article  CAS  Google Scholar 

  30. Salas-Salvadó J, Garcia-Arellano A, Estruch R, Marquez-Sandoval F, Corella D, Fiol M, Gómez-Gracia E, Viñoles E, Arós F, Herrera C, Lahoz C, Lapetra J, Perona JS, Muñoz-Aguado D, Martínez-González MA, Ros E, PREDIMED Investigators (2008) Components of the Mediterranean-type food pattern and serum inflammatory markers among patients at high risk for cardiovascular disease. Eur J Clin Nutr 62:651–659

    Article  Google Scholar 

  31. Estruch R, Martínez-González MA, Corella D, Salas-Salvadó J, Ruiz-Gutiérrez V, Covas MI, Fiol M, Gómez-Gracia E, López-Sabater MC, Vinyoles E, Arós F, Conde M, Lahoz C, Lapetra J, Sáez G, Ros E, PREDIMED Study Investigators (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145:1–11

    Google Scholar 

  32. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286:327–334

    Article  CAS  Google Scholar 

  33. Kaneto H, Katakami N, Matsuhisa M, Matsuoka TA (2010) Role of reactive oxygen species in the progression of type 2 diabetes and atherosclerosis. Mediators Inflamm 2010:453892

    Article  Google Scholar 

  34. Pasceri V, Willerson JT, Yeh ET (2000) Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation 102:2165–2168

    Article  CAS  Google Scholar 

  35. Rubio-Guerra AF, Vargas-Robles H, Serrano AM, Lozano-Nuevo JJ, Escalante-Acosta BA (2009) Correlation between the levels of circulating adhesion molecules and atherosclerosis in type-2 diabetic normotensive patients: circulating adhesion molecules and atherosclerosis. Cell Adh Migr 3:369–372

    Article  Google Scholar 

  36. Paolisso G, D’Amore A, Volpe C, Balbi V, Saccomanno F, Galzerano D, Giugliano D, Varricchio M, D’Onofrio F (1994) Evidence for a relationship between oxidative stress and insulin action in non-insulin-dependent (type II) diabetic patients. Metabolism 43:1426–1429

    Article  CAS  Google Scholar 

  37. Bruce CR, Carey AL, Hawley JA, Febbraio MA (2003) Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes 52:2338–2345

    Article  CAS  Google Scholar 

  38. Ros E, Tapsell LC, Sabaté J (2010) Nuts and berries for heart health. Curr Atheroscler Rep 12:397–406

    Article  CAS  Google Scholar 

  39. Hyson DA, Schneeman BO, Davis PA (2002) Almonds and almond oil have similar effects on plasma lipids and LDL oxidation in healthy men and women. J Nutr 132:703–707

    CAS  Google Scholar 

  40. Jenkins DJ, Kendall CW, Marchie A, Josse AR, Nguyen TH, Faulkner DA, Lapsley KG, Blumberg J (2008) Almonds reduce biomarkers of lipid peroxidation in older hyperlipidemic subjects. J Nutr 138:908–913

    CAS  Google Scholar 

  41. Rytter E, Vessby B, Åsgård R, Johansson C, Sjödin A, Abramsson-Zetterberg L, Möller L, Basu S (2009) Glycaemic status in relation to oxidative stress and inflammation in well-controlled type 2 diabetes subjects. Br J Nutr 101:1423–1426

    Article  CAS  Google Scholar 

  42. Armstrong AM, Chestnutt JE, Gormley MJ, Young IS (1996) The effect of dietary treatment on lipid peroxidation and antioxidant status in newly diagnosed noninsulin dependent diabetes. Free Radic Biol Med 21:719–726

    Article  CAS  Google Scholar 

  43. Paniagua JA, de la Sacristana AG, Sánchez E, Romero I, Vidal-Puig A, Berral FJ, Escribano A, Moyano MJ, Peréz-Martinez P, López-Miranda J, Pérez-Jiménez F (2007) A MUFA-rich diet improves postprandial glucose, lipid and GLP-1 responses in insulin-resistant subjects. J Am Coll Nutr 26:434–444

    CAS  Google Scholar 

  44. Rytter E, Vessby B, Asgård R, Ersson C, Moussavian S, Sjödin A, Abramsson-Zetterberg L, Möller L, Basu S (2010) Supplementation with a combination of antioxidants does not affect glycaemic control, oxidative stress or inflammation in type 2 diabetes subjects. Free Radic Res 44:1445–1453

    Article  CAS  Google Scholar 

  45. Esposito K, Nappo F, Marfella R, Giugliano G, Giugliano F, Ciotola M, Quagliaro L, Ceriello A, Giugliano D (2002) Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 106:2067–2072

    Article  CAS  Google Scholar 

  46. Boizel R, Bruttmann G, Benhamou PY, Halimi S, Stanke-Labesque F (2010) Regulation of oxidative stress and inflammation by glycaemic control: evidence for reversible activation of the 5-lipoxygenase pathway in type 1, but not in type 2 diabetes. Diabetologia 53:2068–2070

    Article  CAS  Google Scholar 

  47. Casas-Agustench P, Bulló M, Salas-Salvadó J (2010) Nuts, inflammation and insulin resistance. Asia Pac J Clin Nutr 19:124–130

    CAS  Google Scholar 

  48. Rayssiguier Y, Libako P, Nowacki W, Rock E (2010) Magnesium deficiency and metabolic syndrome: stress and inflammation may reflect calcium activation. Magnes Res 23:73–80

    CAS  Google Scholar 

  49. Lucotti P, Monti L, Setola E, La Canna G, Castiglioni A, Rossodivita A, Pala MG, Formica F, Paolini G, Catapano AL, Bosi E, Alfieri O, Piatti P (2009) Oral l-arginine supplementation improves endothelial function and ameliorates insulin sensitivity and inflammation in cardiopathic nondiabetic patients after an aortocoronary bypass. Metabolism 58:1270–1276

    Article  CAS  Google Scholar 

  50. Devaraj S, Kasim-Karakas S, Jialal I (2006) The effect of weight loss and dietary fatty acids on inflammation. Curr Atheroscler Rep 8:477–486

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to express our gratitude to the Almond Board of California and LEARN weight management foundation in Taiwan for providing financial supports for the study and the volunteers for participating in the clinical trial.

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Correspondence to C-Y. Oliver Chen.

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The contents of this publication do not necessarily reflect the views or policies of the USDA nor does mention of trade names, commercial products, or organizations imply endorsement by the US government.

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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 52, 927–935 (2013). https://doi.org/10.1007/s00394-012-0400-y

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