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European Journal of Nutrition

, Volume 52, Issue 3, pp 927–935 | Cite as

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

  • Jen-Fang Liu
  • Yen-Hua Liu
  • Chiao-Ming Chen
  • Wen-Hsin Chang
  • C-Y. Oliver Chen
Original Contribution

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.

Keywords

Almonds Antioxidants Inflammation Oxidative stress Type 2 diabetes mellitus 

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

Notes

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.

Conflict of interest

None.

Supplementary material

394_2012_400_MOESM1_ESM.doc (35 kb)
Supplementary material 1 (DOC 35 kb)
394_2012_400_MOESM2_ESM.doc (37 kb)
Supplementary material 2 (DOC 37 kb)

References

  1. 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 100:1134–1146CrossRefGoogle Scholar
  2. 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 339:229–234CrossRefGoogle Scholar
  3. 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 110:380–385CrossRefGoogle Scholar
  4. 4.
    Verma S, Szmitko PE, Ridker PM (2005) C-reactive protein comes of age. Nat Clin Pract Cardiovasc Med 2:29–36CrossRefGoogle Scholar
  5. 5.
    van den Oever IA, Raterman HG, Nurmohamed MT, Simsek S (2010) Endothelial dysfunction, inflammation, and apoptosis in diabetes mellitus. Mediat Inflamm 2010:792393Google Scholar
  6. 6.
    Giacco F, Brownlee M (2010) Oxidative stress and diabetic complications. Circ Res 107:1058–1070CrossRefGoogle Scholar
  7. 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 29:223–256CrossRefGoogle Scholar
  8. 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 19:110–116Google Scholar
  9. 9.
    Chen C-Y, Lapsley K, Blumberg JB (2006) A nutrition and health perspective on almonds. J Sci Food Agric 86:2245–2250CrossRefGoogle Scholar
  10. 10.
    Sabaté J, Ang Y (2009) Nuts and health outcomes: new epidemiologic evidence. Am J Clin Nutr 89:1643S–1648SCrossRefGoogle Scholar
  11. 11.
    Chen C-Y, Blumberg JB (2008) Phytonutrient composition of nuts. Asian Pac J Clin Nutr 17:329–332Google Scholar
  12. 12.
    Jenkins DJ, Hu FB, Tapsell LC, Josse AR, Kendall CW (2008) Possible benefit of nuts in type 2 diabetes. J Nutr 138:1752S–1756SGoogle Scholar
  13. 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–S78CrossRefGoogle Scholar
  14. 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) 8:6CrossRefGoogle Scholar
  15. 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 137:2717–2722Google Scholar
  16. 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 60:474–479CrossRefGoogle Scholar
  17. 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 60:1312–1317CrossRefGoogle Scholar
  18. 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 106:3143–3421Google Scholar
  19. 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 136:2987–2992Google Scholar
  20. 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 135:1366–1373Google Scholar
  21. 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 713:433–437CrossRefGoogle Scholar
  22. 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 286:607–611Google Scholar
  23. 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 299:152–178CrossRefGoogle Scholar
  24. 24.
    Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76CrossRefGoogle Scholar
  25. 25.
    Srikanth S, Deedwania P (2011) Primary and secondary prevention strategy for cardiovascular disease in diabetes mellitus. Cardiol Clin 29:47–70CrossRefGoogle Scholar
  26. 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 103:907–912CrossRefGoogle Scholar
  27. 27.
    Kim JA, Montagnani M, Koh KK, Quon MJ (2006) Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113:1888–1904CrossRefGoogle Scholar
  28. 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 28:333–342Google Scholar
  29. 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 106:1327–1332CrossRefGoogle Scholar
  30. 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 62:651–659CrossRefGoogle Scholar
  31. 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 145:1–11Google Scholar
  32. 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 286:327–334CrossRefGoogle Scholar
  33. 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 2010:453892CrossRefGoogle Scholar
  34. 34.
    Pasceri V, Willerson JT, Yeh ET (2000) Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation 102:2165–2168CrossRefGoogle Scholar
  35. 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 3:369–372CrossRefGoogle Scholar
  36. 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 43:1426–1429CrossRefGoogle Scholar
  37. 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 52:2338–2345CrossRefGoogle Scholar
  38. 38.
    Ros E, Tapsell LC, Sabaté J (2010) Nuts and berries for heart health. Curr Atheroscler Rep 12:397–406CrossRefGoogle Scholar
  39. 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 132:703–707Google Scholar
  40. 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 138:908–913Google Scholar
  41. 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 101:1423–1426CrossRefGoogle Scholar
  42. 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 21:719–726CrossRefGoogle Scholar
  43. 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 26:434–444Google Scholar
  44. 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 44:1445–1453CrossRefGoogle Scholar
  45. 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 106:2067–2072CrossRefGoogle Scholar
  46. 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 53:2068–2070CrossRefGoogle Scholar
  47. 47.
    Casas-Agustench P, Bulló M, Salas-Salvadó J (2010) Nuts, inflammation and insulin resistance. Asia Pac J Clin Nutr 19:124–130Google Scholar
  48. 48.
    Rayssiguier Y, Libako P, Nowacki W, Rock E (2010) Magnesium deficiency and metabolic syndrome: stress and inflammation may reflect calcium activation. Magnes Res 23:73–80Google Scholar
  49. 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 58:1270–1276CrossRefGoogle Scholar
  50. 50.
    Devaraj S, Kasim-Karakas S, Jialal I (2006) The effect of weight loss and dietary fatty acids on inflammation. Curr Atheroscler Rep 8:477–486CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Jen-Fang Liu
    • 1
  • Yen-Hua Liu
    • 1
  • Chiao-Ming Chen
    • 2
  • Wen-Hsin Chang
    • 1
  • C-Y. Oliver Chen
    • 3
  1. 1.School of Nutrition and Health ScienceTaipei Medical UniversityTaipeiTaiwan
  2. 2.Department of Food Science, Nutrition and Nutraceutical BiotechnologyShih-Chien UniversityTaipeiTaiwan
  3. 3.Antioxidants Research Laboratory, Jean Mayer USDA Human Nutrition Research Center on AgingTufts UniversityBostonUSA

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