Resveratrol supplementation decreases blood glucose without changing the circulating CD14 + CD16 + monocytes and inflammatory cytokines in patients with type 2 diabetes: a randomized, double-blind, placebo-controlled study

Nutrition Research

Volumn 54, Issue , 2018, Pages 40-51

  Khodabandehloo, Hadi ^a   Seyyedebrahimi, ShadiSadat ^a   Esfahani, Ensieh Nasli ^b   Razi, Farideh ^b   Meshkani, Reza ^a,b  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

CD14 + CD16 + monocytes; Clinical trial; Inflammation; PBMC; Resveratrol; Type 2 diabetes

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; C REACTIVE PROTEIN; CD14 ANTIGEN; CD16 ANTIGEN; CHOLESTEROL; CREATININE; CYTOKINE; GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACEBO; RESVERATROL; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR; UREA; URIC ACID; ANTIOXIDANT; AUTACOID; BIOLOGICAL MARKER; FC RECEPTOR; INTERLEUKIN DERIVATIVE; LIPOPOLYSACCHARIDE RECEPTOR; PLANT EXTRACT; TOLL LIKE RECEPTOR;

ADULT; AGED; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BLOOD PRESSURE; BODY MASS; BODY WEIGHT; CD14+ CD16+ MONOCYTE; CHOLESTEROL BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CYTOKINE RELEASE; DOUBLE BLIND PROCEDURE; DRUG SAFETY; DRUG TOLERANCE; FEMALE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; HIP CIRCUMFERENCE; HOMEOSTASIS MODEL ASSESSMENT; HUMAN; INSULIN BLOOD LEVEL; MALE; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL; SUPPLEMENTATION; TREATMENT DURATION; UREA BLOOD LEVEL; WAIST CIRCUMFERENCE; WAIST HIP RATIO; BLOOD; COMPLICATION; DIETARY SUPPLEMENT; INFLAMMATION; METABOLISM; MIDDLE AGED;

AGED; ANTIOXIDANTS; BIOMARKERS; BLOOD GLUCOSE; CHEMOKINE CCL2; CYTOKINES; DIABETES MELLITUS, TYPE 2; DIETARY SUPPLEMENTS; DOUBLE-BLIND METHOD; FEMALE; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKINS; LIPOPOLYSACCHARIDE RECEPTORS; MALE; MIDDLE AGED; MONOCYTES; NF-KAPPA B; PLANT EXTRACTS; RECEPTORS, IGG; RESVERATROL; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85046348459     PISSN: 02715317     EISSN: 18790739     Source Type: Journal    
DOI: 10.1016/j.nutres.2018.03.015     Document Type: Article

References (58)

1. Danaei, G., Finucane, M.M., Lu, Y., Singh, G.M., Cowan, M.J., Paciorek, C.J., et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet 378 (2011), 31–40.
2. Khodabandehloo, H., Gorgani-Firuzjaee, S., Panahi, G., Meshkani, R., Molecular and cellular mechanisms linking inflammation to insulin resistance and beta-cell dysfunction. Transl Res 167 (2016), 228–256.
3. Hatanaka, E., Monteagudo, P.T., Marrocos, M.S., Campa, A., Neutrophils and monocytes as potentially important sources of proinflammatory cytokines in diabetes. Clin Exp Immunol 146 (2006), 443–447.
4. Nagasawa, T., Kobayashi, H., Aramaki, M., Kiji, M., Oda, S., Izumi, Y., Expression of CD14, CD16 and CD45RA on monocytes from periodontitis patients. J Periodontal Res 39 (2004), 72–78.
5. Passlick, B., Flieger, D., Ziegler-Heitbrock, H.W., Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 74 (1989), 2527–2534.
6. + monocytes in coronary artery disease and their relationship to serum TNF-alpha levels. Thromb Haemost 92 (2004), 419–424.
7. Sester, U., Sester, M., Heine, G., Kaul, H., Girndt, M., Kohler, H., Strong depletion of CD14(+)CD16(+) monocytes during haemodialysis treatment. Nephrol Dial Transplant 16 (2001), 1402–1408.
8. + monocytes are associated with microinflammation in patients with type 2 diabetes mellitus and diabetic nephropathy uremia. Inflammation 35 (2012), 388–396.
9. Dasu, M.R., Devaraj, S., Park, S., Jialal, I., Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care 33 (2010), 861–868.
10. Gregor, M.F., Hotamisligil, G.S., Inflammatory mechanisms in obesity. Annu Rev Immunol 29 (2011), 415–445.
11. Birrell, M.A., McCluskie, K., Wong, S., Donnelly, L.E., Barnes, P.J., Belvisi, M.G., Resveratrol, an extract of red wine, inhibits lipopolysaccharide induced airway neutrophilia and inflammatory mediators through an NF-kappa B–independent mechanism. FASEB J 19 (2005), 840–841.
12. Rahman, I., Biswas, S.K., Kirkham, P.A., Regulation of inflammation and redox signaling by dietary polyphenols. Biochem Pharmacol 72 (2006), 1439–1452.
13. Smoliga, J.M., Baur, J.A., Hausenblas, H.A., Resveratrol and health—a comprehensive review of human clinical trials. Mol Nutr Food Res 55 (2011), 1129–1141.
14. Liu, K., Zhou, R., Wang, B., Mi, M.-T., Effect of resveratrol on glucose control and insulin sensitivity: a meta-analysis of 11 randomized controlled trials. Am J Clin Nutr 99 (2014), 1510–1519.
15. Csiszar, A., Anti-inflammatory effects of resveratrol: possible role in prevention of age-related cardiovascular disease. Ann N Y Acad Sci 1215 (2011), 117–122.
16. Alarcon De La Lastra, C., Villegas, I., Resveratrol as an anti-inflammatory and anti-aging agent: mechanisms and clinical implications. Mol Nutr Food Res 49 (2005), 405–430.
17. Tome-Carneiro, J., Gonzalvez, M., Larrosa, M., Yanez-Gascon, M.J., Garcia-Almagro, F.J., Ruiz-Ros, J.A., et al. One-year consumption of a grape nutraceutical containing resveratrol improves the inflammatory and fibrinolytic status of patients in primary prevention of cardiovascular disease. Am J Cardiol 110 (2012), 356–363.
18. Faghihzadeh, F., Adibi, P., Rafiei, R., Hekmatdoost, A., Resveratrol supplementation improves inflammatory biomarkers in patients with nonalcoholic fatty liver disease. Nutr Res 34 (2014), 837–843.
19. Pickering, T.G., Hall, J.E., Appel, L.J., Falkner, B.E., Graves, J., Hill, M.N., et al. Recommendations for blood pressure measurement in humans and experimental animals. Circulation 111 (2005), 697–716.
20. Organization WH, Waist circumference and waist-hip ratio: report of a WHO expert consultation, Geneva, 8–11 December 2008. 2011.
21. Panda, S.K., Ravindran, B., Histopaque, F., Isolation of human PBMCs. Bio Protoc, 3, 2013, e323.
22. Panda, S., Ravindran, B., In vitro culture of human PBMCs. Bio Protoc, 3, 2013, e322.
23. Liu, Z., Whole blood staining of human monocyte subsets for flow cytometry. 2011.
24. Poulsen, M.M., Fjeldborg, K., Ornstrup, M.J., Kjaer, T.N., Nohr, M.K., Pedersen, S.B., Resveratrol and inflammation: challenges in translating pre-clinical findings to improved patient outcomes. Biochim Biophys Acta 1852 (2015), 1124–1136.
25. Svajger, U., Jeras, M., Anti-inflammatory effects of resveratrol and its potential use in therapy of immune-mediated diseases. Int Rev Immunol 31 (2012), 202–222.
26. Militaru, C., Donoiu, I., Craciun, A., Scorei, I.D., Bulearca, A.M., Scorei, R.I., Oral resveratrol and calcium fructoborate supplementation in subjects with stable angina pectoris: effects on lipid profiles, inflammation markers, and quality of life. Nutrition 29 (2013), 178–183.
27. Tome-Carneiro, J., Gonzalvez, M., Larrosa, M., Yanez-Gascon, M.J., Garcia-Almagro, F.J., Ruiz-Ros, J.A., et al. Grape resveratrol increases serum adiponectin and downregulates inflammatory genes in peripheral blood mononuclear cells: a triple-blind, placebo-controlled, one-year clinical trial in patients with stable coronary artery disease. Cardiovasc Drugs Ther 27 (2013), 37–48.
28. Chachay, V.S., Macdonald, G.A., Martin, J.H., Whitehead, J.P., O'Moore-Sullivan, T.M., Lee, P., et al. Resveratrol does not benefit patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 12 (2014), 2092–2103 [e6].
29. Olesen, J., Gliemann, L., Biensø R., Schmidt, J., Hellsten, Y., Pilegaard, H., Exercise training, but not resveratrol, improves metabolic and inflammatory status in skeletal muscle of aged men. J Physiol 592 (2014), 1873–1886.
30. Poulsen, M.M., Vestergaard, P.F., Clasen, B.F., Radko, Y., Christensen, L.P., Stodkilde-Jorgensen, H., et al. High-dose resveratrol supplementation in obese men: an investigator-initiated, randomized, placebo-controlled clinical trial of substrate metabolism, insulin sensitivity, and body composition. Diabetes 62 (2013), 1186–1195.
31. van der Made, S.M., Plat, J., Mensink, R.P., Resveratrol does not influence metabolic risk markers related to cardiovascular health in overweight and slightly obese subjects: a randomized, placebo-controlled crossover trial. PLoS One, 10, 2015, e0118393.
32. Yoshino, J., Conte, C., Fontana, L., Mittendorfer, B., Imai, S.-i., Schechtman, K.B., et al. Resveratrol supplementation does not improve metabolic function in nonobese women with normal glucose tolerance. Cell Metab 16 (2012), 658–664.
33. Mukherjee, R., Barman, P.K., Thatoi, P.K., Tripathy, R., Das, B.K., Ravindran, B., Non-classical monocytes display inflammatory features: validation in sepsis and systemic lupus erythematous. Sci Rep, 5, 2015, 13886.
34. Diterich, I., Härter, L., Hassler, D., Wendel, A., Hartung, T., Modulation of cytokine release in ex vivo–stimulated blood from borreliosis patients. Infect Immun 69 (2001), 687–694.
35. Bo, S., Ponzo, V., Ciccone, G., Evangelista, A., Saba, F., Goitre, I., et al. Six months of resveratrol supplementation has no measurable effect in type 2 diabetic patients. A randomized, double blind, placebo-controlled trial. Pharmacol Res 111 (2016), 896–905.
36. Zare Javid, A., Hormoznejad, R., Zakerkish, M., Haghighi-zadeh, M.H., Barzegar, A., Niknejad, N., The effect of resveratrol supplementation in adjunct with non-surgical periodontal treatment on blood glucose, triglyceride, periodontal status and some inflammatory markers in type 2 diabetic patients with periodontal disease. Nutr Food Sci Res 3 (2016), 17–26.
37. Crandall, J.P., Oram, V., Trandafirescu, G., Reid, M., Kishore, P., Hawkins, M., et al. Pilot study of resveratrol in older adults with impaired glucose tolerance. J Gerontol A Biol Sci Med Sci, 67(12), 2012, 1307.
38. Sahebkar, A., Serban, C., Ursoniu, S., Wong, N.D., Muntner, P., Graham, I.M., et al. Lack of efficacy of resveratrol on C-reactive protein and selected cardiovascular risk factors—results from a systematic review and meta-analysis of randomized controlled trials. Int J Cardiol 189 (2015), 47–55.
39. Tome-Carneiro, J., Larrosa, M., Yanez-Gascon, M.J., Davalos, A., Gil-Zamorano, J., Gonzalvez, M., et al. One-year supplementation with a grape extract containing resveratrol modulates inflammatory-related microRNAs and cytokines expression in peripheral blood mononuclear cells of type 2 diabetes and hypertensive patients with coronary artery disease. Pharmacol Res 72 (2013), 69–82.
40. Timmers, S., Konings, E., Bilet, L., Houtkooper, R.H., van de Weijer, T., Goossens, G.H., et al. Calorie restriction–like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab 14 (2011), 612–622.
41. Poulsen, M.M., Vestergaard, P.F., Clasen, B.F., Radko, Y., Christensen, L.P., Stødkilde-Jørgensen, H., et al. High-dose resveratrol supplementation in obese men. Diabetes 62 (2013), 1186–1195.
42. Penumathsa, S.V., Thirunavukkarasu, M., Zhan, L., Maulik, G., Menon, V., Bagchi, D., et al. Resveratrol enhances GLUT-4 translocation to the caveolar lipid raft fractions through AMPK/Akt/eNOS signalling pathway in diabetic myocardium. J Cell Mol Med, 12(61), 2008, 2350.
43. Su, H.-C., Hung, L.-M., Chen, J.-K., Resveratrol, a red wine antioxidant, possesses an insulin-like effect in streptozotocin-induced diabetic rats. Am J Physiol Endocrinol Metab 290 (2006), E1339–E1346.
44. Brasnyo, P., Molnar, G.A., Mohas, M., Marko, L., Laczy, B., Cseh, J., et al. Resveratrol improves insulin sensitivity, reduces oxidative stress and activates the Akt pathway in type 2 diabetic patients. Br J Nutr 106 (2011), 383–389.
45. Movahed, A., Nabipour, I., Lieben Louis, X., Thandapilly, S.J., Yu, L., Kalantarhormozi, M., et al. Antihyperglycemic effects of short term resveratrol supplementation in type 2 diabetic patients. Evid Based Complement Alternat Med, 2013, 2013, 851267.
46. Kumar, B.J., Joghee, N.M., Resveratrol supplementation in patients with type 2 diabetes mellitus: a prospective, open label, randomized controlled trial. Int Res J Pharm 4 (2013), 245–249.
47. Hausenblas, H.A., Schoulda, J.A., Smoliga, J.M., Resveratrol treatment as an adjunct to pharmacological management in type 2 diabetes mellitus—systematic review and meta-analysis. Mol Nutr Food Res 59 (2015), 147–159.
48. Sahebkar, A., Effects of resveratrol supplementation on plasma lipids: a systematic review and meta-analysis of randomized controlled trials. Nutr Rev 71 (2013), 822–835.
49. Elgebaly, A., Radwan, I.A., AboElnas, M.M., Ibrahim, H.H., Eltoomy, M.F., Atta, A.A., et al. Resveratrol supplementation in patients with non-alcoholic fatty liver disease: systematic review and meta-analysis. J Gastrointestin Liver Dis, 2017, 26.
50. Kim, S., Jin, Y., Choi, Y., Park, T., Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem Pharmacol 81 (2011), 1343–1351.
51. Lasa, A., Churruca, I., Eseberri, I., Andrés-Lacueva, C., Portillo, M.P., Delipidating effect of resveratrol metabolites in 3T3-L1 adipocytes. Mol Nutr Food Res 56 (2012), 1559–1568.
52. Wang, S., Liang, X., Yang, Q., Fu, X., Rogers, C.J., Zhu, M., et al. Resveratrol induces brown-like adipocyte formation in white fat through activation of AMP-activated protein kinase (AMPK) α1. Int J Obes 39 (2015), 967–976.
53. Janssen, I., Katzmarzyk, P.T., Ross, R., Waist circumference and not body mass index explains obesity-related health risk. Am J Clin Nutr 79 (2004), 379–384.
54. Theodotou, M., Fokianos, K., Mouzouridou, A., Konstantinou, C., Aristotelous, A., Prodromou, D., et al. The effect of resveratrol on hypertension: a clinical trial. Exp Ther Med 13 (2017), 295–301.
55. Liu, Y., Ma, W., Zhang, P., He, S., Huang, D., Effect of resveratrol on blood pressure: a meta-analysis of randomized controlled trials. Clin Nutr 34 (2015), 27–34.
56. Liu, Z., Song, Y., Zhang, X., Liu, Z., Zhang, W., Mao, W., et al. Effects of trans-resveratrol on hypertension-induced cardiac hypertrophy using the partially nephrectomized rat model. Clin Exp Pharmacol Physiol 32 (2005), 1049–1054.
57. Bhatt, J.K., Thomas, S., Nanjan, M.J., Resveratrol supplementation improves glycemic control in type 2 diabetes mellitus. Nutr Res 32 (2012), 537–541.
58. Thazhath, S.S., Wu, T., Bound, M.J., Checklin, H.L., Standfield, S., Jones, K.L., et al. Administration of resveratrol for 5 wk has no effect on glucagon-like peptide 1 secretion, gastric emptying, or glycemic control in type 2 diabetes: a randomized controlled trial. Am J Clin Nutr 103 (2016), 66–70.