Effects of bee propolis supplementation on glycemic control, lipid profile and insulin resistance indices in patients with type 2 diabetes: a randomized, double-blind clinical trial

Journal of Integrative Medicine

Volumn 15, Issue 2, 2017, Pages 124-134

  Samadi, Nazli ^a   Mozaffari Khosravi, Hassan ^a   Rahmanian, Masoud ^a   Askarishahi, Mohsen ^a  

^a SHAHID SADOUGHI UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

blood glucose; diabetes mellitus, type 2; insulin resistance; propolis

Indexed keywords

GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN; INSULIN; LIPID; LOW DENSITY LIPOPROTEIN; PLACEBO; PROPOLIS; TRIACYLGLYCEROL; GLUCOSE BLOOD LEVEL; GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN A1C PROTEIN, HUMAN;

ADULT; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DEMOGRAPHY; DIET RESTRICTION; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; FEMALE; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; HUMAN; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SUPPLEMENTATION; ANALYSIS; BLOOD; DIABETES MELLITUS, TYPE 2;

ADULT; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; DOUBLE-BLIND METHOD; FEMALE; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; INSULIN RESISTANCE; LIPIDS; MALE; MIDDLE AGED; PROPOLIS;

EID: 85050576938     PISSN: 20954964     EISSN: None     Source Type: Journal    
DOI: 10.1016/S2095-4964(17)60315-7     Document Type: Article

References (63)

1. American Diabetes Association, Diagnosis and classification of diabetes mellitus. Diabetes Care 37:Suppl 1 (2014), S81–S90.
2. Craig, ME, Hattersley, A, Donaghue, KC, Definition, epidemiology and classification of diabetes in children and adolescents. Pediatric Diabetes 10:Suppl 12 (2009), 3–12.
3. Galtier, F, Definition, epidemiology, risk factors. Diabetes Metab 36:6 (2010), 628–651.
4. Melmed, S, Polonsky, KS, Larsen, PR, Kronenberg, HM, Williams textbook of endocrinology, 13th ed., 2015, Elsevier Health Sciences, Philadelphia.
5. Shi, Y, Hu, FB, The global implications of diabetes and cancer. Lancet 383:9933 (2014), 1947–1948.
6. Vos, T, Flaxman, AD, Naghavi, M, Lozano, R, Michaud, C, Ezzati, M, Shibuya, K, Salomon, JA, Abdalla, S, Aboyans, V, et al. Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:9859 (2012), 2163–2196.
7. Wild, S, Roglic, G, Green, A, Sicree, R, King, H, Global prevalence of diabetes estimates for the year 2000 and projections for 2030. Diabetes Care 27:5 (2004), 1047–1053.
8. Toreti, VC, Sato, HH, Pastore, GM, Park, YK, Recent progress of propolis for its biological and chemical compositions and its botanical origin. Evid Based Complement Alternat Med, 2013, 2013, 697390.
9. Búfalo, MC, Candeias, JM, Sforcin, JM, In vitro cytotoxic effect of Brazilian green propolis on human laryngeal epidermoid carcinoma (HEp-2) cells. Evid Based Complement Alternat Med 6:4 (2009), 483–487.
10. Castaldo, S, Capasso, F, Propolis, an old remedy used in modern medicine. Fitoterapia 73:Suppl 1 (2002), S1–S6.
11. Mizrahi, A, Lensky, Y, Bee products: properties, applications, and apitherapy, 1997, Springer Science & Business Media, New York.
12. Ghisalberti, EL, Propolis: a review. Bee World 60:2 (1979), 59–84.
13. Burdock, GA, Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol 36:4 (1998), 347–363.
14. Pietta, PG, Gardana, C, Pietta, AM, Analytical methods for quality control of propolis. Fitoterapia 73:Suppl 1 (2002), S7–S20.
15. Walker, P, Crane, E, Constituents of propolis. Apidologie 18:4 (1987), 327–334.
16. Bueno-Silva, B, Alencar, SM, Koo, H, Ikegaki, M, Silva, GV, Napimoga, MH, Rosalen, PL, Anti-inflammatory and antimicrobial evaluation of neovestitol and vestitol isolated from Brazilian red propolis. J Agric Food Chem 61:19 (2013), 4546–4550.
17. Lopes, AA, Ferreira, TS, Nesi, RT, Lanzetti, M, Pires, KMP, Silva, AM, Borges, RM, Silva, AJR, Valença, SS, Porto, LC, Antioxidant action of propolis on mouse lungs exposed to short-term cigarette smoke. Bioorg Med Chem 21:24 (2013), 7570–7577.
18. Martin, LFT, Rocha, EM, Garcia, SB, Paula, JS, Topical Brazilian propolis improves corneal wound healing and inflammation in rats following alkali burns. BMC Complement Altern Med, 13(1), 2013, 337.
19. Machado, JL, Assunção, AK, da Silva, MC, Dos Reis, AS, Costa, GC, Arruda Dde, S, Rocha, BA, Vaz, MM, Paes, AM, Guerra, RN, Berretta, AA, do Nascimento, FR, Brazilian green propolis: anti-inflammatory property by an immunomodulatory activity. Evid Based Complement Alternat Med, 2012, 2012, 157652.
20. Verma, MK, Pandey, RK, Khanna, R, Agarwal, J, The antimicrobial effectiveness of 25% propolis extract in root canal irrigation of primary teeth. J Indian Soc Pedod Prev Dent, 32(2), 2014, 120.
21. Dota, KF, Consolaro, ME, Svidzinski, TI, Bruschi, ML, Antifungal activity of Brazilian propolis microparticles against yeasts isolated from vulvovaginal candidiasis. Evid Based Complement Alternat Med, 2011, 2011, 201953.
22. Silici, S, Koç NA, Ayangil, D, Çankaya, S, Antifungal activities of propolis collected by different races of honeybees against yeasts isolated from patients with superficial mycoses. J Pharmacol Sci 99:1 (2005), 39–44.
23. Fuliang, HU, Hepburn, H, Xuan, H, Chen, M, Daya, SE, Radloff, S, Effects of propolis on blood glucose, blood lipid and free radicals in rats with diabetes mellitus. Pharmacol Res 51:2 (2005), 147–152.
24. Campos, JF, dos Santos, UP, Macorini, LFB, de Melo, AMMF, Balestieri, JBP, Paredes-Gamero, EJ, Ardoso, CAL, de Picoli Souza, K, dos Santos, EL, Antimicrobial, antioxidant and cytotoxic activities of propolis from Melipona orbignyi (Hymenoptera, Apidae). Food Chem Toxicol 65 (2014), 374–380.
25. Cinegaglia, NC, Bersano, PRO, Araújo, MJAM, Búfalo, MC, Sforcin, JM, Anticancer effects of geopropolis produced by stingless bees on canine osteosarcoma cells in vitro. Evid Based Complement Alternat Med, 2013, 2013, 737386.
26. Omene, C, Kalac, M, Wu, J, Marchi, E, Frenkel, K, O'Connor, OA, Propolis and its active component, caffeic acid phenethyl ester (CAPE), modulate breast cancer therapeutic targets via an epigenetically mediated mechanism of action. J Cancer Sci Ther 5:10 (2013), 334–342.
27. Fan, Y, Ma, L, Zhang, W, Wang, J, Chen, Y, Gao, Y, Feng, W, Zhong, L, Song, X, The design of propolis flavone microemulsion and its effect on enhancing the immunity and antioxidant activity in mice. Int J Biol Macromol 65 (2014), 200–207.
28. Choudhari, MK, Haghniaz, R, Rajwade, JM, Paknikar, KM, Anticancer activity of Indian stingless bee propolis: an in vitro study. Evid Based Complement Alternat Med, 2013, 2013, 928280.
29. Szliszka, E, Krol, W, Polyphenols isolated from propolis augment TRAIL-induced apoptosis in cancer cells. Evid Based Complement Alternat Med, 2013, 2013, 731940.
30. Missima, F, Sforcin, JM, Green Brazilian propolis action on macrophages and lymphoid organs of chronically stressed mice. Evid Based Complement Alternat Med 5:1 (2008), 71–75.
31. Orsatti, CL, Missima, F, Pagliarone, AC, Bachiega, TF, Búfalo, MC, Araújo, JP Jr, Sforcin, JM, Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice. Phytother Res 24:8 (2010), 1141–1146.
32. Maruyama, H, Sumitou, Y, Sakamoto, T, Araki, Y, Hara, H, Antihypertensive effects of flavonoids isolated from Brazilian green propolis in spontaneously hypertensive rats. Biol Pharm Bull 32:7 (2009), 1244–1250.
33. Mishima, S, Yoshida, C, Akino, S, Sakamoto, T, Antihypertensive effects of Brazilian propolis: identification of caffeoylquinic acids as constituents involved in the hypotension in spontaneously hypertensive rats. Biol Pharm Bull 28:10 (2005), 1909–1914.
34. Kolankaya, D, Selmanoĝlu, G, Sorkun, K, Salih, B, Protective effects of Turkish propolis on alcohol-induced serum lipid changes and liver injury in male rats. Food Chem 78:2 (2002), 213–217.
35. Tan-No, K, Nakajima, T, Shoji, T, Nakagawasai, O, Niijima, F, Ishikawa, M, Endo, Y, Sato, T, Satoh, S, Tadano, T, Anti-inflammatory effect of propolis through inhibition of nitric oxide production on carrageenin-induced mouse paw edema. Biol Pharm Bull 29:1 (2006), 96–99.
36. Hoşnuter, M, Gürel, A, Babucçu, O, Armutcu, F, Kargi, E, Işikdemir, A, The effect of CAPE on lipid peroxidation and nitric oxide levels in the plasma of rats following thermal injury. Burns 30:2 (2004), 121–125.
37. Silva, V, Genta, G, Möller, MN, Masner, M, Thomson, L, Romero, N, Radi, R, Fernandes, DC, Laurindo, FR, Heinzen, H, Fierro, W, Denicola, A, Antioxidant activity of uruguayan propolis. In vitro and cellular assays. J Agric Food Chem 59:12 (2011), 6430–6437.
38. Jasprica, I, Mornar, A, Debeljak, Z, Smolcić-Bubalo, A, Medić-Sarić M, Mayer, L, Romić Z, Bućan, K, Balog, T, Sobocanec, S, Sverko, V, In vivo study of propolis supplementation effects on antioxidative status and red blood cells. J Ethnopharmacol 110:3 (2007), 548–554.
39. Zhao, JQ, Wen, YF, Bhadauria, M, Nirala, SK, Sharma, A, Shrivastava, S, Shukla, S, Agrawal, OP, Mathur, R, Protective effects of propolis on inorganic mercury induced oxidative stress in mice. Indian J Exp Biol 47:4 (2009), 264–269.
40. Alyane, M, Kebsa, L, Boussenane, H, Rouibah, H, Lahouel, M, Cardioprotective effects and mechanism of action of polyphenols extracted from propolis against doxorubicin toxicity. Pak J Pharm Sci 21:3 (2008), 201–209.
41. Norata, GD, Marchesi, P, Passamonti, S, Pirillo, A, Violi, F, Catapano, AL, Anti-inflammatory and anti-atherogenic effects of cathechin, caffeic acid and trans-resveratrol in apolipoprotein E deficient mice. Atherosclerosis 191:2 (2007), 265–271.
42. Grassi, D, Aggio, A, Onori, L, Croce, G, Tiberti, S, Ferri, C, Ferri, L, Desideri, G, Tea, flavonoids, and nitric oxide-mediated vascular reactivity. J Nutr 138:8 (2008), 1554S–1560S.
43. Gorinstein, S, Leontowicz, H, Leontowicz, M, Jesion, I, Namiesnik, J, Drzewiecki, J, Park, YS, Ham, KS, Giordani, E, Trakhtenberg, S, Influence of two cultivars of persimmon on atherosclerosis indices in rats fed cholesterol-containing diets: investigation in vitro and in vivo. Nutrition 27:7–8 (2011), 838–846.
44. Tosi, B, Donini, A, Romagnoli, C, Bruni, A, Antimicrobial activity of some commercial extracts of propolis prepared with different solvents. Phytother Res 10:4 (1996), 335–336.
45. Park, YK, Koo, MH, Abreu, JA, Ikegaki, M, Cury, JA, Rosalen, PL, Antimicrobial activity of propolis on oral microorganisms. Curr Microbiol 36:1 (1998), 24–28.
46. Rossi, A, Longo, R, Russo, A, Borrelli, F, Sautebin, L, The role of the phenethyl ester of caffeic acid (CAPE) in the inhibition of rat lung cyclooxygenase activity by propolis. Fitoterapia 73:Suppl 1 (2002), S30–S37.
47. Lee, YJ, Kuo, HC, Chu, CY, Wang, CJ, Lin, WC, Tseng, TH, Involvement of tumor suppressor protein p53 and p38 MAPK in caffeic acid phenethyl ester-induced apoptosis of C6 glioma cells. Biochem Pharmacol 66:12 (2003), 2281–2289.
48. Attia, YA, Al-Hamid, AEA, Ibrahim, MS, Al-Harthi, MA, Bovera, F, Elnaggar, AS, Productive performance, biochemical and hematological traits of broiler chickens supplemented with propolis, bee pollen, and mannan oligosaccharides continuously or intermittently. Livest Sci 164:6 (2014), 87–95.
49. Attia, YA, Bovera, F, El-Tahawy, WS, El-Hanoun, AM, Al-Harthi, MA, Habiba, HI, Productive and reproductive performance of rabbits does as affected by bee pollen and/or propolis, inulin and/or mannan-oligosaccharides. World Rabbit Sci 23:4 (2015), 273–282.
50. Li, Y, Chen, M, Xuan, H, Hu, F, Effects of encapsulated propolis on blood glycemic control, lipid metabolism, and insulin resistance in type 2 diabetes mellitus rats. Evid Based Complement Alternat Med, 2012, 2012, 981896.
51. Abo-Salem, OM, El-Edel, RH, Harisa, GE, El-Halawany, N, Ghonaim, MM, Experimental diabetic nephropathy can be prevented by propolis: effect on metabolic disturbances and renal oxidative parameters. Pak J Pharm Sci 22:2 (2009), 205–210.
52. Kang, LJ, Lee, HB, Bae, HJ, Lee, SG, Antidiabetic effect of propolis: reduction of expression of glucose-6-phosphatase through inhibition of Y279 and Y216 autophosphorylation of GSK-3α/β in HepG2 cells. Phytother Res 24:10 (2010), 1554–1561.
53. Ueda, M, Hayashibara, K, Ashida, H, Propolis extract promotes translocation of glucose transporter 4 and glucose uptake through both PI3K-and AMPK-dependent pathways in skeletal muscle. Biofactors 39:4 (2013), 457–466.
54. Kitamura, H, Naoe, Y, Kimura, S, Miyamoto, T, Okamoto, S, Toda, C, Shimamoto, Y, Iwanaga, T, Miyoshi, I, Beneficial effects of Brazilian propolis on type 2 diabetes in ob/ob mice: possible involvement of immune cells in mesenteric adipose tissue. Adipocyte 2:4 (2013), 227–236.
55. Zhu, W, Chen, M, Shou, Q, Li, Y, Hu, F, Biological activities of Chinese propolis and Brazilian propolis on streptozotocin-induced type 1 diabetes mellitus in rats. Evid Based Complement Alternat Med, 2011, 2011, 468529.
56. Al-Hariri, M, Eldin, TG, Abu-Hozaifa, B, Elnour, A, Glycemic control and anti-osteopathic effect of propolis in diabetic rats. Diabetes Metab Syndr Obes 4 (2011), 377–384.
57. Zamami, Y, Fujiwara, H, Hosoda, M, Hino, H, Hirai, K, Okamoto, K, Jin, X, Takatori, S, Doi-Takaki, S, Kawasaki, H, Ameliorative effect of propolis on insulin resistance in Otsuka Long-Evans Tokushima Fatty (OLETF) rats. Yakugaku Zasshi 130:6 (2010), 833–840 Japanese with abstract in English.
58. Tang, HW, Chan, CH, Lin, YT, Huang, HY, Anti-diabetic effects of propolis in high fat diet fed-streptozotocin-induced type 2 diabetic rat. FASEB J 29:Suppl 1 (2015), 756–757.
59. Murata, K, Yatsunami, K, Fukuda, E, Onodera, S, Mizukami, O, Hoshino, G, Kamei, T, Antihyperglycemic effects of propolis mixed with mulberry leaf extract on patients with type 2 diabetes. Altern Ther Health Med 10:3 (2004), 78–79.
60. Fukuda, T, Fukui, M, Tanaka, M, Senmaru, T, Iwase, H, Yamazaki, M, Aoi, W, Inui, T, Nakamura, N, Marunaka, Y, Effect of Brazilian green propolis in patients with type 2 diabetes: a double-blind randomized placebo-controlled study. Biomed Rep 3:3 (2015), 355–360.
61. Friedwald, W, Leve, R, Fredrichson, D, Estimation of concentration of low density lipoproteins separated by three different methods. Clin Chem 18 (1972), 499–502.
62. Diabetes Trials Unit, University of Oxford, HOMA Calculator v2.2. [2015-08-30]. https://www.dtu.ox.ac.uk/homacalculator/.
63. Borai, A, Livingstone, C, Kaddam, I, Ferns, G, Selection of the appropriate method for the assessment of insulin resistance. BMC Med Res Methodol, 11, 2011, 158.