Generic placeholder image

Cardiovascular & Hematological Disorders-Drug Targets

Editor-in-Chief

ISSN (Print): 1871-529X
ISSN (Online): 2212-4063

Research Article

Beneficial Effect of Saharan Propolis on Glucose Metabolism in Streptozotocin- induced Diabetic Rats

Author(s): Mourad Akdad, Bouchra Azzaoui and Mohamed Eddouks*

Volume 21, Issue 4, 2021

Published on: 08 December, 2021

Page: [243 - 252] Pages: 10

DOI: 10.2174/1871529X21666211118141935

Price: $65

Abstract

Aims: The aim of the study was to evaluate the antihyperglycemic activity of propolis from Saharan region of Morocco.

Background: Propolis is known from ancient times for its beneficial action on health.

Objective: The study aimed to evaluate the effect of Moroccan propolis aqueous extract from the desert region on glycemia and lipid metabolism.

Methods: The antihyperglycemic and antidyslipidemic activities of Moroccan propolis aqueous extract were evaluated in streptozotocin-induced diabetic rats. Glycemia was monitored during acute (6h) and subchronic treatments. Histopathological analysis of the liver and the serum lipid profile was also evaluated in addition to the glucose tolerance.

Results: This work demonstrated that the aqueous extract of Moroccan propolis exhibited a significant antihyperglycemic effect in diabetic rats. Histopathological data demonstrated that propolis acts positively on the liver of diabetic rats. In addition, the preliminary phytochemical screening revealed that Moroccan propolis contains several phytochemicals. Finally, Moroccan propolis had a potent antioxidant activity which may be due to the richness in polyphenols content (90.91 mg EAG/1 g of extract).

Conclusion: The present study shows that Moroccan propolis from the hot desert region possesses a potent antihyperglycemic effect.

Keywords: Propolis, antidiabetic, streptozotocin, phytochimestry, antioxidant activity, medicinal plant.

Graphical Abstract

[1]
Usman, U.Z.; Bakar, A.B.A.; Mohamed, M. Propolis improves pregnancy outcomes and placental oxidative stress status in streptozotocin-induced diabetic rats. BMC Complement. Altern. Med., 2018, 18(1), 324.
[http://dx.doi.org/10.1186/s12906-018-2391-6] [PMID: 30518366]
[2]
Zhao, L.; Pu, L.; Wei, J.; Li, J.; Wu, J.; Xin, Z.; Gao, W.; Guo, C. Brazilian green propolis improves antioxidant function in patients with type 2 diabetes mellitus. Int. J. Environ. Res. Public Health, 2016, 13(5), 498.
[http://dx.doi.org/10.3390/ijerph13050498] [PMID: 27187435]
[3]
Sforcin, J.M. Biological properties and therapeutic applications of propolis. Phytother. Res., 2016, 30(6), 894-905.
[http://dx.doi.org/10.1002/ptr.5605] [PMID: 26988443]
[4]
Zabaiou, N; Fouache, A; Trousson, A. Biological properties of propolis extracts: Something new from an ancient product. Chem. Phys. Lipids, 2017, 207(Pt B), 214-222.
[5]
Huang, S.; Zhang, C.P.; Wang, K.; Li, G.Q.; Hu, F.L. Recent advances in the chemical composition of propolis. Molecules, 2014, 19(12), 19610-19632.
[http://dx.doi.org/10.3390/molecules191219610] [PMID: 25432012]
[6]
Watanabe, M.A.; Amarante, M.K.; Conti, B.J.; Sforcin, J.M. Cytotoxic constituents of propolis inducing anticancer effects: A review. J. Pharm. Pharmacol., 2011, 63(11), 1378-1386.
[http://dx.doi.org/10.1111/j.2042-7158.2011.01331.x] [PMID: 21988419]
[7]
Burdock, GA Review of the biological properties and toxicity of bee propolis (propolis). Food Chem Toxicol, 1998, 36, (4), 347-363.
[8]
Al-Waili, N.; Al-Ghamdi, A.; Ansari, M.J.; Al-Attal, Y.; Salom, K. Synergistic effects of honey and propolis toward drug multi-resistant Staphylococcus aureus, Escherichia coli and Candida albicans isolates in single and polymicrobial cultures. Int. J. Med. Sci., 2012, 9(9), 793-800.
[http://dx.doi.org/10.7150/ijms.4722] [PMID: 23136543]
[9]
Sforcin, JM Propolis and the immune system: A review. J Ethnopharmacol, 2007, 113(1), 1-14.
[10]
El-Awady, M.S.; El-Agamy, D.S.; Suddek, G.M.; Nader, M.A. Propolis protects against high glucose-induced vascular endothelial dysfunction in isolated rat aorta. J. Physiol. Biochem., 2014, 70(1), 247-254.
[http://dx.doi.org/10.1007/s13105-013-0299-7] [PMID: 24234058]
[11]
Okutan, H.; Ozcelik, N.; Yilmaz, H.R.; Uz, E. Effects of caffeic acid phenethyl ester on lipid peroxidation and antioxidant enzymes in diabetic rat heart. Clin. Biochem., 2005, 38(2), 191-196.
[http://dx.doi.org/10.1016/j.clinbiochem.2004.10.003] [PMID: 15642285]
[12]
Shi, Y.Z.; Liu, Y.C.; Zheng, Y.F.; Chen, Y.F.; Si, J.J.; Chen, M.L.; Shou, Q.Y.; Zheng, H.Q.; Hu, F.L. Ethanol extract of chinese propolis attenuates early diabetic retinopathy by protecting the blood-retinal barrier in streptozotocin-induced diabetic rats. J. Food Sci., 2019, 84(2), 358-369.
[http://dx.doi.org/10.1111/1750-3841.14435] [PMID: 30672592]
[13]
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.
[http://dx.doi.org/10.1093/ecam/neq025] [PMID: 21785625]
[14]
Oladayo, MI Nigerian propolis improves blood glucose, glycated hemoglobin A1c, very low-density lipoprotein, and high-density lipoprotein levels in rat models of diabetes. J. Intercult. Ethnopharmacol., 2016, 5(3), 233-238.
[15]
Babatunde, I.R.; Abdulbasit, A.; Oladayo, M.I.; Olasile, O.I.; Olamide, F.R.; Gbolahan, B.W. Hepatoprotective and pancreatoprotective properties of the ethanolic extract of Nigerian propolis. J. Intercult. Ethnopharmacol., 2015, 4(2), 102-108.
[http://dx.doi.org/10.5455/jice.20150202023615] [PMID: 26401394]
[16]
Rifa’i, M.; Widodo, N. Significance of propolis administration for homeostasis of CD4(+)CD25(+) immunoregulatory T cells controlling hyperglycemia. Springerplus, 2014, 3, 526.
[http://dx.doi.org/10.1186/2193-1801-3-526] [PMID: 25279317]
[17]
Nna, V.U.; Abu Bakar, A.B.; Md Lazin, M.R.M.L.; Mohamed, M. Antioxidant, anti-inflammatory and synergistic anti-hyperglycemic effects of Malaysian propolis and metformin in streptozotocin-induced diabetic rats. Food Chem. Toxicol., 2018, 120, 305-320.
[http://dx.doi.org/10.1016/j.fct.2018.07.028] [PMID: 30026088]
[18]
Rivera-Yañez, N.; Rodriguez-Canales, M.; Nieto-Yañez, O.; Jimenez-Estrada, M.; Ibarra-Barajas, M.; Canales-Martinez, M.M.; Rodriguez-Monroy, M.A. Hypoglycaemic and antioxidant effects of propolis of Chihuahua in a model of experimental diabetes. Evid. Based Complement. Alternat. Med., 2018, 2018, 4360356.
[http://dx.doi.org/10.1155/2018/4360356] [PMID: 29713363]
[19]
Sameni, H.R.; Ramhormozi, P.; Bandegi, A.R.; Taherian, A.A.; Mirmohammadkhani, M.; Safari, M. Effects of ethanol extract of propolis on histopathological changes and anti-oxidant defense of kidney in a rat model for type 1 diabetes mellitus. J. Diabetes Investig., 2016, 7(4), 506-513.
[http://dx.doi.org/10.1111/jdi.12459] [PMID: 27181714]
[20]
Aral, C.A.; Kesim, S.; Greenwell, H.; Kara, M.; Çetin, A.; Yakan, B. Alveolar bone protective and hypoglycemic effects of systemic propolis treatment in experimental periodontitis and diabetes mellitus. J. Med. Food, 2015, 18(2), 195-201.
[http://dx.doi.org/10.1089/jmf.2013.3137] [PMID: 25265086]
[21]
Fuliang, H.U.; Hepburn, H.R.; Xuan, H.; Chen, M.; Daya, S.; Radloff, S.E. Effects of propolis on blood glucose, blood lipid and free radicals in rats with diabetes mellitus. Pharmacol. Res., 2005, 51(2), 147-152.
[http://dx.doi.org/10.1016/j.phrs.2004.06.011] [PMID: 15629260]
[22]
Oršolić, N.; Sirovina, D.; Končić, M.Z.; Lacković, G.; Gregorović, G. Effect of Croatian propolis on diabetic nephropathy and liver toxicity in mice. BMC Complement. Altern. Med., 2012, 12, 117.
[http://dx.doi.org/10.1186/1472-6882-12-117] [PMID: 22866906]
[23]
Al-Hariri, M.; Eldin, T.G.; Abu-Hozaifa, B.; Elnour, A. Glycemic control and anti-osteopathic effect of propolis in diabetic rats. Diabetes Metab. Syndr. Obes., 2011, 4, 377-384.
[http://dx.doi.org/10.2147/DMSO.S24159] [PMID: 22253535]
[24]
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.
[http://dx.doi.org/10.1155/2012/981896] [PMID: 21716678]
[25]
Gao, W.; Pu, L.; Wei, J.; Yao, Z.; Wang, Y.; Shi, T.; Zhao, L.; Jiao, C.; Guo, C. Serum antioxidant parameters are significantly increased in patients with type 2 diabetes mellitus after consumption of chinese propolis: a randomized controlled trial based on fasting serum glucose level. Diabetes Ther., 2018, 9(1), 101-111.
[http://dx.doi.org/10.1007/s13300-017-0341-9] [PMID: 29214374]
[26]
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., 2015, 3(3), 355-360.
[http://dx.doi.org/10.3892/br.2015.436] [PMID: 26137235]
[27]
Samadi, N.; Mozaffari-Khosravi, H.; Rahmanian, M.; Askarishahi, M. 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. J. Integr. Med., 2017, 15(2), 124-134.
[http://dx.doi.org/10.1016/S2095-4964(17)60315-7] [PMID: 28285617]
[28]
Ajebli, M.; Eddouks, M. Flavonoid-enriched extract from desert plant warionia saharae improves glucose and cholesterol levels in diabetic rats. Cardiovasc. Hematol. Agents Med. Chem., 2019, 17(1), 28-39.
[http://dx.doi.org/10.2174/1871525717666190121143934] [PMID: 30666919]
[29]
Akdad, M.; Azzane, A.; El Ouady, F.; Moujani, A.; El Khallouki, F.; Eddouks, M. Antihyperglycemic activity of micromeria graeca aqueous extract in streptozotocin-induced diabetic rats. Endocr. Metab. Immune Disord. Drug Targets, 2021, 21(5), 887-894.
[http://dx.doi.org/10.2174/1871530320666200807124940] [PMID: 32767952]
[30]
Swanholm, C.E.; St John, H.; Scheuer, P.J. A survey for alkaloids in Hawaiian plants. Pac. Sci., 1959, 13, 295.
[31]
Moza, B.K. J. Sci. Ind. Res. (India), 1958, 17B, 202.
[32]
Silva, J.K.; Cazarin, C.B.B.; Colomeu, T.C. Antioxidant activity of aqueous extract of passion fruit (Passifloraedulis) leaves: in vitro and in vivo study. Food Res. Int., 2013, 53(2), 882-890.
[http://dx.doi.org/10.1016/j.foodres.2012.12.043]
[33]
Blois, M.S. Antioxidant determinations by the use of a stable free radical. Nature, 1958, 181, 1199-1200.
[http://dx.doi.org/10.1038/1811199a0]
[34]
Ajebli, M.; Eddouks, M. Buxus sempervirens l improves streptozotocin-induced diabetes mellitus in rats. Cardiovasc. Hematol. Disord. Drug Targets, 2017, 17(2), 142-152.
[http://dx.doi.org/10.2174/1871529X17666170918140817] [PMID: 28925906]
[35]
Trinder, P. Enzymatic colorimetric method for glucose determination. Ann. Clin. Biochem., 1969, 6, 24-27.
[http://dx.doi.org/10.1177/000456326900600108]
[36]
Badr, G.; Sayed, E.A.; Waly, H.; Hassan, K.A.; Mahmoud, M.H.; Selamoglu, Z. The therapeutic mechanisms of propolis against ccl4 -mediated liver injury by mediating apoptosis of activated hepatic stellate cells and improving the hepatic architecture through pi3k/akt/mtor, tgf-β/smad2, bcl2/bax/p53 and inos signaling pathways. Cell. Physiol. Biochem., 2019, 53(2), 301-322.
[http://dx.doi.org/10.33594/000000140] [PMID: 31343125]
[37]
Selamoglu, Z.S.; Ozdemir, I.; Ciftci, O.; Gulhan, M.F.; Savci, A. Antioxidant effect of ethanolic extract of propolis in liver of l- name treated rats. Adv. Clin. Exp. Med., 2015, 24(2), 227-232.
[http://dx.doi.org/10.17219/acem/40461] [PMID: 25931353]
[38]
Ozdemir, B.; Gulhan, M.F.; Sahna, E.; Selamoglu, Z. The investigation of antioxidant and anti-inflammatory potentials of apitherapeutic agents on heart tissues in nitric oxide synthase inhibited rats via Nω-nitro-L-arginine methyl ester. Clin. Exp. Hypertens., 2021, 43(1), 69-76.
[http://dx.doi.org/10.1080/10641963.2020.1806294] [PMID: 32799699]
[39]
Ramin, ES; Serdar, D; Mehmet Fuat, G; Merve, D; Huda, A; Zeliha, S The effects of pollen, propolis, and caffeic acid phenethyl ester on tyrosine hydroxylase activity and total RNA levels in hypertensive rats caused by nitric oxide synthase inhibition: experimental, docking and molecular dynamic studies. 2018, 36(3), 609-620.
[40]
Talas, Z.S.; Ozdemir, I.; Ciftci, O.; Cakir, O.; Gulhan, M.F.; Pasaoglu, O.M. Role of propolis on biochemical parameters in kidney and heart tissues against L-NAME induced oxidative injury in rats. Clin. Exp. Hypertens., 2014, 36(7), 492-496.
[http://dx.doi.org/10.3109/10641963.2013.863322] [PMID: 24490594]
[41]
Selamoglu Talas, Z. Propolis reduces oxidative stress in l- NAME-induced hypertension rats. Cell Biochem. Funct., 2014, 32(2), 150-154.
[http://dx.doi.org/10.1002/cbf.2986] [PMID: 23788129]
[42]
Zeliha, S.; Ilknur, O.; Osman, C.; Oguz, C. Propolis attenuates oxidative injury in brain and lung of nitric oxide synthaseinhibited rats. J. Pharm. Care., 2013, 1(2), 45-50.
[43]
Salmas, R.E.; Gulhan, M.F.; Durdagi, S.; Sahna, E.; Abdullah, H.I.; Selamoglu, Z. Effects of propolis, caffeic acid phenethyl ester, and pollen on renal injury in hypertensive rat: An experimental and theoretical approach. Cell Biochem. Funct., 2017, 35(6), 304-314.
[http://dx.doi.org/10.1002/cbf.3277] [PMID: 28833317]
[44]
Lee, E.S.; Uhm, K.O.; Lee, Y.M.; Han, M.; Lee, M.; Park, J.M.; Suh, P.G.; Park, S.H.; Kim, H.S. CAPE (caffeic acid phenethyl ester) stimulates glucose uptake through AMPK (AMP-activated protein kinase) activation in skeletal muscle cells. Biochem. Biophys. Res. Commun., 2007, 361(4), 854-858.
[http://dx.doi.org/10.1016/j.bbrc.2007.07.068] [PMID: 17689496]
[45]
Matsui, T.; Ebuchi, S.; Fujise, T.; Abesundara, K.J.; Doi, S.; Yamada, H.; Matsumoto, K. Strong antihyperglycemic effects of water-soluble fraction of Brazilian propolis and its bioactive constituent, 3,4,5-tri-O-caffeoylquinic acid. Biol. Pharm. Bull., 2004, 27(11), 1797-1803.
[http://dx.doi.org/10.1248/bpb.27.1797] [PMID: 15516726]
[46]
Patel, D.K.; Kumar, R.; Laloo, D.; Hemalatha, S. Diabetes mellitus: An overview on its pharmacological aspects and reported medicinal plants having antidiabetic activity. Asian Pac. J. Trop. Biomed., 2012, 2(5), 411-420.
[http://dx.doi.org/10.1016/S2221-1691(12)60067-7] [PMID: 23569941]
[47]
Šuran, J; Cepanec, I; Mašek, T; Radić, B; Radić, S; Tlak Gajger, I; Vlainić, J. Propolis extract and its bioactive compounds-from traditional to modern extraction technologies. Molecules, 2021, 26(10), 2930.
[48]
Corbi, G.; Conti, V.; Komici, K.; Manzo, V.; Filippelli, A.; Palazzo, M.; Vizzari, F.; Davinelli, S.; Di Costanzo, A.; Scapagnini, G.; Ferrara, N.; Casamassima, D. Phenolic plant extracts induce sirt1 activity and increase antioxidant levels in the rabbit’s heart and liver. Oxid. Med. Cell. Longev., 2018, 2018, 2731289.
[http://dx.doi.org/10.1155/2018/2731289] [PMID: 30116475]
[49]
Hogan, S; Canning, C; Sun, S; Sun, X; Kadouh, H; Zhou, K Dietary supplementation of grape skin extract improves glycemia and inflammation in diet-induced obese mice fed a Western high fat diet. J. Agric. Food Chem., 2011, 59(7), 3035-3041.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy