Effects of Ethanol Extract of Propolis on Repair Optic Nerve Damage in a Rat Model for Diabetes Mellitus (Study of MDA, CRP, Caspase-3, and TGF-β Expression and Histopathological Changes on Optic Nerve Damage)

Authors

  • Nur Shani Meida Department of Medical Science, Universitas Sebelas Maret, Surakarta, Indonesia; Department of Ophthalmology, Medical Education Study Program, Faculty of Medicine and Health Sciences, Universitas Muhammadiyah Yogyakarta, Yogyakarta, Indonesia
  • Bambang Purwanto Department of Medical Science, Universitas Sebelas Maret, Surakarta, Indonesia image/svg+xml
  • Brian Wasita Department of Medical Science, Universitas Sebelas Maret, Surakarta, Indonesia image/svg+xml
  • Senyum Indrakila Department of Medical Science, Universitas Sebelas Maret, Surakarta, Indonesia image/svg+xml
  • Soetrisno Soetrisno Department of Medical Science, Universitas Sebelas Maret, Surakarta, Indonesia image/svg+xml
  • Eti Poncorini Department of Medical Science, Universitas Sebelas Maret, Surakarta, Indonesia image/svg+xml
  • Risya Cilmiaty Department of Medical Science, Universitas Sebelas Maret, Surakarta, Indonesia image/svg+xml

DOI:

https://doi.org/10.3889/oamjms.2022.8646

Keywords:

Diabetes mellitus, Ethanolic extract of propolis, Optic nerve, Oxidative stress

Abstract

Purpose

Hyperglycemia in diabetes increases oxidative stress in the body. It causes optic nerve damage and risk of glaucoma. In this study, we evaluated and analyzed the effect of propolis ethanol extract on repair of optic nerve damage in a rat model for Diabetes Mellitus.

Study Design

Laboratory experimental using the posttest only control group design was used in this study.

Methods

A total of 28 male Wistar rat were randomly divided into the following four groups namely control (K1), diabetes mellitus (K2), diabetes mellitus with propolis treatment (100 mg/kg) (P1) and diabetes mellitus with propolis treatment (200 mg/kg) (P2). Statistical analysis used ANOVA and Kruskal Wallis with a significance of p < 0.05.

Results

The results showed that Gunung Lawu propolis significantly reduced serum glucose levels, malondialdehyde levels and C-reactive protein levels (p<0.01). Furthermore, propolis extract significantly decreased caspase-3 expression and TGF-β expression (p<0.05) in the optic nerve. Propolis can significantly repair optic nerve damage (optic nerve necrosis, thinning of the retinal nerve fiber layer and retinal ganglion cell apoptosis (p < 0.01).

Conclusion

The final results showed that most of the beneficial effects of propolis were mediated by the reduction of blood glucose levels in diabetic rat.

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References

Sahin H, Aliyazicioglu R, Yildiz O, Kolayli S, Innocenti A, Supuran CT. Honey, polien, and propolis extracts show potent inhibitory activity against the zinc metalloenzyme carbonic anhydrase. J Enzyme Inhib Med Chem. 2011;26(3):440-4. http://doi.org/103109/147563662010503610 PMid:20687792 DOI: https://doi.org/10.3109/14756366.2010.503610

Prasetyo DH, Martini, Syarifah I, Sarsono S. IIdentification of caffeic acid phenethyl ester in mountain isolate propolis ethanol extract lawu. J Bahan Alam Indones. 2012;8(2).

Ahmed KA, Muniandy S, Ismail IS. Type 2 Diabetes and vascular complications: A pathophysiologic view. Biomed Res. 2010;21(2):147-55.

Perkeni. Konsensus Pengendalian dan Pencegahan Diabetes Mellitus Tipe 2 di Indonesia 2011. Jakarta: Perkeni; 2011.

Vasudevanand P, Sridhar G. A clinical study of the ocular complications of diabetes mellitus. IOSR J Dent Med Sci. 2018;17(3):45-9. Available from: http://www.iosrjournals.org [Last accessed on 2021 Sep 14].

Vieira-Potter VJ, Karamichos D, Lee DJ. Ocular complications of diabetes and therapeutic approaches. Biomed Res Int. 2016;2016:3801570. http://doi.org/10.1155/2016/3801570 PMid:27119078 DOI: https://doi.org/10.1155/2016/3801570

Zhao YX, Chen XW. Diabetes and risk of glaucoma: Systematic review and a Meta-analysis of prospective cohort studies. Int J Ophthalmol. 2017;10(9):1430-5. http://doi.org/10.18240/ijo.2017.09.16 PMid:28944204 DOI: https://doi.org/10.18240/ijo.2017.09.16

Zhou M, Wang W, Huang W, Zhang X. Diabetes mellitus as a risk factor for open-angle glaucoma: A systematic review and meta-analysis. PLoS One. 2014;9(8):e102972. http://doi.org/10.1371/journal.pone.0102972 PMid:25137059 DOI: https://doi.org/10.1371/journal.pone.0102972

Zhao D, Cho J, Kim MH, Friedman DS, Guallar E. Diabetes, fasting glucose, and the risk of glaucoma: A meta-analysis. Ophthalmology. 2015;122(1):72-8. http://doi.org/10.1016/j.ophtha.2014.07.051 PMid:25283061 DOI: https://doi.org/10.1016/j.ophtha.2014.07.051

Beena R, Senthilkumar TG, Raja R. Incidence of glaucoma and diabetic retinopathy in patients with diabetes mellitus in a teaching hospital. Quest J. 2017;4:31-5.

Reddy MM, Malleswari M, Rani KS. Prevalence of primary open angle glaucoma in diabetic patients. IOSR J Dent Med Sci. 2017;16(6):147-51. DOI: https://doi.org/10.9790/0853-160603147151

Dharmadhikari S, Lohiya K, Chelkar V, Kalyani VK, Dole K, Deshpande M, et al. Magnitude and determinants of glaucoma in Type II diabetics: A hospital based cross-sectional study in Maharashtra, India. Oman J Ophthalmol. 2015;8(1):19-23. http://doi.org/10.4103/0974-620X.149858 PMid:25709269 DOI: https://doi.org/10.4103/0974-620X.149858

Jayanta T, Dipali DC, Santana S. Prevalence of Glaucoma Amongst Diabetic Patients Attending a Tertiary Health Care in North Eastern India; 2016.

Kida T, Hidehiro O, Horie T, Matsuo J, Kobayashi T, Fukumoto M, et al. NADPH oxidase-mediated ROS production determines insulin’s action on the retinal microvasculature. Invest Ophthalmol Vis Sci. 2015;56(11):6754-61. DOI: https://doi.org/10.1167/iovs.15-17534

Wright E Jr., Scism-Bacon J, Glass L. Oxidative stress in Type 2 diabetes: The role of fasting and postprandial glycaemia. Int J Clin Pract. 2006;60(3):308-14. http://doi.org/10.1111/j.1368-5031.2006.00825.x PMid:16494646 DOI: https://doi.org/10.1111/j.1368-5031.2006.00825.x

Singh Z, Karthigesu IP, Singh P, Kaur R. Use of malondialdehyde as a biomarker for assessing oxidative stress in different disease pathologies: A review. Iran J Public Health. 2014;43 Supple 3:7-16. Available from: https://www.ijph.tums.ac.ir/index.php/ijph/article/view/4858 [Last accessed on 2021 Sep 14].

Nucci C, Di Pierro D, Varesi C, Ciuffoletti E, Russo R, Gentile R, et al. Increased malondialdehyde concentration and reduced total antioxidant capacity in aqueous humor and blood samples from patients with glaucoma. Mol Vis. 2013;19:1841-6. PMid:23946639

Rivera-Yañez N, Rodriguez-Canales M, Nieto-Yañez O, Jimenez-Estrada M, Ibarra-Barajas M, Canales-Martinez MM, et al. Hypoglycaemic and antioxidant effects of propolis of chihuahua in a model of experimental diabetes. Evid Based Complement Alternat Med. 2018;2018:4360356. http://doi.org/10.1155/2018/4360356 PMid:29713363 DOI: https://doi.org/10.1155/2018/4360356

Gauthier AC, Liu J. Epigenetics and signaling pathways in glaucoma. Biomed Res Int. 2017;2017:5712341. http://doi.org/10.1155/2017/5712341 PMid:28210622 DOI: https://doi.org/10.1155/2017/5712341

Vidal-Sanz M, Salinas-Navarro M, Nadal-Nicolás FM, Alarcón-Martínez L, Valiente-Soriano FJ, de Imperial JM, et al. Understanding glaucomatous damage: Anatomical and functional data from ocular hypertensive rodent retinas. Prog Retin Eye Res. 2012;31(1):1-27. http://doi.org/10.1016/j.preteyeres.2011.08.001 PMid:21946033 DOI: https://doi.org/10.1016/j.preteyeres.2011.08.001

Galvao J, Davis BM, Cordeiro MF. In vivo imaging of retinal ganglion cell apoptosis. Curr Opin Pharmacol. 2013;13(1):123-7. http://doi.org/10.1016/j.coph.2012.08.007 PMid:22995681 DOI: https://doi.org/10.1016/j.coph.2012.08.007

Agudo-Barriuso M, Villegas-Perez M, de Imperial JM, Vidal-Sanz M. Anatomical and functional damage in experimental glaucoma. Curr Opin Pharmacol. 2012;13(1):5-11. http://doi.org/10.1016/j.coph.2012.09.006 PMid:23041078 DOI: https://doi.org/10.1016/j.coph.2012.09.006

Cvenkel B, Kolko M. Current medical therapy and future trends in the management of glaucoma treatment. J Ophthalmol. 2020;2020:6138132. http://doi.org/10.1155/2020/6138132 PMid:32774906 DOI: https://doi.org/10.1155/2020/6138132

Yu AL, Moraru O, Erb C, Welge-Lussen U. Effects of micronutrients on serum antioxidant status of glaucoma patients: A randomized, placebo-controlled, double-masked pilot study. Ophthalmol Res An Int J. 2014;2(1):1-9. DOI: https://doi.org/10.9734/OR/2014/5926

Garcia-Medina JJ, Garcia-Medina M, Garrido-Fernandez P, Galvan-Espinosa J, Garcia-Maturana C, Zanon-Moreno V, et al. A two-year follow-up of oral antioxidant supplementation in primary open-angle glaucoma: An open-label, randomized, controlled trial. Acta Ophthalmol. 2015;93(6):546-54. http://doi.org/10.1111/aos.12629 PMid:25545196 DOI: https://doi.org/10.1111/aos.12629

Szkudelski T. Streptozotocin-nicotinamide-induced diabetes in the rat. Characteristics of the experimental model. Exp Biol Med. 2012;237:481-90. DOI: https://doi.org/10.1258/ebm.2012.011372

Ghasemi A, Khalifi S, Jedi S. Streptozotocin-nicotinamide-induced rat model of Type 2 diabetes (review). Acta Physiol Hung. 2014;101(4):408-20. http://doi.org/10.1556/APhysiol.101.2014.4.2 PMid:25532953 DOI: https://doi.org/10.1556/APhysiol.101.2014.4.2

El-Gohary OA, Said MA. Protective effect of exenatide (glucagon-like peptide-1 receptor agonist) on renal ischemia-reperfusion injury in diabetic rats. Benha Med J. 2016;33(1):24. Available from: http://www.bmfj.eg.net/article.asp?issn=1110-208x;year=2016;volume=33;issue=1;spage=24;epage=30;aulast=el-gohary [Last accessed on 2021 Sep 13]. DOI: https://doi.org/10.4103/1110-208X.194384

Sankaranarayanan C, Pari L. Influence of thymoquinone on glycoprotein changes in experimental hyperglycemic mice. Int J Nutr Pharmacol Neurol Dis. 2011;1:51-5. DOI: https://doi.org/10.4103/2231-0738.77532

Rajarajeswari N, Pari L. Antioxidant role of coumarin on streptozotocin-nicotinamide-induced Type 2 diabetic rats. J Biochem Mol Toxicol. 2011;25(6):355-61. http://doi.org/10.1002/jbt.20395 PMid:21630391 DOI: https://doi.org/10.1002/jbt.20395

Al-Mahmood SM, Razak TA, Abdullah ST, Fatnoon NA, Mohamed AH, Al-Ani IM. A comprehensive study of chronic diabetes complications in streptozotocin-induced diabetic rat. Makara J Health Res. 2016;20(2):48-56. DOI: https://doi.org/10.7454/msk.v20i2.5889

El Menyiy N, Al-Waili N, El Ghouizi A, El-Guendouz S, Salom K, Lyoussi B. Potential therapeutic effect of Moroccan propolis in hyperglycemia, dyslipidemia, and hepatorenal dysfunction in diabetic rats. Iran J Basic Med Sci. 2019;22(11):1331-9. http://doi.org/10.22038/ijbms.2019.33549.8004 PMid:32128099

Zakerkish M, Jenabi M, Zaeemzadeh N, Hemmati AA, Neisi N. The effect of iranian propolis on glucose metabolism, lipid profile, insulin resistance, renal function and inflammatory biomarkers in patients with Type 2 diabetes mellitus: A randomized double-blind clinical trial. Sci Rep. 2019;9(1):7289. http://doi.org/10.1038/s41598-019-43838-8 PMid:31086222 DOI: https://doi.org/10.1038/s41598-019-43838-8

Hemieda FA, El-Kholy WM, El-Habibi ES, El-Sawah SG. Influence of propolis on oxidative stress, inflammation and apoptosis in streptozotocin-induced diabetic rats. Int J Adv Res. 2015;3(7):831-45. Available from: http://www.journalijar.com [Last accessed on 2021 Sep 13].

Afsharpour F, Hashemipour S, Haghighian HK, Koushanc Y. Effects of Iranian propolis on glycemic status, inflammatory factors, and liver enzyme levels in Type 2 diabetic patients: A randomized, double-blind, placebo-controlled, clinical trial. Clin Trial J Nutr Sci Diet. 2017;3(2):9-14.

Shang H, Bhagavathula AS, Ali Aldhaleei W, Rahmani J, Karam G, Rinaldi G, et al. Effect of propolis supplementation on C-reactive protein levels and other inflammatory factors: A systematic review and meta-analysis of randomized controlled trials. J King Saudi Univ Sci. 2020;32(2):1694-701. DOI: https://doi.org/10.1016/j.jksus.2020.01.003

Nna VU, Bakar AB, Zakaria Z, Othman ZA, Jalil NA, Mohamed M. Malaysian propolis and metformin synergistically mitigate kidney oxidative stress and inflammation in streptozotocin-induced diabetic rats. Molecules. 2021;26(11):3441. http://doi.org/10.3390/molecules26113441 PMid:34198937 DOI: https://doi.org/10.3390/molecules26113441

Taylor AW. Primary open-angle glaucoma: A transforming growth factor-β pathway-mediated disease. Am J Pathol. 2012;180(6):2201-4. http://doi.org/10.1016/j.ajpath.2012.03.011 PMid:22525463 DOI: https://doi.org/10.1016/j.ajpath.2012.03.011

Murphy-Ullrich JE, Downs JC. The Thrombospondin1- TGF-β _pathway and glaucoma. J Ocul Pharmacol Ther. 2015;31(7):371-5. http://doi.org/10.1089/jop.2015.0016 PMid:26352161 DOI: https://doi.org/10.1089/jop.2015.0016

Wang J, Harris A, Prendes MA, Alshawa L, Gross JC, Wentz SM, et al. Targeting transforming growth Factor-β _signaling in primary open-angle glaucoma. J Glaucoma. 2017;26(4):390-5. http://doi.org/10.1097/IJG.0000000000000627 PMid:28169917 DOI: https://doi.org/10.1097/IJG.0000000000000627

Inokuchi Y, Shimazawa M, Nakajima Y, Suemori S, Mishima S, Hara H. Brazilian Green propolis protects against retinal damage in vitro and in vivo. Evid Based Complement Altern Med. 2006;3(1):71-7. http://doi.org/10.1093/ecam/nek005 PMid:16550226 DOI: https://doi.org/10.1093/ecam/nek005

Jia Y, Jiang S, Chen C, Lu G, Xie Y, Sun X, et al. Caffeic acid phenethyl ester attenuates nuclear factor-κB-mediated inflammatory responses in Müller cells and protects against retinal ganglion cell death. Mol Med Rep. 2019;19(6):4863-71. http://doi.org/10.3892/mmr.2019.10151 PMid:31059064 DOI: https://doi.org/10.3892/mmr.2019.10151

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Published

2022-03-05

How to Cite

1.
Meida NS, Purwanto B, Wasita B, Indrakila S, Soetrisno S, Poncorini E, Cilmiaty R. Effects of Ethanol Extract of Propolis on Repair Optic Nerve Damage in a Rat Model for Diabetes Mellitus (Study of MDA, CRP, Caspase-3, and TGF-β Expression and Histopathological Changes on Optic Nerve Damage). Open Access Maced J Med Sci [Internet]. 2022 Mar. 5 [cited 2024 Feb. 23];10(A):444-9. Available from: https://oamjms.eu/index.php/mjms/article/view/8646

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