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Effects of Propolis Extract Supplementation during Pregnancy on Stress Oxidative and Pregnancy Outcome: Levels of Malondialdehyde, 8-Oxo-2′-Deoxogunosine, Maternal Body Weight, and Number of Fetuses

Joko Wahyu Wibowo, Minidian Fasitasari, Siti Thomas Zulaikhah
  Jurnal Kedokteran Brawijaya, Vol 31, No 3 (2021),  pp.156-161  

Abstract


Oxidative stress is related to pregnancy complications that could increase maternal and infant mortality. This study aimed to determine the effect of propolis extract supplementation during pregnancy on oxidative stress level and pregnancy outcomes utilizing Malonedealdehyde (MDA) and 8-Oxo-2′-Deoxogunosine (8-OHdG) levels, maternal body weight, and the average number of fetuses as the parameters. The study was conducted by using a posttest only control group design on 24 pregnant Wistar rats, which were divided into four groups. Group I was control, Group II-IV were the treatment groups given propolis extract of 1.8mg, 3.6mg, and 7.2mg/200gBW/day, respectively. The standard feed given was AIN93G dose of 20g/day and distilled water ad libitum. Propolis extract was given using a gastric feeding tube every morning for 20 days. At the end of the treatment, body weight was meisured and blood collected for assessed MDA and 8-OHdG levels  by ELISA method  and then we performed abdominal surgery to count number of fetuses. The result are there were decreasing level of MDA and 8-OHDG by administration of propolis significantly (p<0.05) group: I: 2,04±0,091, II: 1,55±0,067, III: 1,05±0,176, IV: 0,73±0,075 (mmol/mL) (p=0.001); 8 OHdG level (ng/mL) group I: 10,02±0,403, II: 8,60±0,078, III: 7,89±0,051, IV: 7,53±0,063 (p=0,001). Average of maternal body weight (g) were increased: group I: 228,33±3,93, II: 237,17±4,36, III: 244,83±4,02, IV: 248,00±5,76 (p=0,001) and Average number of fetuses tend to increased as well, group I : 8,5±0,05, II: 7,8±0,41, III: 9,5±1,05, IV: 9,6±0,52 (p=0,02). The conclusion of this research are supplementation of propolis extract in pregnant rats can reduce oxidative stress and improve pregnancy outcomes.


Keywords


8-OHdG; maternal body weight; MDA; number of fetuses; oxidative stress

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References


REFERENCES

Samir D, Dalal D, and Noura A. Study of Oxidative Stress during Pregnancy. Global Journal of Pharmacy and Pharmaceutical Sciences. 2018; 4(5): 1-4.

Sen S, Iyer C, and Meydani SN. Obesity During Pregnancy Alters Maternal Oxidant Balance and Micronutrient Status. Journal of Perinatology Nature Publishing Group; 2014; 34(2): 105–111.

van de Lagemaat EE, de Groot LCPGM, and van den Hauvel EGHM. Vitamin B 12 in Relation to Oxidative Stress: A Systemtic Review. Nutrients. 2019; 11(2): 1–16.

Duhig K, Chappell LC, Shennan AH. Oxidative Stress in Pregnancy and Reproduction. Obstetric Medicine. 2016; 9(3): 113–116.

Dani IC and Budiawan. Pembentukan 8-OHdG dari Zat Toksik Pemicu Radikal Bebas Abstrak. Pharmaceutical Science & Research. 2015; 2(1): 32–46.

Jin L, Yang H, Fu J, Xue X, Yao L, and Qiao L. Association between Oxidative DNA Damage and the Expression of 8-Oxoguanine DNA Glycosylase 1 in Lung Epithelial Cells of Neonatal Rats Exposed to Hyperoxia. Molecular Medicine Reports. 2015; 11(6): 4079–4086.

Roszkowski K. Oxidative Stress In Pregnant Women. Archives of Perinatal Medicine. 2013; 19(3): 150–155.

Halim E, Hardinsyah, Sutandyo N, Sulaeman A, Artika M, Agung AD, and Harahap Y. Kajian Bioaktif dan Zat Gizi Propolis Indonesia dan Brasil. Jurnal Gizi dan Pangan. 2012; 7(1): 1–7.

Mujica V, Orrego R, Pérez J, et al. The Role of Propolis in Oxidative Stress and Lipid Metabolism: A Randomized Controlled Trial. Evidence-based Complementary and Alternative Medicine. 2017; 2017: 1-11.

Fikri AM, Sulaeman A, Handharyani E, Marliyati SA, and Fahrudin FE. The Effect of Propolis Administration on Fetal Development. Heliyon. 2019; 5(10): 1-7.

Kabbash A, El-aasr M, Mansour FR, Hasegawa M, Ataka S, and Yagi A. Nature Treasure: Aloe Vera and Bee-Products. Journal of Gastroenterology and Hepatology Research. 2018; 7(4): 2612–2631.

Usman UZ, Bakar ABA, and Mohamed M. Propolis Improves Pregnancy Outcomes and Placental Oxidative Stress Status in Streptozotocin-Induced Diabetic Rats. BMC Complementary and Alternative Medicine. 2018; 18(1): 1–7.

Hamid HY and Zakaria ZAB. Reproductive Characteristics of the Female Laboratory Rat. African Journal of Biotechnology. 2013; 12(19): 2510–4251.

Badehnoosh B, Karamali K, Zarati M, et al. The Effects of Probiotic Supplementation on Biomarkers of Inflammation, Oxidative Stress and Pregnancy Outcomes in Gestational Diabetes. The Journal of Maternal-fetal & Neonatal Medicine. 2018; 31(9): 1128-1136.

Kaya E, Yılmaz S, and Ceribasi S. Protective Role of Propolis on Low and High Dose Furan-Induced Hepatotoxicity and Oxidative Stress in Rats. Journal of Veterinary Research. 2019; 63(3): 423–431.

Nna VU, Bakar ABA, Ahmad A, Eleazu CO, and Mohamed M. Oxidative Stress , NF- κ B-Mediated Inflammation and Apoptosis in the Testes of Streptozotocin-Induced Diabetic Rats: Combined Protective Effects of Malaysian Propolis and Metformin. Antioxidants. 2019; 8(10): 1–23.

Wahyuwibowo J, Aziz A, Safitri E, Fasitasari M, and Zulaikhah ST. Iron-Folate Supplementation during Pregnancy for Prevent Oxidative Stress in Pregnant Rats: Level of MDA, Creatinine, Glucose, Erythrocite, Blood Pressure, Body Weight and Num. Pharmacognosy Journal. 2020; 12: 186-191.

Seven PT, Yilmaz S, Seven I, et al. The Effects of Propolis in Animals Exposed Oxidative Stress. In: Lushchak V (Ed). Oxydative Stress-Environmental Induction and Dietary Antioxidants. Rijeka, Croatia: InTech Europe; 2012; pp.267-88.

Arabameri A, Sameni H, and Bandegi A. The Effects of Propolis Extract on Ovarian Tissue and Oxidative Stress in Rats with Maternal Separation Stress. International Journal of Reproductive Biomedicine. 2017; 15(8): 509–520.

Hemieda FAE, El-Kholy WM, El-Habibi, and El-Sawah SG. Influence of Propolis on Oxidative Stress, Inflammation and Apoptosis in Streptozotocin-Induced Diabetic Rats. International Journal of Advanced Research. 2015; 3(7): 831–845.

Hesami S, Hashemipour S, Shiri-Shahsavar MR, Koushan Y, and Haghighian HK. Administration of Iranian Propolis Attenuates Oxidative Stress and Blood Glucose in Type II Diabetic Patients: A Randomized, Double-Blind, Placebo-Controlled, Clinical Trial. Caspian Jurnal of Internal Medicine. 2019; 10(1): 48–54.

Carter RJ and Parsons JL. Base Excision Repair, a Pathway Regulated by Posttranslational Modifications. Molecular and Cellular Biology. 2016; 36(10): 1426–37.

Wehinger S. Propolis Extracts Protects Pancreatic Beta Cells from Oxidative Stress in Vitro. Proceeding Scientific Program 15th International Congress on Advances in Natural Medicines Nutraceuticals & Neurocognition. Berlin, Germany, July 8-9, 2019.

Khalaf DA and Thanoon IAJ. Effects of Bee Propolis on Blood Pressure Record and Certain Biochemical Parameter in Healthy Volunteers. Annals of the College of Medicine Mosul. 2018; 40(1): 20–26.

Choobkar N, Kakoolaki S, Mohammadi F, and Rezaeimanesh M. The Effect of Dietary Propolis and Pollen Extracts on Growth Performance and Haematological Responses of Rainbow Trout (Onchorhynchus Mykiss). Iranian Journal of Aquatic Animal Health. 2017; 3(1): 16–25.

Schütz LF, Bernardo J, Le M, et al. Application of Nutraceuticals in Pregnancy Complications: Does Epigenetics Play a Role? In: Patel V and Preedy V (Eds). Handbook of Nutrition, Diet, and Epigenetics. Berlin, Jerman: Springer; 2019; p. 1959.

Zeng Z, Liu F, and Li S. Metabolic Adaptations in Pregnancy: A Review. Annals of Nutrition & Metabolism. 2017; 7(1): 59–65.

Kiss AK. Polyphenols and Histone Acetylation. In: Patel V and Preedy V (Eds). Handbook of Nutrition, Diet, and Epigenetics. Berlin, Jerman: Springer; 2019; p. 1977.

Carter LG, Qi NR, de Cabo R, and Pearson KJ. Maternal Exercise Improves Insulin Sensitivity in Mature Rat Offspring. Medicine and Science in Sports and Exercise. 2013; 45(5): 832-840.

Thakur VS and Gupta S. Plant Polyphenols as Epigenetic Modulators of Glutathione S-Transferase P1 Activity. In: Sarkar FH (Ed). Epigenetics and Cancer. Cleveland: Springer; 2013; p. 231–244.

Akbari A, Jelodar G, Nazifi S, and Sajedianfard J. An Overview of the Characteristics and Function of Vitamin C in Various Tissues: Relying on its Antioxidant Function. Zahedan Journal of Research in Medical Sciences. 2016; 18(11): 1-9.

Sisein EA. Biochemistry of Free Radicals and Antioxidants. Scholar Academic Journal of Biosciences (SAJB). 2014; 2(2): 110-118.

Carr AC and Maggini S. Vitamin C and Immune Function. Nutrients. 2017; 9(11): 1–25.

Pehlivan FE. Vitamin C: An Epigenetic Regulator. London: Intechopen; 2018; p.1-12.

Hore TA, von Meyenn F, Ravichandran M, et al. Retinol and Ascorbate Drive Erasure of Epigenetic Memory and Enhance Reprogramming to Naïve Pluripotency by Complementary Mechanisms. Proceedings of the National Academy of Sciences of the United States of America. 2016; 113(43): 12202-12207.

Chen Z, Gong L, Zhang P, et al. Epigenetic Down-Regulation of Sirt 1 Via DNA Methylation and Oxidative Stress Signaling Contributes to the Gestational DiabeREFERENCES

Samir D, Dalal D, and Noura A. Study of Oxidative Stress during Pregnancy. Global Journal of Pharmacy and Pharmaceutical Sciences. 2018; 4(5): 1-4.

Sen S, Iyer C, and Meydani SN. Obesity During Pregnancy Alters Maternal Oxidant Balance and Micronutrient Status. Journal of Perinatology Nature Publishing Group; 2014; 34(2): 105–111.

van de Lagemaat EE, de Groot LCPGM, and van den Hauvel EGHM. Vitamin B 12 in Relation to Oxidative Stress: A Systemtic Review. Nutrients. 2019; 11(2): 1–16.

Duhig K, Chappell LC, Shennan AH. Oxidative Stress in Pregnancy and Reproduction. Obstetric Medicine. 2016; 9(3): 113–116.

Dani IC and Budiawan. Pembentukan 8-OHdG dari Zat Toksik Pemicu Radikal Bebas Abstrak. Pharmaceutical Science & Research. 2015; 2(1): 32–46.

Jin L, Yang H, Fu J, Xue X, Yao L, and Qiao L. Association between Oxidative DNA Damage and the Expression of 8-Oxoguanine DNA Glycosylase 1 in Lung Epithelial Cells of Neonatal Rats Exposed to Hyperoxia. Molecular Medicine Reports. 2015; 11(6): 4079–4086.

Roszkowski K. Oxidative Stress In Pregnant Women. Archives of Perinatal Medicine. 2013; 19(3): 150–155.

Halim E, Hardinsyah, Sutandyo N, Sulaeman A, Artika M, Agung AD, and Harahap Y. Kajian Bioaktif dan Zat Gizi Propolis Indonesia dan Brasil. Jurnal Gizi dan Pangan. 2012; 7(1): 1–7.

Mujica V, Orrego R, Pérez J, et al. The Role of Propolis in Oxidative Stress and Lipid Metabolism: A Randomized Controlled Trial. Evidence-based Complementary and Alternative Medicine. 2017; 2017: 1-11.

Fikri AM, Sulaeman A, Handharyani E, Marliyati SA, and Fahrudin FE. The Effect of Propolis Administration on Fetal Development. Heliyon. 2019; 5(10): 1-7.

Kabbash A, El-aasr M, Mansour FR, Hasegawa M, Ataka S, and Yagi A. Nature Treasure: Aloe Vera and Bee-Products. Journal of Gastroenterology and Hepatology Research. 2018; 7(4): 2612–2631.

Usman UZ, Bakar ABA, and Mohamed M. Propolis Improves Pregnancy Outcomes and Placental Oxidative Stress Status in Streptozotocin-Induced Diabetic Rats. BMC Complementary and Alternative Medicine. 2018; 18(1): 1–7.

Hamid HY and Zakaria ZAB. Reproductive Characteristics of the Female Laboratory Rat. African Journal of Biotechnology. 2013; 12(19): 2510–4251.

Badehnoosh B, Karamali K, Zarati M, et al. The Effects of Probiotic Supplementation on Biomarkers of Inflammation, Oxidative Stress and Pregnancy Outcomes in Gestational Diabetes. The Journal of Maternal-fetal & Neonatal Medicine. 2018; 31(9): 1128-1136.

Kaya E, Yılmaz S, and Ceribasi S. Protective Role of Propolis on Low and High Dose Furan-Induced Hepatotoxicity and Oxidative Stress in Rats. Journal of Veterinary Research. 2019; 63(3): 423–431.

Nna VU, Bakar ABA, Ahmad A, Eleazu CO, and Mohamed M. Oxidative Stress , NF- κ B-Mediated Inflammation and Apoptosis in the Testes of Streptozotocin-Induced Diabetic Rats: Combined Protective Effects of Malaysian Propolis and Metformin. Antioxidants. 2019; 8(10): 1–23.

Wahyuwibowo J, Aziz A, Safitri E, Fasitasari M, and Zulaikhah ST. Iron-Folate Supplementation during Pregnancy for Prevent Oxidative Stress in Pregnant Rats: Level of MDA, Creatinine, Glucose, Erythrocite, Blood Pressure, Body Weight and Num. Pharmacognosy Journal. 2020; 12: 186-191.

Seven PT, Yilmaz S, Seven I, et al. The Effects of Propolis in Animals Exposed Oxidative Stress. In: Lushchak V (Ed). Oxydative Stress-Environmental Induction and Dietary Antioxidants. Rijeka, Croatia: InTech Europe; 2012; pp.267-88.

Arabameri A, Sameni H, and Bandegi A. The Effects of Propolis Extract on Ovarian Tissue and Oxidative Stress in Rats with Maternal Separation Stress. International Journal of Reproductive Biomedicine. 2017; 15(8): 509–520.

Hemieda FAE, El-Kholy WM, El-Habibi, and El-Sawah SG. Influence of Propolis on Oxidative Stress, Inflammation and Apoptosis in Streptozotocin-Induced Diabetic Rats. International Journal of Advanced Research. 2015; 3(7): 831–845.

Hesami S, Hashemipour S, Shiri-Shahsavar MR, Koushan Y, and Haghighian HK. Administration of Iranian Propolis Attenuates Oxidative Stress and Blood Glucose in Type II Diabetic Patients: A Randomized, Double-Blind, Placebo-Controlled, Clinical Trial. Caspian Jurnal of Internal Medicine. 2019; 10(1): 48–54.

Carter RJ and Parsons JL. Base Excision Repair, a Pathway Regulated by Posttranslational Modifications. Molecular and Cellular Biology. 2016; 36(10): 1426–37.

Wehinger S. Propolis Extracts Protects Pancreatic Beta Cells from Oxidative Stress in Vitro. Proceeding Scientific Program 15th International Congress on Advances in Natural Medicines Nutraceuticals & Neurocognition. Berlin, Germany, July 8-9, 2019.

Khalaf DA and Thanoon IAJ. Effects of Bee Propolis on Blood Pressure Record and Certain Biochemical Parameter in Healthy Volunteers. Annals of the College of Medicine Mosul. 2018; 40(1): 20–26.

Choobkar N, Kakoolaki S, Mohammadi F, and Rezaeimanesh M. The Effect of Dietary Propolis and Pollen Extracts on Growth Performance and Haematological Responses of Rainbow Trout (Onchorhynchus Mykiss). Iranian Journal of Aquatic Animal Health. 2017; 3(1): 16–25.

Schütz LF, Bernardo J, Le M, et al. Application of Nutraceuticals in Pregnancy Complications: Does Epigenetics Play a Role? In: Patel V and Preedy V (Eds). Handbook of Nutrition, Diet, and Epigenetics. Berlin, Jerman: Springer; 2019; p. 1959.

Zeng Z, Liu F, and Li S. Metabolic Adaptations in Pregnancy: A Review. Annals of Nutrition & Metabolism. 2017; 7(1): 59–65.

Kiss AK. Polyphenols and Histone Acetylation. In: Patel V and Preedy V (Eds). Handbook of Nutrition, Diet, and Epigenetics. Berlin, Jerman: Springer; 2019; p. 1977.

Carter LG, Qi NR, de Cabo R, and Pearson KJ. Maternal Exercise Improves Insulin Sensitivity in Mature Rat Offspring. Medicine and Science in Sports and Exercise. 2013; 45(5): 832-840.

Thakur VS and Gupta S. Plant Polyphenols as Epigenetic Modulators of Glutathione S-Transferase P1 Activity. In: Sarkar FH (Ed). Epigenetics and Cancer. Cleveland: Springer; 2013; p. 231–244.

Akbari A, Jelodar G, Nazifi S, and Sajedianfard J. An Overview of the Characteristics and Function of Vitamin C in Various Tissues: Relying on its Antioxidant Function. Zahedan Journal of Research in Medical Sciences. 2016; 18(11): 1-9.

Sisein EA. Biochemistry of Free Radicals and Antioxidants. Scholar Academic Journal of Biosciences (SAJB). 2014; 2(2): 110-118.

Carr AC and Maggini S. Vitamin C and Immune Function. Nutrients. 2017; 9(11): 1–25.

Pehlivan FE. Vitamin C: An Epigenetic Regulator. London: Intechopen; 2018; p.1-12.

Hore TA, von Meyenn F, Ravichandran M, et al. Retinol and Ascorbate Drive Erasure of Epigenetic Memory and Enhance Reprogramming to Naïve Pluripotency by Complementary Mechanisms. Proceedings of the National Academy of Sciences of the United States of America. 2016; 113(43): 12202-12207.

Chen Z, Gong L, Zhang P, et al. Epigenetic Down-Regulation of Sirt 1 Via DNA Methylation and Oxidative Stress Signaling Contributes to the Gestational Diabetes Mellitus-Induced Fetal Programming of Heart Ischemia-Sensitive Phenotype in Late Life. International Journal of Biological Sciences. 2019; 15(6): 1240-1251.

Gerhauser C. Impact Of Dietary Gut Microbial Metabolites On The Epigenome. Philosophical Transactions of the Royal Society of London. 2018; 373(1748): 1-13tes Mellitus-Induced Fetal Programming of Heart Ischemia-Sensitive Phenotype in Late Life. International Journal of Biological Sciences. 2019; 15(6): 1240-1251.

Gerhauser C. Impact Of Dietary Gut Microbial Metabolites On The Epigenome. Philosophical Transactions of the Royal Society of London. 2018; 373(1748): 1-13




DOI: http://dx.doi.org/10.21776/ub.jkb.2021.031.03.5

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