Sains Malaysiana 51(9)(2022): 2873-2883

http://doi.org/10.17576/jsm-2022-5109-11

Sweet Potato (Ipomoea batatas L.) Leaves Ethanol Extract Increases Endogenous Antioxidant Activities in Hyperlipidemic Rats

(Ekstrak Etanol Daun Ubi Keledek (Ipomoea batatas L.) Meningkatkan Aktiviti Antioksidan Endogen pada Tikus Hiperlipidemik)

NURKHASANAH MAHFUDH^1,*, NANIK SULISTYANI¹, ASIILAH FATIHATUL KHOIROT¹, TSANAWIYAH INDAH SAFIRA¹, FEZAH OTHMAN² & ZAINUL AMIRUDDIN ZAKARIA³

¹Faculty of Pharmacy, Universitas Ahmad Dahlan, Yogyakarta, Indonesia

²Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, 43400 Serdang, Selangor Darul Ehsan, Malaysia

³Department of Biomedical Science, Faculty of Medicine and Health Sciences, Universiti Malaysia Sabah, 88400 Kota Kinabalu, Sabah, Malaysia

Received: 26 November 2021/Accepted: 19 March 2022

Abstract

Consumption of high-fat foods can induce the formation of free radicals and trigger oxidative stress. The leave of sweet potato (Ipomoea batatas L.) has been reported to be a potent antioxidant in vitro. This study investigates the effect of ethanol extract of purple sweet potato leaves on the endogenous antioxidant activity in hyperlipidemic rats. The sweet potato leaves were oven-dried and extracted using 70% ethanol in a ratio of 1:7 w/v for 24 h, followed by vacuum evaporation. The five groups of test animals were created: normal control-which was given a standard diet, negative control (high-fat diet (HFD) for 14 days), and three treated groups which treated with HFD for 14 days and start for the same time treated with sweet potato leaves extract (SPLE) at the doses of 100, 200, and 400 mg/kg BW for 28 days. The antioxidant activity was measured from liver homogenate on the 29th day. Superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GSH-Px) activities, and malondialdehyde (MDA) levels were quantified using spectrophotometry. The high-performance liquid chromatography (HPLC) analysis found rutin as a major chemical content of the SPLE. HFD significantly (p<0.05) decreased the activity of endogenous antioxidants (SOD, CAT, and GSH-Px) and increased the MDA level significantly (p<0.05) compared with the normal group. On the contrary, the treatment with the SPLE significantly (p<0.05) increased the activity of SOD, CAT, and GSH-Px and lowered MDA levels significantly (p<0.05) in a dose-dependent manner compared to the negative control. SPLE increase the activities of endogenous enzymatic antioxidants in hyperlipidemic rats. 

Keywords: Catalase (CAT); glutathione peroxidase (GSH-Px); malondialdehyde (MDA); superoxide dismutase (SOD); sweet potato leaves

Abstrak

Pengambilan makanan yang tinggi lemak boleh mendorong kepada pembentukan radikal bebas dan mencetuskan tekanan oksidatif. Daun ubi keledek (Ipomoea batatas L.) telah dilaporkan sebagai antioksidan yang kuat secara in vitro. Penyelidikan ini mengkaji tentang kesan ekstrak etanol daun ubi keledek ke atas aktiviti antioksidan endogen dalam tikus hiperlipidemik. Daun ubi keledek telah dikeringkan dengan ketuhar gelombang dan diekstrak menggunakan etanol 70% dalam nisbah 1:7 w/v selama 24 jam, diikuti dengan penyejatan vakum. Lima kumpulan haiwan ujian telah disediakan: kawalan normal iaitu yang diberi diet piawai, kawalan negatif (diet tinggi lemak (HFD) selama 14 hari) dan tiga kumpulan terawat yang dirawat dengan HFD selama 14 hari dan dirawat dengan ekstrak daun ubi keledek (SPLE) pada dos 100, 200 dan 400 mg/kg BW selama 28 hari. Aktiviti antioksidan diukur daripada homogenat hati pada hari ke-29. Aktiviti superoksida dismutes (SOD), katales (CAT), glutation peroksides (GSH-Px), dan tahap malondialdehid (MDA) dihitung menggunakan spektrofotometri. Analisis kromatografi cecair (HPLC) berprestasi tinggi mendapati terdapat kandungan kimia utama iaitu SPLE. HFD secara signifikan (p<0.05) menurunkan aktiviti antioksidan endogen (SOD, CAT & GSH-Px) dan meningkatkan tahap MDA dengan ketara (p<0.05) berbanding kumpulan normal. Sebaliknya, rawatan dengan SPLE (p<0.05) meningkatkan aktiviti SOD, CAT dan GSH-Px serta menurunkan tahap MDA dengan ketara (p<0.05) bergantung kepada dos berbanding kawalan negatif. SPLE meningkatkan aktiviti antioksidan enzimatik endogen dalam tikus hiperlipidemik.

Kata kunci: Daun keladi; glutation peroksides (GSH-Px); katales (CAT); malondialdehid (MDA); superoksida dismutes (SOD)

References

Aguilar, T.A.F., Navarro, B.C.H.  & Pérez, J.A.M. 2016. Endogenous antioxidants: A review of their role in oxidative stress. doi: 10.5772/65715.

Al-rejaie, S.S., Aleisa, A.M., Sayed-Ahmed, M.M., Al-shabanah, O.A., Abuohashish, H.M., Ahmed, M.M., Al-hosaini, K.K. & Hafez, M.M. 2013. Protective effect of rutin on the antioxidant genes expression in hypercholestrolemic male westar rat. BMC Complementary & Alternative Medicine 13: 136.

Araujo, F.B., Barbosa, D.S., Hsin, C.Y., Maranhão, R.C. & Abdalla, D.S.P. 1995. Evaluation of oxidative stress in patients with hyperlipidemia. Atherosclerosis 117(1): 61-71.

Barkas, F., Nomikos, T., Liberopoulos, E. & Panagiotakos, D. 2020. Diet and cardiovascular disease risk among individuals with familial hypercholesterolemia: Systematic review and meta-analysis. Nutrients 12(8): 2436.

Birben, E., Sahiner, U.M., Sackesen, C., Erzurum, S. & Kalayci, O. 2012. Oxidative stress and antioxidant defense. WAO Journal 5: 9-19.

Canadian Council of Animal Care. 2010. Canadian Council on Animal Care in Science CCAC Guidelines on Euthanasia of Animals Used. Ottawa, Canada.

Chang, H.H., Lan, Y.C., Chung, S.D. & Chien, C.T. 2021. Sweet potato leaf feeding decreases cholesterol, oxidative stress and thrombosis formation in Syrian hamsters with a high-cholesterol diet. Life 11(8): 802.

Chao, P.Y., Huang, W.Y., Hu, S.P., Lo, H.F., Lin, K.H. & Huang, M.Y. 2013. Indigenous purple vegetable extracts protect against hydrogen peroxide-induced DNA damage in human lymphocytes. Food and Nutrition Sciences 4: 62-70.

Chen, W., Mao, T.-J. Fan, L., Zhou, Y., Yu, J., Jin, Y. & Hou, P.-C. 2011. Effect of purple sweet potato on lipid metabolism and oxidative stress in hyperlipidemic rats. Journal of Zhejiang University. Medical Sciences 40(4): 360-364.

Ebele, I.J., Jenniger, I.A., Nnabugo, E.C., Sidney, O.I., Chibuike, O.K., Chukwuma, O.O., Daniel, N. & Anayochukwu, E.A. 2016. Oxidative stress/lipid peroxidation and antioxidant enzymes in apparently healthy individuals involved in physical exercise. Asian Journal of Medical Sciences 7(6): 16-19.

Enogieru, A.B., Haylett, W., Hiss, D.C., Bardien, S. & Ekpo, O.E. 2018. Review article rutin as a potent antioxidant: Implications for neurodegenerative disorders. Oxidative Medicine and Cellular Longevity 2018(1): 1-17.

Girsang, E., Lister, I.N.E., Ginting, C.N., Sholihah, I.A., Raif, M.A. & Kunardi, S. 2020. Antioxidant and antiaging activity of rutin and caffeic acid. Pharmaciana 10(2): 147-156.

Gusti, A.M.T., Qusti, S.Y., Alshammari, E.M., Toraih, E.A. & Fawzy, M.S. 2021. Antioxidants-related superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPX), glutathione-s-transferase (GST), and nitric oxide synthase (NOS) gene variants analysis in an obese population: A preliminary case-control study. Antioxidants 10(4): 595.

Halder, S. & Bhattacharyya, M. 2014. Oxidative stress: Lipid peroxidation products as predictors in disease progression. Journal of Experimental and Integrative Medicine 4(3): 151.

Hariri, N. & Thibault, L. 2010. High-fat diet-induced obesity in animal models. Nutrition Research Reviews 23(2): 270-299.

Heriwijaya, I.P.P.D., Jawi, I.M. & Satriyasa, B.K. 2020. Uji efektivitas ekstrak air daun ubi jalar ungu (Ipomoea batatas) terhadap profil lipid tikus putih jantan galur wistar yang diinduksi pakan dislipidemia. Intisari Sains Medis 11(2): 452-456.

Hue, S-M., Boyce, A.N. & Somasundram, C. 2011. Comparative study on the antioxidant activity of leaf extract and carotenoids extract from Ipomoea batatas var. oren (sweet potato) leaves. International Journal of Nutrition and Food Engineering 5(10): 604-607.

Ihwah, A., Deoranto, P., Wijana, S. & Dewi, I.A. 2018. Comparative study between federer and gomez method for number of replication in complete randomized design using simulation: Study of areca palm (Areca catechu) as organic waste for producing handicraft paper comparative study between federer and gomez. IOP Conf. Series: Earth and Environmental Science 13(1): 012049.

Isken, F., Klaus, S., Osterhoff, M., Pfeiffer, A.F.H. & Weickert, M.O. 2010. Effects of long-termsoluble vs. insoluble dietary fiber intake on high-fat diet-induced obesity in C57BL/6J mice. The Journal of Nutritional Biochemistry 21(4): 278-284.

Islam, S. 2006. Sweetpotato (Ipomoea batatas L.) leaf: Its potential effect on human health and nutrition. Journal of Food Science 71(2): R13-121.

Islam, S., Yoshimoto, M., Ishiguro, K. & Yamakawa, O. 2016. Bioactive compounds in Ipomoea batatas leaves. In Proc XXVI IHC - Issues and Advances in Postharvest Hort. pp. 693-699.

Jang, I-S. & Choi, M-J. 2019. Effects of isoflavone supplementation on lipid profiles and antioxidant enzyme activities in growing rats fed high fat diet. Clinical Nutrition Research 8(4): 296-306.

Jawi, I.M. & Indrayani, A.W. 2015. Aqueous extract of Balinese purple sweet potato (Ipomoea batatas L.) prevents oxidative stress and decreases blood interleukin-1 in hypercholesterolemic rabbits. Bali Medical Journal 4(1): 37-40.

Kamalakkannan, N., Stanely, P. & Prince, M. 2006. Antihyperglycaemic and antioxidant effect of rutin, a polyphenolic flavonoid in streptozotocin-induced diabetic wistar rats. Pharmacology & Toxicology 98(1): 97-103.

Khoubnasab Jafari, M., Ansarin, K. & Jouyban, A. 2015. Comments on ‘use of malondialdehyde as a biomarker for assesing oxidative stress in different disease pathologies: A review. Iranian Journal of Public Health 44(5): 714-715.

Kodydková, J., Vávrová, L., Kocík, M. & A Žák, A. 2014. Review article human catalase, its polymorphisms, regulation and changes of its activity in different diseases. Folia Biologica (Praha) 60: 153-167.

Koncic, M.Z., Petlevski, R. & Kalodera, Z. 2013. Antioxidant activity of Ipomoea batatas L. Lam. leaf grown in continental Croatia and its effect on glutathione level in glucose-induced oxidative stress. International Journal of Food Properties 16(5): 964-973.

Krochmal-marczak, B., Cebulak, T., Kapusta, I., Kaszuba, J. & Zurek, N. 2020. The content of phenolic acids and flavonols in the leaves of nine varieties of sweet potatoes (Ipomoea batatas L.) depending on their development, grown in central Europe. Molecules 25: 3473.

Kumar, V., Khan, A.A., Tripathi, A., Dixit, P.K. & Bajaj, U.K. 2015. Role of oxidative stress in various diseases: Relevance of dietary antioxidants. The Journal of Phytopharmacology 4(2): 126-132.

Kurata, R., Kobayashi, T., Ishii, T., Niimi, H., Nisaka, S., Kubo, M. & Kishimoto, M. 2017. Influence of sweet potato (Ipomoea batatas L.) leaf consumption on rat lipid metabolism. Food Science and Technology Research 23(1): 57-62.

Lattimer, J.M. & Haub, M.D. 2010. Effects of dietary fiber and its components on metabolic health. Nutrients 2(12): 1266-1289.

Lee, C.L., Lee, S.L., Chen, C.J., Chen, H.C., Kao, M.C., Liu, C.H., Chen, J.Y., Lai, Y.T. & Wu, Y.C. 2016. Characterization of secondary metabolites from purple Ipomoea batatas leaves and their effects on glucose uptake. Molecules 21(6): 745.

Mahfudh, N., Sulistyani, N., Syakbani, M. & Dewi, A.C. 2021. The antihyperlipidaemic and hepatoprotective effect of Ipomoea batatas L. leaves extract in high-fat diet rats. International Journal of Public Health Science 10(3): 558-564.

Meira, M., da Silva, E.P., David, J.M. & David J.P. 2012. Review of the genus Ipomoea: Traditional uses, chemistry and biological activities. Brazilian Journal of Pharmacognosy 22(3): 682-713.

Nagai, M., Tani, M., Kishimoto, Y., Iizuka, M., Saita, E., Toyozaki, M., Kamiya, T., Ikeguchi, M. & Kazuo, K. 2011. Sweet potato (Ipomoea Batatas L.) leaves suppressed oxidation of low density lipoprotein (LDL) in vitro and in human subjects. J. Clin. Biochem. Nutr. 48(3): 203-208.

Noori, S. 2012. An overview of oxidative stress and antioxidant defensive system. Open Access Sci. Reports 1(8): 1-9.

Phahlane, C.J., Laurie, S.M., Shoko, T., Manhivi, V.E. & Sivakumar, D. 2021. An evaluation of phenolic compounds, carotenoids and antioxidant properties in leaves of South African cultivars, Peruvian 199062.1 and USA's Beauregard. Frontiers in Nutrition 8: 773550.

Poli, A., Barbagallo, C.M., Cicero, A.F.G., Corsini, A., Manzato, E., Trimarco, B., Bernini, F., Visisoli, F., Bianchi, A., Canzone, G., Crescini, C., de Kreutzenberg, S., Ferrara, N., Gambacciani, M., Ghiselli, A., Lubrano, C., Marelli, G., Marrocco, W., Montemurro, V., Parretti, D., Pedretti, R., Perticone, F., Stella, R. & Marangoni, F. 2018. Nutraceuticals and functional foods for the control of plasma cholesterol levels. An intersociety position paper. Pharmacological Research 134(May): 51-60.

Rodríguez, E., Arqués, J.L., Rodríguez, R., Nuñez, M., Medina, M., Talarico, T.L. & Casas, I.A. 1989. Antioxidant compounds and their antioxidant mechanism. Intech Open 32: 137-144.

Rumbaoa, R.G.O., Cornago, D.F. & Geronimo, I.M. 2009. Phenolic content and antioxidant capacity of Philippine sweet potato (Ipomoea batatas) varieties. Food Chemistry 113(4): 1133-1138.

Sari, N., Nurkhasanah & Sulistyani, N. 2020. The antioxidant effect of bangle (Zingiber cassumunar) rhizome extract on superoxide dismutase (SOD) activity in hyperlipidemic rats. Research Journal of Chemistry and Environment 24(1): 78-81.

Singh, S., Panda, V., Sudhamani, S. & Dande, P. 2020. Protective effect of a polyherbal bioactive fraction in propylthiouracil-induced thyroid toxicity in ratsby modulation of the hypothalamic–pituitary–thyroid and hypothalamic–pituitary–adrenal axes. Toxicology Reports 7(2020): 730-742.

Sumardika, I.W. & Jawi, I.M. 2012. Water extract of sweet potato leaf imrpoved lipid profile and blood SOD content of rats with high cholesterol diet. Medicina 43(2): 67-70.

Switala, J. & Loewen, P.C. 2002. Diversity of properties among catalases. Archives of Biochemistry and Biophysics 401: 145-154.

Valko, M., Leibfritz, D., Moncol, J., Cronin, M.T.D., Mazur, M. & Telser, J. 2007. Free radicals and antioxidants in normal physiological functions and human disease. International Journal of Biochemistry and Cell Biology 39(1): 44-84.

Walker, J.M. 1996. The Protein Protocols Handbook. Hatfield, University of Hertfordshire: Humana Totowa.

Wang, S., Nie, S. & Zhu, F. 2016. Chemical constituents and health effects of sweet potato. Food Research International 89: 90-116.

Yang, J.X., Guo, J. & Yuan, J. 2008. In vitro antioxidant properties of rutin. LWT - Food Science and Technology 41(6): 1060-1066.

Zhang, C., Liu, D., Wu, L., Jianming, Z., Li, X. & Wu, W. 2019. Chemical characterization and antioxidant properties of ethanolic extract and its fractions from sweet potato (Ipomoea Batatas L.) leaves. Foods 9(1): 15.

^*Corresponding author; email: nurkhasanah@pharm.uad.ac.id