The effect of purple passion fruit juice on superoxide dismutase and malondialdehyde levels in hypercholesterolemic rats

Main Article Content

Alfi Muntafiah
Johanes Hasian Siahaan
Sofyan Hardi
Dody Novrial
Hernayanti Hernayanti

Abstract

Background
Hypercholesterolemia due to a high cholesterol diet can increase free radicals resulting in oxidative stress. Superoxide dismutase (SOD) and malondialdehyde (MDA) have been used as the study markers of oxidative stress in cases of hypercholesterolemia. Purple passion fruit contains various compounds that may reduce free radicals. This study aimed to determine the effect of purple passion fruit juice on SOD and MDA levels in hypercholesterolemic rats.


Methods
An experimental analysis with post-test only control group design involving 28 male Wistar rats. They were divided into 4 groups: normal control (K1), hypercholesterolemic control (K2), purple passion fruit juice treatment at 4.2 mL/200 gBW/day (K3), and simvastatin treatment at 0.018 mg/200 gBW/day (K4). The purple passion fruit juice at 4.2 mL/200 gBW/day was administered for 14 days. SOD levels were examined by enzymatic colorimetric methods using the Ransod kit and MDA levels by the TBARS method.


Results
The Kruskal-Wallis test showed a significant difference in SOD levels between the tested groups (p<0.05). One-way ANOVA test for MDA levels showed a significant difference (p<0.05). Post Hoc test (Mann-Whitney for SOD and LSD for MDA levels) also showed significant differences: K1 vs. K2, K2 vs. K3, K2 vs. K4, and K3 vs. K4 (p<0.05).


Conclusion
This study demonstrated that purple passion fruit juice significantly increases the SOD and lowers the MDA level in hypercholesterolemic male Wistar rats. Consumption of purple passion fruit juice may help to modulate oxidative stress caused by hypercholesterolemia in rats.

Article Details

How to Cite
Muntafiah, A., Siahaan, J. H. ., Hardi, S. ., Novrial, D. ., & Hernayanti, H. . (2022). The effect of purple passion fruit juice on superoxide dismutase and malondialdehyde levels in hypercholesterolemic rats. Universa Medicina, 41(2), 139–148. https://doi.org/10.18051/UnivMed.2022.v41.139-148
Section
Original Articles

References

Huhtaniemi I, Martini L, editors. Encyclopedia of endocrine diseases. 2nd ed. Oxford: Academic Press; 2019.

Setiawan DI, Tjahyono K, Afifah DN. Pemberian kecambah kacang kedelai terhadap kadar malondialdehid (MDA) dan superoxide dismutase (SOD) tikus Sprague Dawley hiperkolesterolemia. Jurnal Gizi Klinik Indonesia 2016;13:20–6.

Nelson RH. Hyperlipidemia as a risk factor for cardiovascular disease. Prim Care 2013;40:195-211. DOI: 10.1016/j.pop.2012.11.003.

World Health Organization. Noncommunicable diseases country profiles 2018. Geneva, Switzerland: World Health Organization; 2018.

Kementerian Kesehatan RI. Laporan Nasional Riskesdas 2018. Jakarta: Lembaga Penerbit Badan Penelitian dan Pengembangan Kesehatan (LPB); 2018.

Singh UN, Kumar S, Dhakal S. Study of oxidative stress in hypercholesterolemia. Int J Contemp Med Res 2017; 4:1204-7.

Rodwell VW, Bender DA, Botham KM, Kennelly PJ, Weil PA, editors. Harper’s illustrated biochemistry. 31st ed. New York: McGraw-Hill Education; 2018.

Berawi KN, Agverianti T. Efek aktivitas fisik pada proses pembentukan radikal bebas sebagai faktor risiko aterosklerosis. Majority 2017;6:85–90.

Ighodaro OM, Akinloye OA. First-line defense antioxidants - superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria J Med 2018; 54:287-93. https://doi.org/10.1016/j.ajme. 2017.09.001.

Simanjuntak E, Zulham. Superoksida dismutase (SOD) dan radikal bebas. J Keperawatan Fisioterapi 2020;2:124–9.

Younus H. Therapeutic potentials of superoxide dismutase. Int J Health Sci 2018;12:88-93.

Grundy SM, Stone NJ, Bailey AL, et al. 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA Guideline on the Management of Blood Cholesterol: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice GuidelinesGuideline on the management of blood cholesterol. J Am Coll Cardiol 2019;73: e285–350. Doi: 10.1161/cir.0000000000000625.

Ramkumar S, Raghunath A, Raghunath S. Statin therapy: review of safety and potential side effects. Acta Cardiol Sin 2016;32:631–9. DOI: 10.6515/acs20160611a.

Pengurus Besar Perkumpulan Endokrinologi Indonesia (PERKENI). Pedoman Pengelolaan Dislipidemia di Indonesia 2019. Jakarta: PB PERKENI; 2019.

Kim K, Vance TM, Chun OK. Greater total antioxidant capacity from diet and supplements is associated with a less atherogenic blood profile in U.S. adults. Nutrients 2016;8:15. DOI: 10.3390/nu8010015.

Hani RC, Milanda T. Manfaat antioksidan pada tanaman buah di Indonesia. Farmaka 2016;14:184–90.

Rahmi H. Aktivitas antioksidan dari berbagai sumber buah-buahan di Indonesia. JAI 2017;2: 34–8.

Medeiros NS, Almeida DC, Lima JD, et al. In vitro antioxidant activity of passion fruit (Passiflora alata) extract by different kinds of treatment on rat liver. Curr Bioact Compd 2018;14:21–5. DOI: 10.2174/1573407213666161118120014.

Zas P, John S. Diabetes and medicinal benefits of Passiflora edulis. World J Pharm Res 2016;5:453–65.

Marpaung AE, Karsinah, Karo BB. Karakterisasi dan evaluasi markisa asam hibrid hasil persilangan markisa asam ungu dan merah (Passiflora sp.). J Hortikultura 2016;26:163–70.

Kuete V. Medicinal spices and vegetables from Africa: therapeutic potential against metabolic, inflammatory, infectious and systemic diseases. Amsterdam: Academic Press 2017.

Hasanah N. Aktivitas antioksidan ekstrak etanol daun salam. J Pena Medika 2015;5:55–9.

He X, Luan F, Yang Y, et al. Passiflora edulis: an insight into current researches on phytochemistry and pharmacology. Front Pharmacol 2020; 11:617. DOI: 10.3389/fphar.2020.00617.

Muntafiah A, Ernawati DA, Suryandhana L, Pratiwi RD, Marie IA. Pengaruh sari markisa ungu (Passiflora edulis var edulis) berbagai dosis terhadap profil lipid tikus Wistar model hiperkolesterolemia. Penelitian Gizi Makanan 2017;40:1–8.

Muntafiah A, Pratama TS, Rachmawati A, Wulandari DW, Santosa Q. Comparison of purple passion juice (Passiflora edulis var. edulis) and simvastatin on lipid-lowering effect of hyperlipidemic rats model. In: Proceedings of the 1st Jenderal Soedirman International Conference in Conjunction with the 5th Annual Scientific Meeting (Temilnas) Consortium of Biomedical Sciences Indonesia 2020; pages 148-54. DOI: 10-5220/0010489301480154.

Silva RO, Damasceno SRB, Brito TV, et al. Polysaccharide fraction isolated from Passiflora edulis inhibits the inflammatory response and the oxidative stress in mice. J Pharm Pharmacol 2015; 67:1017–27. DOI: 10.1111/jphp.12399.

De Souza MDSS, Barbalho SM, Damasceno DC, et al. Effects of Passiflora edulis (yellow passion) on serum lipids and oxidative stress status of Wistar rats. J Med Food 2012;15:78–82. https://doi.org/10.1089/jmf.2011.0056.

Arifin WN, Zahiruddin WM. Sample size calculation in animal studies using resource equation approach. Malays J Med Sci 2017; 24: 101–5. https://doi.org/10.21315/mjms2017.24.5.11.

Willems RA. Regulatory issues regarding the use of food and water restriction in laboratory animals. Lab Anim 2009;38:325–8. DOI: 10.1038/laban1009-325.

Muntafiah A, Pratama TS, Ati VRB. Evaluasi potensi antidiabetes sari buah markisa ungu (Passiflora edulis var edulis) pada tikus model diabetes melitus yang diinduksi aloksan. J K B 2019;30:191–6. DOI: http://dx.doi.org/10.21776/ub.jkb.2019.030.03.5.

Dahlan MS. Statistik untuk kedokteran dan kesehatan. Edisi 6. Jakarta: Epidemiologi Indonesia; 2014.

Panelli MF, Pierine DT, de Souza SLB, et al. Bark of Passiflora edulis treatment stimulates antioxidant capacity, and reduces dyslipidemia and body fat in db/db mice. Antioxidants (Basel) 2018;7: 120. DOI: 10.3390/antiox7090120.

Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev 2014;2014: 360438. oi: 10.1155/2014/360438.

Zulkarnain Z, Triyono A, Novianto F. Jamu formula could reduce plasma cholesterol patients with mild hypercholesterolemia. Health Sci J Indones 2018;9:87–92. DOI: https://doi.org/10.22435/hsji.v9i2.808.

Kandandapani S, Balaraman AK, Ahamed HN. Extracts of passion fruit peel and seed of Passiflora edulis (Passifloraceae) attenuate oxidative stress in diabetic rats. Chin J Nat Med 2015;13:680–6. DOI: 10.1016/S1875-5364(15)30066-2.

Doungue HT, Kengne APN, Kuate D. Neuroprotective effect and antioxidant activity of Passiflora edulis fruit flavonoid fraction, aqueous extract, and juice in aluminum chloride-induced Alzheimer’s disease rats. Nutrire 2018; 43:1–12. https://doi.org/10.1186/s41110-018-0082-1.

Hu M, Du J, Du L, Luo Q, Xiong J. Anti-fatigue activity of purified anthocyanins prepared from purple passion fruit (P. edulis Sim) epicarp in mice. J Funct Foods 2020;65:1–8. https://doi.org/10.1016/j.jff.2019.103725.

Kamilatussaniah, Yuniastuti A, Iswari RS. Pengaruh suplementasi madu kelengkeng terhadap kadar TSA dan MDA tikus putih yang diinduksi timbal (Pb). J MIPA 2015;38:108–14. ISSN 0215-9945.

Fitriani LI, Murbawani EA, Nissa C. Hubungan asupan vitamin C, vitamin E, dan Â-karoten dengan kadar gula darah puasa pada wanita usia 35-50 tahun. J Nutr Coll 2018;7:84–91. DOI: https://doi.org/10.14710/jnc.v7i2.20827.

Eger GA, Ferreira VV, Batista CR, et al. Antioxidant effect of simvastatin throught oxidative imbalance caused by lisdexamfetamine dimesylate. An Acad Bras Ciênc 2016;88:335–48. https://doi.org/10.1590/0001-3765201620140490.

Yang R, Guo P, Ma Z, et al. Effects of simvastatin on iNOS and caspase 3 levels and oxidative stress following smoke inhalation injury. Mol Med Rep 2020;22: 3405–17. PMID: 32945441.

Simatupang A. Statin (HMG-CoA reductase inhibitor): Bukti terbaru pengalaman penggunaannya. Jakarta: Fakultas Kedokteran Universitas Kristen Indonesia; 2017.

Saraswati RA, Maharani N, Utomo AW. Pengaruh ekstrak kulit manggis (Garcinia mangostana L.) terhadap kadar enzim superoxide dismutase (SOD) tikus yang diinduksi minyak jelantah. J Kedokter Diponegoro 2018;7:1511–19. DOI: https://doi.org/10.14710/dmj.v7i2.21470.

Septembre-Malaterre A, Stanislas G, Douraguia E, Gonthier M. Evaluation of nutritional and antioxidant properties of the tropical fruits banana, litchi, mango, papaya, passion fruit, and pineapple cultivated in Réunion French island. Food Chem 2016;212:225–33. DOI: 10.1016/j.foodchem.2016.05.147.

Pretti IR, da Luz AC, Perdigão TL, Araújo RA, Batitucci MCP. Gene expression and antioxidant enzymatic activity in passion fruit exposed to aluminum. Afr J Agric Res 2018;13:115–20. https://doi.org/10.5897/AJAR2017.12834.