Generic placeholder image

Current Bioactive Compounds

Editor-in-Chief

ISSN (Print): 1573-4072
ISSN (Online): 1875-6646

Research Article

Chemical Composition and Therapeutic Potential of Syngonium podophyllum L. Leaves against Hypercholesterolemia in Rats: Liver, Kidney, and Heart Crosstalk

Author(s): Yomna R. Ahmed, Ali M. El-Hagrassi, Noha N. Nasr, Walid E. Abdallah and Manal A. Hamed*

Volume 20, Issue 6, 2024

Published on: 21 November, 2023

Article ID: e211123223665 Pages: 16

DOI: 10.2174/0115734072270545231107044558

Price: $65

Abstract

Background: One of the main risk factors for atherosclerosis is hypercholesterolemia.

Objective: This study aimed to assess hypercholesterolemia's effect on the liver, heart, and kidney and the impact of Syngonium podophyllum L. leaves methanolic extract as a treating agent in a rat model.

Methods: Flavonoid components were isolated and identified from the methanolic extract of Syngonium podophyllum L. leaves. Total serum leptin, total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), triglycerides (TG), aspartate and alanine aminotransferases (AST and ALT), urea, and creatinine levels were all measured as part of the biochemical evaluation. The liver tissue was tested for levels of malondialdehyde (MDA), glutathione (GSH), superoxide dismutase (SOD), and DNA fragmentation.

Results: Thirty-nine compounds were identified by GC/MS profiling of the n-hexane fraction of Syngonium podophyllum L leaves. The major volatile constituents were decane, 4-methyl, decane, N-acetyl 3-pentenyl, 1-amine, 2-methyl, 1-hexene, and 3-hydroxy, propanenitrile, while the major phenolic compounds isolated from methanolic extract were luteolin-7- α-L rhamnoside-4'- O-β-glucopyranoside (1), apigenin 6, 8-di-C-β-glucopyranoside (vicenin 2) (2), quercetin-3-O- α-L-rhamnoside (3), quercetin-7-O-β-glucoside compound (4), luteolin-7-O-β-glucoside (5), 5- hydroxy-6,7,8,4'-tetramethoxy flavone (6), gallic acid (7) and quercetin (8). Hypercholesterolemic rats revealed significant alterations (p ≤ 0.05) in the lipid profile, liver and kidney function, DNA fragmentation pattern and antioxidant indices. With oral cholesterol administration of 30 mg/0.3 mL (0.7% tween)/rats fed a high-fat diet for nine weeks, treatment with leaves extract (250 mg/kg body weight) was able to restore all biochemical parameters as well as the architectures of the liver and heart.

Conclusion: Due to its abundance in physiologically active phenolic and flavonoid components, the methanolic extract of Syngonium podophyllum L. leaves successfully served as a hypolipidemic, anti-atherosclerotic, and antioxidant therapeutic agent.

Graphical Abstract

[1]
Csonka, C.; Sárközy, M.; Pipicz, M.; Dux, L.; Csont, T. Modulation of Hypercholesterolemia- Induced Oxidative/Nitrative Stress in the Heart. In: Oxidative Med. Cell. Longev., 2016, 23, 23.
[2]
Makkos, A.; Szántai, Á.; Pálóczi, J.; Pipis, J.; Kiss, B.; Poggi, P.; Ferdinandy, P.; Chatgilialoglu, A.; Görbe, A. A comorbidity model of myocardial ischemia reperfusion injury and hypercholesterolemia in rat cardiac myocyte cultures. Front. Physiol., 2020, 10, 1564.
[http://dx.doi.org/10.3389/fphys.2019.01564] [PMID: 31992989]
[3]
Kim, J.B. Dynamic cross talk between metabolic organs in obesity and metabolic diseases. Exp. Mol. Med., 2016, 48(3), e214.
[http://dx.doi.org/10.1038/emm.2015.119] [PMID: 26964830]
[4]
Csont, T.; Balogh, G.; Csonka, C.; Boros, I.; Horváth, I.; Vigh, L.; Ferdinandy, P. Hyperlipidemia induced by high cholesterol diet inhibits heat shock response in rat hearts. Biochem. Biophys. Res. Commun., 2002, 290(5), 1535-1538.
[http://dx.doi.org/10.1006/bbrc.2002.6377] [PMID: 11820796]
[5]
Ashique, S. A short note on Atherosclerosis. J. Appl. Pharm., 2022, 14(2), 335.
[6]
Bonomini, F.; Tengattini, S.; Fabiano, A.; Bianchi, R.; Rezzani, R. Atherosclerosis and oxidative stress. Histol. Histopathol., 2008, 23(3), 381-390.
[PMID: 18072094]
[7]
Pluijmert, N.J.; den Haan, M.C.; van Zuylen, V.L.; Steendijk, P.; de Boer, H.C.; van Zonneveld, A.J.; Fibbe, W.E.; Schalij, M.J.; Quax, P.H.A.; Atsma, D.E. Hypercholesterolemia affects cardiac function, infarct size and inflammation in APOE*3-Leiden mice following myocardial ischemia-reperfusion injury. PLoS One, 2019, 14(6), e0217582.
[http://dx.doi.org/10.1371/journal.pone.0217582] [PMID: 31199833]
[8]
Inoue, T.; Node, K. Vascular failure: A new clinical entity for vascular disease. J. Hypertens., 2006, 24(11), 2121-2130.
[http://dx.doi.org/10.1097/01.hjh.0000249684.76296.4f] [PMID: 17053528]
[9]
Otunola, G.; Oloyede, O.; Oladiji, A.; Afolayan, A. Effects of diet-induced hypercholesterolemia on the lipid profile and some enzyme activities in female Wistar rat. Afr. J. Biochem. Res., 2010, 4, 149-154.
[10]
Burns, M.P.; Igbavboa, U.; Wang, L.; Wood, W.G.; Duff, K. Cholesterol distribution, not total levels, correlate with altered amyloid precursor protein processing in statin-treated mice. Neuromolecular Med., 2006, 8(3), 319-328.
[http://dx.doi.org/10.1385/NMM:8:3:319] [PMID: 16775383]
[11]
Qadir, M.I.; Manzoor, A.; Akash, M.S.H. Potential role of medicinal plants for anti-atherosclerosis activity. Bangladesh J. Pharmacol., 2018, 13(1), 59-66.
[http://dx.doi.org/10.3329/bjp.v13i1.33478]
[12]
Adegbola, P.; Aderibigbe, I.; Hammed, W.; Omotayo, T. Antioxidant and anti-inflammatory medicinal plants have potential role in the treatment of cardiovascular disease: A review. Am. J. Cardiovasc. Dis., 2017, 7(2), 19-32.
[PMID: 28533927]
[13]
Matloub, A.A.; El-Souda, S.S.M.; El-Senousy, W.M.; Hamed, M.; Aly, H.; Ali, S.A.; Mohammed, R.S.; Mahmoud, K.; El-Hallouty, S.; Ibrahim, N.A.; Awad, N.A.; El-Rafaie, H.M. In vitro antiviral, cytotoxic, antioxidant and hypolipidemic activities of polysaccharide isolated from marine algae. IJPPR, 2015, 7, 1099-1111.
[14]
Murad, S.; Mastoi, M.I.; Mastoi, A.G.; Hussain, A.; Mahar, M.R.; Murad, J.S. Lipids, atherosclerosis, and medicinal plants. Thromb. Haemost. Res., 2019, 3(3), 1029.
[15]
Kumar, S.; Kumar, R.; Dwivedi, A.; Pandey, A.K. In vitro antioxidant, antibacterial, and cytotoxic activity and in vivo effect of Syngonium podophyllum and Eichhornia crassipes leaf extracts on isoniazid induced oxidative stress and hepatic markers. BioMed Res. Int., 2014, 2014, 1-11.
[http://dx.doi.org/10.1155/2014/459452] [PMID: 25162013]
[16]
Hossain, M.S.; Uddin, M.S.; Kabir, M.T.; Begum, M.M.; Koushal, P.; Herrera-Calderon, O.; Akter, R.; Asaduzzaman, M.; Abdel-Daim, M.M. In vitro screening for phytochemicals and antioxidant activities of Syngonium podophyllum L.: An incredible therapeutic plant. Biomed. Pharmacol. J., 2017, 10(3), 1267-1277.
[http://dx.doi.org/10.13005/bpj/1229]
[17]
Hossain, M.; Uddin, M.; Kabir, M.; Akhter, S.; Goswami, S.; Mamun, A.; Herrera-Calderon, O.; Abdel-Daim, M.; Abdel-Daim, M.M. In vivo screening for analgesic and anti-inflammatory activities of Syngonium podophyllum L.: A remarkable herbal medicine. Annu. Res. Rev. Biol., 2017, 16(3), 1-12.
[http://dx.doi.org/10.9734/ARRB/2017/35692]
[18]
Siasos, G.; Tousoulis, D.; Tsigkou, V.; Kokkou, E.; Oikonomou, E.; Vavuranakis, M.; Basdra, E.K.; Papavassiliou, A.G.; Stefanadis, C. Flavonoids in atherosclerosis: An overview of their mechanisms of action. Curr. Med. Chem., 2013, 20(21), 2641-2660.
[http://dx.doi.org/10.2174/0929867311320210003] [PMID: 23627935]
[19]
Adams, R.P. Identification of essential oil components by gas chromatography/mass spectrometry Allured Publishing Corporation: US , 2007.
[20]
Mabry, T.; Markham, K.R.; Thomas, M.B. The systematic identification of flavonoids; Springer: New York, 1970, pp. 35-109.
[http://dx.doi.org/10.1007/978-3-642-88458-0_4]
[21]
Markham, K. Techniques of flavonoid identification; Academic Press: London, 1982, p. 113.
[22]
Swanston-Flatt, S.K.; Day, C.; Bailey, C.J.; Flatt, P.R. Traditional plant treatments for diabetes. Studies in normal and streptozotocin diabetic mice. Diabetologia, 1990, 33(8), 462-464.
[http://dx.doi.org/10.1007/BF00405106] [PMID: 2210118]
[23]
Partridge, S.M. Aniline hydrogen phthalate as a spraying reagent for chromatography of sugars. Nature, 1949, 164(4167), 443-447.
[http://dx.doi.org/10.1038/164443a0] [PMID: 18140444]
[24]
Al-wakeel, S.A.M.; El-Garf, I.; Saleh, N.A.M. Distribution of flavonoids in Fagonia thebaica complex. Biochem. Syst. Ecol., 1988, 16(1), 57-58.
[http://dx.doi.org/10.1016/0305-1978(88)90118-4]
[25]
Saleh, N.A.M.; El-Hadidi, M.N.; Al-Wakeel, S.A.M. Phytochemistry and phylogenetic affinities among Egyptian species of Fagonia. Biochem. Syst. Ecol., 1990, 18(1), 49-52.
[http://dx.doi.org/10.1016/0305-1978(90)90033-C]
[26]
Adaramoye, O.A.; Akintayo, O.; Achem, J.; Fafunso, M.A. Lipid lower in effects of methanolic extract of Vernonia amygdalina leaves in rats fed on high cholesterol diet. J. Am. Coll. Nutr., 2008, 15, 289-294.
[27]
Awad, N.E.; Abdelkawy, M.A.; Hamed, M.A.; Aboshehata, M.M. Quantitation and HPLC identification of flavonoids and phenolics of Ficus racemosa (L.) butanol fraction and in vivo assessment of its hypolipidemic and hepatoprotective activities in rats. Int. J. Biol. & Pharmaceut. Res., 2015, 6, 626-638.
[28]
Sadeghi, R.; Asadpour-Piranfar, M.; Asadollahi, M.; Taherkhani, M.; Baseri, F. The effects of different doses of atorvastatin on serum lipid profile, glycemic control, and liver enzymes in patients with ischemic cerebrovascular accident. ARYA Atheroscler., 2014, 10(6), 298-304.
[PMID: 25815019]
[29]
Hirsch, C.; Zouain, C.S.; Alves, J.B.; Goes, A.M. Induction of protective immunity and modulation of granulomatous hypersensitivity in mice using PIII, an anionic fraction of Schistosoma mansoni adult worm. Parasitology, 1997, 115(1), 21-28.
[http://dx.doi.org/10.1017/S0031182097001078] [PMID: 9280892]
[30]
Meiattini, F.; Prencipe, L.; Bardelli, F.; Giannini, G.; Tarli, P. The 4-hydroxybenzoate/4-aminophenazone chromogenic system used in the enzymic determination of serum cholesterol. Clin. Chem., 1978, 24(12), 2161-2165.
[http://dx.doi.org/10.1093/clinchem/24.12.2161] [PMID: 719864]
[31]
Bustein, M.; Schoirick, H.R.; Morfin, R. Rapid method for the isolation of lipoproteins from human serum by perciption with polyanions. Scand. J. Clin. Lab. Invest., 1980, 40, 583-595.
[32]
Assmann, G.; Gotto, A.M., Jr; Cagen, J.R. HDL cholesterol and protective factors in atherosclerosis. Circulation, 2004, 109(23_suppl_1)(Suppl. 1), III8-III14.
[http://dx.doi.org/10.1161/01.CIR.0000131512.50667.46] [PMID: 15198960]
[33]
Fossati, P.; Prencipe, L. Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin. Chem., 1982, 28(10), 2077-2080.
[http://dx.doi.org/10.1093/clinchem/28.10.2077] [PMID: 6812986]
[34]
Buege, J.A.; Aust, S.D. Microsomal lipid peroxidation. Methods Enzymol., 1978, 52, 302-310.
[http://dx.doi.org/10.1016/S0076-6879(78)52032-6] [PMID: 672633]
[35]
Moron, M.; Depierre, J.; Mannervik, B. Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim. Biophys. Acta, Gen. Subj., 1979, 582(1), 67-78.
[http://dx.doi.org/10.1016/0304-4165(79)90289-7] [PMID: 760819]
[36]
Nishikimi, M.; Appaji Rao, N.; Yagi, K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem. Biophys. Res. Commun., 1972, 46(2), 849-854.
[http://dx.doi.org/10.1016/S0006-291X(72)80218-3] [PMID: 4400444]
[37]
Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 1976, 72(1-2), 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[38]
Gella, F.J.; Olivella, T.; Pastor, M.C.; Arenas, J.; Moreno, R.; Durban, R.; Gomez, J.A. A simple procedure for the routine determination of aspartate aminotransferase and alanine aminotransferase with pyridoxal phosphate. Clin. Chim. Acta, 1985, 153(3), 241-247.
[http://dx.doi.org/10.1016/0009-8981(85)90358-4] [PMID: 4075530]
[39]
Tabacco, A.; Meiattini, F.; Moda, E.; Tarli, P. Simplified enzymic/colorimetric serum urea nitrogen determination. Clin. Chem., 1979, 25(2), 336-337.
[http://dx.doi.org/10.1093/clinchem/25.2.336a] [PMID: 759035]
[40]
Bartels, H.; Böhmer, M. Micro-determination of creatinine. Clin. Chim. Acta, 1971, 32(1), 81-85.
[PMID: 5096431]
[41]
Singh, N.P.; McCoy, M.T.; Tice, R.R.; Schneider, E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res., 1988, 175(1), 184-191.
[http://dx.doi.org/10.1016/0014-4827(88)90265-0] [PMID: 3345800]
[42]
Hawas, U.W.; El-Desoky, S.K.; Kawashty, S.A.; Sharaf, M. Two new flavonoids from Origanum vulgare. Nat. Prod. Res., 2008, 22(17), 1540-1543.
[http://dx.doi.org/10.1080/14786410600898987] [PMID: 19023817]
[43]
Gopi, K.; Anbarasu, K.; Renu, K.; Jayanthi, S.; Vishwanath, B.S.; Jayaraman, G. Quercetin-3-O-rhamnoside from Euphorbia hirta protects against snake Venom induced toxicity. Biochim. Biophys. Acta, Gen. Subj., 2016, 1860(7), 1528-1540.
[http://dx.doi.org/10.1016/j.bbagen.2016.03.031] [PMID: 27033089]
[44]
Elshabrawy, M.; Ahmed Elkhateeb, A.; Hussein, S.R.; Kassem, M.; Kawashty, S.; Saleh, E.; Marzouk, M. Comparative chemical investigation of Brachychiton australis (Schott & Endl.) A. Terracc. and Brachychiton discolor F. Muell. Egypt. J. Chem., 2021, 64, 5529-5536.
[45]
Priest, C.; Tontonoz, P. Inter-organ cross-talk in metabolic syndrome. Nat. Metab., 2019, 1(12), 1177-1188.
[http://dx.doi.org/10.1038/s42255-019-0145-5] [PMID: 32694672]
[46]
Azemi, N.; Azemi, A.; Abu-Bakar, L.; Sevakumaran, V.; Tengku Muhammad, T.; Ismail, N. Effect of linoleic acid on cholesterol levels in a hgh-fat diet-induced hypercholesterolemia rat model. Metabolites, 2023, 13, 1-15.
[47]
Sáinz, N.; Barrenetxe, J.; Moreno-Aliaga, M.J.; Martínez, J.A. Leptin resistance and diet-induced obesity: central and peripheral actions of leptin. Metabolism, 2015, 64(1), 35-46.
[http://dx.doi.org/10.1016/j.metabol.2014.10.015] [PMID: 25497342]
[48]
Taha, N.M.; Abdel-Hamid, H.S.; Sadek, K.M.; Abdalaziz, A.Z. Effect of garlic and atorvastatin on liptin and lipid profile in triton-x- 100 induced hyperlipidemia in rats. Kafrelsheikh Veterinary Medical Journal, 2014, 12(2), 109-127.
[http://dx.doi.org/10.21608/kvmj.2014.110154]
[49]
Mzhelskaya, K.V.; Shipelin, V.A.; Shumakova, A.A.; Musaeva, A.D.; Soto, J.S.; Riger, N.A.; Trusov, N.V.; Kirbaeva, N.V.; Apryatin, S.A.; Gmoshinski, I.V. Effects of quercetin on the neuromotor function and behavioral responses of wistar and zucker rats fed a high-fat and high-carbohydrate diet. Behav. Brain Res., 2020, 378, 112270.
[http://dx.doi.org/10.1016/j.bbr.2019.112270] [PMID: 31585131]
[50]
Salil, G.; Rajamohan, T. Hypolipidemic and antiperoxidative effect of coconut protein in hypercholesterolemic rats. Indian J. Exp. Biol., 2001, 39(10), 1028-1034.
[PMID: 11883511]
[51]
Fungwe, T.V.; Cagen, L.M.; Cook, G.A.; Wilcox, H.G.; Heimberg, M. Dietary cholesterol stimulates hepatic biosynthesis of triglyceride and reduces oxidation of fatty acids in the rat. J. Lipid Res., 1993, 34(6), 933-941.
[http://dx.doi.org/10.1016/S0022-2275(20)39680-2] [PMID: 8354959]
[52]
El-Feky, A.; Elbatanony, M.; Aboul Naser, A.; Kutkat, O.; El-Sayed, A.; Hamed, M. Phytoconstituents and in vitro anti-oxidant, anti-viral, anti-hyperlipidemic and anticancer effects of Chlorella vulgaris microalga in normal and stress conditions. Pharma Chem., 2020, 12, 9-20.
[53]
Gundamaraju, R.; Hwi, K.; Singla, R.; Vemuri, R.; Mulapalli, S. Antihyperlipidemic potential of Albizia amara (Roxb) Boiv. bark against Triton X-100 induced hyperlipidemic condition in rats. Pharmacognosy Res., 2014, 6(4), 267-273.
[http://dx.doi.org/10.4103/0974-8490.138237] [PMID: 25276061]
[54]
Pareek, A.; Chandurkar, N.; Tenpe, C.R.; Yeole, P.G.; Payghan, R. Effect of atorvastatin and hydroxychloroquine combination on triton WR 1339 induced hyperlipidemia in rats. Mol. Pharmacol., 2014, 1, 1-3.
[55]
Miettinen, T.A. Inhibition of cholesterol absorption by HMG-CoA reductase inhibitor. Eur. J. Clin. Pharmacol., 1991, 40(S1)(Suppl. 1), S19-S21.
[http://dx.doi.org/10.1007/BF03216283] [PMID: 1904356]
[56]
Awad, N.E.; Seida, A.A.; Hamed, M.A.; Elbatanony, M.M. Hypolipidaemic and antioxidant activities of Ficus microcarpa (L.) in hypercholesterolemic rats. Nat. Prod. Res., 2011, 25(12), 1202-1207.
[http://dx.doi.org/10.1080/14786419.2010.538015] [PMID: 21740287]
[57]
Rackley, C.E. Monotherapy with hMG-CoA reductase inhibitors and secondary prevention in coronary artery disease. Clin. Cardiol., 1996, 19(9), 683-689.
[http://dx.doi.org/10.1002/clc.4960190903] [PMID: 8874986]
[58]
Awad, N.E.; Hamed, M.A.; Seida, A.A.; Elbatanony, M.M.; Elbatanony, M.M. Efficacy of Ficus spp. on renal injury induced by hypercholesterolaemia. Nat. Prod. Res., 2012, 26(16), 1561-1564.
[http://dx.doi.org/10.1080/14786419.2011.570760] [PMID: 22432976]
[59]
Kim, Y.M.; Jeong, Y.K.; Wang, M.H.; Lee, W.Y.; Rhee, H.I. Inhibitory effect of Pine erglycemia. Nutrition, 2005, 21, 756-761.
[http://dx.doi.org/10.1016/j.nut.2004.10.014] [PMID: 15925302]
[60]
Ashfaq, F.; Butt, M.S.; Bilal, A.; Suleria, H.A.R. Hepatoprotective effects of red cabbage in hypercholesterolemic diet-induced oxidative stressed rabbits. Curr. Bioact. Compd., 2020, 16(4), 469-480.
[http://dx.doi.org/10.2174/1573407215666190124113738]
[61]
Sheela, C.G.; Augusti, K.T. Antiperoxide effects of S-allyl cysteine sulphoxide isolated from Allium sativum Linn and gugulipid in cholesterol diet fed rats. Indian J. Exp. Biol., 1995, 33(5), 337-341.
[PMID: 7558192]
[62]
El-Hagrassi, A.; Aboul Naser, A.; Osman, A.F.; Hamed, M. Phytophenolics composition of Ocimum basilieum L. leaves methanol extract and its role in mitigating hypercholesterolemia in a rat model. Curr. Bioactive Comp, 2021, 17.
[63]
Ónody, A.; Csonka, C.; Giricz, Z.; Ferdinandy, P. Hyperlipidemia induced by a cholesterol-rich diet leads to enhanced peroxynitrite formation in rat hearts. Cardiovasc. Res., 2003, 58(3), 663-670.
[http://dx.doi.org/10.1016/S0008-6363(03)00330-4] [PMID: 12798440]
[64]
Abudunia, A.M.; Marmouzi, I.; Kharbach, M.; Jemli, M.E.; Sayah, K.; Bouyahya, A.; Al-kaf, A.; Alyahawi, A.; Ansar, M.H.; Bouklouze, A.; Faouzi, M.E.A.; Ibrahimi, A. Hypoglycemic effect of Calendula arvensis flowers is mediated by digestive Enzyme inhibition. Curr. Bioact. Compd., 2020, 16(5), 588-592.
[http://dx.doi.org/10.2174/1573407215666190219094407]
[65]
Mollica, A.; Zengin, G.; Locatelli, M.; Stefanucci, A.; Mocan, A.; Macedonio, G.; Carradori, S.; Onaolapo, O.; Onaolapo, A.; Adegoke, J.; Olaniyan, M.; Aktumsek, A.; Novellino, E. Anti-diabetic and anti-hyperlipidemic properties of Capparis spinosa L.: In vivo and in vitro evaluation of its nutraceutical potential. J. Funct. Foods, 2017, 35, 32-42.
[http://dx.doi.org/10.1016/j.jff.2017.05.001]
[66]
Prasad, K. Effects of vitamin E on serum enzymes and electrolytes in hypercholesterolemia. Mol. Cell. Biochem., 2010, 335(1-2), 67-74.
[http://dx.doi.org/10.1007/s11010-009-0243-x] [PMID: 19730989]
[67]
Botto, N.; Rizza, A.; Colombo, M.G.; Mazzone, A.M.; Manfredi, S.; Masetti, S.; Clerico, A.; Biagini, A.; Andreassi, M.G. Evidence for DNA damage in patients with coronary artery disease. Mutat. Res. Genet. Toxicol. Environ. Mutagen., 2001, 493(1-2), 23-30.
[http://dx.doi.org/10.1016/S1383-5718(01)00162-0] [PMID: 11516712]
[68]
Harangi, M.; Remenyik, É.; Seres, I.; Varga, Z.; Katona, E.; Paragh, G. Determination of DNA damage induced by oxidative stress in hyperlipidemic patients. Mutat. Res. Genet. Toxicol. Environ. Mutagen., 2002, 513(1-2), 17-25.
[http://dx.doi.org/10.1016/S1383-5718(01)00285-6] [PMID: 11719086]
[69]
Alderman, M.; Aiyer, K.J.V. Uric acid: Role in cardiovascular disease and effects of losartan. Curr. Med. Res. Opin., 2004, 20(3), 369-379.
[http://dx.doi.org/10.1185/030079904125002982] [PMID: 15025846]
[70]
Deepa, P.R.; Varalakshmi, P. Protective effects of certoparin sodium, a low molecular weight heparin derivative, in experimental atherosclerosis. Clin. Chim. Acta, 2004, 339(1-2), 105-115.
[http://dx.doi.org/10.1016/j.cccn.2003.09.021] [PMID: 14687900]
[71]
Hashem, A.N.; Soliman, M.S.; Hamed, M.A.; Swilam, N.F.; Lindequist, U.; Nawwar, M.A. Beta vulgaris subspecies cicla var. flavescens (Swiss chard): flavonoids, hepatoprotective and hypolipidemic activities. Pharmazie, 2016, 71(4), 227-232.
[PMID: 27209705]
[72]
Dawood, A.; Hareedy, H. Differential effect of high fat diet (HFD) on the cardiac muscle of adult and aged female mice and the possible protective role of artichoke treatment: Histomorphometric and ultrastructural study. J. Med. Histol., 2019, 3(1), 36-54.
[http://dx.doi.org/10.21608/jmh.2019.11528.1053]
[73]
Rasheed, R.; Othman, M.; Hussein, U.; Embaby, A.S. The possible ameliorative influence of quercetin on cardiac muscle changes induced by high fat diet in adult male albino rats: Light and electron microscopic study. EJH, 2022, 45, 937-948.

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