Download PDF
Planta Med 2018; 84(17): 1271-1279
DOI: 10.1055/a-0644-2794
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Heart-Protective Effects of Echinodorus grandiflorus in Rabbits That Are Fed a High-cholesterol Diet

Francielly Mourão Gasparotto
1   Laboratório de Eletrofisiologia e Farmacologia Cardiovascular, Faculdade de Ciências da Saúde, Universidade Federal da Grande Dourados, Dourados, MS, Brazil
,
Francislaine Aparecida dos Reis Lívero
2   Laboratório de Pesquisa Pré-Clínica de Produtos Naturais, Universidade Paranaense, Umuarama, PR, Brazil
,
Rhanany Allan Caloi Palozi
1   Laboratório de Eletrofisiologia e Farmacologia Cardiovascular, Faculdade de Ciências da Saúde, Universidade Federal da Grande Dourados, Dourados, MS, Brazil
,
Maria Leticia Ames
2   Laboratório de Pesquisa Pré-Clínica de Produtos Naturais, Universidade Paranaense, Umuarama, PR, Brazil
,
Bruna Nunes
2   Laboratório de Pesquisa Pré-Clínica de Produtos Naturais, Universidade Paranaense, Umuarama, PR, Brazil
,
Guilherme Donadel
2   Laboratório de Pesquisa Pré-Clínica de Produtos Naturais, Universidade Paranaense, Umuarama, PR, Brazil
,
Rita de Cassia Lima Ribeiro
2   Laboratório de Pesquisa Pré-Clínica de Produtos Naturais, Universidade Paranaense, Umuarama, PR, Brazil
,
Emerson Luiz Botelho Lourenço
2   Laboratório de Pesquisa Pré-Clínica de Produtos Naturais, Universidade Paranaense, Umuarama, PR, Brazil
,
Cândida Aparecida Leite Kassuya
1   Laboratório de Eletrofisiologia e Farmacologia Cardiovascular, Faculdade de Ciências da Saúde, Universidade Federal da Grande Dourados, Dourados, MS, Brazil
,
Arquimedes Gasparotto Junior
1   Laboratório de Eletrofisiologia e Farmacologia Cardiovascular, Faculdade de Ciências da Saúde, Universidade Federal da Grande Dourados, Dourados, MS, Brazil
› Author Affiliations
Further Information

Publication History

received 13 April 2018
revised 05 May 2018

accepted 11 June 2018

Publication Date:
21 June 2018 (online)

Also available at
    Permissions and Reprints

Abstract

Excess weight and dyslipidemia are among the most serious health problems in Western societies. These conditions enhance the risk of cardiac disease and have been linked with a higher prevalence of cardiac arrhythmias and sudden death. The present study investigated the cardioprotective effects of Echinodorus grandiflorus on ventricular remodeling in rabbits that were fed a 1% cholesterol-rich diet. We first obtained an ethanol-soluble fraction of E. grandiflorus and performed a detailed phytochemical study by liquid chromatography-DAD/ESI-MS. For 60 days, male rabbits were fed the cholesterol-rich diet or a diet without the addition of cholesterol. After 30 days, different groups of rabbits were treated with the ethanol-soluble fraction of E. grandiflorus (10, 30, and 100 mg/kg, p. o.), simvastatin (2.5 mg/kg), or vehicle once daily for 30 days. At the end of 60 days, the serum lipoprotein ratio, electrocardiographic profile, histopathological alterations, and the cardiac antioxidant defense system were investigated. Echocardiographic analysis showed morphological and functional alterations in cholesterol-rich diet-fed animals, indicating left ventricle hypertrophy. The total cholesterol/high-density lipoprotein ratio and low-density lipoprotein/high-density lipoprotein ratio were significantly higher in cholesterol-rich diet-fed rabbits. Myocardial flaccidity, fatty degeneration, and concentric left ventricular hypertrophy were observed. An increase in lipid peroxidation levels, a decrease in superoxide dismutase activity, and a decrease in reduced glutathione levels were observed in the myocardium of all cholesterol-rich diet-fed rabbits. Treatment with the ethanol-soluble fraction of E. grandiflorus, especially the highest dose, significantly reduced all of these alterations, thus demonstrating the cardioprotective effect of the ethanol-soluble fraction of E. grandiflorus on cardiac changes that are induced by a cholesterol-rich diet.

Key words

Alismataceae - antioxidant - atherosclerosis - dyslipidemia - Echinodorus grandiflorus - ventricular hypertrophy
 

  • References

  • 1 Saklayen MG. The global epidemic of the metabolic syndrome. Curr Hypertens Rep 2018; 20: 1-12
    CrossrefPubMedGoogle Scholar
  • 2 Mu M, Xu LF, Hu D, Wu J, Bai MJ. Dietary patterns and overweight/abesity: a review article. Iran J Public Health 2017; 46: 869-876
    PubMedGoogle Scholar
  • 3 Bowen KJ, Sullivan VK, Kris-Etherton PM, Petersen KS. Nutrition and cardiovascular disease – an update. Curr Atheroscler Rep 2018; 20: 1-8
    CrossrefPubMedGoogle Scholar
  • 4 Parisi V, Leosco D, Ferro G, Bevilacqua A, Pagano G, de Lucia C, Perrone Filardi P, Caruso A, Rengo G, Ferrara N. The lipid theory in the pathogenesis of calcific aortic stenosis. Nutr Metab Cardiovasc Dis 2015; 25: 519-525
    CrossrefPubMedGoogle Scholar
  • 5 Tune JD, Goodwill AG, Sassoon DJ, Mather KJ. Cardiovascular consequences of metabolic syndrome. Transl Res 2017; 183: 57-70
    CrossrefPubMedGoogle Scholar
  • 6 Puddu PE, Schiariti M, Torromeo C. Gender and cardiovascular mortality in Northern and Southern European populations. Curr Pharm Des 2016; 22: 3893-3904
    CrossrefPubMedGoogle Scholar
  • 7 Ribeiro RV, Bieski IGC, Balogun SO, Martins DTO. Ethnobotanical study of medicinal plants used by Ribeirinhos in the North Araguaia microregion, Mato Grosso, Brazil. J Ethnopharmacol 2017; 205: 69-102
    CrossrefPubMedGoogle Scholar
  • 8 Pedrollo CT, Kinupp VF, Shepard jr. G, Heinrich M. Medicinal plants at Rio Jauaperi, Brazilian Amazon: Ethnobotanical survey and environmental conservation. J Ethnopharmacol 2016; 186: 111-124
    CrossrefPubMedGoogle Scholar
  • 9 Marques AM, Provance jr. DW, Kaplan MAC, Figueiredo MR. Echinodorus grandiflorus: Ethnobotanical, phytochemical and pharmacological overview of a medicinal plant used in Brazil. Food Chem Toxicol 2017; 109(Pt 2): 1032-1047
    CrossrefPubMedGoogle Scholar
  • 10 Maleki T, Akhani H. Ethnobotanical and ethnomedicinal studies in Baluchi tribes: A case study in Mt. Taftan, southeastern Iran. J Ethnopharmacol 2018; 217: 163-177
    CrossrefPubMedGoogle Scholar
  • 11 El-Tantawy WH, Temraz A. Natural products for controlling hyperlipidemia: review. Arch Physiol Biochem 2018; 19: 1-8
    PubMedGoogle Scholar
  • 12 Santiago PG, Gasparotto FM, Gebara KS, Bacha FB, Lívero FADR, Strapazon MA, Junior ELC, Kassuya CAL, de Souza LM, Gasparotto Junior A. Mechanisms underlying antiatherosclerotic properties of an enriched fraction obtained from Ilex paraguariensis A. St.-Hil. Phytomedicine 2017; 34: 162-170
    CrossrefPubMedGoogle Scholar
  • 13 Cavalera M, Axling U, Rippe C, Swärd K, Holm C. Dietary rose hip exerts antiatherosclerotic effects and increases nitric oxide-mediated dilation in ApoE-null mice. J Nutr Biochem 2017; 44: 52-59
    CrossrefPubMedGoogle Scholar
  • 14 Bolson M, Hefler SR, Chaves EID, Gasparotto Junior A, Cardozo Junior EL. Ethno-medicinal study of plants used for treatment of human ailments, with residents of the surrounding region of forest fregments of Paraná, Brazil. J Ethnopharmacol 2015; 161: 1-10
    CrossrefPubMedGoogle Scholar
  • 15 Brugiolo SSS, Borges LV, Pimenta DS, Brugioro ASS, Peters VM, Guerra MO. Ethnobotany and experimental Pharmacology of Echinodorus grandiflorus (chapéu-de-couro). In: Alejandro V, Jasiah I. eds. Medicinal Plants: Classification, Biosynthesis and Pharmacology. New York: Nova Science Publishers; 2009: 243-254
    Google Scholar
  • 16 Brasil. Farmacopeia Brasileira, volume 2/Agência Nacional de Vigilância Sanitária. Brasília: Anvisa; 2010: 546-1v/il
    Google Scholar
  • 17 Brasil. Agência Nacional de Vigilância Sanitária. Formulário de Fitoterápicos da Farmacopéia Brasileira/Agência Nacional de Vigilância Sanitária. Brasília: Anvisa; 2011: 126
    Google Scholar
  • 18 Garcia EF, Oliveira MA, Godin AM, Ferreira WC, Bastos LF, Coelho MM, Braga FC. Antiedematogenic activity and phytochemical composition of preparations from Echinodorus grandiflorus leaves. Phytomedicine 2010; 18: 80-86
    CrossrefPubMedGoogle Scholar
  • 19 Prando TBL, Barboza LN, Gasparotto FM, Araújo VO, Tirloni CAS, de Souza LM, Lourenço ELB, Gasparotto Junior A. Ethnopharmacological investigation of the diuretic and hemodynamic properties of native species of the Brazilian biodiversity. J Ethnopharmacol 2015; 174: 369-378
    CrossrefPubMedGoogle Scholar
  • 20 Prando TB, Barboza LN, Araújo VO, Gasparotto FM, de Souza LM, Lourenço EL, Gasparotto Junior A. Involvement of bradykinin B2 and muscarinic receptors in the prolonged diuretic and antihypertensive properties of Echinodorus grandiflorus (Cham. & Schltdl.) Micheli. Phytomedicine 2016; 23: 1249-1258
    CrossrefPubMedGoogle Scholar
  • 21 Garcia Ede F, de Oliveira MA, Dourado LP, de Souza DG, Teixeira MM, Braga FC. In vitro TNF-α inhibition elicited by extracts from Echinodorus grandiflorus leaves and correlation with their phytochemical composition. Planta Med 2016; 82: 337-343
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 Garcia Ede F, de Oliveira MA, Candido LC, Coelho FM, Costa VV, Queiroz-Junior CM, Boff D, Amaral FA, de Souza Dda G, Teixeira MM, Braga FC. Effect of the hydroethanolic extract from Echinodorus grandiflorus leaves and a fraction enriched in flavone-C-glycosides on antigen-induced arthritis in mice. Planta Med 2016; 82: 407-413
    Article in Thieme ConnectPubMedGoogle Scholar
  • 23 Lessa MA, Araújo CV, Kaplan MA, Pimenta D, Figueiredo MR, Tibiriçá E. Antihypertensive effects of crude extracts from leaves of Echinodorus grandiflorus . Fundam Clin Pharm 2008; 22: 161-168
    CrossrefPubMedGoogle Scholar
  • 24 Tibiriçá E, Almeida A, Caillleaux S, Pimenta D, Kaplan MA, Lessa MA, Figueiredo MR. Pharmacological mechanisms involved in the vasodilator effects of extracts from Echinodorus grandiflorus . J Ethnopharmacol 2007; 111: 50-55
    CrossrefPubMedGoogle Scholar
  • 25 Ambapkar SN, Shetty N, Dwivedy A, Malve HO. Statin-induced rhabdomyolysis in patient with renal failure and underlying undiagnosed hypothyroidism. Indian J Crit Care Med 2016; 20: 305-307
    CrossrefPubMedGoogle Scholar
  • 26 Jose J. Statins and its hepatic effects: Newer data, implications, and changing recommendations. J Pharm Bioallied Sci 2016; 8: 23-28
    CrossrefPubMedGoogle Scholar
  • 27 Millán J, Pintó X, Muñoz A, Zúñiga M, Rubiés-Prat J, Pallardo LF, Masana L, Mangas A, Hernández-Mijares A, González-Santos P, Ascaso JF, Pedro-Botet J. Lipoprotein ratios: Physiological significance and clinical usefulness in cardiovascular prevention. J Vasc Health Risk Manag 2009; 5: 757-765
    PubMedGoogle Scholar
  • 28 Kinosian B, Glick H, Garland G. Cholesterol and coronary heart disease: predicting risks by levels and ratios. Ann Intern Med 1994; 121: 641-647
    PubMedGoogle Scholar
  • 29 Wong ZW, Thanikachalam PV, Ramamurthy S. Molecular understanding of the protective role of natural products on isoproterenol-induced myocardial infarction: A review. Biomed Pharmacother 2017; 94: 1145-1166
    CrossrefPubMedGoogle Scholar
  • 30 Hung LM, Chen JK, Huang SS, Lee RS, Su MJ. Cardioprotective effect of resveratrol, a natural antioxidant derived from grapes. Cardiovasc Res 2000; 47: 549-555
    CrossrefPubMedGoogle Scholar
  • 31 Gormaz JG, Valls N, Sotomayor C, Turner T, Rodrigo R. Potential role of polyphenols in the prevention of cardiovascular diseases: molecular bases. Curr Med Chem 2016; 23: 115-128
    CrossrefPubMedGoogle Scholar
  • 32 Oak MH, Auger C, Belcastro E, Park H, Lee H, Schini-Kerth VB. Potential mechanisms underlying cardiovascular protection by polyphenols: Role of the endothelium. Free Radic Biol Med 2018; S0891-5849: 30121-30127
    PubMedGoogle Scholar
  • 33 Wagner H. Multitarget therapy-the future of treatment for more than just functional dyspepsia. Phytomedicine 2006; 13: 122-129
    CrossrefPubMedGoogle Scholar
  • 34 Schillaci G, Vaudo G, Reboldi G, Verdecchia P, Lupattelli G, Pasqualini L, Porcellati C, Mannarino E. High-density lipoprotein cholesterol and left ventricular hypertrophy in essential hypertension. J Hypertens 2001; 19: 2265-2270
    CrossrefPubMedGoogle Scholar
  • 35 Kannel WB. Prevalence and natural history of electrocardiographic left ventricular hypertrophy. Am J Med 1983; 75: 4-11
    PubMedGoogle Scholar
  • 36 Levy D, Labib SB, Anderson KM, Christiansen JC, Kannel WB, Castelli WP. Determinants of sensitivity and specificity of eletrocardiographic criteria for left ventricular hypertrophy. Circulation 1990; 81: 815-820
    CrossrefPubMedGoogle Scholar
  • 37 Brugada P, Brugada J, Mont L, Smeets J, Andries EW. A new approach to the differential diagnosis of a regular tachycardia with a wide QRS complex. Circulation 1991; 83: 1649-1659
    CrossrefPubMedGoogle Scholar
  • 38 Giordano FJ. Oxygen oxidative stress, hypoxia, and heart failure. J Clin Invest 2005; 115: 500-508
    CrossrefPubMedGoogle Scholar
  • 39 Tsutsui H, Kinugawa S, Matsushima S. Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol 2011; 301: H2181-H2190
    CrossrefPubMedGoogle Scholar
  • 40 Ng TB, Liu F, Wang ZT. Antioxidative activity of natural products from plants. Life Sci 2000; 66: 709-723
    CrossrefPubMedGoogle Scholar
  • 41 Ota H, Eto M, Kano MR. Induction of endothelial nitric oxide synthase, SIRT1, and catalase by statins inhibits endothelial senescence through the Akt pathway. Arterioscler Thromb Vasc Biol 2010; 30: 2205-2211
    CrossrefPubMedGoogle Scholar
  • 42 Barboza LN, Lívero FA, Prando TB, Ribeiro Rde C, Lourenço EL, Budel JM, de Souza LM, Acco A, Dalsenter PR, Gasparotto Junior A. Atheroprotective effects of Cuphea carthagenensis (Jacq.) J. F. Macbr. in New Zealand rabbits fed with cholesterol-rich diet. J Ethnopharmacol 2016; 187: 134-145
    CrossrefPubMedGoogle Scholar
  • 43 Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of LDL cholesterol in plasma, without use of the preparative ultra-centrifuge. Clin Chem 1972; 18: 499-502
    CrossrefPubMedGoogle Scholar
  • 44 Gao SJ, Zhao GC, Luo GM, Yang TS, Shen JC. Antioxidant effects of superoxide dismutase and horseradish peroxidase on lipid peroxidation. Ann N Y Acad Sci 1998; 864: 284-287
    CrossrefPubMedGoogle Scholar
  • 45 Jiang ZY, Hunt JV, Wolff SP. Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein. Anal Biochem 1992; 202: 384-389
    CrossrefPubMedGoogle Scholar
  • 46 Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellmanʼs reagent. Anal Biochem 1968; 25: 192-205
    CrossrefPubMedGoogle Scholar
  • 47 Bradford 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: 248-254
    CrossrefPubMedGoogle Scholar