Beneficial Effects of Pomegranate Fruit Consumption in Cardiovascular Diseases Prevention

Authors

  • L. Benchagra Department of Biology, Polydisciplinary Faculty, University Sultan Moulay Slimane, Beni Mellal, Morocco
  • A. Hajjaji Department of Biology, Polydisciplinary Faculty, University Sultan Moulay Slimane, Beni Mellal, Morocco
  • M. Ramchoun Department of Biology, Polydisciplinary Faculty, University Sultan Moulay Slimane, Beni Mellal, Morocco
  • A. Khalil Department of Medicine, Geriatrics Service, Faculty of Medicine and Health Sciences, University of Sherbrooke, Canada
  • H. Berrougui Department of Biology, Polydisciplinary Faculty, University Sultan Moulay Slimane, Beni Mellal, Morocco

DOI:

https://doi.org/10.6000/1929-5634.2018.07.03.3

Keywords:

Pomegranate, atherosclerosis, antioxidants, cardiovascular diseases, oxidation.

Abstract

Oxidative stress, dyslipidemia, hypercoagulability, endothelial dysfunction and inflammation are key elements in the development of atherosclerosis. Oxidative stress has been implicated as well in most of the key steps in the pathophysiology of atherosclerosis and the consequential clinical manifestations of cardiovascular diseases. In addition to the formation of atherosclerosis, oxidative stress acute thrombotic events, including dyslipidemia, the oxidation of low-density lipoproteins (LDLs) and plaque rupture leading to atherothrombosis and myocardial infarction. In the last decades, multiple experimental studies and clinical trials have demonstrated that diet plays a central role in the prevention of atherosclerosis. Pomegranate (Punica granatum L.) is one of nature’s most concentrated sources of antioxidants. It contains some very potent antioxidants (i.e. tannins, anthocyanins and flavonoids), which provide a wide spectrum of action against free radicals and are considered to be potent anti-atherogenic products. These properties make pomegranate a healthy fruit with a high potential in preventing cardiovascular diseases. In this review, we give an overview on the newest insights in the role of pomegranate in therapy of vascular diseases.

References

Legein B, Temmerman L, Biessen EAL, Lutgens E. Inflammation and immune system interactions in atherosclerosis. Cell Mol Life Sci 2013; 70: 3847-69. https://doi.org/10.1007/s00018-013-1289-1 DOI: https://doi.org/10.1007/s00018-013-1289-1

Grassi D, Desideri G, Ferri C. Flavonoids: Antioxidants Against Atherosclerosis. Nutrients 2010; 2: 889-902. https://doi.org/10.3390/nu2080889 DOI: https://doi.org/10.3390/nu2080889

Steinbrecher UP, Parthasarathy S, Leake DS, Witztum JL, Steinberg D. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc Natl Acad Sci 1984; 81: 3883-7. https://doi.org/10.1073/pnas.81.12.3883 DOI: https://doi.org/10.1073/pnas.81.12.3883

Lusis AJ. Atherosclerosis. Nature 2000; 407: 233-41. https://doi.org/10.1038/35025203 DOI: https://doi.org/10.1038/35025203

Chuang C-C, McIntosh MK. Potential Mechanisms by Which Polyphenol-Rich Grapes Prevent Obesity-Mediated Inflammation and Metabolic Diseases. Annu Rev Nutr 2011; 31: 155-76. https://doi.org/10.1146/annurev-nutr-072610-145149 DOI: https://doi.org/10.1146/annurev-nutr-072610-145149

Ebrahimi A, Schluesener H. Natural polyphenols against neurodegenerative disorders: Potentials and pitfalls. Ageing Res Rev 2012; 11: 329-45. https://doi.org/10.1016/j.arr.2012.01.006 DOI: https://doi.org/10.1016/j.arr.2012.01.006

Zern TL, Wood RJ, Greene C, West KL, Liu Y, Aggarwal D, et al. Grape Polyphenols Exert a Cardioprotective Effect in Pre- and Postmenopausal Women by Lowering Plasma Lipids and Reducing Oxidative Stress. J Nutr 2005; 135: 1911-7. https://doi.org/10.1093/jn/135.8.1911 DOI: https://doi.org/10.1093/jn/135.8.1911

Castilla P, Echarri R, Dávalos A, Cerrato F, Ortega H, Teruel JL, et al. Concentrated red grape juice exerts antioxidant, hypolipidemic, and antiinflammatory effects in both hemodialysis patients and healthy subjects. Am J Clin Nutr 2006; 84: 252-62. https://doi.org/10.1093/ajcn/84.1.252 DOI: https://doi.org/10.1093/ajcn/84.1.252

Schroeter H, Heiss C, Balzer J, Kleinbongard P, Keen CL, Hollenberg NK, et al. (-)-Epicatechin mediates beneficial effects of flavanol-rich cocoa on vascular function in humans. Proc Natl Acad Sci 2006; 103: 1024-9. https://doi.org/10.1073/pnas.0510168103 DOI: https://doi.org/10.1073/pnas.0510168103

Widlansky ME, Duffy SJ, Hamburg NM, Gokce N, Warden BA, Wiseman S, et al. Effects of black tea consumption on plasma catechins and markers of oxidative stress and inflammation in patients with coronary artery disease. Free Radic Biol Med 2005; 38: 499-506. https://doi.org/10.1016/j.freeradbiomed.2004.11.013 DOI: https://doi.org/10.1016/j.freeradbiomed.2004.11.013

Asgary S, Javanmard S, Zarfeshany A. Potent health effects of pomegranate. Adv Biomed Res 2014; 3: 100. https://doi.org/10.4103/2277-9175.129371 DOI: https://doi.org/10.4103/2277-9175.129371

Howell AB, D’Souza DH. The Pomegranate: Effects on Bacteria and Viruses That Influence Human Health. Evid Based Complement Alternat Med 2013; 2013: 1-11. https://doi.org/10.1155/2013/606212 DOI: https://doi.org/10.1155/2013/606212

Rom O, Aviram M. Paraoxsonase2 (PON2) and oxidative stress involvement in pomegranate juice protection against cigarette smoke-induced macrophage cholesterol accumulation. Chem Biol Interact 2016; 259: 394-400. https://doi.org/10.1016/j.cbi.2016.05.009 DOI: https://doi.org/10.1016/j.cbi.2016.05.009

Rojanathammanee L, Puig KL, Combs CK. Pomegranate Polyphenols and Extract Inhibit Nuclear Factor of Activated T-Cell Activity and Microglial Activation In vitro and in a Transgenic Mouse Model of Alzheimer Disease. J Nutr 2013; 143: 597-605. https://doi.org/10.3945/jn.112.169516 DOI: https://doi.org/10.3945/jn.112.169516

Yuan T, Ma H, Liu W, Niesen DB, Shah N, Crews R, et al. Pomegranate’s Neuroprotective Effects against Alzheimer’s Disease Are Mediated by Urolithins, Its Ellagitannin-Gut Microbial Derived Metabolites. ACS Chem Neurosci 2016; 7: 26-33. https://doi.org/10.1021/acschemneuro.5b00260 DOI: https://doi.org/10.1021/acschemneuro.5b00260

Lansky EP, Newman RA. Punica granatum (pomegranate) and its potential for prevention and treatment of inflammation and cancer. J Ethnopharmacol 2007; 109: 177-206. https://doi.org/10.1016/j.jep.2006.09.006 DOI: https://doi.org/10.1016/j.jep.2006.09.006

Celik I, Temur A, Isik I. Hepatoprotective role and antioxidant capacity of pomegranate (Punica granatum) flowers infusion against trichloroacetic acid-exposed in rats. Food Chem Toxicol 2009; 47: 145-9. https://doi.org/10.1016/j.fct.2008.10.020 DOI: https://doi.org/10.1016/j.fct.2008.10.020

Kulkarni AP, Mahal HS, Kapoor S, Aradhya SM. In vitro Studies on the Binding, Antioxidant, and Cytotoxic Actions of Punicalagin. J Agric Food Chem 2007; 55: 1491-500. https://doi.org/10.1021/jf0626720 DOI: https://doi.org/10.1021/jf0626720

Faria A, Calhau C. The Bioactivity of Pomegranate: Impact on Health and Disease. Crit Rev Food Sci Nutr 2011; 51: 626-34. https://doi.org/10.1080/10408391003748100 DOI: https://doi.org/10.1080/10408391003748100

Cerdá B, Cerón JJ, Tomás-Barberán FA, Espín JC. Repeated Oral Administration of High Doses of the Pomegranate Ellagitannin Punicalagin to Rats for 37 Days Is Not Toxic. J Agric Food Chem 2003; 51: 3493-501. https://doi.org/10.1021/jf020842c DOI: https://doi.org/10.1021/jf020842c

Larrosa M, González-Sarrías A, García-Conesa MT, Tomás-Barberán FA, Espín JC. Urolithins, Ellagic Acid-Derived Metabolites Produced by Human Colonic Microflora, Exhibit Estrogenic and Antiestrogenic Activities. J Agric Food Chem 2006; 54: 1611-20. https://doi.org/10.1021/jf0527403 DOI: https://doi.org/10.1021/jf0527403

Gil MI, Tomás-Barberán FA, Hess-Pierce B, Holcroft DM, Kader AA. Antioxidant Activity of Pomegranate Juice and Its Relationship with Phenolic Composition and Processing. J Agric Food Chem 2000; 48: 4581-9. https://doi.org/10.1021/jf000404a DOI: https://doi.org/10.1021/jf000404a

Amakura Y, Okada M, Tsuji S, Tonogai Y. High-performance liquid chromatographic determination with photodiode array detection of ellagic acid in fresh and processed fruits. J Chromatogr A 2000; 896: 87-93. https://doi.org/10.1016/S0021-9673(00)00414-3 DOI: https://doi.org/10.1016/S0021-9673(00)00414-3

Huang T, Peng G, Kota B, Li G, Yamahara J, Roufogalis B, et al. Anti-diabetic action of flower extract: Activation of PPAR-γ and identification of an active component. Toxicol Appl Pharmacol 2005; 207: 160-9. https://doi.org/10.1016/j.taap.2004.12.009 DOI: https://doi.org/10.1016/j.taap.2004.12.009

Mphahlele RR, Stander MA, Fawole OA, Opara UL. Effect of fruit maturity and growing location on the postharvest contents of flavonoids, phenolic acids, vitamin C and antioxidant activity of pomegranate juice (cv. Wonderful). Sci Hortic 2014; 179: 36-45. https://doi.org/10.1016/j.scienta.2014.09.007 DOI: https://doi.org/10.1016/j.scienta.2014.09.007

Fanali C, Belluomo MG, Cirilli M, Cristofori V, Zecchini M, Cacciola F, et al. Antioxidant activity evaluation and HPLC-photodiode array/MS polyphenols analysis of pomegranate juice from selected italian cultivars: A comparative study: General. Electrophoresis 2016; 37: 1947-55. https://doi.org/10.1002/elps.201500501 DOI: https://doi.org/10.1002/elps.201500501

Wang R-F, Xie W-D, Zhang, Xing D-M, Ding Y, Wang W, et al. Bioactive Compounds from the Seeds of Punica g ranatum (Pomegranate). J Nat Prod 2004; 67: 2096-8. https://doi.org/10.1021/np0498051 DOI: https://doi.org/10.1021/np0498051

Jain V. Isolation and Standardization of Various Phytochemical Constituents from Methanolic Extracts of Fruit Rinds of Punica granatum. Chin J Nat Med 2011: 8.

Wafa BA, Makni M, Ammar S, Khannous L, Hassana AB, Bouaziz M, et al. Antimicrobial effect of the Tunisian Nana variety Punica granatum L. extracts against Salmonella enterica (serovars Kentucky and Enteritidis) isolated from chicken meat and phenolic composition of its peel extract. Int J Food Microbiol 2017; 241: 123-31. https://doi.org/10.1016/j.ijfoodmicro.2016.10.007 DOI: https://doi.org/10.1016/j.ijfoodmicro.2016.10.007

Amakura Y, Okada M, Tsuji S, Tonogai Y. Determination of phenolic acids in fruit juices by isocratic column liquid chromatography. J Chromatogr A 2000; 891: 183-8. https://doi.org/10.1016/S0021-9673(00)00625-7 DOI: https://doi.org/10.1016/S0021-9673(00)00625-7

Lantzouraki DZ, Sinanoglou VJ, Zoumpoulakis PG, Glamočlija J, Ćirić A, Soković M, et al. Antiradical-antimicrobial activity and phenolic profile of pomegranate (Punica granatum L.) juices from different cultivars: a comparative study. RSC Adv 2015; 5: 2602-14. https://doi.org/10.1039/C4RA11795F DOI: https://doi.org/10.1039/C4RA11795F

Ehling S, Cole S. Analysis of Organic Acids in Fruit Juices by Liquid Chromatography−Mass Spectrometry: An Enhanced Tool for Authenticity Testing. J Agric Food Chem 2011; 59: 2229-34. https://doi.org/10.1021/jf104527e DOI: https://doi.org/10.1021/jf104527e

de Pascual-Teresa S, Santos-Buelga C, Rivas-Gonzalo JC. Quantitative Analysis of Flavan-3-ols in Spanish Foodstuffs and Beverages. J Agric Food Chem 2000; 48: 5331-7. https://doi.org/10.1021/jf000549h DOI: https://doi.org/10.1021/jf000549h

Ambigaipalan P, de Camargo AC, Shahidi F. Phenolic Compounds of Pomegranate Byproducts (Outer Skin, Mesocarp, Divider Membrane) and Their Antioxidant Activities. J Agric Food Chem 2016; 64: 6584-604. https://doi.org/10.1021/acs.jafc.6b02950 DOI: https://doi.org/10.1021/acs.jafc.6b02950

Borges G, Crozier A. HPLC-PDA-MS fingerprinting to assess the authenticity of pomegranate beverages. Food Chem 2012; 135: 1863-7. https://doi.org/10.1016/j.foodchem.2012.05.108 DOI: https://doi.org/10.1016/j.foodchem.2012.05.108

Lingling Han, Zhaohe Yuan, Lijuan Feng, Yanlei Yin. Changes in the composition and contents of pomegranate polyphenols during fruit DEVELOPMENT. Acta Hortic 2015: 53-61. DOI: https://doi.org/10.17660/ActaHortic.2015.1089.5

van Elswijk DA, Schobel UP, Lansky EP, Irth H, van der Greef J. Rapid dereplication of estrogenic compounds in pomegranate (Punica granatum) using on-line biochemical detection coupled to mass spectrometry. Phytochemistry 2004; 65: 233-41. https://doi.org/10.1016/j.phytochem.2003.07.001 DOI: https://doi.org/10.1016/j.phytochem.2003.07.001

Nawwar MAM, Hussein SAM, Merfort I. Leaf phenolics of Punica granatum. Phytochemistry 1994; 37: 1175-7. https://doi.org/10.1016/S0031-9422(00)89552-7 DOI: https://doi.org/10.1016/S0031-9422(00)89552-7

Anibal PC, Peixoto ITA, Foglio MA, Höfling JF. Antifungal activity of the ethanolic extracts of Punica granatum L. and evaluation of the morphological and structural modifications of its compounds upon the cells of Candida spp. Braz J Microbiol 2013; 44: 839-48. https://doi.org/10.1590/S1517-83822013005000060 DOI: https://doi.org/10.1590/S1517-83822013005000060

Tzulker R, Glazer I, Bar-Ilan I, Holland D, Aviram M, Amir R. Antioxidant Activity, Polyphenol Content, and Related Compounds in Different Fruit Juices and Homogenates Prepared from 29 Different Pomegranate Accessions. J Agric Food Chem 2007; 55: 9559-70. https://doi.org/10.1021/jf071413n DOI: https://doi.org/10.1021/jf071413n

Noda Y, Kaneyuki T, Mori A, Packer L. Antioxidant Activities of Pomegranate Fruit Extract and Its Anthocyanidins: Delphinidin, Cyanidin, and Pelargonidin. J Agric Food Chem 2002; 50: 166-71. https://doi.org/10.1021/jf0108765 DOI: https://doi.org/10.1021/jf0108765

Fischer UA, Carle R, Kammerer DR. Identification and quantification of phenolic compounds from pomegranate (Punica granatum L.) peel, mesocarp, aril and differently produced juices by HPLC-DAD-ESI/MSn. Food Chem 2011; 127: 807-21. https://doi.org/10.1016/j.foodchem.2010.12.156 DOI: https://doi.org/10.1016/j.foodchem.2010.12.156

Slavin JL, Lloyd B. Health Benefits of Fruits and Vegetables. Adv Nutr 2012; 3: 506-16. https://doi.org/10.3945/an.112.002154 DOI: https://doi.org/10.3945/an.112.002154

Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: How are they linked? Free Radic Biol Med 2010; 49: 1603-16. https://doi.org/10.1016/j.freeradbiomed.2010.09.006 DOI: https://doi.org/10.1016/j.freeradbiomed.2010.09.006

Harman D. Aging: A Theory Based on Free Radical and Radiation Chemistry. J Gerontol 1956; 11: 298-300. https://doi.org/10.1093/geronj/11.3.298 DOI: https://doi.org/10.1093/geronj/11.3.298

Beckman KB, Ames BN. The Free Radical Theory of Aging Matures. Physiol Rev 1998; 78: 547-81. https://doi.org/10.1152/physrev.1998.78.2.547 DOI: https://doi.org/10.1152/physrev.1998.78.2.547

Sestili P, Martinelli C, Ricci D, Fraternale D, Bucchini A, Gia-mperi L, et al. Cytoprotective effect of preparations from var-ious parts of Punica granatum L. fruits in oxidatively injured mammalian cells in comparison with their antioxidant cap-acity in cell free systems. Pharmacol Res 2007; 56: 18-26. https://doi.org/10.1016/j.phrs.2007.02.003 DOI: https://doi.org/10.1016/j.phrs.2007.02.003

Seeram NP, Aviram M, Zhang Y, Henning SM, Feng L, Dreher M, et al. Comparison of Antioxidant Potency of Commonly Consumed Polyphenol-Rich Beverages in the United States. J Agric Food Chem 2008; 56: 1415-22. https://doi.org/10.1021/jf073035s DOI: https://doi.org/10.1021/jf073035s

Fu L, Xu B-T, Xu X-R, Gan R-Y, Zhang Y, Xia E-Q, et al. Antioxidant capacities and total phenolic contents of 62 fruits. Food Chem 2011; 129: 345-50. https://doi.org/10.1016/j.foodchem.2011.04.079 DOI: https://doi.org/10.1016/j.foodchem.2011.04.079

Javad Mottaghipisheh, Mehdi Ayanmanesh, Ramin Babadayei-Samani, Alireza Javid, Mina Sanaeifard SV, Marcello Iriti. Total anthocyanin, flavonoid, polyphenol and tannin contents of seven pomegranate cultivars grown in Iran [pdf]. Acta Sci Pol Technol Aliment 2018; 17: 211-7. https://doi.org/10.17306/J.AFS.2018.0584 DOI: https://doi.org/10.17306/J.AFS.2018.0584

Aviram M, Rosenblat M. Pomegranate Protection against Cardiovascular Diseases. Evid Based Complement Alternat Med 2012; 2012: 1-20. https://doi.org/10.1155/2012/382763 DOI: https://doi.org/10.1155/2012/382763

Masci A, Coccia A, Lendaro E, Mosca L, Paolicelli P, Cesa S. Evaluation of different extraction methods from pomegranate whole fruit or peels and the antioxidant and antiproliferative activity of the polyphenolic fraction. Food Chem 2016; 202: 59-69. https://doi.org/10.1016/j.foodchem.2016.01.106 DOI: https://doi.org/10.1016/j.foodchem.2016.01.106

Saußele S, Berger U, Aul C, Büchner T, Döhner H, Ehninger G, et al. Klinische Forschung im Kompetenznetz „Akute und chronische Leukämien“. Med Klin 2006; 101: 414-20. https://doi.org/10.1007/s00063-006-1056-2 DOI: https://doi.org/10.1007/s00063-006-1056-2

Seeram NP, Lee R, Heber D. Bioavailability of ellagic acid in human plasma after consumption of ellagitannins from pomegranate (Punica granatum L.) juice. Clin Chim Acta 2004; 348: 63-8. https://doi.org/10.1016/j.cccn.2004.04.029 DOI: https://doi.org/10.1016/j.cccn.2004.04.029

Kalaycıoğlu Z, Erim FB. Total phenolic contents, antioxidant activities, and bioactive ingredients of juices from pomegranate cultivars worldwide. Food Chem 2017; 221: 496-507. https://doi.org/10.1016/j.foodchem.2016.10.084 DOI: https://doi.org/10.1016/j.foodchem.2016.10.084

de Nigris F, Williams-Ignarro S, Botti C, Sica V, Ignarro LJ, Napoli C. Pomegranate juice reduces oxidized low-density lipoprotein downregulation of endothelial nitric oxide synthase in human coronary endothelial cells. Nitric Oxide 2006; 15: 259-63. https://doi.org/10.1016/j.niox.2005.12.004 DOI: https://doi.org/10.1016/j.niox.2005.12.004

Aviram M, Dornfeld L, Rosenblat M, Volkova N, Kaplan M, Coleman R, et al. Pomegranate juice consumption reduces oxidative stress, atherogenic modifications to LDL, and platelet aggregation: studies in humans and in atherosclerotic apolipoprotein E-deficient mice. Am J Clin Nutr 2000; 71: 1062-76. https://doi.org/10.1093/ajcn/71.5.1062 DOI: https://doi.org/10.1093/ajcn/71.5.1062

Aviram M, Rosenblat M, Gaitini D, Nitecki S, Hoffman A, Dornfeld L, et al. Pomegranate juice consumption for 3 years by patients with carotid artery stenosis reduces common carotid intima-media thickness, blood pressure and LDL oxidation. Clin Nutr 2004; 23: 423-33. https://doi.org/10.1016/j.clnu.2003.10.002 DOI: https://doi.org/10.1016/j.clnu.2003.10.002

Basu A, Penugonda K. Pomegranate juice: a heart-healthy fruit juice. Nutr Rev 2009; 67: 49-56. https://doi.org/10.1111/j.1753-4887.2008.00133.x DOI: https://doi.org/10.1111/j.1753-4887.2008.00133.x

Khateeb J, Gantman A, Kreitenberg AJ, Aviram M, Fuhrman B. Paraoxonase 1 (PON1) expression in hepatocytes is upregulated by pomegranate polyphenols: A role for PPAR-γ pathway. Atherosclerosis 2010; 208: 119-25. https://doi.org/10.1016/j.atherosclerosis.2009.08.051 DOI: https://doi.org/10.1016/j.atherosclerosis.2009.08.051

Davidson MH, Maki KC, Dicklin MR, Feinstein SB, Witchger M, Bell M, et al. Effects of Consumption of Pomegranate Juice on Carotid Intima-Media Thickness in Men and Women at Moderate Risk for Coronary Heart Disease. Am J Cardiol 2009; 104: 936-42. https://doi.org/10.1016/j.amjcard.2009.05.037 DOI: https://doi.org/10.1016/j.amjcard.2009.05.037

Kaplan M, Hayek T, Raz A, Coleman R, Dornfeld L, Vaya J, et al. Pomegranate Juice Supplementation to Atherosclerotic Mice Reduces Macrophage Lipid Peroxidation, Cellular Cholesterol Accumulation and Development of Atherosclerosis. J Nutr 2001; 131: 2082-9. https://doi.org/10.1093/jn/131.8.2082 DOI: https://doi.org/10.1093/jn/131.8.2082

Al-Jarallah A, Igdoura F, Zhang Y, Tenedero CB, White EJ, MacDonald ME, et al. The effect of pomegranate extract on coronary artery atherosclerosis in SR-BI/APOE double knockout mice. Atherosclerosis 2013; 228: 80-9. https://doi.org/10.1016/j.atherosclerosis.2013.02.025 DOI: https://doi.org/10.1016/j.atherosclerosis.2013.02.025

Berrougui H, Loued S, Khalil A. Purified human paraoxonase-1 interacts with plasma membrane lipid rafts and mediates cholesterol efflux from macrophages. Free Radic Biol Med 2012; 52: 1372-81. https://doi.org/10.1016/j.freeradbiomed.2012.01.019 DOI: https://doi.org/10.1016/j.freeradbiomed.2012.01.019

Fuhrman B, Volkova N, Aviram M. Pomegranate juice polyphenols increase recombinant paraoxonase-1 binding to

high-density lipoprotein: Studies in vitro and in diabetic patients. Nutrition 2010; 26: 359-66. https://doi.org/10.1016/j.nut.2009.05.003 DOI: https://doi.org/10.1016/j.nut.2009.05.003

Parsaeyan N, Mozaffari-Khosravi H, Mozayan M. Effect of pomegranate juice on paraoxonase enzyme activity in patients with type 2 diabetes. J Diabetes Metab Disord 2012; 11: 11. https://doi.org/10.1186/2251-6581-11-11 DOI: https://doi.org/10.1186/2251-6581-11-11

Estrada-Luna D, Martínez-Hinojosa E, Cancino-Diaz JC, Belefant-Miller H, López-Rodríguez G, Betanzos-Cabrera G. Daily supplementation with fresh pomegranate juice increases paraoxonase 1 expression and activity in mice fed a high-fat diet. Eur J Nutr 2018; 57: 383-9. https://doi.org/10.1007/s00394-017-1394-2 DOI: https://doi.org/10.1007/s00394-017-1394-2

Aviram M, Kaplan M, Rosenblat M, Fuhrman B. Dietary Antioxidants and Paraoxonases Against LDL Oxidation and Atherosclerosis Development. In: von Eckardstein A, editor. Atheroscler. Diet Drugs, vol. 170, Berlin, Heidelberg: Springer Berlin Heidelberg; 2005, p. 263-300. https://doi.org/10.1007/3-540-27661-0_9 DOI: https://doi.org/10.1007/3-540-27661-0_9

Zhao S, Li J, Wang L, Wu X. Pomegranate peel polyphenols inhibit lipid accumulation and enhance cholesterol efflux in raw264.7 macrophages. Food Funct 2016; 7: 3201-10. https://doi.org/10.1039/C6FO00347H DOI: https://doi.org/10.1039/C6FO00347H

Fuhrman B, Volkova N, Aviram M. Pomegranate juice inhibits oxidized LDL uptake and cholesterol biosynthesis in macrophages. J Nutr Biochem 2005; 16: 570-6. https://doi.org/10.1016/j.jnutbio.2005.02.009 DOI: https://doi.org/10.1016/j.jnutbio.2005.02.009

Liu R, Li J, Cheng Y, Huo T, Xue J, Liu Y, et al. Effects of ellagic acid-rich extract of pomegranates peel on regulation of cholesterol metabolism and its molecular mechanism in hamsters. Food Funct 2015; 6: 780-7. https://doi.org/10.1039/C4FO00759J DOI: https://doi.org/10.1039/C4FO00759J

Ricci D, Giamperi L, Bucchini A, Fraternale D. Antioxidant activity of Punica granatum fruits. Fitoterapia 2006; 77: 310-2. https://doi.org/10.1016/j.fitote.2006.01.008 DOI: https://doi.org/10.1016/j.fitote.2006.01.008

Les F, Prieto JM, Arbonés-Mainar JM, Valero MS, López V. Bioactive properties of commercialised pomegranate (Punica granatum) juice: antioxidant, antiproliferative and enzyme inhibiting activities. Food Funct 2015; 6: 2049-57. https://doi.org/10.1039/C5FO00426H DOI: https://doi.org/10.1039/C5FO00426H

Arun KB, Jayamurthy P, Anusha CV, Mahesh SK, Nisha P. Studies on Activity Guided Fractionation of Pomegranate Peel Extracts and Its Effect on Antidiabetic and Cardiovascular Protection Properties: Pomegranate peel against diabetes and allied issues. J Food Process Preserv 2017; 41: e13108. https://doi.org/10.1111/jfpp.13108 DOI: https://doi.org/10.1111/jfpp.13108

Mohan M, Waghulde H, Kasture S. Effect of pomegranate juice on Angiotensin II-induced hypertension in diabetic wistar rats. Phytother Res 2010; 24: S196-203. https://doi.org/10.1002/ptr.3090 DOI: https://doi.org/10.1002/ptr.3090

dos Santos RL, Dellacqua LO, Delgado NTB, Rouver WN, Podratz PL, Lima LCF, et al. Pomegranate peel extract attenuates oxidative stress by decreasing coronary angiotensin-converting enzyme (ACE) activity in hypertensive female rats. J Toxicol Environ Health A 2016; 79: 998-1007. https://doi.org/10.1080/15287394.2016.1213690 DOI: https://doi.org/10.1080/15287394.2016.1213690

Huang TH-W, Peng G, Kota BP, Li GQ, Yamahara J, Roufogalis BD, et al. Pomegranate flower improves cardiac lipid metabolism in a diabetic rat model: role of lowering circulating lipids. Br J Pharmacol 2005; 145: 767-74. https://doi.org/10.1038/sj.bjp.0706245 DOI: https://doi.org/10.1038/sj.bjp.0706245

Shiner M, Fuhrman B, Aviram M. Macrophage paraoxonase 2 (PON2) expression is up-regulated by pomegranate juice phenolic anti-oxidants via PPARγ and AP-1 pathway activation. Atherosclerosis 2007; 195: 313-21. https://doi.org/10.1016/j.atherosclerosis.2007.01.007 DOI: https://doi.org/10.1016/j.atherosclerosis.2007.01.007

Cairns JA. The coxibs and traditional nonsteroidal anti-inflammatory drugs: A current perspective on cardiovascular risks. Can J Cardiol 2007; 23: 125-31. https://doi.org/10.1016/S0828-282X(07)70732-8 DOI: https://doi.org/10.1016/S0828-282X(07)70732-8

Kalliolias GD, Ivashkiv LB. TNF biology, pathogenic mechanisms and emerging therapeutic strategies. Nat Rev Rheumatol 2016; 12: 49-62. https://doi.org/10.1038/nrrheum.2015.169 DOI: https://doi.org/10.1038/nrrheum.2015.169

Barnes PJ. How corticosteroids control inflammation: Quintiles Prize Lecture 2005: Corticosteroids and inflammation. Br J Pharmacol 2009; 148: 245-54. https://doi.org/10.1038/sj.bjp.0706736 DOI: https://doi.org/10.1038/sj.bjp.0706736

Kawaii S, Lansky EP. Differentiation-Promoting Activity of Pomegranate ( Punica granatum ) Fruit Extracts in HL-60 Human Promyelocytic Leukemia Cells. J Med Food 2004; 7: 13-8. https://doi.org/10.1089/109662004322984644 DOI: https://doi.org/10.1089/109662004322984644

Afaq F, Saleem M, Krueger CG, Reed JD, Mukhtar H. Anthocyanin- and hydrolyzable tannin-rich pomegranate fruit extract modulates MAPK and NF-?B pathways and inhibits skin tumorigenesis in CD-1 mice. Int J Cancer 2005; 113: 423-33. https://doi.org/10.1002/ijc.20587 DOI: https://doi.org/10.1002/ijc.20587

Seeram N, Adams L, Henning S, Niu Y, Zhang Y, Nair M, et al. In vitro antiproliferative, apoptotic and antioxidant activities of punicalagin, ellagic acid and a total pomegranate tannin extract are enhanced in combination with other polyphenols as found in pomegranate juice. J Nutr Biochem 2005; 16: 360-7. https://doi.org/10.1016/j.jnutbio.2005.01.006 DOI: https://doi.org/10.1016/j.jnutbio.2005.01.006

Pacheco-Palencia LA, Noratto G, Hingorani L, Talcott ST, Mertens-Talcott SU. Protective Effects of Standardized Pomegranate ( Punica granatum L.) Polyphenolic Extract in Ultraviolet-Irradiated Human Skin Fibroblasts. J Agric Food Chem 2008; 56: 8434-41. https://doi.org/10.1021/jf8005307 DOI: https://doi.org/10.1021/jf8005307

Zhong X, Shi Y, Chen J, Xu J, Wang L, Beier RC, et al. Polyphenol Extracts from Punica granatum and Terminalia chebula Are Anti-inflammatory and Increase the Survival Rate of Chickens Challenged with Escherichia coli. Biol Pharm Bull 2014; 37: 1575-82. https://doi.org/10.1248/bpb.b14-00163 DOI: https://doi.org/10.1248/bpb.b14-00163

Park S, Seok JK, Kwak JY, Suh H-J, Kim YM, Boo YC. Anti-Inflammatory Effects of Pomegranate Peel Extract in THP-1 Cells Exposed to Particulate Matter PM10. Evid Based Complement Alternat Med 2016; 2016: 1-11. https://doi.org/10.1155/2016/6836080 DOI: https://doi.org/10.1155/2016/6836080

Xu J, Zhao Y, Aisa HA. Anti-inflammatory effect of pomegranate flower in lipopolysaccharide (LPS)-stimulated RAW264.7 macrophages. Pharm Biol 2017; 55: 2095-101. https://doi.org/10.1080/13880209.2017.1357737 DOI: https://doi.org/10.1080/13880209.2017.1357737

Marques L, Pinheiro A, Araújo J, de Oliveira R, Silva S, Abreu I, et al. Anti-Inflammatory Effects of a Pomegranate Leaf Extract in LPS-Induced Peritonitis. Planta Med 2016; 82: 1463-7. https://doi.org/10.1055/s-0042-108856 DOI: https://doi.org/10.1055/s-0042-108856

Bachoual R, Talmoudi W, Boussetta T, Braut F, El-Benna J. An aqueous pomegranate peel extract inhibits neutrophil myeloperoxidase in vitro and attenuates lung inflammation in mice. Food Chem Toxicol 2011; 49: 1224-8. https://doi.org/10.1016/j.fct.2011.02.024 DOI: https://doi.org/10.1016/j.fct.2011.02.024

Mo J, Panichayupakaranant P, Kaewnopparat N, Songkro S, Reanmongkol W. Topical Anti-inflammatory Potential of Standardized Pomegranate Rind Extract and Ellagic Acid in Contact Dermatitis: Standardized pomegranate rind extract for contact dermatitis. Phytother Res 2014; 28: 629-32. https://doi.org/10.1002/ptr.5039 DOI: https://doi.org/10.1002/ptr.5039

de Nigris F, Balestrieri ML, Williams-Ignarro S, D’Armiento FP, Fiorito C, Ignarro LJ, et al. The influence of pomegranate fruit extract in comparison to regular pomegranate juice and seed oil on nitric oxide and arterial function in obese Zucker rats. Nitric Oxide 2007; 17: 50-4. https://doi.org/10.1016/j.niox.2007.04.005 DOI: https://doi.org/10.1016/j.niox.2007.04.005

Shishehbor F, Mohammad shahi M, Zarei M, Saki A, Zakerkish M, Shirani F, et al. Effects of Concentrated Pomegranate Juice on Subclinical Inflammation and Cardiometabolic Risk Factors for Type 2 Diabetes: A Quasi-Experimental Study. Int J Endocrinol Metab 2016; 14. DOI: https://doi.org/10.5812/ijem.33835

Shema-Didi L, Sela S, Ore L, Shapiro G, Geron R, Moshe G, et al. One year of pomegranate juice intake decreases oxidative stress, inflammation, and incidence of infections in hemodialysis patients: A randomized placebo-controlled trial. Free Radic Biol Med 2012; 53: 297-304. https://doi.org/10.1016/j.freeradbiomed.2012.05.013 DOI: https://doi.org/10.1016/j.freeradbiomed.2012.05.013

Labsi M, Khelifi L, Mezioug D, Soufli I, Touil-Boukoffa C. Antihydatic and immunomodulatory effects of Punica granatum peel aqueous extract in a murine model of echinococcosis. Asian Pac J Trop Med 2016; 9: 211-20. https://doi.org/10.1016/j.apjtm.2016.01.038 DOI: https://doi.org/10.1016/j.apjtm.2016.01.038

Malik A. Prostate Cancer Prevention Through Pomegranate Fruit. Cell Cycle n.d.: 3.

Paller CJ, Ye X, Wozniak PJ, Gillespie BK, Sieber PR, Greengold RH, et al. A randomized phase II study of pomegranate extract for men with rising PSA following initial therapy for localized prostate cancer. Prostate Cancer Prostatic Dis 2013; 16: 50-5. https://doi.org/10.1038/pcan.2012.20 DOI: https://doi.org/10.1038/pcan.2012.20

Pantuck AJ. Phase II Study of Pomegranate Juice for Men with Rising Prostate-Specific Antigen following Surgery or Radiation for Prostate Cancer. Clin Cancer Res 2006; 12: 4018-26. https://doi.org/10.1158/1078-0432.CCR-05-2290 DOI: https://doi.org/10.1158/1078-0432.CCR-05-2290

Adams LS, Seeram NP, Aggarwal BB, Takada Y, Sand D, Heber D. Pomegranate Juice, Total Pomegranate Ellagitannins, and Punicalagin Suppress Inflammatory Cell Signaling in Colon Cancer Cells. J Agric Food Chem 2006; 54: 980-5. https://doi.org/10.1021/jf052005r DOI: https://doi.org/10.1021/jf052005r

Moazzen H, Alizadeh M. Effects of Pomegranate Juice on Cardiovascular Risk Factors in Patients with Metabolic Syndrome: a Double-Blinded, Randomized Crossover Controlled Trial. Plant Foods Hum Nutr 2017; 72: 126-33. https://doi.org/10.1007/s11130-017-0605-6 DOI: https://doi.org/10.1007/s11130-017-0605-6

Braidy N, Essa MM, Poljak A, Selvaraju S, Al-Adawi S, Manivasagm T, et al. Consumption of pomegranates improves synaptic function in a transgenic mice model of Alzheimer’ s disease. Oncotarget 2016; 7. DOI: https://doi.org/10.18632/oncotarget.10905

Essa MM, Subash S, Akbar M, Al-Adawi S, Guillemin GJ. Long-Term Dietary Supplementation of Pomegranates, Figs and Dates Alleviate Neuroinflammation in a Transgenic Mouse Model of Alzheimer’s Disease. PLOS ONE 2015; 10: e0120964. https://doi.org/10.1371/journal.pone.0120964 DOI: https://doi.org/10.1371/journal.pone.0120964

Tapias V, Cannon JR, Greenamyre JT. Pomegranate juice exacerbates oxidative stress and nigrostriatal degeneration in Parkinson’s disease. Neurobiol Aging 2014; 35: 1162-76. https://doi.org/10.1016/j.neurobiolaging.2013.10.077 DOI: https://doi.org/10.1016/j.neurobiolaging.2013.10.077

Downloads

Published

2019-01-18

How to Cite

Benchagra, L., Hajjaji, A., Ramchoun, M., Khalil, A., & Berrougui, H. (2019). Beneficial Effects of Pomegranate Fruit Consumption in Cardiovascular Diseases Prevention. Journal of Nutritional Therapeutics, 7(3), 84–94. https://doi.org/10.6000/1929-5634.2018.07.03.3

Issue

Section

Articles