Antithrombotic activity of flavonoids and polyphenols rich plant species

1. E. J. Benjamin, P. Muntner, A. Alonso, M. S. Bittencourt, C. W. Callaway, A. P. Carson, A. M. Chamberlain, A. R. Chang, S. Cheng, S. R. Das, F. N. Delling, L. Djousse, M. S. V. Elkind, J. F. Ferguson, M. Fornage, L. C. Jordan, S. S. Khan, B. M. Kissela, K. L. Knutson, T. W. Kwan, D. T. Lackland, T. T. Lewis, J. H. Lichtman, C. T. Longenecker, M. S. Loop, P. L. Lutsey, S. S. Martin, K. Matsushita, A. E. Moran, M. E. Mussolino, M. O’Flaherty, A. Pandey, A. M. Perak, W. D. Rosamond, G. A. Roth, U. K. A. Sampson, G. M. Satou, E. B. Schroeder, S. H. Shah, N. L. Spartano, A. Stokes, D. L. Tirschwell, C. W. Tsao, M. P. Turakhia, L. B. VanWagner, J. T. Wilkins, S. S. Wong and S. S. Virani, Heart disease and stroke statistics-2019 update: A report from the American Heart Association, Circulation139 (2019) e56–e528; https://doi.org/10.1161/cir.000000000000065910.1161/CIR.0000000000000659Search in Google Scholar

2. M. J. Budoff, S. Achenbach, R. S. Blumenthal, J. J. Carr, J. G. Goldin, P. Greenland, A. D. Guerci, J. A. Lima, D. J. Rader, G. D. Rubin, L. J. Shaw and S. E. Wiegers, Assessment of coronary artery disease by cardiac computed tomography: a scientific statement from the American Heart Association Committee on Cardiovascular Imaging and Intervention, Council on Cardiovascular Radiology and Intervention, and Committee on Cardiac Imaging, Council on Clinical Cardiology, Circulation114 (2006) 1761–1791; https://doi.org/10.1161/circulationaha.106.17845810.1161/CIRCULATIONAHA.106.178458Search in Google Scholar

3. P. Greenland, J. S. Alpert, G. A. Beller, E. J. Benjamin, M. J. Budoff, Z. A. Fayad, E. Foster, M. A. Hlatky, J. M. Hodgson, F. G. Kushner, M. S. Lauer, L. J. Shaw, S. C. Smith, A. J. Taylor, W. S. Weintraub and N. K. Wenger, 2010 ACCF/AHA guideline for assessment of cardiovascular risk in asymptomatic adults: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, Circulation122 (2010) e584–e636; https://doi.org/10.1161/cir.0b013e3182051b4c10.1161/CIR.0b013e3182051b4cSearch in Google Scholar

4. D. L. Bhatt, Can clopidogrel and aspirin lower mortality in patients with acute myocardial infarction? Nat. Clin. Pract. Cardiovasc. Med.3 (2006) 182–183; https://doi.org/10.1038/ncpcardio050810.1038/ncpcardio0508Search in Google Scholar

5. J. Sullivan and N. Amarshi, Dual antiplatelet therapy with clopidogrel and aspirin, Am. J. Health Syst. Pharm.65 (2008) 1134–1143; https://doi.org/10.2146/ajhp06066210.2146/ajhp060662Search in Google Scholar

6. A. Algra and J. van Gijn, Is clopidogrel superior to aspirin in secondary prevention of vascular disease? Curr. Control Trials Cardiovasc. Med.1 (2000) 143–145; https://doi.org/10.1186/cvm-1-3-14310.1186/CVM-1-3-143Search in Google Scholar

7. A. Grzybowski and K. Pietrzak, Albert Szent-Györgyi (1893-1986): the scientist who discovered vitamin C, Clin. Dermatol.31 (2013) 327–331; https://doi.org/10.1016/j.clindermatol.2012.08.00110.1016/j.clindermatol.2012.08.001Search in Google Scholar

8. B. Havsteen, Flavonoids, a class of natural products of high pharmacological potency, Biochem. Pharmacol.32 (1983) 1141–1148; https://doi.org/10.1016/S0163-7258(02)00298-X10.1016/S0163-7258(02)00298-XSearch in Google Scholar

9. K. Janssen, R. P. Mensink, F. J. Cox, J. L. Harryvan, R. Hovenier, P. C. Hollman and M. B. Katan, Effects of the flavonoids quercetin and apigenin on hemostasis in healthy volunteers: results from an in vitro and a dietary supplement study, Am. J. Clin. Nutr.67 (1998) 255–262; https://doi.org/10.1093/ajcn/67.2.25510.1093/ajcn/67.2.2559459373Search in Google Scholar

10. U. T. Seyfert, H. Haubelt, A. Vogt and P. Hellstern, Variables influencing Multiplate whole blood impedance platelet aggregometry and turbidimetric platelet aggregation in healthy individuals, Platelets18 (2007) 199–206. https://doi.org/10.1080/0953710060094427710.1080/0953710060094427717497431Search in Google Scholar

11. M. Bojić, Ž. Debeljak, M. Medić-Šarić and M. Tomičić, Interference of selected flavonoid aglycons in platelet aggregation assay, Clin. Chem. Lab. Med.50 (2012) 1403–1408; https://doi.org/10.1515/cclm-2011-096010.1515/cclm-2011-0960Search in Google Scholar

12. M. Bojić, Ž. Debeljak, M. Tomičić, M. Medić-Šarić and S. Tomić, Evaluation of antiaggregatory activity of flavonoid aglycone series, Nutr. J.10 (2011) Article ID 73 (8 pages); https://doi.org/10.1186/1475-2891-10-7310.1186/1475-2891-10-73Search in Google Scholar

13. A. Calatzis, R. M. Loreth and M. Spannagl, Multiplate^®Platelet Function Analysis – Application and Interpretation, Dynabyte GmbH, Munich 2006.Search in Google Scholar

14. M. Bijak, A. Sut, A. Kosiorek, J. Saluk-Bijak and J. Golanski J, Dual anticoagulant/antiplatelet activity of polyphenolic grape seeds extract, Nutrients11 (2019) Article ID 93 (9 pages); https://doi.org/10.3390/nu1101009310.3390/nu11010093Search in Google Scholar

15. A. Meshkini and M. Tahmasbi, Antiplatelet aggregation activity of walnut hull extract via suppression of reactive oxygen species generation and caspase activation, J. Acupunct. Meridian Stud.10 (2017) 193–203; https://doi.org/10.1016/j.jams.2017.02.00710.1016/j.jams.2017.02.007Search in Google Scholar

16. E. K. Yoon, S. K. Ku, W. Lee, S. Kwak, H. Kang, B. Jung and S. Bae, Antitcoagulant and antiplatelet activities of scolymoside, BMB Rep.48 (2015) 577–582; https://doi.org/10.5483/BMBRep.2015.48.10.04410.5483/BMBRep.2015.48.10.044Search in Google Scholar

17. S. K. Ku and J. S. Bae, Antithrombotic activities of wogonin and wogonoside via inhibiting platelet aggregation, Fitoterapia98 (2014) 27–35; https://doi.org/10.1016/j.fitote.2014.07.00610.1016/j.fitote.2014.07.006Search in Google Scholar

18. W. Lee W and J. S. Bae, Antithrombotic and antiplatelet activities of vicenin-2, Blood Coagul. Fibrinolysis26 (2015) 628–634; https://doi.org/10.1097/MBC.000000000000032010.1097/MBC.0000000000000320Search in Google Scholar

19. A. Saija, M. Scalese, M. Lanza, D. Marzullo, F. Bonina and F. Castelli, Flavonoids as antioxidant agents: importance of their interaction with biomembranes, Free Radic. Biol. Med.19 (1995) 481‒486; https://doi.org/10.1016/0891-5849(94)00240-K10.1016/0891-5849(94)00240-KSearch in Google Scholar

20. A. Polette, D. Lemaitre, M. Lagarde and E. Véricel, n-3 fatty acid-induced lipid peroxidation in human platelets is prevented by catechins, Thromb. Haemost.75 (1996) 945‒949; https://doi.org/10.1055/s-0038-165039910.1055/s-0038-1650399Search in Google Scholar

21. T. J. Neiva, L. Morais, M. Polack, C. M. Simões and E. A. D’Amico, Effects of catechins on human blood platelet aggregation and lipid peroxidation, Phytother. Res.13 (1999) 597‒600; https://doi.org/10.1002/(SICI)1099-1573(199911)13:7<597::AID-PTR512>3.0.CO;2-Z10.1002/(SICI)1099-1573(199911)13:7<597::AID-PTR512>3.0.CO;2-ZSearch in Google Scholar

22. S. L. Hwang and G. C. Yen, Modulation of Akt, JNK, and p38 activation is involved in citrus flavonoid-mediated cytoprotection of PC12 cells challenged by hydrogen peroxide, J. Agric. Food. Chem.57 (2009) 2576‒2582; https://doi.org/10.1021/jf803360710.1021/jf803360719222219Search in Google Scholar

23. F. Orallo, E. Alvarez, H. Basaran and C. Lugnier, Comparative study of the vasorelaxant activity, superoxide-scavenging ability and cyclic nucleotide phosphodiesterase-inhibitory effects of hesperetin and hesperidin, Naunyn. Schmiedebergs Arch. Pharmacol.370 (2004) 452‒463; https://doi.org/10.1007/s00210-004-0994-610.1007/s00210-004-0994-615599707Search in Google Scholar

24. T. P. Dew, A. J. Day and M. R. Morgan, Xanthine oxidase activity in vitro: effects of food extracts and components, J. Agric. Food Chem.53 (2005) 6510‒6515; https://doi.org/10.1021/jf050716j10.1021/jf050716j16076142Search in Google Scholar

25. D. S. Chou, J. J. Lee, G. Hsiao, C. Y. Hsieh, Y. J. Tsai, T. F. Chen and J. R. Sheu, Baicalein induction of hydroxyl radical formation via 12-lipoxygenase in human platelets: an ESR study, J. Agric. Food Chem.55 (2007) 649‒655; https://doi.org/10.1021/jf062584f10.1021/jf062584f17263456Search in Google Scholar

26. Y. R. Jin, X. H. Han, Y. H. Zhang, J. J. Lee, Y. Lim, J. H. Chung and Y. P. Yun, Antiplatelet activity of hesperetin, a bioflavonoid, is mainly mediated by inhibition of PLC-gamma2 phosphorylation and cyclooxygenase-1 activity, Atherosclerosis194 (2007) 144‒152; https://doi.org/10.1016/j.atherosclerosis.2006.10.01110.1016/j.atherosclerosis.2006.10.01117092506Search in Google Scholar

27. O. A. Ogunbayo, R. M. Harris, R. H. Waring, C. J. Kirk and F. Michelangeli, Inhibition of the sarcoplasmic/endoplasmic reticulum Ca²⁺-ATPase by flavonoids: a quantitative structure-activity relationship study, IUBMB Life60 (2008) 853‒858; https://doi.org/10.1002/iub.13210.1002/iub.13218785622Search in Google Scholar

28. G. P. Hubbard, S. Wolffram, J. A. Lovegrove and J. M. Gibbins, Ingestion of quercetin inhibits platelet aggregation and essential components of the collagen-stimulated platelet activation pathway in humans, J. Thromb. Haemost.2 (2004) 2138‒2145. https://doi.org/10.1111/j.1538-7836.2004.01067.x10.1111/j.1538-7836.2004.01067.x15613018Search in Google Scholar

29. B. Wright, L. A. Moraes, C. F. Kemp, W. Mullen, A. Crozier, J. A. Lovegrove and J. M. Gibbins, A structural basis for the inhibition of collagen-stimulated platelet function by quercetin and structurally related flavonoids, Br. J. Pharmacol.159 (2010) 1312‒1325; https://doi.org/10.1111/j.1476-5381.2009.00632.x10.1111/j.1476-5381.2009.00632.x284893520148891Search in Google Scholar

30. L. Liu, D. M. Xu and Y. Y. Cheng, Distinct effects of naringenin and hesperetin on nitric oxide production from endothelial cells, J. Agric. Food Chem.56 (2008) 824‒829; https://doi.org/10.1021/jf072300710.1021/jf072300718197618Search in Google Scholar

31. M. Dell’Agli, O. Maschi, G. V. Galli, R. Fagnani, E. Dal Cero, D. Caruso and E. Bosisio, Inhibition of platelet aggregation by olive oil phenols via cAMP-phosphodiesterase, Br. J. Nutr.99 (2008) 945‒951; https://doi.org/10.1017/S000711450783747010.1017/S000711450783747017927845Search in Google Scholar

32. J. H. Lee and G. H. Kim, Evaluation of antioxidant and inhibitory activities for different subclasses flavonoids on enzymes for rheumatoid arthritis, J. Food Sci.75 (2010) H212‒H217; https://doi.org/10.1111/j.1750-3841.2010.01755.x10.1111/j.1750-3841.2010.01755.xSearch in Google Scholar

33. J. Vibes, B. Lasserre, J. Gleye and C. Declume, Inhibition of thromboxane A2 biosynthesis in vitro by the main components of Crataegus oxyacantha (Hawthorn) flower heads, Prostaglandins Leukot. Essent. Fatty Acids50 (1994) 173‒175; https://doi.org/10.1016/0952-3278(94)90141-410.1016/0952-3278(94)90141-4Search in Google Scholar

34. I. Babić, M. Bojić, Ž. Maleš, R. Zadro, K. Gojčeta, I. Duka, H. Rimac and I. Jukić, Influence of flavonoids’ lipophilicity on platelet aggregation, Acta Pharm. 69 (2019) (this issue).10.2478/acph-2019-004031639087Search in Google Scholar

35. M. L. Liang, X. W. Da, A. D. He, G. Q. Yao, W. Xie, G. Liu, J. Z. Xiang and Z. Y. Ming, Pentamethylquercetin (PMQ) reduces thrombus formation by inhibiting platelet function, Sci. Rep.5 (2015) 11142 (11 pages); https://doi.org/10.1038/srep1114210.1038/srep11142446191926059557Search in Google Scholar

36. Ž. Maleš, A. Antolić, I. Babić, S. Jurić and M. Bojić, Quantitative analysis of phenolic acids and anti-platelet activity of Melissa officinalis leaf extracts, Nat. Prod. Commun.12 (2017) 93–94; https://doi.org/10.1177/1934578X170120012610.1177/1934578X1701200126Search in Google Scholar

37. O. Estrada, W. Contreras, G. Acha, E. Lucena, W. Venturini, A. Cardozo and C. Alvarado-Castillo, Chemical constituents from Licania cruegeriana and their cardiovascular and antiplatelet effects, Molecules19 (2014) 21215–21225; https://doi.org/10.3390/molecules19122121510.3390/molecules191221215627079025525822Search in Google Scholar

38. R. Kasimu, Z. Fan, X. Wang, J. Hu, P. Wang and J. Wang, Anti-platelet aggregation activities of different fractions in leaves of Apocynum venetum L., J. Ethnopharmacol.168 (2015) 116–121; https://doi.org/10.1016/j.jep.2015.03.0130378-8741Search in Google Scholar

39. J. Y. Ro, J. H. Ryu, H. J. Park and H. J. Cho, Onion (Allium cepa L.) peel extract has anti-platelet effects in rat platelets, Springerplus4 (2015) 17 (8 pages); https://doi.org/10.1186/s40064-015-0786-010.1186/s40064-015-0786-0430360225628983Search in Google Scholar

40. A. Antolić, Ž. Maleš, M. Tomičić and M. Bojić, The effect of short-toothed and Dalmatian sage extracts on platelet aggregation, Food Technol. Biotech.56 (2018) 265–269; https://doi.org/10.17113/ftb.56.02.18.547410.17113/ftb.56.02.18.5474611799530228801Search in Google Scholar

41. A. D. Assefa, E. Y. Ko, S. H. Moon and Y. S. Keum, Antioxidant and antiplatelet activities of flavonoid-rich fractions of three citrus fruits from Korea, 3 Biotech. 6 (2016) 109 (10 pages); https://doi.org/10.1007/s13205-016-0424-810.1007/s13205-016-0424-8483776428330179Search in Google Scholar

42. M. Bojić, A. Antolić, M. Tomičić, Ž. Debeljak and Ž. Maleš, Propolis ethanolic extracts reduce adenosine diphosphate induced platelet aggregation determined on whole blood, Nutr. J.17 (2018) 52 (8 pages); https://doi.org/10.1186/s12937-018-0361-y10.1186/s12937-018-0361-y595265029759064Search in Google Scholar

43. C. H. Lescano, F. Freitas de Lima, C. B. Mendes-Silvério, A. F. O. Justo, D. da Silva Baldivia, C. P. Vieira, E. J. Sanjinez-Argandoña, C. A. L. Cardoso, F. Z. Mónica and I. Pires de Oliveira, Effect of polyphenols from Campomanesia adamantium on platelet aggregation and inhibition of cyclooxygenases: Molecular docking and in vitro analysis, Front. Pharmacol.9 (2018) 617 (13 pages); https://doi.org/10.3389/fphar.2018.0061710.3389/fphar.2018.00617Search in Google Scholar

44. A. Mira, W. Alkhiary and K. Shimizu, Antiplatelet and anticoagulant activities of Angelica shikokiana extract and its isolated compounds, Clin. Appl. Thromb. Hemost.23 (2017) 91–99; https://doi.org/10.1177/107602961559587910.1177/1076029615595879Search in Google Scholar

45. A. A. Boligon, V. C. Pimentel, M. D. Bagatini and M. L. Athayde, Effect of Scutia buxifolia Reissek in nucleotidase activities and inhibition of platelet aggregation, J. Nat. Med.69 (2015) 46–54; https://doi.org/10.1007/s11418-014-0858-410.1007/s11418-014-0858-4Search in Google Scholar

46. S. U. Kwon, H. Y. Lee, M. Xin, S. J. Ji, H. K. Cho, D. S. Kim, D. K. Kim and Y. M. Lee, Antithrombotic activity of Vitis labrusca extract on rat platelet aggregation, Blood Coagul. Fibrin.27 (2016) 141–146; https://doi.org/10.1097/MBC.000000000000039410.1097/MBC.0000000000000394Search in Google Scholar

47. M. S. Rajput, N. Balekar and D. K. Jain, Inhibition of ADP-induced platelet aggregation and involvement of non-cellular blood chemical mediators are responsible for the antithrombotic potential of the fruits of Lagenaria siceraria, Chin. J. Nat. Med.12 (2014) 599–606; https://doi.org/10.1016/S1875-5364(14)60091-110.1016/S1875-5364(14)60091-1Search in Google Scholar

48. J. Rywaniak, B. Luzak, A. Podsedek, D. Dudzinska, M. Rozalski and C. Watala, Comparison of cytotoxic and anti-platelet activities of polyphenolic extracts from Arnica montana flowers and Juglans regia husks, Platelets26 (2015) 168–176; https://doi.org/10.3109/09537104.2014.89497010.3109/09537104.2014.89497024679412Search in Google Scholar

49. R. Zamora-Ros, V. Knaze, L. Luján-Barroso, N. Slimani, I. Romieu, V. Fedirko, M. S. Magistris, U. Ericson, P. Amiano, A. Trichopoulou, V. Dilis, A. Naska, D. Engeset, G. Skeie, A. Cassidy, K. Overvad, P. H. M. Peeters, J. M. Huerta, M.-J. Sánchez, J. R. Quirós, C. Sacerdote, S. Grioni, R. Tumino, G. Johansson, I. Johansson, I. Drake, F. L. Crowe, A. Barricarte, R. Kaaks, B. Teucher, H. B. Bueno-de-Mesquita, C. T. M. Rossum, T. Norat, D. Romaguera, A.-C. Vergnaud, A. Tjønneland, J. Halkjær, F. Clavel-Chapelon, M.-C. Boutron-Ruault, M. Touillaud, S. Salvini, K.-T. Khaw, N. Wareham, H. Boeing, J. Förster, E. Riboli and C. A. González, Estimated dietary intakes of flavonols, flavanones and flavones in the European Prospective Investigation into Cancer and Nutrition (EPIC) 24 hour dietary recall cohort, Br. J. Nutr.106 (2011) 1915–1925; https://doi.org/10.1017/S000711451100239X10.1017/S000711451100239X21679483Search in Google Scholar

50. P. C. Hollman, J. H. de Vries, S. D. van Leeuwen, M. J. Mengelers and M. B. Katan, Absorption of dietary quercetin glycosides and quercetin in healthy ileostomy volunteers, Am. J. Clin. Nutr.62 (1995) 1276‒1282; https://doi.org/10.1093/ajcn/62.6.127610.1093/ajcn/62.6.12767491892Search in Google Scholar

51. C. Manach, G. Williamson, C. Morand, A. Scalbert and C. Rémésy, Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies, Am. J. Clin. Nutr.81 (2005) 230S–242S; https://doi.org/10.1093/ajcn/81.1.230S10.1093/ajcn/81.1.230S15640486Search in Google Scholar

52. K. S. Krogholm, L. Bredsdorff, P. Knuthsen, J. Haraldsdóttir and S. E. Rasmussen, Relative bioavailability of the flavonoids quercetin, hesperetin and naringenin given simultaneously through diet, Eur. J. Clin. Nutr.64 (2010) 432–435; http://doi.org/10.1038/ejcn.2010.610.1038/ejcn.2010.620125185Search in Google Scholar

53. I. Palomo, A. Concha-Meyer, M. Lutz, M. Said, B. Sáez, A. Vásquez and E. Fuentes, Chemical characterization and antiplatelet potential of bioactive extract from tomato pomace (byproduct of tomato paste), Nutrients11 (2019) Article ID 456 (10 pages); https://doi.org/10.3390/nu1102045610.3390/nu11020456641268430813256Search in Google Scholar

54. T. Nickel, K. Lackermair, J. Scherr, A. Calatzis, M. Vogeser, H. Hanssen, G. Waidhauser, U. Schönermark, H. Methe, S. Horster, U. Wilbert-Lampen and M. Halle, Influence of high polyphenol beverage on stress-induced platelet activation, J. Nutr. Health Aging20 (2016) 586–593; https://doi.org/10.1007/s12603-016-0697-y10.1007/s12603-016-0697-y27273347Search in Google Scholar

55. K. Thompson, H. Hosking, W. Pederick, I. Singh and A. B. Santhakumar, The effect of anthocyanin supplementation in modulating platelet function in sedentary population: a randomised, double-blind, placebo-controlled, cross-over trial, Br. J. Nutr.118 (2017) 368–374; https://doi.org/10.1017/S000711451700212410.1017/S000711451700212428901892Search in Google Scholar

56. J. J. Peterson, J. T. Dwyer, P. F. Jacques and M. L. McCullough, Do flavonoids reduce cardiovascular disease incidence or mortality in US and European populations? Nutr. Rev.70 (2012) 491–508; https://doi.org/10.1111/j.1753-4887.2012.00508.x10.1111/j.1753-4887.2012.00508.x413017422946850Search in Google Scholar

57. Z. M. Wang, D. Zhao, Z. L. Nie, H. Zhao, B. Zhou, W. Gao, L. S. Wang and Z. J. Yang, Flavonol intake and stroke risk: a meta-analysis of cohort studies, Nutrition30 (2014) 518–523; https://doi.org/10.1016/j.nut.2013.10.00910.1016/j.nut.2013.10.00924342529Search in Google Scholar