Anti-atherosclerotic effects of a phytoestrogen-rich herbal preparation in postmenopausal women

International Journal of Molecular Sciences

Volumn 17, Issue 8, 2016, Pages

  Myasoedova, Veronika A ^a,b   Kirichenko, Tatyana V ^c   Melnichenko, Alexandra A ^b   Orekhova, Varvara A ^c,d   Ravani, Alessio ^a   Poggio, Paolo ^a   Sobenin, Igor A ^b,d   Bobryshev, Yuri V ^b,e,f   Orekhov, Alexander N ^b,c,g  

^a CENTRO CARDIOLOGICO MONZINO   (Italy)

^b INSTITUTE OF GENERAL PATHOLOGY AND PATHOPHYSIOLOGY   (Russian Federation)

^c Institute for Atherosclerosis Research   (Russian Federation)

^d INSTITUTE OF EXPERIMENTAL CARDIOLOGY   (Russian Federation)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f UNIVERSITY OF WESTERN SYDNEY   (Australia)

^g MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Atherosclerosis; Herbal preparation; Intimal medial thickens; Isoflavonoids; Menopause; Phytoestrogens; Prevention

Indexed keywords

DAIDZEIN; FLAVONE; GENISTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PHYTOESTROGEN; PLACEBO; POLYPHENOL; PROCYANIDIN; RESVERATROL; TRIACYLGLYCEROL; ISOFLAVONE DERIVATIVE; PLANT MEDICINAL PRODUCT;

ADULT; AGED; ANTHROPOMETRIC PARAMETERS; ARTERIAL WALL THICKNESS; ARTICLE; ATHEROSCLEROSIS; CAMELLIA SINENSIS; CARDIOVASCULAR RISK; CONTROLLED STUDY; DIETARY INTAKE; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; ECHOGRAPHY; FEMALE; FOLLOW UP; GARLIC; GRAPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMULUS LUPULUS; MAJOR CLINICAL STUDY; MENOPAUSAL SYNDROME; PROGNOSIS; RANDOMIZED CONTROLLED TRIAL; BLOOD; CARDIOVASCULAR DISEASES; DRUG EFFECTS; MIDDLE AGED; POSTMENOPAUSE;

AGED; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; DOUBLE-BLIND METHOD; FEMALE; HUMANS; ISOFLAVONES; MIDDLE AGED; PHYTOESTROGENS; PLANT PREPARATIONS; POSTMENOPAUSE; TRIGLYCERIDES;

EID: 84981516946     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17081318     Document Type: Article

References (61)

1. Rossi, R.; Grimaldi, T.; Origliani, G.; Fantini, G.; Coppi, F.; Modena, M.G. Menopause and cardiovascular risk. Pathophysiol. Haemost. Thromb. 2002, 32, 325–328.
2. Rossi, R.; Cioni, E.; Nuzzo, A.; Origliani, G.; Modena, M.G. Endothelial-dependent vasodilation and incidence of type 2 diabetes in a population of healthy postmenopausal women. Diabetes Care 2005, 28, 702–707.
3. Hulley, S.; Grady, D.; Bush, T.; Furberg, C.; Herrington, D.; Riggs, B.; Vittinghoff, E. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. Heart and Estrogen/progestin Replacement Study (HERS) Research Group. J. Am. Med. Assoc. 1998, 280, 605–613.
4. Grady, D.; Herrington, D.; Bittner, V.; Blumenthal, R.; Davidson, M.; Hlatky, M.; Hsia, J.; Hulley, S.; Herd, A.; Khan, S.; et al. HERS Research Group. Cardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/progestin Replacement Study follow-up (HERS II). J. Am. Med. Assoc. 2002, 288, 49–57.
5. Gompel, A.; Santen, R.J. Hormone therapy and breast cancer risk 10 years after the WHI. Climacteric 2012, 15, 241–249.
6. Justenhoven, C.; Obazee, O.; Brauch, H. The pharmacogenomics of sex hormone metabolism: Breast cancer risk in menopausal hormone therapy. Pharmacogenomics 2012, 13, 659–675.
7. Rossouw, J.E.; Anderson, G.L.; Prentice, R.L.; LaCroix, A.Z.; Kooperberg, C.; Stefanick, M.L.; Jackson, R.D.; Beresford, S.A.; Howard, B.V.; Johnson, K.C. et al. Writing Group for the Women's Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: Principal results from the Women’s Health Initiative randomized controlled trial. J. Am. Med. Assoc. 2002, 288, 321–333.
8. Rossouw, J.E.; Prentice, R.L.; Manson, J.E.; Wu, L.; Barad, D.; Barnabei, V.M.; Ko, M.; LaCroix, A.Z.; Margolis, K.L.; Stefanick, M.L. Postmenopausal hormone therapy and risk of cardiovascular disease by age and years since menopause. J. Am. Med. Assoc. 2007, 297, 1465–1477.
9. Manson, J.E.; Chlebowski, R.T.; Stefanick, M.L.; Aragaki, A.K.; Rossouw, J.E.; Prentice, R.L.; Anderson, G.; Howard, B.V.; Thomson, C.A.; LaCroix, A.Z. et al. Menopausal hormone therapy and health outcomes during the intervention and extended poststopping phases of the Women's Health Initiative randomized trials. J. Am. Med. Assoc. 2013, 310, 1353–1368.
10. American College of Obstetricians and Gynecologists Committee on Gynecologic Practice. ACOG Committee Opinion No. 420, November 2008: Hormone therapy and heart disease. Obstet. Gynecol. 2008, 112, 1189–1192.
11. Mosca, L.; Benjamin, E.J.; Berra, K.; Bezanson, J.L.; Dolor, R.J.; Lloyd-Jones, D.M.; Newby, L.K.; Piña I.L.; Roger, V.L.; Shaw, L.J. et al. Effectiveness-based guidelines for the prevention of cardiovascular disease in women -2011 Update: A Guideline from the American Heart Association. Circulation 2011, 123, 1243–1262
12. Glazier, M.G.; Bowman, M.A. A review of the evidence for the use of phytoestrogens as a replacement for traditional estrogen replacement therapy. Arch. Intern. Med. 2001, 161, 1161–7112.
13. Sandoval, M.J.; Cutini, P.H.; Rauschemberger, M.B.; Massheimer, V.L. The soyabean isoflavone genistein modulates endothelial cell behaviour. Br. J. Nutr. 2010, 104, 171–179.
14. Finking, G.; Wohlfrom, M.; Lenz, C.; Wolkenhauer, M.; Eberle, C.; Hanke, H. The phytoestrogens genistein and daidzein, and 17 beta-estradiol inhibit development of neointima in aortas from male and female rabbits in vitro after injury. Coron. Artery Dis. 1999, 10, 607–615.
15. Shen, J.; White, M.; Husband, A.J.; Hambly, B.D.; Bao, S. Phytoestrogen derivatives differentially inhibit arterial neointimal proliferation in a mouse model. Eur. J. Pharmacol. 2006, 548, 123–128.
16. Safari, M.R.; Sheikh, N. Effects of flavonoids on the susceptibility of low-density lipoprotein to oxidative modification. Prostaglandins Leukot. Essent. Fatty Acids 2003, 69, 73–77.
17. Nikitina, N.A.; Sobenin, I.A.; Myasoedova, V.A.; Korennaya, V.V.; Mel’nichenko, A.A.; Khalilov, E.M.; Orekhov, A.N. Antiatherogenic effect of grape flavonoids in an ex vivo model. Bull. Exp. Biol. Med. 2006, 141, 712–715.
18. Guo, Y.; Wu, G.; Su, X.; Yang, H.; Zhang, J. Antiobesity action of a daidzein derivative on male obese mice induced by a high-fat diet. Nutr. Res. 2009, 29, 656–663.
19. Cao, C.; Li, S.; Dai, X.; Chen, Y.; Feng, Z.; Zhao, Y.; Wu, J. Genistein inhibits proliferation and functions of hypertrophic scar fibroblasts. Burns 2009, 35, 89–97.
20. Dharmappa, K.K.; Mohamed, R.; Shivaprasad, H.V.; Vishwanath, B.S. Genistein, a potent inhibitor of secretory phospholipase A2: A new insight in down regulation of inflammation. Inflammopharmacology 2010, 18, 25–31.
21. Lee, C.S.; Kwon, S.J.; Na, S.Y.; Lim, S.P.; Lee, J.H. Genistein supplementation inhibits atherosclerosis with stabilization of the lesions in hypercholesterolemic rabbits. J. Korean Med. Sci. 2004, 19, 656–661.
22. Wang, Z.; Zou, J.; Cao, K.; Hsieh, T.C.; Huang, Y.; Wu, J.M. Dealcoholized red wine containing known amounts of resveratrol suppresses atherosclerosis in hypercholesterolemic rabbits without affecting plasma lipid levels. Int. J. Mol. Med. 2005, 16, 533–540.
23. Zou, J.; Huang, Y.; Cao, K.; Yang, G.; Yin, H.; Len, J.; Hsieh, T.C.; Wu, J.M. Effect of resveratrol on intimal hyperplasia after endothelial denudation in an experimental rabbit model. Life Sci. 2000, 68, 153–163.
24. Brito, P.; Almeida, L.M.; Dinis, T.C. The interaction of resveratrol with ferrylmyoglobin and peroxynitrite; protection against LDL oxidation. Free Radic. Res. 2002, 36, 621–631.
25. Stein, J.H.; Korcarz, C.E.; Post, W.S. Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: Summary and discussion of the American Society of Echocardiography consensus statement. Prev. Cardiol. 2009, 12, 34–38.
26. Amato, M.; Montorsi, P.; Ravani, A.; Oldani, E.; Galli, S.; Ravagnani, P.M.; Tremoli, E.; Baldassarre, D. Carotid intima-media thickness by B-mode ultrasound as surrogate of coronary atherosclerosis: Correlation with quantitative coronary angiography and coronary intravascular ultrasound findings. Eur. Heart J. 2007, 28, 2094–2101.
27. Chambless, L.E.; Heiss, G.; Folsom, A.R.; Rosamond, W.; Szklo, M.; Sharrett, A.R.; Clegg, L.X. Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: The Atherosclerosis Risk in Communities (ARIC) Study, 1987–1993. Am. J. Epidemiol. 1997, 146, 483–494.
28. Hodis, H.N.; Mack, W.J.; Kono, N.; Azen, S.P.; Shoupe, D.; Hwang-Levine, J.; Petitti, D.; Whitfield-Maxwell, L.; Yan, M.; Franke, A.A. et al. Women’s Isoflavone Soy Health Research Group. Isoflavone soy protein supplementation and atherosclerosis progression in healthy postmenopausal women: A randomized controlled trial. Stroke 2011, 42, 3168–3175.
29. Hodis, H.N.; Mack, W.J.; Henderson, V.W.; Shoupe, D.; Budoff, M.J.; Hwang-Levine, J.; Li, Y.; Feng, M.; Dustin, L.; Kono, N. et al. ELITE Research Group. Vascular effects of early versus late postmenopausal treatment with estradiol. N. Engl. J. Med. 2016, 374, 1221–1231.
30. Harman, S.M. Effects of oral conjugated estrogen or transdermal estradiol plus oral progesterone treatment on common carotid artery intima media thickness (CIMT) and coronary artery calcium (CAC) in menopausal women: Initial results from the Kronos Early Estrogen Prevention Study (KEEPS). Menopause 2012, 19, 1365.
31. Colacurci, N.; Fornaro, F.; Cobellis, L.; de Franciscis, P.; Torella, M.; Sepe, E.; Arciello, A.; Cacciapuoti, F.; Paolisso, G.; Manzella, D. Raloxifene slows down the progression of intima-media thickness in postmenopausal women. Menopause 2007, 14, 879–884.
32. Bairey Merz, C.N.; Johnson, B.D.; Braunstein, G.D.; Pepine, C.J.; Reis, S.E.; Paul-Labrador, M.; Hale, G.; Sharaf, B.L.; Bittner, V.; Sopko, G. et al. Phytoestrogens and lipoproteins in women. J. Clin. Endocrinol. Metab. 2006, 91, 2209–2213.
33. Crouse, J.R., 3rd; Morgan, T.; Terry, J.G.; Ellis, J.; Vitolins, M.; Burke, G.L. A randomized trial comparing the effect of casein with that of soy protein containing varying amounts of isoflavones on plasma concentrations of lipids and lipoproteins. Arch. Intern. Med. 1999, 159, 2070–2076.
34. Sobenin, I.A.; Chistiakov, D.A.; Bobryshev, Y.V.; Orekhov, A.N. Blood atherogenicity as a target for anti-atherosclerotic therapy. Curr. Pharm. Des. 2013, 19, 5954–5962.
35. Myasoedova, V.A.; Sobenin, I.A. Background, rationale and design of clinical study of the effect of isoflavonoid-rich botanicals on natural history of atherosclerosis in women. Atheroscler. Suppl. 2008, 9, 171.
36. Lorenz, M.W.; Markus, H.S.; Bots, M.L.; Rosvall, M.; Sitzer, M. Prediction of clinical cardiovascular events with carotid intima-media thickness: A systematic review and meta-analysis. Circulation 2007, 115, 459–467.
37. Rossi, R.; Nuzzo, A.; Olaru, A.I.; Origliani, G.; Modena, M.G. Endothelial function affects early carotid atherosclerosis progression in hypertensive postmenopausal women. J. Hypertens. 2011, 29, 1136–1144.
38. Wang, H.; Liu, Y.; Zhu, L.; Wang, W.; Wan, Z.; Chen, F.; Wu, Y.; Zhou, J.; Yuan, Z. 17β-estradiol promotes cholesterol efflux from vascular smooth muscle cells through a liver X receptor α-dependent pathway. Int. J. Mol. Med. 2014, 33, 550–558.
39. Seli, E.; Selam, B.; Mor, G.; Kayisli, U.A.; Pehlivan, T.; Arici, A. Estradiol regulates monocyte chemotactic protein-1 in human coronary artery smooth muscle cells: A mechanism for its antiatherogenic effect. Menopause 2001, 8, 296–301.
40. O’Sullivan, M.G.; Goodrich, J.A.; Adams, M.R. Increased prostacyclin synthesis by atherosclerotic arteries from estrogen-treated monkeys. Life Sci. 2001, 69, 395–401.
41. Honisett, S.Y.; Stojanovska, L.; Sudhir, K.; Kingwell, B.A.; Dawood, T.; Komesaroff, P.A. Hormone therapy impairs endothelial function in postmenopausal women with type 2 diabetes mellitus treated with rosiglitazone. J. Clin. Endocrinol. Metab. 2004, 89, 4615–4619.
42. Gourdy, P.; Schambourg, A.; Filipe, C.; Douin-Echinard, V.; Garmy-Susini, B.; Calippe, B.; Tercé, F.; Bayard, F.; Arnal, J.F. Transforming growth factor activity is a key determinant for the effect of estradiol on fatty streak deposit in hypercholesterolemic mice. Arterioscler. Thromb. Vasc. Biol. 2007, 27, 2214–2221.
43. Sun, J.; Ma, X.; Chen, Y.X.; Rayner, K.; Hibbert, B.; McNulty, M.; Dhaliwal, B.; Simard, T.; Ramirez, D.; O’Brien, E. Attenuation of atherogenesis via the anti-inflammatory effects of the selective estrogen receptor beta modulator 8β-VE2. J. Cardiovasc. Pharmacol. 2011, 58, 399–405.
44. Chacko, B.K.; Chandler, R.T.; Mundhekar, A.; Khoo, N.; Pruitt, H.M.; Kucik, D.F.; Parks, D.A.; Kevil, C.G.; Barnes, S.; Patel, R.P. Revealing anti-inflammatory mechanisms of soy isoflavones by flow: Modulation of leukocyte-endothelial cell interactions. Am. J. Physiol. Heart Circ. Physiol. 2005, 289, H908–H915.
45. Simoncini, T.; Garibaldi, S.; Fu, X.D.; Pisaneschi, S.; Begliuomini, S.; Baldacci, C.; Lenzi, E.; Goglia, L.; Giretti, M.S.; Genazzani, A.R. Effects of phytoestrogens derived from red clover on atherogenic adhesion molecules in human endothelial cells. Menopause 2008, 15, 542–550.
46. Andrade, C.M.; Sá, M.F.; Toloi, M.R. Effects of phytoestrogens derived from soy bean on expression of adhesion molecules on HUVEC. Climacteric 2012, 15, 186–194.
47. Liu, T.; Hou, D.D.; Zhao, Q.; Liu, W.; Zhen, P.P.; Xu, J.P.; Wang, K.; Huang, H.X.; Li, X.; Zhang, H.; et al. Phytoestrogen α-Zearalanol attenuates homocysteine-induced apoptosis in human umbilical vein endothelial cells. BioMed Res. Int. 2013, 2013, 813450.
48. Orekhov, A.N.; Sobenin, I.A.; Korneev, N.V.; Kirichenko, T.V.; Myasoedova, V.A.; Melnichenko, A.A.; Balcells, M.; Edelman, E.R.; Bobryshev, Y.V. Anti-atherosclerotic therapy based on botanicals. Recent Pat. Cardiovasc. Drug Discov. 2013, 8, 56–66.
49. Sobenin, I.A.; Myasoedova, V.A.; Orekhov, A.N. Phytoestrogen-rich dietary supplements in anti-atherosclerotic therapy in postmenopausal women. Curr. Pharm. Des. 2016, 22, 152–163.
50. Alder, E. The Blatt-Kupperman menopausal index: A critique. Maturitas 1998, 29, 19–24.
51. Harman, S.M.; Brinton, E.A.; Cedars, M.; Lobo, R.; Manson, J.E.; Merriam, G.R.; Miller, V.M.; Naftolin, F.; Santoro, N. KEEPS: The Kronos Early Estrogen Prevention Study. Climacteric 2005, 8, 3–12.
52. Artom, N.; Montecucco, F.; Dallegri, F.; Pende, A. Carotid atherosclerotic plaque stenosis: The stabilizing role of statins. Eur. J. Clin. Investig. 2014, 44, 1122–1134.
53. Huang, Y.; Li, W.; Dong, L.; Li, R.; Wu, Y. Effect of statin therapy on the progression of common carotid artery intima-media thickness: An updated systematic review and meta-analysis of randomized controlled trials. J. Atheroscler. Thromb. 2013, 20, 108–121.
54. Papanas, N.; Maltezos, E. Oral antidiabetic agents: Anti-atherosclerotic properties beyond glucose lowering? Curr. Pharm. Des. 2009, 15, 3179–3192.
55. Katakami, N.; Kaneto, H.; Matsuhisa, M.; Shimomura, I.; Yamasaki, Y. Effects of glimepiride and glibenclamide on carotid atherosclerosis in type 2 diabetic patients. Diabetes Res. Clin. Pract. 2011, 92, e20–e22.
56. Mackinnon, A.D.; Jerrard-Dunne, P.; Sitzer, M.; Buehler, A.; von Kegler, S.; Markus, H.S. Rates and determinants of site-specific progression of carotid artery intima-media thickness: The carotid atherosclerosis progression study. Stroke 2004, 35, 2150–2154.
57. Koyasu, M.; Ishii, H.; Watarai, M.; Takemoto, K.; Inden, Y.; Takeshita, K.; Amano, T.; Yoshikawa, D.; Matsubara, T.; Murohara, T. Impact of acarbose on carotid intima-media thickness in patients with newly diagnosed impaired glucose tolerance or mild type 2 diabetes mellitus: A one-year, prospective, randomized, open-label, parallel-group study in Japanese adults with established coronary artery disease. Clin. Ther. 2010, 32, 1610–1617.
58. Odell, P.M.; Anderson, K.M.; Kannel, W.B. New models for predicting cardiovascular events. J. Clin. Epidemiol. 1994, 47, 583–592.
59. Tunstall-Pedoe, H.; Kuulasmaa, K.; Mähönen, M.; Tolonen, H.; Ruokokoski, E.; Amouyel, P. Contribution of trends in survival and coronary-event rates to changes in coronary heart disease mortality: 10-year results from 37 WHO MONICA project populations. Monitoring trends and determinants in cardiovascular disease. Lancet 1999, 353, 1547–1557.
60. Salonen, R.; Nyyssönen, K.; Porkkala, E.; Rummukainen, J.; Belder, R.; Park, J.S.; Salonen, J.T. Kuopio Atherosclerosis Prevention Study (KAPS). A population-based primary preventive trial of the effect of LDL lowering on atherosclerotic progression in carotid and femoral arteries. Circulation 1995, 92, 1758–1764.
61. Baldassarre, D.; Nyyssönen, K.; Rauramaa, R.; de Faire, U.; Hamsten, A.; Smit, A.J.; Mannarino, E.; Humphries, S.E.; Giral, P.; Grossi, E. et al. IMPROVE study group. Cross-sectional analysis of baseline data to identify the major determinants of carotid intima-media thickness in a European population: The IMPROVE study. Eur. Heart J. 2010, 31, 614–622.