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Bratisl Lek Listy 2002; 103 (4–5): 159–165 Effects of red wine polyphenolic compounds on the cardiovascular Institute of Normal and Pathological Physiology, Slovak Academy of Sciences, Bratislava, Phenolic phytochemicals are widely distributed in the plant kingdom. Regarding the protective effects on organisms, the polyphenol group is the most important. In different experiments, it has been shown that selected polyphenols, mainly flavonoids, possess protective effects on the cardiovascular system, as well as anticancer, antiviral and antiallergic properties. In coronary heart disease, the protective effects include mainly antithrombic, antioxidant, anti-ischaemic and vasorelaxant properties of flavonoids. It has been hypothesised that the phenomenon of a low incidence of coronary heart disease in French people may be partially related to the pharmacological properties of polyphenolic compounds included in red wine. Many epidemiological studies have shown that regular flavonoid intake is associated with reduced risk of cardiovascular diseases.
This review article discusses the chemical structure of polyphenols and their beneficial properties in the cardiovascular system. (Fig. 1, Ref. 74.) Key words: polyphenols, flavonoids, antithrombic effect, antioxidant activity, antiischaemic effect, Consumption of diets high in saturated fat and cholesterol is plant polyphenols is their antioxidant property that may explain associated with increased risk of cardiovascular disease. Howe- many of their beneficial effects on cardiovascular function ver, epidemiological evidence has shown that cardiovascular di- (4, 5, 6). Polyphenols also act on other targets involved in the sease is less prevalent in the French than expected in the light of metabolism of mammalian cells, including nitric oxide (NO), their saturated fat intake and serum cholesterol levels. This para- which by itself regulates haemostasis (7, 5), thrombus develop- doxical finding has been attributed to regular consumption of ment (8) and vascular tone (9, 10). The beneficial properties of fresh vegetables, fruit and red wine (1, 2).
NO may therefore explain in part the antiischaemic activities of Law and Wald (3), however, predicted that it would be only a matter of time before the “French paradox” resolved itself as The purpose of this review is to describe protective effects the only recently comparable pattern of risk factors (animal fat of red wine polyphenolic compounds on cardiovascular disea- consumption, serum cholesterol concentrations and blood pres- se, particularly their antithrombic, antioxidant, antiischaemic, sure) between France and Britain would become translated into vasorelaxant and antihypertensive properties and clinical ap- similar death rates from coronary disease. Although red wine consumption remains higher in France than in Britain, the au-thors rejected this as a possible explanation because they con- Institute of Normal and Pathological Physiology, Slovak Academy of sider that wine intake greater than one unit a day confers no greater benefit (3). However, the protective effect of moderate consump- Address for correspondence: Woineshet Zenebe, MVD, Institute of tion (2–3 units) of red wine on the risk of cardiovascular disease Normal and Pathological Physiology, SAV, Sienkiewiczova 1, SK-813 71 morbidity and mortality has been consistently seen in many epi- demiological studies (2). Phenolic compounds and especially a Phone: +421.2.52926271, Fax: +421.2.52968516 group of flavonoids seem to be responsible for the majority of This work was supported by The Slovak Grant Agency for Science, grants No. 2/7165/21 and 2/7240/21 and 2/7156/21.
the protective effects of red wine. One of the major activities of Bratisl Lek Listy 2002; 103 (4–5): 159–165 From the chemical point of view, natural polyphenols are derivatives of chroman. There is a wide range of polyphenols which have desirable biological properties for man. Among themare flavonoids, phenolic acids, 3,4-trihydroxystilbens and leu- Due to the beneficial effects on the cardiovascular system, the group of flavonoids has been the most studied. The presenceof over 4000 naturally available flavonoids is widespread among plants and plant products (5). Flavonoids are derivatives of phe-nylchroman. Depending on structural features, they can be divi- ded into different subgroups: flavanes, flavanones, flavones, fla-vonoles and anthocyanidins. The basic structure is comprised of two benzene rings linked through a heterocyclic pyran or pyronering in the middle (Fig. 1). Flavonoids and tocopherols (vitamin Fig. 1. The three ring structure of flavonoids.
E) share a common structure, i.e., the chromane ring (12). Fla-vonoids differ from one to another in the orientation of hydroxy- Other authors also reported that the position and degree of lation or methylation, in the position of benzoid substituent and hydroxylation is the key to the antioxidant activity of flavonoids in the degree of unsaturation. They usually occur in the form of (21, 22). Bors et al (23) and Sichel et al (24) generalised that for glycosides. The characteristics of flavonoids appear also to be flavonoids to accomplish radical scavenging activity they need required especially for their antioxidant and antiproliferative the o-dihydroxy structure in the B ring which gives a higher sta- bility to the radical form and participates in electron delocalisa- As mentioned in different works, polyphenols act as redu- tion. The 2,3 double bond in conjugation with a 4-oxo junction cing agents, hydrogen donating antioxidants and metal chela- in the C ring is responsible for electron delocalisation from the tors. Since little is known about the relationship between their B ring, while the 3- and 5-OH groups with 4-oxo junction are structure and antioxidant activity, Cao et al (14), Arora et al (15) responsible in A and C rings. It was also reported that glycosyla- and Wang and Joseph (16) examined structurally different poly- tion of flavonoids reduces their activity compared to the aglyco- phenols. They reported that hydroxyl substituents on the flavo- noid ring increased the antioxidant activity while substitution by It can be concluded that the structure of different favonoids methoxy groups decreased this activity. Mabry et al (17) and is responsible for their different reducing capacity and antioxi- Markham (18) reported the relationship between spectroscopic identification and structural characteristics of polyphenols. Ac-cording to their measurements, most flavones and flavonols showed two absorption bands in ultraviolet visible region, re-presenting B ring and A ring absorptions. They also observed Polyphenols have been shown to be able to modulate the pro- that an increase in the numbers of hydroxyl groups results in a cess of thrombosis in several systems. Fuster et al (25) reported red shift, for example, from 367 nm in kaempferol with hydroxyl that reduction of the rate of atherosclerosis and coronary heart substitutions in positions 3,5,7,4' to 371 nm in quercetin with disease caused by daily intake of flavonoids was based mainly on hydroxyl groups in positions 3,5,7,3',4'. The shorter wave length the ability of flavonoids to inhibit acute thrombus formation.
in flavones is the result of the absence of a 3-OH group in their In both platelets and leukocytes, interference with the ara- structure. In flavanones with a saturated heterocyclic C ring, chidonic acid metabolism has been demonstrated, resulting in lack of conjugation between ring A and B is defined by the inhibition of platelet aggregation and reduction of prothrombic very strong maximum UV spectra and with lower antioxidant and proinflammatory mediator synthesis in humans (26, 27) and also in experimental models (28, 29). In humans, Pace-Asciak et A flavonol, quercetin, has the same number of hydroxyl gro- al (27) showed that polyphenolic compounds from red wine, es- ups in the same positions as catechin which is a flavane, hence it pecially quercetin, catechin and resveratrol, inhibited the synthesis also contains the 2,3 double bond in the C ring and the 4-oxo of thromboxane in platelets and of leukotrien in neutrophils. In junction. This conjugation of 3-OH group with the 2,3-double their experiments, resveratrol and quercetin exhibited a dose- bond adjacent to the 4-carbonyl in the C ring gives to quercetin its dependent inhibition of thromboxane-induced and ADP-indu- antioxidant activity (19). Shahidi et al (20) and Rice Evans et al ced platelet aggregation, while epicatechin, α-tocopherol and bu- (19) reported that flavanones with only one hydroxyl group on the tylated hydroxytoluene were inactive. Trans-resveratrol also in- B ring possessed little antioxidant activity. As a result of the unsa- hibited the synthesis of thromboxane B , hydroxyheptadecatrie- turated heterocyclic ring quercetin has a two fold higher antioxi- noate, and slightly of 12-hydroxyeicosatetraenoate (12-HETE).
dant activity than the saturated heterocyclic ring of catechin (19).
Alcohol-free red wine inhibited the synthesis of thromboxane B2 Zenebe W, Pechanova O. Effects of red wine polyphenolic compounds.
but not that of 12-HETE. Other investigators studying platelet a radical chain reaction leading to lipid hydroperoxides, which aggregation and lipid levels in humans consuming red or white can stimulate vascular cell to produce monocyte-chemotactic and wine found an increase in high density lipoprotein (HDL) levels macrophage-stimulating factors, resulting in formation of so-cal- in both groups and a decrease in ADP-induced platelet aggrega- led foam cells and atherosclerotic plaques (32, 33). Oxidised low- tion in humans consuming red wine (30).
density lipoproteins (LDLs) also play a role in thrombus develop- With the goal of studying the platelet inhibitory effects of ment, since they stimulate procoagulant activities in endothelial different compounds including wine, the Folt’s coronary throm- cells and monocytes and inhibit vasodilatation by decreasing ex- bosis model of platelet aggregation and thrombus formation ba- pression of endothelial NO synthase. In the prevention of cardio- sed on measurement of cyclic reductions in coronary flow (CFRs) vascular disease, many of the observed effects of polyphenols can in mechanically stenosed coronary artery was used (28). The therefore be attributed to their recognised antioxidant and radical authors showed that CFRs were eliminated by red wine and gra- scavenging properties, which may delay the onset of atherogene- pe juice when given intravenously as well as intragastrically, sis by reducing chemically and enzymatically mediated peroxida- however a 2.5-times greater amount of grape juice than red wine tive reactions (34). According to the work of Rice Evans and Mil- was needed for the elimination of CFRs. In the case of white ler (35), which contributed to the understanding of structure-acti- wine, the elimination of CFRs was not significant. These results vity relationship of the antioxidant effects of flavonoids, querce- suggest that there are antiaggregative compounds present in red tin, the common red wine flavonoid, appears to be an extremely wine and grape juice that are absent in white wine. Quercetin efficient radical scavenger. Indeed, reduced progression of athe- and rutine were also found to eliminate CFRs in the same model.
rosclerosis in apolipoprotein E-deficient mice was shown after Measurement of quercetin, rutine and resveratrol content of red consumption of quercetin or red wine. Reduction in atherosclero- wine, white wine and grape juice indicated that the flavonoid sis progression was associated with decreased susceptibility of LDL content was severalfold higher in red wine and grape juice com- to oxidation and aggregation (36). The studies of De Whally et al pared to white wine (28, 8). Red wine polyphenols were capable (37) and Miyagi et al (38) showed that red wine significantly inhi- of reducing the level of thromboxane A similar to aspirin. Poly- bited Cu2+-catalised LDL oxidation, yet white wine and beer fai- phenols had a shorter-term effect on coronary blood flow in con- led to do so. Similarly to red wine, grape juice with a large amount trast to aspirin, however they could interfere with glycoprotein of flavonoids also significantly inhibited oxidation of LDL. Howe- receptors on endothelial cells. As a result of this interference, ver, in the experiment on 20 volunteers, the antioxidant activity platelets were not able to adhere on the vessel wall and therefo- was not significantly increased after ingestion of grape juice, sug- re, thrombus formation was inhibited (31).
gesting that flavonoids in red wine can be absorbed from the in- Ruf et al (29) reported that except decreasing prostanoid synthe- testine more easily than those in grape juice. It was concluded that sis from arachidonate, wine polyphenols were able to reduce pla- the antioxidant properties of flavonoids concerning LDL oxida- telet activity by nitric oxide mediation. In agreement with this stu- tion were associated with absorption of flavonoids from the intes- dy, Wollny et al (8) found that red wine supplementation, either tine into the circulation (6). Recently, Nidgikar et al (39) confir- after 10-day or acute administration in rats, markedly prolonged med the finding of De Whally et al (37) and Miyagi et al (38), bleeding time and inhibited platelet adhesion to fibrilar collagen showing that 2-week consumption of red wine, but not white wine, by NO-dependent mechanism. NG-nitro-L-arginine methyl ester enhanced antioxidant capacity, as measured by decreased plasma (L-NAME), an inhibitor of NO formation, prevented these effects lipid peroxides, conjugated diens and Cu2+-catalised peroxidation of red wine. The possibility to revert the effect of L-NAME by L- of LDL. Serafini et al (40) showed that the total radical-trapping -arginine, the substrate for NO synthase, but not by its stereoiso- antioxidant capacity of red wine was at least 20-times stronger mer D-arginine, strengthens the role of NO in red wine-induced than that of white wine. Frankel et al (4) reported that quercetin effects. Regarding the mechanisms of NO increase, it is possible and trans-resveratrol were more effective than α-tocopherol in that red wine polyphenols decrease degradation of basal levels of inhibiting the oxidation of human LDL. Moreover, flavonoids may NO, preventing its destruction by superoxides and/or stimulate protect -tocopherol from oxidation by being themselves oxidi- NO synthase in endothelial cells. It is conceivable that both me- sed by free radicals or by regenerating active α-tocopherol (12).
chanisms are active in in vivo conditions (10, 8).
The antioxidant activities of flavonoids and their glycosides were Adhesion of platelets to the subendothelial matrix, after ves- even higher than those of vitamin C and E (19). Red wine con- sel damage, is a triggering mechanism of thrombus formation, sumption was also found to increase plasma HDL levels charac- and thus platelet inhibition by red wine could partially explain terised by their antiatherogenic effects (41). All the mechanisms by which red wine polyphenols exert their antiatherogenic effect appear to be crucial in the prevention and treatment of cardio- Increase in reactive oxygen species in the organism leads to oxidative stress with subsequent damage of many biological mole-cules. Proteins, DNA and lipids of cell membranes are significant The protective role of flavonoids in cardiac ischaemia may targets of cellular injury (32). Lipid peroxidation in vivo involves be related mainly to their ability to scavenge oxygen free radi- Bratisl Lek Listy 2002; 103 (4–5): 159–165 cals (42), to maintain NO concentration (43, 10) and to inhibit not observed. However Andriambeloson et al (10) reported rela- xation induced by leucocyanidol and catechin in aortic rings both The study of Sato et al (42) found that an ethanol-free red with and without endothelium. However a 1000-times greater wine extract as well as trans-resveratrol protected the hearts from amount of these substances was needed to induce relaxation in detrimental effects of ischaemia/reperfusion injury, as eviden- endothelium-denuded arteries. NG-monomethyl-L-arginine and ced by improved postischaemic ventricular function and redu- NG-nitro-L-arginine, inhibitors of NO synthesis, reversed the ced myocardial infarction. Both the red wine extracts and trans- relaxation induced by grape skin extracts. Using electron para- resveratrol reduced the oxidative stress in the heart, as indicated magnetic resonance, acute administration of red wine polyphe- by decreasing malondialdehyde formation. These compounds nolic compounds was found to elevate NO synthesis in the en- were also found to be highly effective in direct scavenging of dothelium (55). However, the mechanism of NO synthase acti- peroxyl radicals. Direct perfusion of ethanol into the hearts may vation by red wine polyphenolic compounds is not satisfactorily however cause development of oxidative stress resulting in a understood. Recently, Andriambeloson et al (51) observed that completely different effects on the hearts (45). A reduction ef- red wine polyphenolic compounds produced NO-induced Ca2+- fect of several flavonoids on acute regional myocardial ischae- dependent vasorelaxation of the rat aorta. Martin et al (56) sug- mia in isolated rabbit hearts was also reported (45). Ning et al gested that the rise in intercellular Ca2+ involves both Ca2+ relea- (46) showed that flavone administration improved functional se and Ca2+ entry, the latter being an essential step for NO pro- recovery in the reperfused heart after a bout of global ischaemia.
duction in the endothelial cells. However, the mechanisms of The effect of flavone on postischaemic recovery was proposed Ca2+ handling among different polyphenolic compounds could to be caused by its stimulation of the cytochrome P450 system.
differ with regard to the type of intracellular Ca2+ stores mobili- It has been suggested that flavone might act as an allosteric ef- zed and the nature of G proteins implicated. It has been sugges- fector of cytochrome P450 reductase, which improves catalytic ted that phospholipase C and tyrosine kinase pathways are in- efficiency, thereby diminishing production of free radicals. Qu- ercetin was reported to exert a protective effect by preventing Since red wine polyphenols consist of hydroxycinnamic acid, the decrease in the xanthine dehydrogenase/oxidase ratio obser- proanthocyanidins, anthocyanins, flavanes, and flavonols, the ved during ischaemia-reperfusion in rats (47). Inhibition of question which substance(s) may be responsible for the eleva- xanthine oxidase by flavonoids was also described (48). In addi- tion of NO synthesis had to be addressed. From anthocyanin- tion, flavonoids were found to possess positive chronotropic and enriched wine extracts, aglycone-, monoglycoside- as well as antiarrhythmic effects and to minimise mitochondrial ischaemia/ diglycoside-enriched fractions were capable to induce endothe- lium-dependent vasorelaxation, similar to that elicited by origi- Since changes in NO concentration were found during is- nal red wine polyphenolic extract. Of the anthocyanins, only chaemia-reperfusion in rats (50), the effects of red wine poly- delphinidin, but not cyanidin or malvidin, mimicked the effect phenols on NO stability and generation are crucial in prevention of the original extract (57). The representative derivatives of against ischaemia. Recent studies reported an increase in NO phenolic acid (benzoic, vanillic and gallic acid), hydroxycinna- synthase activity due to the red wine polyphenolic compounds mic acid (p-coumaric and caffeic acid), flavanols (catechine and treatment in the heart (51) and also in aorta (51, 52). The protec- epicatechine), as well as the higher polymer-enriched fraction of tive effects of flavonoids in cardiac ischaemia are also associa- condensed tannins failed to induce endothelium-dependent va- ted with their ability to inhibit mast cell secretion, which may be involved in cardiovascular inflammation, at present consi- Mechanisms implicated in the vasorelaxant effects of flavo- dered one of the key factors in coronary artery disease (44).
noids may include also inhibition of cyclic nucleotide phospho- Quercetin and some other flavonoids were found to inhibit the diesterases (59) and activation of Ca2+-activated K+ channels (60), release of rat mast cell histamine in a concentration-dependent both pathways are linked to the effects of flavonoids on smooth muscle cells rather than the endothelium. Ferrell et al (61) pro- posed that the flavonoid inhibitory activity on phosphodiestera- ses could be ascribed to the structural mimicry of the purine ring in cAMP and cGMP and the pyranone ring of active flavonoids.
The idea that phenolic compounds in grape juice, red wine Both increase in NO synthase activity and decrease in phospho- and in some other beverages have a protective effect on cardio- diesterase activity may lead to increase in cGMP concentration vascular disease led investigators to think about the effect of these resulting in vasorelaxation and inhibition of platelet aggrega- compounds on vascular functions. Polyphenolic compounds have the ability to relax precontracted smooth muscle of aortic rings with intact endothelium, moreover, some of them are able to re- lax endothelium-denuded arteries (9, 10).
Fitzpatrick et al (9) reported that in aortic rings with endo- The ability of polyphenolic compounds to activate the NO- thelium, skin extracts from red grapes caused relaxation. On the cGMP system seems to be associated also with their antihyper- contrary, in endothelium-denuded aortic rings, relaxation was tensive effect. The effects of the red wine extract provinol was Zenebe W, Pechanova O. Effects of red wine polyphenolic compounds.
tested on the experimental model of L-NAME-induced hyper- coronary heart disease (1). A cohort study based on data collec- tension, which was developed by long-term inhibition of NO ted at the Finnish mobile clinic was carried out over 27 years.
synthase activity. Provinol partially prevented increase in blood Similar to Gr•nbaek et al(1) these authors reported an inverse pressure when given simultaneously with NO synthase inhibitor relation between flavonoid intake and mortality from coronary L-NAME (51). In rats with developed hypertension, provinol- heart disease. The major sources of flavonoids in this study were treatment resulted in a greater readiness to blood pressure decre- apples and onions (70). The protective effect of tea polyphenols ase and higher elevation of NO synthase activity in the heart and as a result of their antioxidative effect has been done in human aorta compared to rats with spontaneous recovery (62). Similar- volunteers by Serafini et al (71) and they expressed both green ly, Hara (63) and Mitzuani et al (64) reported that in vivo admi- and black tea as the source of the antioxidant polyphenols.
nistration of an extract of polyphenolic compounds from tea and Flavonol and flavone intake and the risk of stroke had been wine, respectively, resulted in the former study in an attenuation studied in a group of 550 men for 15 years. The result showed of elevated blood pressure in spontaneously hypertensive rats, that men with the highest intake of flavonol and flavone showed and in the later study in a reduced blood pressure and decreased a decreased risk of coronary heart disease (72). A non-signifi- risk of stroke in susceptible rats. The improvement of the biome- cant inverse association between flavonoid intake and mortality chanical properties of aorta, lowering of cholesterol levels and from coronary heart disease was found in men with previous his- inhibition of LDL oxidation were suggested as the mechanisms tory of coronary heart disease (73). Schmidt et al (74) reported a responsible for blood pressure reduction (63, 64). Recently Die- decrease in blood pressure and heart rate in men with chronic bolt et al (65) found that short term oral administration of red heart disease who received flavonoids from hawthorn extract.
wine polyphenolic compounds produced a decrease in blood pres- To summarise the above mentioned results, epidemiological sure in normotensive rats. This hemodynamic effect of red wine evidence demonstrates that regularly consumption of flavonoids polyphenolic compounds was associated with an augmentation reduces the risk of cardiovascular disease.
of endothelium-dependent relaxation and a modest induction of gene expression of inducible NO synthase and cyclooxygenase As shown in the above review, it is evident that natural poly- 2 within the arterial wall which together maintained unchanged phenolic compounds possess antithrombic, antioxidant, anti-is- chaemic, vasorelaxant and antihypertensive properties. All the- The effects of decaffeinated green tea were studied on mice se effects improve cardiovascular functions and potentially re- exposed to various intensities of social stress associated with sult in decreased morbidity and mortality due to the coronary hypertension. In decaffeinated green tea drinking mice, blood heart diseases. Red wine, as opposed to other sources of poly- pressure fell from 150 to 133 mmHg. It is speculated that the phenols is unique in a number of selected dietary polyphenols as sympathetic adrenal medullary system may be involved in the well as in their ingestion and bioavailability.
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