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Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies^1,2,3,4

¹ From the Nutrient Bioavailability Group, Nestlé Research Center, Lausanne, Switzerland (GW), and the Unité des Maladies Métaboliques et Micronutriments, Institut National de la Recherche Agronomique, Saint-Genès Champanelle, France (CM)

² Presented at the 1st International Conference on Polyphenols and Health, held in Vichy, France, November 18–21, 2004.

³ Supported by Nestlé (Vevey, Switzerland).

⁴ Address reprint requests and correspondence to G Williamson, Nutrient Bioavailability Group, Nestlé Research Center, Vers chez les Blanc, 1000 Lausanne 26, Switzerland. E-mail: gary.williamson{at}rdls.nestle.com.

ABSTRACT

For some classes of dietary polyphenols, there are now sufficient intervention studies to indicate the type and magnitude of effects among humans in vivo, on the basis of short-term changes in biomarkers. Isoflavones (genistein and daidzein, found in soy) have significant effects on bone health among postmenopausal women, together with some weak hormonal effects. Monomeric catechins (found at especially high concentrations in tea) have effects on plasma antioxidant biomarkers and energy metabolism. Procyanidins (oligomeric catechins found at high concentrations in red wine, grapes, cocoa, cranberries, apples, and some supplements such as Pycnogenol) have pronounced effects on the vascular system, including but not limited to plasma antioxidant activity. Quercetin (the main representative of the flavonol class, found at high concentrations in onions, apples, red wine, broccoli, tea, and Ginkgo biloba) influences some carcinogenesis markers and has small effects on plasma antioxidant biomarkers in vivo, although some studies failed to find this effect. Compared with the effects of polyphenols in vitro, the effects in vivo, although significant, are more limited. The reasons for this are 1) lack of validated in vivo biomarkers, especially in the area of carcinogenesis; 2) lack of long-term studies; and 3) lack of understanding or consideration of bioavailability in the in vitro studies, which are subsequently used for the design of in vivo experiments. It is time to rethink the design of in vitro and in vivo studies, so that these issues are carefully considered. The length of human intervention studies should be increased, to more closely reflect the long-term dietary consumption of polyphenols.

Key Words: Polyphenols • flavonoids • procyanidin • bioavailability • isoflavone • quercetin • catechin

INTRODUCTION

It is clear that food components must, by definition, be bioavailable in some form to exert biological effects. There have been major advances in the past few years in our knowledge regarding polyphenol absorption and metabolism (1–4), and it is apparent that most classes of polyphenols are sufficiently absorbed to have the potential to exert biological effects. For example, quercetin after a meal containing onions, catechins after red wine consumption, and isoflavones after soy consumption reach micromolar concentrations in the blood (1, 2, 5–7). These findings demonstrate that polyphenols cross the intestinal barrier and reach concentrations in the bloodstream that have been shown to exert effects in vitro, in some studies.

There are thousands of articles on the effects of polyphenols on biological systems in vitro. However, many of those studies did not take bioavailability and metabolism factors into consideration, and the effects reported in those studies do not necessarily occur in vivo. Although most polyphenols are absorbed to some extent, this is very dependent on the type of polyphenol. The range of concentrations required for an effect in vitro varies from <0.1 µmol/L to >100 µmol/L. Because physiologic concentrations do not exceed 10 µmol/L, the effects of polyphenols in vitro at concentrations of >10 µmol/L are generally not valid, with the possible (but unproven) exception of the intestinal lumen. Furthermore, absorption is accompanied by extensive conjugation and metabolism, and the forms appearing in the blood are usually different from the forms found in food. This indicates that in vitro experiments with the form of polyphenols found in food (the aglycone) are not necessarily relevant to the in vivo situation (8).

There are now intervention studies in the literature, of varying quality, that demonstrate significant biological effects of polyphenol consumption among humans, with the use of many different biomarkers (Tables 1–4). This review examines the effects demonstrated in some of the intervention studies reported in the literature. It considers most of the reports on quercetin, catechins, and procyanidins and some of those on isoflavones. Some of the reports described intervention studies involving consumption of foods and, in many of those cases, it was not proved that the observed effects were attributable to the polyphenol component. This situation may improve in the future, for example, with the use of isogenic lines of onions that differ only in their quercetin contents, allowing comparisons between groups consuming the same food but with different polyphenol contents. The bioavailability issues for each group of polyphenols are discussed in the context of the intervention studies.

Flavonols (including quercetin)
Quercetin is found at high concentrations in onions, apples, tea, broccoli, and red wine and as a component of Ginkgo biloba. Intervention studies with quercetin are shown in Table 1. Some diverse effects have been demonstrated for Ginkgo biloba, but these may also be attributable to the terpenoid component of these extracts. Other studies have shown effects on antioxidant biomarkers, such as increased resistance of lymphocyte DNA to strand breakage, decreased urinary 8-hydroxy-2'-deoxyguanosine concentrations, increased plasma antioxidant capacity, decreased tissue inhibitor of matrix metalloproteinase-1 expression, altered renal function, improved prostatitis symptoms, and improved oxidative resistance to LDL. However, there are also studies that show no effects on these biomarkers.

Despite the lack of convincing evidence for consistent effects of quercetin in vivo in humans, there are numerous studies on the properties of quercetin in vitro. The apparent discrepancy between in vitro and in vivo studies may be partly attributable to absorption and metabolism. Generally, quercetin is not found in the plasma as the free form or as the parent glucoside. At the doses used in the intervention studies noted in Table 1 (21–1000 mg), it would be found exclusively as methyl, sulfate, or glucuronic acid conjugates (102); when added together, these compounds would represent the equivalent of 1–5 µmol/L aglycone equivalents at the highest dose. Lower doses of quercetin are more methylated than higher doses in humans (103). Quercetin has a relatively long plasma half-life of 11–28 h, and a 50-mg dose would lead to concentrations of up to 0.75–1.5 µmol/L in plasma (1, 4). There is only limited information on the properties of the conjugates in vitro, although it can be concluded that the conjugates have quantitatively different properties and are generally less biologically active, compared with the aglycones (104, 105). However, deconjugation could occur in some tissues such as the liver (106) or at sites of inflammation (107), leading to reactivation of the conjugated quercetin. The bioavailability issues may partially account for the lack of biological activity in vivo, although the lack of activity may reflect the short-term nature of the studies of quercetin and the selection of inappropriate biomarkers.

Isoflavones (genistein and daidzein)
The intervention studies on isoflavones are the most advanced and sophisticated of those for all of the polyphenols. Studies of the consumption of isoflavones lasting up to 1 year have shown effects on bone biomarkers, such as significant increases in bone mineral density and bone mineral content and changes in bone biomarkers, such as reduced excretion of pyridinium cross-links and increased serum concentrations of bone-specific alkaline phosphatase and osteocalcin. Other effects include changes in LDL and HDL cholesterol concentrations, increases in LDL oxidation lag time, and changes in menopausal symptoms and hot flashes. Many, but not all, of the changes could be related to binding to the estrogen receptor, and this has been reviewed (108, 109).

Isoflavones occur in soy as glycosides, but some fermented products contain free aglycones (110). Consumption of isoflavone-rich foods or of the purified isoflavones themselves leads to appearance in the plasma, with a peak of absorption at 6–8 h (7). A dose of 50 mg of either daidzein or genistein, as typically used in intervention studies (the intervention studies noted in Table 1 used 37–128 mg per person per day), yields a peak plasma concentration of 2 µmol/L at 6 h (4). The glycosides are not present in plasma, and most of the isoflavones are conjugated as sulfates or glucuronides; some free aglycone is also present, and Setchell et al (7) found 8% of the total daidzein as unconjugated aglycone 2 h after consumption of a dose of 50 mg. This decreased to 3% at steady state, which would apply to the intervention studies, because the studies were conducted for 14–365 d. After 4 wk of 30 mg/d isoflavones, the peak plasma concentrations showed no significant changes at the measurement times of 2 and 4 wk (111), which indicates that the bioavailability of isoflavones does not decrease during long periods of intake. However, we have unpublished data showing that isoflavone bioavailability increases during an extended period of intake (C Manach, unpublished observations, 2004), and this issue is currently unresolved. When administered in intervention studies, the isoflavones are clearly active and affect several biomarkers, especially related to bone. It is not known whether this effect is derived from free aglycone in the plasma, whether the conjugated forms are also active, or whether active deconjugation occurs in the relevant tissues. Some of the isoflavone conjugates are active in vitro (112), although information is very limited.

Catechins [(+)-catechin, (–)-epicatechin, (–)-epigallocatechin, (–)-epicatechin gallate, and (–)-epigallocatechin gallate]
(+)-Catechin and (–)-epicatechin are widely distributed in foods. Catechin concentrations are especially high in broad beans, black grapes, apricots, and strawberries. (–)-Epicatechin is found at high concentrations in apples, blackberries, broad beans, cherries, black grapes, pears, raspberries, and chocolate. The gallates and the gallocatechins are found almost exclusively in tea, especially green tea. Deducing the intake of catechins during intervention studies is more difficult than for isoflavones, because the non-galloylated forms are widespread and can complicate intake estimates. This can lead to consumption of additional sources of catechins; furthermore, the amounts were not measured in some cases. The situation is clearer for the gallates or galloylated catechins, because they are almost exclusive to green tea. It is difficult to estimate the total flavonoid intake from black tea, because the fermentation process gives rise to a variety of structurally different oligomers. However, the amounts of remaining monomeric catechins can be readily estimated. Catechins are biologically active molecules that have a wide range of effects in vitro.

In human intervention studies (Table 3), catechins increased plasma antioxidant activity, as assessed with a variety of assays, decreased plasma lipid peroxide and malondialdehyde concentrations, increased plasma ascorbate concentrations, decreased nonheme iron absorption, and increased the resistance of LDL to oxidation. In addition, the green tea catechins, including the galloylated catechins, increased fat oxidation and energy expenditure and decreased the respiratory quotient and body weight. There were also some effects on vascular dilation.

For the non-galloylated catechins, doses of 35 or 160 mg (+)-catechin (in red wine or chocolate) yielded plasma concentrations of 0.1–0.2 µmol/L (6, 114), and a similar dose of (–)-epicatechin yielded 0.2 µmol/L in plasma (114, 115). Both (+)-catechin and (–)-epicatechin are present in plasma exclusively as conjugates with methyl, sulfate, or glucuronic acid groups (6, 113, 116). Generally, catechins have short plasma half-lives (2–3 h).

In summary, the intervention studies with monomeric catechins give rise to plasma concentrations on the order of 0.1–0.5 µmol/L, but with rapid clearance. Substantial amounts of unconjugated forms of EGCG would be present in plasma, but all (+)-catechin and (–)-epicatechin is predicted to be conjugated. The percentage of catechins in the plasma that are sulfated or glucuronidated depends on the dose, but this is not usually measured in intervention studies.

Procyanidins [oligomeric (+)-catechin and (–)-epicatechin]
Procyanidins are oligomeric catechins, covalently linked together. Dimers and trimers are most common, but the degree of oligomerization can be quite high. Procyanidins are present at particularly high concentrations in cocoa, grapes/wine, and apples and are also found in many fruits, such as blackberries, cherries, figs, and plums (117). Purified procyanidins are weakly bioactive in vitro but exhibit numerous effects in vivo in intervention studies. It is important to note that procyanidins usually occur together with monomeric (+)-catechin and (–)-epicatechin; therefore, it is not clear whether the observed effects are attributable to the procyanidin component, the monomeric component, or both. The predominant effects are on the vascular system and include substantial increases in plasma antioxidant activity, decreased platelet aggregation (both stimulated and unstimulated), decreased plasma concentrations of lipid peroxide and thiobarbituric acid-reactive substances, decreased LDL cholesterol concentrations, increased HDL cholesterol concentrations, decreased susceptibility of LDL to oxidation, endothelium-dependent blood vessel dilation and decreased blood pressure, beneficial effects on capillary fragility and permeability, increased plasma ascorbate concentrations, decreased P-selectin expression, increased concentrations of nitrosated/nitrosylated species, decreased serum thromboxane concentrations, increased diameters of microvessels, reduced serum thromboxane B2 concentrations, increased plasma homocysteine concentrations, increased plasma vitamin B6 concentrations, maintenance of endothelial function (compared with loss with a high-fat diet), increased platelet-derived nitric oxide production, decreased superoxide release, increased -tocopherol concentrations, and decreased concentrations of circulating autoantibodies to oxidized LDL (Table 4).

The metabolic fate of procyanidins after consumption is still a mystery. After consumption of 2 g of high-procyanidin grape seed extract by volunteers, the plasma concentrations of procyanidin B1 reached only 10 nmol/L (118); after consumption of 0.375 g cocoa/kg body wt, the plasma concentrations of procyanidin B2 reached only 41 nmol/L (114). When administered in a purified form to rats, procyanidin dimer B3 was not found in the plasma (119). However, human intervention studies with procyanidin-rich foods, as discussed above, show biological effects (Table 4). Either the effects are attributable to currently unidentified metabolites of the procyanidins or the effects are attributable to another component, such as the monomeric catechins (or both).

Microbial metabolites of polyphenols
The data on the bioavailability of polyphenols presented above considered only the presence of intact polyphenols in the blood, ie, the ingested compound or its conjugates. The extensive microflora in the colon also plays a critical role in the metabolism of polyphenols. After microbial enzyme-catalyzed deconjugation of any polyphenol conjugates that reach the colon, there are 2 possible routes available, namely, absorption of the intact polyphenol through the colonic epithelium and passage into the bloodstream (as free or conjugated forms) or breakdown of the original polyphenol structure into metabolites. The absorption data presented above include the contribution of the absorption of intact polyphenols in the colon but do not include the breakdown contribution. Microbial metabolism deserves special consideration, because many of the diverse polyphenols are broken down into simpler phenolic compounds that are common to many different polyphenols. In addition, some of the microbial metabolites could have unique biological effects. For example, the isoflavone daidzein is converted to equol by gut microflora in 30–40% of the population, and the equol is absorbed into the bloodstream in these people. There is emerging evidence that "equol producers" demonstrate better effects on some biomarkers, such as bone mineral density, after isoflavone consumption, compared with nonproducers (109). This is an example in which microflora activate a polyphenol to a more potent biologically active compound. Although intervention studies demonstrate an effect for procyanidins, the identity of the active component (or components) is not clear. Although intact procyanidins have some biological effects, they are poorly absorbed in an intact form (114, 118, 119). The active species could therefore be metabolites. Some low-molecular weight metabolites were identified in humans in vivo after consumption of cocoa procyanidins (120), but the biological activities of these metabolites are not known and remain to be investigated.

In summary, there are now many human intervention studies in the literature that show biological effects, but the exact effects depend on the class of polyphenol used. There are clear gaps. Most of the studies were short term, and there is a real need for longer-term studies; very few studies demonstrated a dose-response relationship, and this is also needed for convincing evidence. In addition, most studies, with the exception of those with isoflavones, administered food instead of pure compounds, and the effects noted may thus be attributable to some other component in that food. Finally, metabolism by microflora needs to be understood, because the gut microflora probably plays a major role in the biological activity of many polyphenols.

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