Dietary Flavonoids as Cancer Chemopreventive Agents: An Updated Review of Human Studies
Abstract
:1. Introduction
2. Methodology
3. Biosynthesis and Subclasses of Flavonoids
4. Dietary Flavonoids
5. Pharmacokinetics
6. Worldwide Flavonoid Intake
6.1. Asia
6.2. Europe
6.3. Oceania
6.4. North America
7. Antioxidant Activity of Dietary Flavonoids and Cancer Incidence
8. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Fruits | ANT | DYC | FVA | FVO | Total |
---|---|---|---|---|---|
Berries | |||||
Aestivalis grape | 79.74 | - | - | 1.7 | 81.44 |
American cranberry | 49.89 | - | - | 43.84 | 93.73 |
Black chokeberry | 878.11 | - | - | 134.87 | 1012.98 |
Black elderberry | 1316.66 | - | - | 42 | 1358.66 |
Black raspberry | - | - | - | 19 | 19 |
Blackberry | 172.59 | - | 13.87 | 16.87 | 203.33 |
Blackcurrant | 593.58 | - | 1.17 | 13.68 | 608.43 |
Black grape | 72.15 | - | 14.03 | 4.01 | 90.19 |
Green grape | - | - | 3.78 | 2.49 | 6.27 |
Green currant | - | - | - | 11.07 | 11.07 |
Highbush blueberry | 156.6 | - | 1.11 | 54.77 | 212.48 |
Lingonberry | 60.21 | - | - | 48.98 | 109.19 |
Lowbush blueberry | 204.56 | - | - | - | 204.56 |
Red raspberry | 72.47 | - | 5.73 | 16.26 | 94.46 |
Redcurrant | 33.13 | - | 4.68 | 0.77 | 38.58 |
Strawberry | 26.87 | - | 9.1075 | 2.32 | 38.29 |
Drupes | |||||
Nectarine | 0.86 | - | 17.65 | 1.35 | 19.86 |
Peach | 0.28 | - | 45.18 | 1.42 | 46.88 |
Plum | 47.79 | - | 46.9 | 6.98 | 101.67 |
Sour cherry | 54.43 | - | 0.2 | - | 54.63 |
Sweet cherry | 170.18 | - | 14.87 | - | 185.05 |
Pomes | |||||
Apple | 0.93 | 5.38 | 39.42 | 10.62 | 56.35 |
Pear | - | - | 4.98 | 0.84 | 5.82 |
Quince | - | - | 7.49 | 0.67 | 8.16 |
Tropical Fruits | |||||
Banana | - | - | 1.55 | - | 1.55 |
Kiwi | - | - | 0.7 | - | 0.7 |
Mango | - | - | 1.72 | - | 1.72 |
Persimmon | - | - | 1.28 | - | 1.28 |
Pomegranate | - | - | 1.1 | - | 1.1 |
Vegetables | ANT | CHA | FVA | FNE | FVE | FVO | Total |
---|---|---|---|---|---|---|---|
Cabbages | |||||||
Broccoli | - | - | - | - | - | 27.8 | 27.8 |
Fruit Vegetables | |||||||
Avocado | - | - | 0.55 | - | - | - | 0.55 |
Black olive | 82.97 | - | - | - | 27.43 | 49.43 | 159.83 |
Green olive | - | - | - | - | 0.56 | - | 0.56 |
Green sweet pepper | - | - | - | - | 2.11 | 5.49 | 7.6 |
Red sweet pepper | - | - | - | - | 0.05 | 0.24 | 0.29 |
Tomato | - | - | - | 0.14 | - | 0.014 | 0.15 |
Leaf Vegetables | |||||||
Curly | - | - | - | - | - | 24.06 | 24.06 |
Escarole | - | - | - | - | - | 18.23 | 18.23 |
Green lettuce | - | - | - | - | 0.4 | 3.99 | 4.39 |
Red lettuce | 3.53 | - | - | 2.51 | 16.74 | 22.78 | |
Spinach | - | - | - | - | - | 119.27 | 119.27 |
Onion-Family Vegetables | |||||||
Red onion | 9 | - | - | - | - | 122.51 | 131.51 |
White onion | - | - | - | - | - | 5.4 | 5.4 |
Yellow onion | - | - | - | - | - | 59.1 | 59.1 |
Shallot | - | - | - | - | - | 112.22 | 112.22 |
Pod Vegetables | |||||||
Broad bean pod | - | 0.08 | 154.45 | - | 0.37 | 34.64 | 189.54 |
Green bean | - | - | 2.42 | - | - | 5.55 | 7.97 |
Shoot Vegetables | |||||||
Asparagus | - | - | - | - | - | 23.19 | 23.19 |
Globe artichoke, heads | - | - | - | - | 57.8 | - | 57.8 |
Seeds | ANT | FVA | FNE | FVE | FVO | IFA | Total |
---|---|---|---|---|---|---|---|
Nuts | |||||||
Almond | - | 4.93 | 0.5 | - | 3.81 | 0.06 | 9.3 |
Cashew nut | - | 1.1 | - | - | - | - | 1.1 |
Chestnut | - | 0.05 | - | - | - | - | 0.05 |
Hazelnut | - | 5.7 | - | - | - | - | 5.7 |
Peanut | - | - | - | - | - | 0.51 | 0.51 |
Pecan nut | - | 16.7 | - | - | - | - | 16.7 |
Pistachio | 6.9 | 0.12 | 0.103 | 0.07 | 7.193 | ||
Common Bean | |||||||
Black common bean | 41.05 | - | - | - | 10 | 1.4 | 52.45 |
Others common bean | 7.42 | - | - | - | 69.58 | 0.2 | 77.2 |
White common bean | 0.13 | - | - | - | 49.96 | 0.5 | 50.59 |
Other Beans | |||||||
Broad bean seed whole | - | 49.37 | - | - | - | - | 49.37 |
Sunflower seed meal | - | - | - | - | - | 0.02 | 0.02 |
LENTILS | |||||||
Lentils | - | 5.17 | 0.95 | 1.09 | - | 7.21 | |
Soy Products | |||||||
Soy paste miso | - | - | - | - | - | 63.09 | 63.09 |
Soy tempeh | - | - | - | - | - | 147.74 | 147.74 |
Soy tofu | - | - | - | - | - | 39.24 | 39.24 |
Soybean roasted | - | - | - | - | - | 253.11 | 253.11 |
Cereals | FVA | FVE | FVO | Total |
---|---|---|---|---|
Cereals | ||||
Barley, whole grain flour | 35.2 | - | - | 35.2 |
Buckwheat groats, thermally treated | - | - | 8.96 | 8.96 |
Buckwheat, refined flour | - | - | 5.86 | 5.86 |
Buckwheat, whole grain flour | - | 0.9 | 36.14 | 37.04 |
Common wheat, refined flour | - | 18.4 | 0.08 | 18.48 |
Common wheat, whole grain flour | - | 77.29 | 0.11 | 77.4 |
Cocoa | FVA | FVO | Total |
---|---|---|---|
Cocoa | |||
Chocolate dark | 212.36 | 25 | 237.36 |
Chocolate milk | 19.22 | - | 19.22 |
Cocoa powder | 511.62 | - | 511.62 |
Oils | FVE | Total |
---|---|---|
Oils | ||
Extra virgin olive oil | 1.53 | 1.53 |
Virgin olive oil | 0.23 | 0.23 |
Refined olive oil | 0.15 | 0.15 |
Non-Alcoholic Beverages | ANT | DYC | FVA | FNE | FVE | FVO | IFA | Total |
---|---|---|---|---|---|---|---|---|
Cocoa Beverage | ||||||||
Chocolate, milk | - | - | 20.33 | - | - | - | - | 20.33 |
Fruit Juices | ||||||||
Berry Juices | ||||||||
Fox grape juice | - | - | 5.9 | - | - | - | - | 5.9 |
Green grape juice | - | - | 3.88 | - | - | - | - | 3.88 |
Grapefruit juice | - | - | - | 46.44 | - | 0.68 | - | 47.12 |
Citrus Juices | ||||||||
Lemon juice | - | - | - | 32.66 | 4.77 | - | - | 37.43 |
Lime juice | - | - | - | 19.61 | - | - | - | 19.61 |
Orange juice | 3.17 | - | - | 37.63 | 6.14 | 1.08 | - | 48.02 |
Pummelo juice | - | - | - | 8.48 | - | - | - | 8.48 |
Red raspberry juice | - | - | - | - | - | 9.58 | - | 9.58 |
Rowanberry | - | - | - | - | - | 7.04 | - | 7.04 |
Drupe Juices | ||||||||
Plum juice | - | 5.85 | 24.7 | - | - | - | - | 30.55 |
Pome Juices | ||||||||
Apple juice | - | 4.39 | 48.45 | - | - | 2.15 | - | 54.99 |
Apple (cider) juice | - | 4.78 | 22.66 | - | - | - | - | 27.44 |
Pear juice | - | - | 3.24 | - | - | - | - | 3.24 |
Tropical Juices | ||||||||
Kiwi juice | - | - | 0.38 | - | - | 0.09 | - | 0.47 |
Pomegranate juice | 10.13 | 0.1 | - | - | - | 0.25 | - | 10.48 |
Herb Infusions | ||||||||
German chamomile, tea | - | - | 2.07 | - | - | - | - | 2.07 |
Lemon verbena | - | - | 10.6 | - | - | - | - | 10.6 |
Peppermint, tea | - | - | 10.23 | - | - | - | - | 10.23 |
Tea Infusion | ||||||||
Fennel tea | - | - | - | - | - | 3.26 | - | 3.26 |
Black tea | - | - | 73.29 | - | - | 10.06 | - | 83.35 |
Green tea | - | - | 71.18 | - | - | 6.26 | - | 77.44 |
Oolong tea | - | - | 35.72 | - | - | - | - | 35.72 |
Soy Products | ||||||||
Soy milk | - | - | - | - | - | - | 18 | 18 |
Alcoholic Beverages | ANT | DYC | DYF | FVA | FNE | FVE | FVO | IFA | Total |
---|---|---|---|---|---|---|---|---|---|
Beer | |||||||||
Beer (alcohol free) | - | 0.0003 | - | 0.11 | 0.01 | - | - | - | 0.12 |
Beer (ale) | - | 0.01 | - | 0.38 | 0.24 | - | - | 0.02 | 0.65 |
Beer (dark) | - | 0.03 | - | 0.03 | 0.15 | - | - | - | 0.21 |
Beer (regular) | - | 0.001 | - | 0.61 | 0.04 | 0.004 | 0.09 | 0.02 | 0.77 |
Wines | |||||||||
Red wine | 23.3 | - | 5.44 | 47.02 | 0.85 | - | 7.35 | - | 83.96 |
Rosé wine | - | - | 0.38 | 2 | - | - | - | - | 2.38 |
White wine | 0.04 | - | 0.57 | 2.07 | 0.23 | - | 0.695 | - | 3.61 |
Country | Intake (mg/d) | Subclass | Food Sources |
---|---|---|---|
Asia | 107 | Protanthocyanidins > flavonols > isoflavons > flavan-3-ols > anthocyanidins > flavanones > flavones | Kimchi, green tea, persimmons, soybeans, onions |
Southern europe | 313 | Proanthocyanidins > flavanones > flavan-3-ols > flavonols > anthocyanidins > flavones > isoflavones | Apples, red wine, oranges, beans, pears, peaches |
Northern europe | 348 | Flavan-3-ols > flavones > anthocyanidins > flavonols > flavanones > isoflavones | Tea, citrus fruits, berries |
Central europe | 506 | Flavan-3-ols > anthocyanidins > proanthocyanidins > flavanones > flavonols > flavones > isoflavones | Tea, non-citrus fruits, wine |
Oceania | 351 | Flavan-3-ols > anthocyanidins > flavonols > flavanones > isoflavones > flavones | Black tea, oranges, grapes, wine, apples |
North America | 230 | Flavan-3-ols > flavanones > flavonols > anthocyanidins > flavones > isoflavones | Apples, wine, citrus fruit juices and tea. |
Authors | Methods | Results |
---|---|---|
Breast | ||
Itziar Gardeazabal et al. (2018) [97] | Prospective Cohort Study 10,713 Spanish Women Food Frequency Questionnaire (FFQ) Phenol-Explorer database HPLC | There was not a statistically significant association between total flavonoids and breast cancer risk. However, in postmenopausal women, the data indicate an inverse association between breast risk cancer and total polyphenol intake (HR: 0.31, 95% CI: 0.13–0.77) |
Oh, J.K et al. (2015) [93] | Prospective Cohort Study 42,099 Swedish Women 30–49 years FFQ | Data showed that compared with no consumption, women who consumed >1 cup tea/day had an increased breast cancer risk (Relative Risk (RR): 1.19, 95% Confidence Interval (CI): 1.00–1.42), but women with a high intake of coffee (3–4 cups/day) had a decreased breast cancer risk (RR: 0.87, 95% CI: 0.76–1.00). |
Raul Zamora-Ros et al. (2013) [91] | Prospective Cohort Study 334,850 women, 35–70 years 11.5 years follow up FFQ Phenol-Explorer database | There was no statistically significant association between total flavonoid (Hazard Ratio (HR) 0.97, 95% CI: 0.90–1.07) and isoflavone (HR 1, 95%CI: 0.91–1.10) intake and breast cancer risk. |
Wang et al. (2011) [95] | Case-Control Study. 400 cases and 400 controls. Daily intake of soy isoflavones data Gene sequencing | They suggested a protective role of high soy isoflavone intake against breast cancer risk based on the relation of oestrogen metabolites, breast cancer, and isoflavone metabolism. |
Boggs et al. (2010) [92] | Prospective Cohort Study 52,062 women, 21–69 years 12 years follow up FFQ | Data showed that the intake of coffee (Internal Rate of Return (IRR): 1.03, 95% CI: 0.77–1.39) or tea (IRR: 1.13, 95% CI: 0.78–1.63) was not associated with risk of breast cancer in participants. |
Luo JF et al. (2010) [94] | Case-Control Study 353 cases, 701 controls, 40–70 years FFQ Liquid chromatography | There was an inverse association between breast cancer risk and urinary excretion of epicatechin (Odds Ratio (OR) 0.59, 95% CI: 0.39–0.88). |
Lung | ||
Christensen KY et al. (2012) [99] | Case-Control Study 1061 cases and 1425 controls FFQ | A low intake of flavonoids was related to an increased risk of lung cancer. OR: 0.63, 95% CI: 0.47–0.85. |
Cutler et al. (2008) [14] | Prospective Cohort Study USDA database FFQ | There was an inverse association between isoflavone intake and cancer incidence (HR: 0.93, 95% CI: 0.86–1.00) and an inverse association between proanthocyanidin (HR: 0.75, 95% CI: 0.57–0.97) and flavanone (HR: 0.68, 95% CI: 0.53–0.86) intake with lung cancer incidence. |
Prostate | ||
Giulio Reale et al. (2018) [100] | Case-Control study 118 cases and 222 controls FFQ Prostate Specific Antigen | High intake of some subclasses of flavonoids (catechin (OR: 0.12, 95% CI: 0.04–0.36) and flavonol (OR: 0.19, 95% CI: 0.06–0.56) significantly reduces the risk of prostate cancer. |
Authors, Year | Methods | Results |
---|---|---|
Gastric Adenocarcinoma | ||
Sun L et al. (2017) [102] | Prospective cohort study 469,008 participants 12 years follow up FFQ | Data suggested that total flavonoid intake was associated with a reduced risk of neck and head cancer (HR: 0.76, 95% CI: 0.66–0.86). |
Hae Donw Woo et al. (2014) [101] | Case-Control study. 334 cases and 334 controls, aged 35–75 years, from Korea. FFQ USDA database | Total flavonoids and their subclasses were significantly associated with a reduced risk of gastric cancer in women (OR 0.33, 95% CI 0.15–0.73) but not in men. |
Zamora-Ros et al. (2012) [68] | Observational study 477,312 subjects, aged 35–70 years, from 10 European countries. Average Follow-up of 11 years FFQ USDA and Phenol Explorer Databases. | Total dietary intake was associated with a significant reduction in the risk of gastric adenocarcinoma in women (HR 0.81, 95% CI 0.70, 0.94). |
Pancreatic Cancer | ||
Molina-Montes E. et al. (2016) [103] | Prospective cohort 477,309 participants Average Follow-up of 11 years FFQ USDA and Phenol Explorer Databases. | There was no association with pancreatic cancer risk and dietary flavonoid intake (HR: 1.09, 95% CI: 0.95–1.11); however, there was an inverse association, but not statistically significant, between prostate cancer risk and flavanone intake. |
Colorectal Cancer | ||
Nimptsch K et al. (2016) [104] | Prospective cohort 42,478 male 76,364 female 26 years follow up FFQ | Data did not show an association between colorectal cancer risk and flavonoid subclass intake. RR (95% IC) values were 0.98 (0.81, 1.19) for anthocyanins, 1.07 (0.95, 1.21) for flavan-3-ols, 0.96 (0.84, 1.10) for flavanones, 1.01 (0.89, 1.15) for flavones, and 1.04 (0.91, 1.18) for flavonols. |
Xu M. et al. (2016) [105] | Case-Control study 1632 cases and 1632 controls FFQ | There was an inverse association between colorectal cancer risk and flavone (OR: 0.54, 95% CI 0.43, 0·67), flavanone (OR: 0.28, 95% CI: 0.22–0.36), and anthocyanidin (OR: 0.80, 95% CI: 0.64–1.00) intake. |
Zamora Ros et al. (2015) [107] | Case-control study 523 participants FFQ | Flavonoid intake was not associated with colorectal cancer survival or recurrence. |
Zamora Ros et al. (2013) [108] | Case-Control study 424 cases and 401 hospital-based controls FFQ Phenol Explorer Database | Data showed an inverse correlation between risk of colorectal cancer and intake of total flavonoids (OR: 0.59, 95% CI, 0.35–0.99) and some flavonoid subclasses (such as proanthocyanidins and flavones) |
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Rodríguez-García, C.; Sánchez-Quesada, C.; Gaforio, J.J. Dietary Flavonoids as Cancer Chemopreventive Agents: An Updated Review of Human Studies. Antioxidants 2019, 8, 137. https://doi.org/10.3390/antiox8050137
Rodríguez-García C, Sánchez-Quesada C, Gaforio JJ. Dietary Flavonoids as Cancer Chemopreventive Agents: An Updated Review of Human Studies. Antioxidants. 2019; 8(5):137. https://doi.org/10.3390/antiox8050137
Chicago/Turabian StyleRodríguez-García, Carmen, Cristina Sánchez-Quesada, and José J. Gaforio. 2019. "Dietary Flavonoids as Cancer Chemopreventive Agents: An Updated Review of Human Studies" Antioxidants 8, no. 5: 137. https://doi.org/10.3390/antiox8050137