Tea Is the Major Source of Flavan-3-ol and Flavonol in the U.S. Diet 1,2

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1 The Journal of Nutrition Proceedings of the Fourth International Scientific Symposium on Tea and Human Health Tea Is the Major Source of Flavan-3-ol and Flavonol in the U.S. Diet 1,2 Won O. Song 3 * and Ock K. Chun 4 3 Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI and 4 Department of Nutritional Sciences, University of Connecticut, Storrs, CT Abstract Flavonoid intake is inversely associated with the incidence of chronic diseases, but the sources of flavonoid intake in freeliving U.S. adults have not yet been reported. We tested hypotheses that tea is the major dietary source of flavonoids in U.S. adults; tea consumers differ from those of tea nonconsumers in sociodemographics, health-related behaviors, and dietary and beverage sources of flavonoid intake. We matched the flavonoid contents of the USDA Flavonoid Databases with dietary intake data of adults (n ¼ 8809) included in NHANES of Only 21.3% of U.S. adults reported drinking tea daily. Daily total flavonoid intake of tea consumers was over 20 times that of tea nonconsumers (697.9 vs mg/d); per capita flavonoid intake from tea was 157 mg/d. Tea consumers are more likely to be older, female, white, and to have higher income than tea nonconsumers (P, 0.001); to have lower nonleisure-time physical activity level (P, 0.01); and to take dietary supplements (P, 0.001) than tea nonconsumers. Intake of flavonols and flavan-3-ols, the major tea flavonoids, differed between the 2 groups (P, 0.01). Other dietary flavonoid sources after tea were citrus juice, wine, and citrus fruits for both tea consumer and nonconsumer groups. For tea nonconsumers, flavonoid intake from wine, fruitades, and fruit drinks was higher than that in tea consumers. Flavonoid intake differs among subgroups, mainly because of the percentage of tea consumers and the prevalence of tea consumption within each subgroup. J. Nutr. 138: 1543S 1547S, Introduction 1 Published in a supplement to The Journal of Nutrition. Presented at the conference Fourth International Scientific Symposium on Tea and Human Health, held in Washington, DC at the U.S. Department of Agriculture on September 18, The conference was organized by the Tea Council of the U.S.A. and was cosponsored by the American Cancer Society, the American College of Nutrition, the American Medical Women s Association, the American Society for Nutrition, and the Linus Pauling Institute. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the Tea Council of the U.S.A. or the cosponsoring organizations. Supplement coordinators for the supplement publication were Lenore Arab, University of California, Los Angeles, CA and Jeffrey Blumberg, Tufts University, Boston, MA. Supplement coordinator disclosure: L. Arab and J. Blumberg received honorarium and travel support from the Tea Council of the U.S.A. for cochairing the Fourth International Scientific Symposium on Tea and Human Health and for editorial services provided for this supplement publication; they also serve as members of the Scientific Advisory Panel of the Tea Council of the U.S.A. 2 Author disclosures: W. O. Song received an honorarium and travel support from the Tea Council of the U.S.A. for speaking at the Fourth International Scientific Symposium on Tea and Human Health and for preparing this manuscript for publication; O. K. Chun, no conflicts of interest. * To whom correspondence should be addressed. song@msu.edu. Flavonoid intake has been inversely associated with the incidence of chronic diseases, presumably because of the antioxidant properties of flavonoids (1 5). Green tea, one of the most popular beverages consumed in Asian countries, contains a class of polyphenols known as catechins, which consist mainly of epigallocatechin gallate, epicatechin gallate, gallocatechin, and epigallocatechin. Green tea and catechins have been reported to have a variety of nutritional and pharmacological properties, including anticarcinogenic (6), antidiabetic (7), and antiatherogenic effects (8). Several studies have reported the identification of tea flavonoids and their antioxidant properties (9 11). However, limited information has been available on the differences in sociodemographic characteristics, major foods, and food groups that contribute to flavonoid intakes between tea consumers and nonconsumers. Recently our research team reported the estimated dietary flavonoid intake of the U.S. population (12). We have also reported that tea was the most prominent source of flavonoids from food and beverages in the U.S. diet. This article covers the chemical properties of tea flavonoids, a new approach to estimating flavonoid intake of the U.S. population, major flavonoid sources in the U.S. diet, and sociodemographic characteristics of tea consumers. Tea flavonoids Flavonoids are the largest and most common plant polyphenolics. They have the common structure of diphenylpropane (C 6 - C 3 -C 6 ), which has 2 benzene rings on either side of a 3-carbon ring. Multiple combinations of hydroxyl groups, sugars, oxygens, and methyl groups attached to these structures create the various classes of flavonoids, i.e., anthocyanidins, flavan-3-ols, flavonols, flavones, flavanones, and isoflavones. Flavonoids have several hydroxyl groups in their structure and function as electron donors to other free radicals or scavenge other reactive oxygen species. The antioxidant activities of each compound differ by the number of hydroxyl groups and their positions (13). All teas are derived from the leaves of Camellia sinensis, but different processing methods produce different types of tea. Fresh tea leaves are rich in flavonoids known as catechins (14). Tea /08 $8.00 ª 2008 American Society for Nutrition. 1543S

2 TABLE 1 Dietary total and individual flavonoid intakes of U.S. adults by sociodemographic and lifestyle factors 1,2 Subgroups Stratified sample Flavonols Flavones Flavanones Flavan-3-ols Anthocyanidins Isoflavones Total P-value 3 n mg/d All Gender Men NS Women Age y , y y y Ethnicity Non-Hispanic white ,0.01 Non-Hispanic black Mexican-American Others Poverty income ratio 4, , $ Alcohol consumption 5 No ,0.01 Yes Vitamin supplement use 6 No ,0.01 Yes Adapted with permission from Chun et al. (12). 2 Values are means 6 SEM, n ¼ P-values are for overall difference by t-test by gender, age, ethnicity, income levels, alcohol consumption, and vitamin supplement use. N.S., not significant (P. 0.05). 4 Ratio of the median family income over the poverty index. A poverty income ratio of #1.30 is required to be eligible for food assistance programs. 5 Alcohol consumption: yes means to have consumed at least 12 alcoholic drinks per year. 6 Vitamin supplement use denotes taking dietary vitamin supplements. leaves also contain polyphenol oxidase enzymes in separate compartments from catechins (15,16). When tea leaves are intentionally broken or rolled during processing, catechins exposed to polyphenol oxidase form dimers and polymers, which are known as theaflavins and thearubigins, respectively (16). This oxidation process is known in the tea industry as fermentation. Steaming or firing tea leaves inactivates polyphenol oxidase and stops the fermentation process. Although there are thousands of tea varieties, teas may be divided into 3 groups based on the amount of fermentation they undergo during processing (14). White teas are unfermented teas made from very young tea leaves or buds that are steamed immediately after harvest to inactivate polyphenol oxidase and then dried. Consequently, white teas usually contain higher concentrations of catechins than other teas. Tea leaves that are destined to become green teas are withered by air drying before heat inactivation of polyphenol oxidase. Although still rich in catechins, green teas may have slightly lower catechin concentrations than white teas. During the processing of black teas, tea leaves are rolled and allowed to oxidize or ferment fully, resulting in high concentrations of theaflavins and thearubigins and relatively low catechin concentrations (16). Oolong teas are only partially fermented they are allowed to oxidize for shorter periods than black teas. Consequently, oolong teas fall between green and black teas with respect to their catechin concentrations. Because different categories of tea contain various amounts of catechins, theaflavins, and thearubigins and have different bioavailability, it is important to distinguish different categories of tea consumed when examining tea consumption and chronic disease risk. Estimation of dietary flavonoid intake of the U.S. population As the first step of the project on antioxidant research, our research team estimated the individual and total flavonoid intake of U.S. adults by utilizing the NHANES and the USDA flavonoid databases (12). The USDA has recently released 2 separate databases for flavonoid and isoflavone content in food commodities. The flavonoid database presents the most abundant 19 individual flavonoid compounds in 234 selected food items (17). The isoflavone database was generated by extensive sampling of 108 soy-containing foods and subsequent analysis at Iowa State University (18). By linking these 2 databases combined with individual food consumption data and individual serum or urinary biomarkers, we estimated the individual flavonoid intake to investigate the role of flavonoid intake on reducing risks of certain chronic diseases. To link the NHANES food consumption data to the USDA flavonoid databases, we took the following steps in this study: food items in NHANES dietary recalls were converted to the USDA standard reference codes using the food recipe book; weight of food consumed was adjusted using moisture content adjustment data; and separately, both flavonoid databases were combined (flavonoids plus isoflavones); and then, individual food consumption data were linked to this combined flavonoid 1544S Supplement

3 TABLE 2 Compound Major food sources of dietary total and individual flavonoid intakes of U.S. adults 1 Rank Intake, mg/d Food or food group % TABLE 3 Sociodemographic lifestyles and dietary characteristics of tea consumers and tea nonconsumers 1 Subgroup Tea consumers Tea nonconsumers P-value 2 Total flavonoids Tea Citrus fruit juice Wine Citrus fruits Fruitades and fruit drinks 1.4 Flavonols Tea Other vegetable Mixture mainly meat, poultry, and fish Mixture mainly grain Apple 4.3 Flavones Mixture mainly grain Other vegetable Fat, oil, and dressing Mixture mainly meat, poultry, and fish Mixture mainly vegetable 2.1 Flavanones Citrus fruit juice Citrus fruits Fruitades and fruit drink Noncitrus juice and nectar Miscellaneous alcoholic beverage 0.9 Flavan-3-ols Tea Wine Apple Other fruit and mixture Milk drink 0.1 Anthocyanidins Wine Melon and berries Other fruit and mixture Cake, pie, and pastries Quick bread, pancakes, waffles, French 1.9 toast Isoflavones Legumes Fluid milk Mixture mainly grain Mixture mainly meat, poultry, and fish Other vegetable Adapted with permission from Chun et al. (12); n ¼ 8,809. database. Individual flavonoid intake was determined by multiplying the content of the individual flavonoid by the daily consumption of the selected food item. The total flavonoid intake was the sum of individual flavonoid intakes. Estimated mean daily total flavonoid intake, mg/d, was mainly from flavan-3-ols (83.5%), followed by flavanones (7.6%), flavonols (6.8%), anthocyanidins (1.6%), flavones (0.8%), and isoflavones (0.6%) (Table 1) (12). The flavonoid density of diets increased with age (P, 0.01) and income (P, 0.05): higher in women (P, 0.01), whites (P, 0.01), and vitamin supplement users (P, 0.01); and lower in adults with high levels of nonleisure-time physical activity (P, 0.01) compared with their counterparts (12). The mean daily intake of flavonoids was mainly from the following foods: tea (157 mg), citrus juices (8 mg), wine (4 mg), and citrus fruits (3 mg) (Table 2). Sociodemographic and dietary characteristics of tea consumers Limited information has been available on correlation among sociodemographic characteristics, major foods and food groups, Sample, n Energy intake, kj/d NS Age, y ,0.01 Woman, % ,0.01 White, % ,0.01 Poverty income ratio ,0.01 Physical activity level ,0.01 Dietary supplement use, 6 % ,0.01 Total flavonoid intake, g/d ,0.01 Flavonols ,0.01 Flavones NS Flavanones NS Flavan-3-ols ,0.01 Anthocyanidines NS Isoflavones NS 1 Divided into 2 groups according to tea consumption based on a 24-h dietary recall of U.S. adults in the NHANES P-values are from t-test for the difference of means between tea consumers and nonconsumers. NS, not significant (P $ 0.05). 3 Values are percentages or means 6 SEM, n ¼ Ratio of the median family income over the poverty index. A poverty income ratio of #1.30 is required to be eligible for food assistance programs. 5 Nonleisure-time physical activity level: daily activities including work, housework if a homemaker, going to and attending classes if a student, and normal activities throughout a typical day if a retiree or unemployed: 1 ¼ sitting during the day and not walking about very much; 2 ¼ standing or walking about a lot during the day but not having to carry or lift things very often; 3 ¼ lifting a light load or having to climb stairs or hills often; 4 ¼ doing heavy work or carrying a heavy load. 6 Dietary supplement use denotes taking any dietary supplements. and flavonoid intake associated with tea consumption. The second study aimed to test these specific hypotheses: 1) tea consumers and nonconsumers share common sociodemographic characteristics; 2) tea consumers health-related behaviors differ from those of tea nonconsumers; 3) tea consumers total flavonoid intake and its component compounds differ from those in tea nonconsumers; and 4) the major food sources of dietary flavonoid intake of tea consumers differ from those of tea nonconsumers. Tea consumers comprised 21.3% of the 8809 U.S. adults who participated in the NHANES and were more likely to be older, female, white, and to have lower income than tea nonconsumers (P, 0.01) (Table 3). Tea consumers tend to have lower physical activity levels (P, 0.01) and to take dietary supplements (P, 0.01) than their counterparts. Flavonoid FIGURE 1 Flavonoid intake by deciles of U.S. adult tea consumers and nonconsumers: NHANES Major contribution of tea to flavonoid intake 1545S

4 TABLE 4 Daily dietary total and individual flavonoid intakes of U.S. adult tea consumers and nonconsumers 1 Flavonols Flavones Flavanones Flavan-3-ols Anthocyanidins Isoflavones Total Tea consumers, n ¼ 1875 mg/d Bread, cereal, rice, and pasta Vegetables Fruits Milk, yogurt, and cheese Meat, poultry, fish, dry beans, eggs, and nuts Fats Sweets and beverages Tea nonconsumers, n ¼ 6934 Bread, cereal, rice, and pasta Vegetables Fruits Milk, yogurt, and cheese Meat, poultry, fish, dry beans, eggs, and nuts Fats Sweets and beverages Values are means 6 SEM. intake of tea consumers was far higher than that of tea nonconsumers (697.9 vs mg/d) (Fig. 1), and flavonols and flavan-3-ols, major tea flavonoids, were primarily responsible for the difference (P, 0.01) (Table 4). Tea, citrus juices, citrus fruits, and wines were the major food source of flavonoids for tea consumers; and citrus juices, wines, citrus fruits, fruitades, and fruit drinks provided major sources for tea nonconsumers. The difference in flavonoid intake between tea consumers and nonconsumers was not a result of differences in dietary selections but of the percentage of tea consumers and prevalence of tea consumption. Future research direction Because both flavonoids and antioxidant vitamins exert antioxidant activities, the logical progression of future research efforts is to estimate total antioxidant activities in dietary intake. Continued efforts are also required to update the recently released USDA flavonoid databases, to differentiate different types of teas, and to estimate amounts of antioxidants taken through various supplements. Sociodemographic characteristics differ in antioxidant intake and also in chronic disease prevalence. The implied relation between antioxidant intake and the prevalence of chronic diseases should be investigated further. Dietary assessment of flavonoid intake by way of tea consumption is required to establish the optimal level of tea consumption. Well-controlled interventional trials are also needed to solidify the evidence of the protective effects of tea consumption on reducing the risks of chronic diseases in a free-living population. Other articles in this supplement include references (19 28). Literature Cited 1. Knekt P, Kumpulainen J, Jarvinen R, Rissanen H, Heliovaara M, Reunanen A, Hakulinen T, Aromaa A. Flavonoid intake and risk of chronic diseases. Am J Clin Nutr. 2002;76: Hertog MGL, Feskens EJM, Hollman PCH, Katan MB, Kromhout D. Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen elderly study. Lancet. 1993;342: Hertog MGL, Kromhout D, Aravanis C, Blackburn H, Buzina R, Fidanza F, Giampaoli S, Jansen A, Menotti A, et al. Flavonoid intake and long-term risk of coronary heart disease and cancer in the seven countries study. Arch Intern Med. 1995;155: Hollman P, Hertog M, Katan M. Role of dietary flavonoids in protection against cancer and coronary heart disease. 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Introduction to the Proceedings of the Fourth International Scientific Symposium on Tea and Human Health. J Nutr. 2008;138:1526S 8S. 20. Henning SM, Choo JJ, Heber D. Nongallated compared with gallated flavan-3-ols in green and black tea are more bioavailable. J Nutr. 2008;138:1529S 34S. 21. Auger C, Mullen W, Hara Y, Crozier A. Bioavailability of polyphenon E flavan-3-ols in humans with an ileostomy. J Nutr. 2008;138:1535S 42S. 1546S Supplement

5 22. Kuriyama S. The relation between green tea consumption and cardiovascular disease as evidenced by epidemiological studies. J Nutr. 2008; 138:1548S 53S. 23. Grassi D, Aggio A, Onori L, Croce G, Tiberti S, Ferri C, Ferri L, Desideri G. Tea, flavonoids, and NO-mediated vascular reactivity. J Nutr. 2008;138:1554S 60S. 24. Arts ICW. A review of the epidemiological evidence on tea, flavonoids, and lung cancer. J Nutr. 2008;138:1561S 6S. 25. Hakim IA, Chow HHS, Harris RB. Green tea consumption is associated with decreased DNA damage among GSTM1 positive smokers regardless of their hogg1 genotype. J Nutr. 2008;138: 1567S 71S. 26. Kelly SP, Gomez-Ramirez M, Montesi JL, Foxe JJ. L-Theanine and caffeine in combination affect human cognition as evidenced by oscillatory alphaband activity and attention task performance. J Nutr. 2008;138:1572S 7S. 27. Mandel SA, Amit T, Kalfon L, Reznichenko L, Youdim MBH. Targeting multiple neurodegenerative diseases etiologies with multimodal-acting green tea catechins. J Nutr. 2008;138:1578S 83S. 28. Stote KS, Baer DJ. Tea consumption may improve biomarkers of insulin sensitivity and risk factors for diabetes. J Nutr. 2008;138:1584S 8S. Major contribution of tea to flavonoid intake 1547S