The Journal of Nutrition Nutrient Requirements and Optimal Nutrition

Estimation of Antioxidant Intakes from Diet and Supplements in U.S. Adults1–3 Ock K. Chun,4* Anna Floegel,4 Sang-Jin Chung,5 Chin Eun Chung,6 Won O. Song,7 and Sung I. Koo4 4 Department of Nutritional Sciences, University of Connecticut, Storrs, CT 06269; 5Department Foods and Nutrition, Kookmin University, Seoul, Korea 136-702; 6Department of Food and Nutrition, Ansan College, Ansan, Korea 426-701; and 7Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI 48824

Abstract The importance of antioxidants in reducing risks of chronic diseases has been well established; however, antioxidant intakes by a free-living population have not yet been estimated adequately. In this study, we aimed to estimate total antioxidant intakes from diets and supplement sources in the U.S. population. The USDA Flavonoid Database, food consumption data, and dietary supplement use data of 8809 U.S. adults aged $19 y in NHANES 1999–2000 and 2001–2002 were used in this study. Daily total antioxidant intake was 208 mg vitamin C (46 and 54% from diets and supplements, respectively), 20 mg a-tocopherol (36 and 64), 223 mg retinol activity equivalents carotenes (86 and 14), 122 mg selenium (89 and 11), and 210 mg flavonoids (98 and 2). Antioxidant intakes differed among sociodemographic subgroups and lifestyle behaviors. Energy-adjusted dietary antioxidant intakes were higher in women, older adults, Caucasians, nonconsumers of alcohol (only for vitamin C and carotenes), nonsmokers (only for vitamin C, vitamin E, and carotenes), and in those with a higher income and exercise level (except for flavonoids) than in their counterparts (P , 0.05). Consumption of fruits, vegetables, and whole grains may be a good strategy to increase antioxidant intake. The possible association between antioxidant intake and the prevalence of chronic diseases should be investigated further. J. Nutr. 140: 317–324, 2010.

Introduction An inverse association has been well established between dietary intake of fruits and vegetables, which are rich sources of antioxidants, and cardiovascular disease (CVD),8 when environmental and lifestyle risk factors are controlled (1,2). With the advancement of science, varying forms of natural antioxidants with different strengths are being discovered in dietary sources and dietary supplements. However, the health benefits of antioxidant intake in reducing oxidative stress and inflammatory process remains inconclusive (3–5). This is partially due to the incompleteness of the intake data in various forms and doses of antioxidants. Furthermore, antioxidants are present in human diets in many different chemical forms, e.g. flavonoids, carotenes, vitamin C, vitamin E, and selenium. In fruits and vegetables, vitamin C contributes only ~14% of the total antioxidant capacity and phenolic phytochemicals such as flavonoids contribute the most (6,7). The phenolic compounds that are the major sources of total antioxidant capacity and prevent LDL oxidation are quercetin in apples 1

Supported by Beginning Grant in Aid no. 0865092E from the AHA. Author disclosures: O. K. Chun, A. Floegel, S-J. Chung, C. E. Chung, W. O. Song, and S. I. Koo, no conflicts of interest. 3 Supplemental Tables 1 and 2 are available with the online posting of this paper at jn.nutrition.org. 8 Abbreviations used: CVD, cardiovascular disease; DR, dietary recall; MET, metabolic equivalent; PIR, poverty income ratio; RAE, retinol activity equivalent. * To whom correspondence should be addressed. E-mail: [email protected]. 2

and onions; catechin, procyanidin, quercetin, and kaempferol in grapes and wines; and genistein in soybeans (8–10). Recently, high consumption of flavonoids and isoflavones by Japanese women was related to their lower incidence of CVD (11). Flavonoids and their derivatives are the most abundant group of polyphenolics with antioxidant properties in diets (7). The protective effect of flavonoid-rich foods on risk of chronic diseases has been explained by their antioxidant properties (12–15), whereas others reported no associations between flavonoid intake and CVD risks (16–19). In 3 European studies conducted in Finland (20), 7 European countries (21), and the Netherlands (Zutphen) (22), the sum of dietary intakes of only 5 common flavonoids (apigenin, luteolin, kaempferol, myricetin, and quercetin) was inversely associated with the risks of CVD. In studies conducted in the US (17–19), however, no association was observed between flavonoid intake and CVD risks. These studies quantitated only partial intakes of all antioxidants because of methodological limitations imposed by lack of flavonoid composition in foods, which were not available until recently. The importance of antioxidants in reducing risks of chronic diseases has been extensively studied; however, antioxidant intake in a free-living population has not yet been estimated adequately. Recently, our research group reported estimates of the total dietary flavonoid intake of the U.S. population based on the recently released USDA flavonoid databases matched with food consumption data from the NHANES 1999–2002 (23). Building

0022-3166/08 $8.00 ã 2010 American Society for Nutrition. Manuscript received August 13, 2009. Initial review completed September 08, 2009. Revision accepted November 24, 2009. First published online December 23, 2009; doi:10.3945/jn.109.114413.

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upon our previous research scheme to estimate flavonoid intake, the present study aimed to document total antioxidant intakes from diets and supplement sources in U.S. adults and sociodemographic subgroups.

Materials and Methods Study population. The National Center for Health Statistics has conducted the NHANES to obtain nationally representative information on the health and nutritional status of the U.S. population. All interviewed persons were invited to the mobile examination center, where the 24-h dietary recall (DR) and questionnaires on dietary supplement use were administered. A total of 8809 individuals over 19 y old in NHANES 1999–2000 and 2001–2002 were included in this study. This study included vitamin C, vitamin E, carotene, flavonoid, and selenium intakes from diet and dietary supplements to estimate the individual and total antioxidant intakes. The U.S. adult population was grouped by sociodemographic and lifestyle variables: age (19–30, 31–50, 51–70, $70 y), gender, ethnicity (non-Hispanic white; non-Hispanic black; Mexican-American; others), BMI (,20, 20–24.9, 25–29.9, $30), poverty income ratios (PIR) (,1.85, $1.85), alcohol consumption (yes or no to “at least 12 drinks/ y”), current smoking (yes or no to “current smoking” and “smoked cigarettes, cigars, or pipes and/or used chewing tobacco or snuff at least once during the past 30 d”), and exercise levels [expressed as the metabolic equivalent (MET) score calculated by combining the intensity level of the leisure time activities reported, mean duration, and frequency] (24,25). Food consumption data. Dietary antioxidant vitamin, selenium, and flavonoid intakes were estimated based on one 24-h DR (midnight to midnight) of the NHANES 1999–2002 (24,25). DR data contained all foods and beverages consumed by the respondents except for plain drinking water. To minimize errors from misreporting, individuals with unreliable or incomplete DR records were excluded as noted by the National Center for Health Statistics (26). USDA flavonoid databases. Details of the datasets used in this study were reported in our previous study (23). Briefly, we created 1 flavonoid database from 2 different data sets released in recent years: 1) the USDA Database for the Flavonoid Content of Selected Food (27) includes the most abundant 19 individual flavonoid compounds in 5 flavonoid subgroups (flavonols, flavones, flavanones, flavan-3-ols, and anthocyanidins) in 234 selected foods; 2) The USDA-Iowa State University Database on the Isoflavone Content of Foods (28) was created by extensive sampling of 108 soy-containing foods and subsequent analysis at Iowa State University. The combined flavonoid database consisted of 24 flavonoid compounds: flavonols (quercetin, kaempferol, myricetin, isorhamnetin), flavones (luteolin, apigenin), flavanones (eriodictyol, hesperetin, naringenin), flavan-3-ols (catechins, epicatechins, theaflavins, thearubigins), anthocyanidins (cyanidin, delphinidin, malvidin, pelargonidin, peonidin, petunidin), and isoflavones (daidzein, genistein, glycitein, biochanin A, formononetin). To improve the coverage of the estimated flavonoid intake, we expanded the flavonoid database according to the preestablished protocol that has been described extensively in a separate publication (23). Estimation of dietary antioxidant intakes. We matched the NHANES food consumption data with the flavonoid database following the steps described in our previous work (23): 1) conversion of food items in NHANES DR to USDA Standard Reference codes using food recipe book and food description data file for NHANES food codes; 2) weight adjustment using moisture content; 3) code modification using the USDA food unit conversion search program; and 4) linking food intake data with the flavonoid database. Daily individual flavonoid intake from selected foods was determined by multiplying the content of the individual flavonoid (mg aglycone equivalent/100 g food) by the daily consumption (g/d) of the selected food item. Data on individual 318

Chun et al.

participants’ daily dietary intakes of antioxidant vitamins and selenium were available in the NHANES 1999–2002 (24,25). Estimation of antioxidant intakes from dietary supplement use. The information on dietary supplement use in NHANES 1999–2002 enables investigators to estimate the individual participant’s antioxidant vitamin, selenium, and flavonoid intakes from dietary supplements. Dietary supplement data files in the NHANES 1999–2000 and 2001– 2002 consist of 5 files: supplement counts, supplement records, supplement information, ingredient information, and blend information (24,25). To calculate the intakes of antioxidant nutrients from the supplement, vitamin C, vitamin E, carotenes, selenium, and flavonoids were selected from the ingredient information file. Next, nutrient composition table of supplements containing the antioxidants was made using the supplement information file. The antioxidant intakes from the supplements were calculated using the supplement counts file, supplement records file, and the nutrient composition table of supplements. Ingredient units in the supplements were converted to the Dietary Reference Intakes units. Nutrient compounds in the supplement were converted to the elemental nutrients; e.g. the conversion factor of 43% for ascorbyl palmitate to ascorbic acid was used (29). In merging the nutrient intake datasets of NHANES 1999–2000 and 2001–2002, dietary intake data on carotenoids and vitamin E needed to match their nutrient units. Among 6 carotenoids (a-carotene, bcarotene, b-cryptoxanthin, lycopene, lutein, and zeaxanthin) available in the NHANES 2001–2002 dataset, only a-carotene and b-carotene intake data were used in this study to estimate carotene intake in the form of retinol activity equivalent (RAE), because the NHANES 1999– 2000 provides carotene intake (a-carotene + b-carotene) data only. For the supplement label expressed as “b-carotene-% of vitamin A,” the content of b-carotene in the supplements was calculated after the content of vitamin A in the supplement was found. Vitamin E has several different units for the expression of its activity. In the 1980 Recommended Dietary Allowances (30), units for vitamin E were changed from IU to a-tocopherol equivalents taking into account the activity of not only a-tocopherol, but also gtocopherol and d-tocopherol and tocotrienols. The 2000 Recommended Dietary Allowances and estimated average requirements (29) for vitamin E were based only on 2 R, 49 R, 89 R-(RRR)-a-tocopherol, the form found in food, and the 2R-stereoisomeric forms of a-tocopherol that occur in fortified foods and supplements. The other tocopherols and tocotrienols do not contribute toward meeting the vitamin E requirement (29). Vitamin E was represented as a-tocopherol equivalents in the NHANES 1999–2000 data file but as mg of a-tocopherol in the NHANES 2001–2002 data file. Therefore, in merging the both data files, a-tocopherol intake from diet and dietary supplements were solely taken into consideration as vitamin E intake and expressed as mg of a-tocopherol. In merging the dietary supplement data of NHANES 1999–2000 and 2001–2002, the flavonoid intake from dietary supplements was expressed on the total amount of flavonoid intake regardless of the subcategories of flavonoids consumed. Lists of antioxidant nutrients in NHANES 1999–2000 and NHANES 2001–2002 are shown in Supplemental Table 2. Statistical analyses. All statistical analyses were carried out with SAS software, release 8.1, 2000 (SAS Institute) and the Survey Data Analysis for multi-stage sample designs professional software package (SUDAAN, release 8.0.2, 2003, Research Triangle Institute). Sample weights were applied to all analyses to account for the unequal probability of selection, noncoverage, and nonresponse bias resulting from oversampling of low-income persons, adolescents, the elderly, African-Americans, and Mexican-Americans. Arithmetic means of dietary total and individual antioxidant intake of subpopulations grouped by sociodemographic and lifestyle variables were determined. SEM was calculated by the linearization (Taylor series) variance estimation method for population parameters by SUDAAN. We used t tests and ANOVA to test for overall differences of antioxidant intakes from diet and supplements by sociodemographic and lifestyle variables such as gender, income, and smoking, etc. The

trends of antioxidant intakes by the weight and frequency of specific food groups consumed were tested using linear contrasts after adjusting for gender, age, ethnicity, BMI, PIR, current smoking status, and exercise level. The contribution of each food group to the daily total antioxidant intake was calculated as the ratio of the antioxidant intake from that food group to the total intake from all foods. Values in the text are means 6 SD.

Results Daily antioxidant intakes from diets. The individual and total antioxidant intakes from diet were estimated by combin-

TABLE 1

ing the USDA Flavonoid databases and 24-h DR in the NHANES 1999–2002 (Table 1). Energy-adjusted dietary antioxidant intake increased with age (P-trend , 0.001), income (P-trend , 0.01), and exercise level (P-trend , 0.05, except for flavonoids). BMI was positively associated with selenium intake (P-trend , 0.01) but inversely associated with vitamin C (P-trend , 0.01) and E (P-trend , 0.1) intakes. Energy-adjusted dietary antioxidant intake was also higher in women than in men (P , 0.001 except for selenium). Alcohol consumers had lower vitamin C and carotene intakes than nonconsumers of alcohol (P , 0.01) and current smokers consumed less vitamin C, vitamin E, and carotenes from diet

Daily antioxidant intakes from diet by U.S. adults aged $19 y and by sociodemographic and lifestyle subgroups (NHANES 1999–2002)1

Survey phase Phase I (1999–2000) Phase II (2001–2002) Gender All Men Women Age, y 9–30 31–50 51–70 $70 Ethnicity Non-Hispanic white Non-Hispanic black Mexican-American Others BMI ,20 20 to #25 25 to #30 $30 PIR3 ,1.0 1.0–1.3 1.3–1.85 $1.85 Alcohol consumption4 No Yes Current smoking5 No Yes Exercise level6 0 T1 T2 T3

Vitamin C

Vitamin E

Carotenes

Stratified sample, n

mg/d

P-value2 mg/d a-tocopherol P-value2

mg/d RAE

4175 4634

97.2 6 4.7 94.0 6 3.3

7.0 6 0.1 7.1 6 0.2

195.9 6 11.7 189.2 6 9.2

8809 4461 4348 8809 1873 2835 2582 1519 8809 4212 1762 2141 694 8527 471 2415 3031 2610 7897 1503 820 1078 4496 7953 2531 5422 8335 4247 4088 8045 3329 1581 1566 1569

95.5 6 2.8 104.6 6 3.4 86.6 6 2.7

,0.001

7.1 6 0.1 8.0 6 0.1 6.2 6 0.1

,0.001 96.5 93.2 99.4 93.0

6 6 6 6

4.2 4.2 3. 2.8

92.3 103.1 115.9 96.2

6 6 6 6

3.2 4.2 2.9 4.6

99.5 104.5 92.5 90.1

6 6 6 6

90.6 80.1 84.0 101.1

6 6 6 6

6 0.1 6 0.2 6 0.2 6 0.2

,0.001

7.4 6.2 6.5 5.9

6 0.1 6 0.2 6 0.1 6 0.2

9.1 3.9 2.6 2.8

,0.01

7.1 7.4 7.0 7.0

3.4 6.4 3.7 3.2

,0.01

6.0 5.8 6.7 7.5

95.2 6 2.9 94.6 6 3.2 102.1 6 3.2 88.1 6 3.1 6 6 6 6

2.3 4.3 3.4 5.7

192.3 6 7.4 185.9 6 8.1 198.6 6 9.8

,0.001 6.8 7.5 47.1 6.0

81.5 88.9 106.1 113.8

,0.001

6 9.3 6 12.0 6 8.3 6 12.0

,0.001

192.5 213.2 163.6 189.3

6 9.4 6 18.5 6 8.1 6 16.4

6 0.4 6 0.2 6 0.1 6 0.2

,0.1

198.4 208.5 188.1 180.9

6 18.1 6 10.7 6 9.5 6 6.8

6 0.2 6 0.2 6 0.5 6 0.1

,0.001

182.6 145.6 161.0 205.2

6 14.9 6 11.5 6 13.4 6 8.9

,0.001

6.4 6 0.1 7.3 6 0.1

0.393

,0.001

7.2 6 0.1 6.9 6 0.1

,0.001

6.2 7.2 7.6 8.0

Flavonoids

P-value2

mg/d

109.4 6 1.4 107.7 6 1.6 ,0.001

108.5 6 1.1 128.5 6 1.6 89.2 6 1.3

,0.001 143.5 194.7 217.6 215.9

6 0.1 6 0.2 6 0.2 6 0.3

Selenium

P-value2

mg/d

P-value2

209.8 6 18.9 204.5 6 14.5 0.896

207.0 6 11.8 214.1 6 13.8 200.2 6 12.1

,0.001

,0.001

,0.001

114.5 6 113.9 6 104.9 6 85.0 6

1.6 1.7 1.5 1.3

6 6 6 6

1.3 2.2 2.7 3.4

102.5 6 110.0 6 109.7 6 108.3 6

2.7 2.1 1.5 1.6

,0.01

99.5 6 97.7 6 103.5 6 113.0 6

2.2 2.9 2.7 1.3

203.9 6 13.5 187.4 6 6.9

,0.001

94.7 6 1.7 114.1 6 1.2

0.264

173.1 6 12.1 222.5 6 13.7

0.281

,0.05

213.5 6 9.3 174.1 6 7.6

,0.001

106.6 6 1.3 110.2 6 1.7

0.318

204.2 6 12.8 211.2 6 14.5

0.772

,0.001

178.1 172.6 220.8 214.9

,0.05

102.6 110.8 113.0 115.3

197.1 6 214.3 6 198.8 6 229.7 6

0.620

6 6.4 6 9.6 6 13.7 6 16.1

,0.01

0.168

109.5 106.4 108.6 103.7

6 6 6 6

1.8 2.0 2.2 2.9

189.9 6 210.1 6 233.7 6 163.0 6

18.0 13.3 16.8 11.5

235.3 6 142.8 6 114.6 6 138.8 6

14.9 9.6 9.3 18.0

,0.001

,0.01

178.9 6 206.3 6 205.7 6 219.3 6

25.9 15.6 16.1 14.7

0.168

,0.01

144.7 6 193.3 6 160.5 6 232.6 6

12.8 18.1 17.9 14.4

0.272

,0.01

11.5 22.0 14.6 15.1

,0.01

Values are means 6 SD. P-values are for overall difference by t test or ANOVA among males and females, age subgroups, ethnicities, income levels, alcohol consumption, smoking, and exercise levels after adjusting for total energy intake. 3 Ratio of the median family income:poverty index. A PIR #1.30 is required to be eligible for food assistance programs. 4 Yes means to consume $12 alcoholic beverages/y. 5 Yes means smoked cigarettes, cigars, or pipes, or used chewing tobaccos or snuffs at least once during the past 30 d. 6 Exercise levels, expressed as the MET score, were calculated by combining the intensity level of the leisure time activities reported, mean duration, and frequency. 1 2

Antioxidant intake from the U.S. diet and supplements

319

than nonsmokers (P , 0.05). Caucasians consumed more vitamin E and flavonoids (P-trend , 0.001) and less vitamin C and carotenes from diet (P-trend , 0.01). Antioxidant intakes from dietary supplements. The individual and total antioxidant intakes from dietary supplements were estimated based on the data of dietary supplement use in the NHANES 1999–2002 (Table 2). Almost one-half of the participants (48%) took at least 1 supplement per day and antioxidant intake from supplements differed among sociodemographic subgroups of U.S. adults (data not shown). Energy-adjusted antioxidant intakes from dietary supplements

TABLE 2

were higher in women (P , 0.05), older adults (P-trend , 0.001 except for flavonoids, P-trend , 0.1), Caucasians (P-trend , 0.01), those with higher exercise levels (except for flavonoids), and higher income subgroups (P-trend , 0.01). Total antioxidant intakes. Total antioxidant intakes were calculated by summing each participant’s antioxidant intake from diet and dietary supplements. Daily total antioxidant intake was 207.9 6 7.1 mg vitamin C (46 and 54% from diets and supplements, respectively), 19.8 6 0.7 mg a-tocopherol (36 and 64%), 222.6 6 8.1 mg RAE carotenes (86 and 14%),

Daily antioxidant intakes from dietary supplements by U.S. adults aged $19 y and by sociodemographic and lifestyle subgroups (NHANES 1999–2002)1

Survey phase Phase I (1999–2000) Phase II (2001–2002) Gender All Men Women Age, y 19–30 31–50 51–70 $70 Ethnicity Non-Hispanic white Non-Hispanic black Mexican-American Others BMI ,20 20 to #25 25 to # 30 $30 PIR3 ,1.0 1.0–1.3 1.3–1.85 $1.85 Alcohol consupmtion4 No Yes Current smoking5 No Yes Exercise level6 0 T1 T2 T3

Vitamin C

Stratified sample, n

mg/d

4175 4634

114.9 6 7.7 110.3 6 10.0

8809 4461 4348 8809 1873 2835 2582 1519 8809 4212 1762 2141 694 8527 471 2415 3031 2610 7897 1503 820 1078 4496 7953 2531 5422 8335 4247 4088 8045 3329 1581 1566 1569

112.4 6 6.4 100.3 6 7.3 124.1 6 8.3

Vitamin E

P-value2

mg/d a-tocopherol

Carotenes P-value2

13.8 6 1.1 11.7 6 0.8

,0.001

12.7 6 0.7 11.3 6 0.7 14.1 6 0.9

mg RAE

P-value2

35.5 6 3.1 25.7 6 2.6

,0.001

30.3 6 2.0 31.4 6 3.0 29.2 6 1.8

Selenium mg/d

Flavonoids

P-value2

13.2 6 1.2 14.4 6 1.2

,0.05

13.8 6 0.8 13.6 6 1.0 14.0 6 0.9

mg/d

P-value2

3.6 6 1.1 2.9 6 0.7

,0.01

3.2 6 0.6 2.0 6 0.3 4.3 6 1.1

,0.01

51.0 103.7 159.3 150.4

6 6.6 6 8.5 6 13.5 6 10.2

,0.001

2.8 6 9.5 6 21.8 6 22.2 6

0.4 0.9 1.3 1.3

,0.001

14.5 31.4 35.6 43.7

6 2.2 6 3.6 6 3.8 6 4.9

,0.001

6.5 6 14.3 6 17.6 6 16.7 6

0.9 1.3 1.4 1.5

,0.001

2.7 6 2.1 6 5.7 6 2.5 6

1.7 0.4 1.5 0.7

,0.1

134.4 44.9 45.6 74.0

6 8.7 6 4.5 6 5.6 6 9.5

,0.001

15.4 6 5.8 6 4.9 6 6.4 6

0.9 0.6 0.5 1.0

,0.001

35.9 17.4 12.6 16.7

6 2.7 6 2.6 6 1.3 6 2.2

,0.001

16.2 6 7.3 6 7.2 6 8.4 6

1.0 0.8 0.9 1.2

,0.001

4.1 6 0.9 6 1.6 6 0.8 6

0.9 0.3 0.6 0.2

,0.01

98.7 126.9 112.2 103.1

6 22.0 6 12.2 6 6.6 6 9.0

0.138

10.1 6 14.1 6 12.9 6 11.9 6

2.2 1.1 0.7 1.0

0.158

28.3 30.1 27.1 35.8

6 8.3 6 3.2 6 2.4 6 4.9

0.483

6 6 6 6

2.9 1.1 1.1 1.6

0.845

2.4 6 4.9 6 2.6 6 2.5 6

0.9 1.7 0.6 0.6

46.2 73.7 61.6 139.4

6 5.7 6 10.5 6 7.1 6 9.5

,0.001

5.1 6 8.4 6 9.0 6 15.3 6

0.7 1.5 1.6 0.9

,0.001

12.9 20.5 20.3 37.5

6 3.4 6 2.7 6 5.2 6 3.1

,0.001

8.5 6 15.6 6 8.8 6 16.2 6

1.6 3.7 1.5 1.0

,0.001

1.2 6 0.7 6 1.8 6 3.7 6

0.5 0.2 0.7 0.7

,0.05

31.3 6 3.7 31.2 6 2.9

0.263

13.4 6 1.3 14.5 6 0.9

0.577

3.4 6 1.1 2.8 6 0.5

0.337

32.2 6 2.9 29.3 6 2.2

0.266

13.9 6 0.9 14.0 6 1.2

0.444

3.6 6 0.9 2.9 6 0.6

0.819

6 2.7 6 3.9 6 5.3 6 3.8

,0.001

2.5 6 2.8 6 4.3 6 2.9 6

0.344

103.2 6 7.2 118.5 6 8.3

0.569

14.6 6 1.4 12.6 6 0.7

112.5 6 5.3 115.1 6 9.5

0.756

12.7 6 0.7 13.2 6 0.9

76.4 113.0 139.8 140.9

6 5.5 6 12.2 6 12.4 6 12.4

,0.001

9.4 6 11.7 6 15.9 6 15.7 6

0.6 1.3 1.3 1.2

0.858

,0.01

19.9 30.3 39.9 38.0

12.0 13.7 14.0 14.3

9.5 6 16.0 6 14.1 6 17.7 6

1.2 1.7 1.0 1.4

,0.01

1.2 0.7 1.3 0.5

0.553

,0.01

Values are means 6 SD. P-values are for overall difference by t test or ANOVA among males and females, age subgroups, ethnicities, income levels, alcohol consumption, smoking, and exercise levels after adjusting for total energy intake. 3 Ratio of the median family income:poverty index. A PIR #1.30 is required to be eligible for food assistance programs. 4 Yes means to consume $12 alcoholic beverages/y. 5 Yes means smoked cigarettes, cigars, pipes or used chewing tobaccos or snuffs at least once during the past 30 d. 6 Exercise levels, expressed on the MET score, were calculated by combining the intensity level of the leisure time activities reported, mean duration, and frequency. 1 2

320

Chun et al.

122.3 6 1.2 mg selenium (89 and 11%), and 210.2 6 12.0 mg flavonoids (98 and 2%). The impact of the consumption of specific food groups or foods on individual antioxidant intakes was investigated by testing the linear tends in individual dietary and total antioxidant intakes by the consumption of specific food groups, such as fruits and fruit juices, vegetables and vegetable products, wines, and teas. Only flavonoid intake from diet was used in the analysis, because intake from was accounted for ,2% of the total in this study. After adjusting for gender, age, ethnicity, BMI, PIR, current smoking, and exercise level, fruit and fruit juice consumption was positively associated with dietary and total intake of vitamin C, carotenes, vitamin E, and selenium (P , 0.05). Vegetable and vegetable product consumption was positively associated with dietary and total intakes of all individual antioxidants (P , 0.001); wine consumption with total carotene and dietary flavonoid intake (P , 0.1); tea consumption with total selenium intake (P , 0.05); and dietary flavonoid intake (P , 0.001) (Table 3). Participants’ selfreported frequency of food group intake based on FFQ also showed a consistent, but weaker association than the results obtained from weight-based food consumption data (Supplemental Table 1). Major dietary antioxidant sources. The major dietary sources for the dietary vitamin C intake were: citrus fruit juices, fruitaides and drinks, and other vegetables; vitamin E: mixture mainly grain, fat, oil and dressing, and mixture mainly meat, poultry, fish; carotenes: deep-yellow vegetables, dark-green vegetables, and other vegetables; selenium: yeast breads, rolls, mixture mainly meat, poultry, fish, and mixture mainly grain; and total flavonoids: tea, citrus fruit juice, and beers and ales (Table 4). Mixtures mainly grain includes foods such as burritos, tacos, pizza, egg rolls, quiche, spaghetti with sauce, rice, and pasta mixtures; frozen meals in which the main course is a grain mixture; noodle and rice soups; and baby-food macaroni and spaghetti mixtures. Citrus fruit juices were the major sources of vitamin C, contributing 23% of daily dietary vitamin C intake; vegetables were the major sources for carotene, contributing 58% of daily dietary carotene intake; and teas were identified as the most remarkable sources of flavonoids, contributing 77% of daily flavonoid intake.

Discussion The mean daily vitamin C intake in U.S. adults was 95.5 mg from diet only and 207.9 mg from both diet and supplement in the present study, suggesting that supplements are a major source for vitamin C intake in the US. Compared with our results, the Prostate, Lung, Colorectal and Ovarian Cancer Trial (31) reported a higher mean vitamin C intake of 159.7 mg/d for men who did not consume vitamin supplements compared with a lower total vitamin C intake of 177.8 mg/d for male supplement users. Data on supplement use in the Prostate, Lung, Colorectal and Ovarian Cancer Trial was, however, limited to 12 individual supplements only. In 2009, the European Prospective Investigation into Cancer and Nutrition Study (32) reported that the mean daily intake of dietary vitamin C in Europe ranged from 80.1 mg (Norway) to 200.8 mg (Greece), which is in accordance with our findings. Another European study (33) reported that the mean daily vitamin C intake from diet in elderly adults in Spain was 125.4 mg for men and 136.3 mg for women. The dietary vitamin C intake of

Europeans is overall higher than that of the U.S. population presented in this study and the difference can be explained by the fact that fruit and vegetable intake in Europe on average is higher compared with in the US (34). We reported a dietary a-tocopherol intake of 7.1 mg/d in this study, which was a bit lower than that of the European population, ranging from 7.3 mg (Sweden) to 13.3 mg (France), in the European Prospective Investigation into Cancer and Nutrition Study (32). In the present study, vitamin E intake was significantly higher in nonsmokers (7.2 mg) than in smokers (6.9 mg), which was slightly lower than, but in a good accordance with, the previous study by the Minnesota Heart Survey (35). Our estimation of vitamin E intake might be underestimated, because in our study, only a-tocopherol intake was counted for the estimation. The same study reported a mean b-carotene intake of 1064–1408 mg from diet. Dietary b-carotene intake in Europe ranged from 1600 mg/d (Spain) to 4480 mg/d (Greece) (32). Dietary flavonoid intake in our study (207 mg/d) was much higher than previous reports (36,37). This is due to the fact that previous studies were limited to a small number of flavonoids. Daily dietary selenium intake in this study (108.5 mg) was slightly lower than selenium intake reported in a Japanese study (129 6 23 mg) (38). However, the dietary selenium intake of women in this study (89.2 mg) was in accordance with a previous study of 74 young health Spanish women (83.3 mg) (39). The selenium contents in foodstuffs depend on the soil for plant food items, the feed for stockbreeding products, and the sea conditions for marine products (38). Therefore, the levels vary by dietary patterns, geographic regions, and agricultural practices. Our study found that individual and total antioxidant intake from diet and supplement differed among sociodemographic subgroups. Energy-adjusted antioxidant intake from diet increased with age, income, and exercise level (except for flavonoids) in agreement with previous studies (23,40). In 2004, Gu et al. (40) reported proanthocyanidin intake was highest in men older than 60 y. As previously reported by our research group (23), flavonoid density of the diet increased with age, income, physical activity, Caucasian descent, female sex, and vitamin supplement use. In our study, smokers consumed less vitamin C, vitamin E, and carotenes than nonsmokers. This is consistent with previous findings (35,41). Nevertheless, it raises a serious public health concern, because smokers are exposed to increased oxidative stress and have a higher demand for antioxidant vitamins than nonsmokers. Energy-adjusted antioxidant intake from supplement was higher in women, older adults (except flavonoids), Caucasians, and those with higher exercise level (except flavonoids) and higher income compared with their counterparts. These findings are in agreement with previous studies (42–44). Evaluating the NHANES III survey, Balluz et al. (42) reported that the use of supplements was highest in women, non-Hispanic whites, and participants with the highest levels of education and income. Lyle et al. (43) identified supplement users among 2152 middleand older age adults in Wisconsin. They found women; participants with high levels of education, low BMI, and active lifestyles; and nonsmokers take more supplements than their counterparts. Jasti et al. (44) reported that middle-aged or older women, Caucasians, those well-educated and with higher income levels, and residents of western parts of the US were more likely to use supplements than their counterparts. We found that consumption of fruits, fruit juices, vegetables, and wine were positively associated with dietary and total antioxidant intake. Fruit, fruit juices, and vegetables have previously been identified as major sources of antioxidant Antioxidant intake from the U.S. diet and supplements

321

TABLE 3

Mean antioxidant intake of U.S. adults aged $19 y by food group consumed from one 24-h DR (NHANES 1999–2002)1

Food group

Nonconsumers2

Fruit and fruit juices Intake, g/d 0 Participants, n 2963 Vitamin C, mg/d Food 49.2 Total 132.1 Vitamin E, mg/d a-tocopherol Food 6.2 Total 15.0 Carotenes, mg/d RAE Food 121.0 Total 145.6 Selenium, mg/d Food 103.5 Total 114.3 Dietary flavonoids, mg/d 199.4 Vegetables and vegetable products Intake, g/d 0 Participants, n 729 Vitamin C, mg/d Food 58.0 Total 145.0 Vitamin E, mg/d a-tocopherol Food 4.5 Total 13.2 Carotenes, mg/d RAE Food 42.2 Total 71.2 Selenium, mg/d Food 87.6 Total 98.6 Dietary flavonoids, mg/d 127.4 Wines Intake, g/d 0 Subjects, n 8159 Vitamin C, mg/d Food 94.7 Total 203.6 Vitamin E, mg/d a-tocopherol Food 6.9 Total 19.4 Carotenes, mg/d RAE Food 185.9 Total 214.9 Selenium, mg/d Food 107.4 Total 120.9 Dietary flavonoids, mg/d 204.0 Teas Intake, g/d 0 Subjects, n 6934 Vitamin C, mg/d Food 96.1 Total 196.9

T13

T2

Chun et al.

Food group

#124.5 #300.8 .300.8 1978 1921 1947 67.9 179.0

108.9 248.7

193.5 330.4

,0.001 ,0.001

6.9 19.2

7.4 23.5

8.4 24.8

,0.001 ,0.05

Continued Nonconsumers2

Vitamin E, mg/d a-tocopherol Food Total Carotenes, mg/d RAE Food Total Selenium, mg/d Food Total Dietary flavonoids, mg/d

P-value4

T3

T13

T2

T3

P-value4

7.1 18.6

6.7 24.3

6.9 24.7

7.5 22.3

0.176 0.209

181.8 212.2

229.1 265.5

211.4 237.4

236.4 264.8

0.132 0.316

108.0 121.2 48.7

106.4 120.5 205.6

106.0 122.6 486.5

116.0 132.3 1264.1

0.168 ,0.05 ,0.001

Values are means 6 SD. All participants who did not consume the food in the 1-d, 24-h DR were grouped as nonconsumers and all consumers were divided into tertiles by the amount of consumption. 3 T1, T2, and T3 stand for the first, second, and 3rd tertile, respectively. 4 P-values for linear trend, adjusted for gender, age, ethnicity, BMI, PIR, smoking, and exercise level. 1 2

166.3 193.7

237.3 275.2

299.4 335.3

,0.001 ,0.001

109.5 123.6 203.1

111.0 129.4 203.7

113.5 127.1 228.0

,0.01 ,0.001 0.280

#123 2693

#261.1 .261.1 2696 2691

68.9 159.4

86.9 212.9

137.5 262.6

,0.001 ,0.001

5.6 16.2

6.9 19.9

9.3 24.6

,0.001 ,0.001

75.4 100.9

172.0 205.1

356.1 388.4

,0.001 ,0.001

94.1 107.0 160.9

106.1 120.2 211.8

129.1 144.0 263.5

,0.001 ,0.001 ,0.001

#27.4 #206.5 .206.5 217 226 207 106.6 209.4

100.2 269.6

103.5 273.4

0.567 0.261

8.4 21.3

7.5 24.5

8.9 25.5

0.133 0.666

270.1 299.1

261.8 298.5

245.1 307.0

0.116 ,0.05

125.5 140.5 186.6

112.4 129.4 233.4

121.6 139.9 285.5

0.135 0.224 ,0.1

#296 641 93.7 228.3

#606.8 .606.8 613 621 98.3 269.8

89.2 233.5

0.422 0.112

(Continued)

322

TABLE 3

vitamins (45,46). Wine consumption has been associated with higher total carotene and dietary flavonoid intake in our study. It has previously been reported that supplement users have a higher intake of micronutrients from food, including vitamin C, vitamin E, and carotenoids, independent of antioxidant intake from supplements (43). This finding is similar to a previous study in that supplement users were identified to consume more wine than nonusers (42). We identified the major food sources of dietary vitamin C in the US as citrus fruit juice, fruitades, potatoes, tomatoes, and other vegetables. In agreement with our findings, Hampl et al. (45) reported the leading sources of vitamin C in the U.S. diet as fruits and fruit juices, vegetables, and vitamin C-fortified fruit drinks. A Spanish study (46) found that fruits (mainly oranges), tomato, and sweet pepper were the major sources for vitamin C in the Spanish diet. According to our findings, dietary vitamin E in the US was mainly derived from grain, fat, oil, dressing, meat, poultry, fish, potatoes, nuts, and seeds. Our findings are consistent with the reports by the U.S. Department of Health and Human Services and the USDA, who identified food items with high amounts of vitamin E (47), except for potatoes, meat, and poultry. The latter 3 are most likely to contribute to vitamin E intake because of their high amount of consumption by U.S. adults. Major food sources of dietary vitamin E in Spain were vegetable oils (sunflower and olive), noncitrus fruits, nuts, and seeds (48). Our study found deep-yellow vegetables, dark green vegetables, and other vegetables were the major food source of carotenes in the U.S. diet. This is in agreement with previous studies (46,47). The antioxidant mineral selenium was mainly consumed in yeast breads, grains, meat, poultry, fish, and eggs by U.S. adults. In agreement with our findings, a Japanese study (38) reported fish, shellfish, cereals, meat, and dairy products as the major food sources for selenium. Dietary flavonoids were primarily consumed in tea, followed by citrus fruit juice, beer, wine, and citrus fruits. Previous studies reported that onion is the major source of flavonoids in the U.S. (36). and Japanese (11) diets. However, these studies did not consider intake of tea catechins, which have previously been shown to be major contributors to total flavonoid intake by our group (23). In the Zutphen elderly study, the major sources of flavonoid intake were reported as tea, onion, and apple (37). In 2004, a research group found tea to be the major flavonoid source in the

TABLE 4

Major food sources of dietary total and individual antioxidant intakes of the U.S. population aged $19 y (n = 8809) (NHANES 1999–2002)

Compound Vitamin C, mg/d

Vitamin E, mg/d a-tocopherol

Carotenes, mg/d RAE

Selenium, mg/d

Total flavonoids, mg/d

Rank Intake

Food group

%

1 2 3 4 5 6 7 8 9 10 1

21.6 12.2 10.5 5.9 5.7 5.1 4.3 4.2 4.0 3.6 0.7

Citrus fruit juice Fruitades and drink Other vegetable Potatoes Tomatoes and mixtures Dark-green vegetable Mixture mainly meat, poultry, fish Mixture mainly grain1 Melon and berries Citrus fruits Mixture mainly grain1

22.7 12.8 11.0 6.2 5.9 5.4 4.6 4.4 4.2 3.8 9.4

2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 10

0.6 0.6 0.5 0.5 0.4 0.3 0.3 0.3 0.2 59.3 26.1 25.1 19.5 12.2 9.9 9.0 4.9 4.5 3.9 14.1 13.1 13.0 11.2 6.3 5.7 5.4 4.3 4.2 3.3

9.1 8.7 7.5 7.4 5.5 4.0 3.8 3.6 3.5 30.8 13.6 13.1 10.1 6.3 5.1 4.7 2.5 2.4 2.0 13.2 12.2 12.1 10.5 5.9 5.3 5.1 4.0 4.0 3.1

1 2 3 4 5 6 7 8 9 10

158.9 7.7 5.9 5.0 3.5 3.0 2.9 2.7 2.4 2.2

Fat, oil, and dressing Mixture mainly meat, poultry, fish Potatoes Nut and seed Ready-to-eat cereals Tomatoes and mixtures Salty snack (popcorn, pretzel, corn chip) Cake, pie, pastries Eggs Deep-yellow vegetable Dark-green vegetable Other vegetable Mixture mainly meat, poultry, fish Tomatoes and mixtures Mixture mainly grain1 Melon and berries Other fruit and mixture Citrus fruit juice Mixture mainly vegetable Yeast breads, roll Mixture mainly meat, poultry, fish Mixture mainly grain1 Meat (beef, pork, lamb) Eggs Fish and shellfish Poultry Organ meats, sausages, lunchmeats Fluid milk Quick bread, pancakes, waffles, French toast Tea Citrus fruit juice Beers and ales Wines Citrus fruits Melon and berries Other vegetable Fruitades and drinks Banana Other fruit and mixture

76.8 3.7 2.9 2.4 1.7 1.4 1.4 1.3 1.2 1.1

1 Mixture mainly grains includes foods such as burritos, tacos, pizza, egg rolls, quiche, spaghetti with sauce, rice, and pasta mixtures; frozen meals in which the main course is a grain mixture; noodle and rice soups; and baby-food macaroni and spaghetti mixtures.

Australian diet, followed by orange (48). They also found that flavonoid sources varied among different age groups. In adults, red wine was a major catechin and epicatechin source, whereas in children it was apples, apricots, and grapes. Our findings are interpreted based on several assumptions: first, the USDA food composition databases were constructed based on U.S. representative food samples, including varying cultivars, geographic origin, growing seasons, agricultural practices, and analytical methods. Second, this study focused on antioxidant intake, not bioavailability and metabolism in the human body or changes during processing and food preparation. Third, dietary intake data were based on a 24-h DR that might be a limitation of this study, because there is no scientific agreement on the minimum period of dietary data collection to obtain an approximation of usual intake for the antioxidants. However, despite within-person variability, a 24-h DR can produce adequate estimates of mean intake of a group that can be useful for contrasting the dietary status of the group with different levels of risk factors for certain diseases (49). In summary, the results of this study demonstrated that daily antioxidant intakes from diet and dietary supplements are significantly different in adult subgroups having different sociodemographic characteristics and lifestyle behaviors. In this study, we focused on the documentation of the antioxidant intake levels based on food composition tables; thus, further research is needed to study individual bioavailability, metabolism in the human body, and changes during processing and food preparation. Estimated total antioxidant intake from both diets and supplement is a prerequisite to investigating the implicated relation between the antioxidant intake and the prevalence of chronic diseases within a population and its subgroups. To our knowledge, this was the first documentation on the antioxidant intake status of U.S. adults and subgroups on a large scale. Having a reliable and valid assessment of dietary intake is the first step to establishing recommended dietary intakes that promote public health. The findings of this study will play a pivotal role in promoting and protecting national health through concerted efforts of policymakers, public health officers, nutrition and health educators in the government, the food and supplement industry, and academia. Furthermore, the welldocumented health disparity in the US may also be partially explained by the marked differences in antioxidant intake among different socioeconomic subgroups. Acknowledgments We thank Dr. Seung Ho Kang, Associate Professor of the Department of Applied Statistics in Yonsei University, for his statistical consultation throughout this project. O.K.C., W.O.S., and S.I.K. designed research; O.K.C. and A.F. conducted research; S.J.C., C.E.C., and A.F. analyzed data; O.K.C. and A.F. wrote the paper. O.K.C. had primary responsibility for final content. All authors read the final version of the manuscript, approve it for publication, and take public responsibility for its content. Neither this manuscript nor one with substantially similar content under our authorship has been published or is being considered for publication elsewhere.

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