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Dietary Intake of Phytonutrients in Relation to Fruit and Vegetable Consumption in Korea
RESEARCH Research and Professional Briefs
Dietary Intake of Phytonutrients in Relation to Fruit and Vegetable Consumption in Korea Haeng-Shin Lee, PhD; Yang-Hee Cho, PhD; Juyeon Park, PhD; Hye-Rim Shin, MS; Mi-Kyung Sung, PhD ARTICLE INFORMATION
ABSTRACT
Article history:
The purpose of this study was to provide baseline data for health policy creation by estimating phytonutrient intake and identifying major food sources of phytonutrients. Dietary recall data collected in the 2008 Korea National Health and Nutrition Examination Survey and phytonutrient database of the Korea National Academy of Agricultural Science were used in this study. The proportions of the population satisfying recommended dietary guidelines for fruits and vegetables were estimated, and phytonutrient intake was compared between populations who consumed the recommended intake and those who did not. The study found that 5.3% of subjects satisfied the recommended fruit and vegetable intake. In particular, the proportions of adolescents (13 to 18 years of age) and young adults (19 to 39 years of age) meeting the recommended fruit and vegetable intake were lower than other age groups (P<0.001). Intakes of major carotenoids (alpha-carotene, beta-carotene, beta-cryptoxanthin, lutein/ zeaxanthin, and lycopene), flavonoids (anthocyanidins, hesperitin, quercetin, catechin, and isoflavones), and one phenolic compound (gallic acid) were significantly higher (P<0.001) among subjects who met the recommendations for fruit and vegetable consumption compared with those who did not. Carrots, sweet potatoes, squash, tomatoes, and watermelons were found to be major sources of carotenoids. Flavonoids were mainly obtained from persimmons, mandarins, apples, grapes, onions, soybeans, and chestnuts. However, one or two food items contributed to nearly all intake of each phytonutrient, suggesting a lack of variety. In conclusion, the Korean population needs to consume a larger quantity and variety of fruits and vegetables.
Accepted 22 April 2013 Available online 3 July 2013
Keywords: Fruit Phytonutrient Vegetables Copyright ª 2013 by the Academy of Nutrition and Dietetics. 2212-2672/$36.00 doi:10.1016/j.jand.2013.04.022
J Acad Nutr Diet. 2013;113:1194-1199.
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ANY COUNTRIES HAVE ESTABLISHED A SET OF dietary guidelines that emphasize the importance of the sufficient intake of fruits and vegetables (F/V) as a component of good health. F/V intake has been inversely associated with many chronic diseases, including cardiovascular disease, cancer, and diabetes.1-3 F/V are rich in vitamins, minerals, and many other nutrients, including phytonutrients. Phytonutrients are not established nutrients but nevertheless seem to contribute substantially to preventing degenerative diseases.4,5 To date, many studies have explored population-based F/V consumption.6,7 However, few studies have focused on dietary phytonutrient intake using a representative national dataset.8,9 Only recently have specific phytonutrients been isolated, identified, and studied for their many specific nutritional properties and health benefits. Therefore, it is important to evaluate the association between the intake of each phytonutrient and its health benefits. The traditional Korean diet includes a wide variety of vegetables and fruits, with less food derived from animal sources. However, there have been dramatic changes in dietary habits in recent years, and, at the same time, mortality from noncommunicable diseases, including cancer, cardiovascular heart diseases, and diabetes, has increased. Therefore, this study attempted to 1194
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estimate phytonutrient intake of the Korean population using the Korea National Health and Nutrition Examination Survey (KNHANES) database.
METHODS Study Population This study used data collected from the 2008 KNHANES conducted by the Korea Centers for Disease Control and Prevention (KCDC).10 KNHANES is a cross-sectional health and nutrition examination survey using multistage, stratified area probability samples of noninstitutionalized Korean civilians age 1 year and older. A total of 8,502 subjects age 2 years and older who had completed a 24-hour dietary recall in the 2008 KNHANES were selected for this study. The KNHANES data collection was approved by the KCDC Institutional Review Board.
Dietary Intake Data Collection Trained dietitians collected recalled dietary intake data in person and also gathered recipes for each food item consumed by respondents in the previous 24-hour time period. For children younger than 8 years of age, one of the parents answered the dietary recall, and children older than ª 2013 by the Academy of Nutrition and Dietetics.
RESEARCH 8 years old were allowed to be assisted by their parents. Based on the recipes collected from each household, the weight of each ingredient was estimated from the volume of food ingested using the KNHANES Recipe Database.11
Assessment of Phytonutrient Intake The food composition table supplied by the Korea National Academy of Agricultural Science12 was used to quantify each carotenoid, flavonoid, and phenolic compound present in all foods. Dietary intake of 11 phytonutrients including five carotenoids (alpha-carotene, beta-carotene, beta-cryptoxanthin, lutein/zeaxanthin, and lycopene); five flavonoids (anthocyanidins, hesperitin, quercetin, catechin, and lycopene); three isoflavones (daidzein, genistein and glycitein); and one phenolic compound (gallic acid) were analyzed. These are the most commonly consumed phytonutrients according to previous phytonutrient intake studies13,14 and as compounds of health-related interests.15,16 The phytonutrient content for each food was calculated based on raw food weight. Food group categorization was based on food group criteria provided by the KCDC.17 The KNHANES 2008 reported that a total of 337 F/V foods were consumed. The percentage of F/V foods covered by the phytonutrient database were 96%, 65%, 87%, 90%, 85%, 75%, and 85% for carotenoids, anthocyanidins, hesperitin, catechin, quercetin, isoflavones, and gallic acid, respectively. These percentages were calculated using the same estimation method described by Yang and colleagues.18
Identification of Subjects Who Met or Did Not Meet the Recommended F/V Intake The energy contribution of F/V intake in the study population was estimated by adding the calories from each serving of F/V. Dietary guidelines for Koreans recommend one to three servings of fruits and five to seven servings of vegetables, depending on age and sex.19 Using these recommendations, individuals who satisfied the recommended energy intake from F/V were identified. The methods used to identify those who met the recommended intake and those who did not were based on a previous study by Murphy and colleagues.13
Statistical Analysis Percentages of the population who satisfied or did not satisfy the recommended daily intake of F/V for Koreans in different age and sex groups were compared using a c2 test. A t test was used to assess differences in the mean intake of phytonutrients between the respective populations. All means and percentages were weighted to be nationally representative. Weights indicating the probability of being sampled were assigned to each respondent, enabling the results to represent the entire Korean population using a sample weight developed by the Korea Centers for Disease Control to adjust for age and sex.20 All statistical analyses were done using SAS (release 9.2, 2010, SAS Institute Inc), and specified procedures (to account for the complex sampling design using variance estimation methods) were applied.21
RESULTS AND DISCUSSION The percentage of the population who consumed the recommended daily intake of F/V for Koreans is calculated according the method described in the Methods section September 2013 Volume 113 Number 9
(Figure). Of the total study population, 21.4% consumed the recommended amount of vegetables (five to seven servings per day) and 23.5% consumed the recommended amount of fruits (one to three servings). Only 5.3% of the study population complied with the guidelines for both F/V. A higher proportion of women than men met the recommended intake of F/V (P<0.001). A previous study reported that 25.7% of the Korean population meets the recommended intake of F/V when applying the WHO guidelines of 400 g/day.22 This estimation was based on the consumption of total number of servings (6 to 10 servings/day) supplied by either fruits or vegetables. Also, the WHO recommendation of 400 g/day is less than the recommended intake used in this study, and therefore a greater proportion of the population meets the WHO guidelines. In the present study, 20.9% of the population satisfied the recommended intake when proportions were calculated based on the WHO guidelines of 6 to 10 servings/day of either fruits or vegetables, which is similar to a previous report.22 Centers for Disease Control and Prevention (CDC) surveys reported that 33% of American adults consumed the recommended serving of fruits and 27% met the recommendation for vegetables.23 Despite the belief that Koreans consume enough F/V from traditional dietary patterns, the present study provides evidence that this may not be true, although Korean dietary guidelines recommend a greater intake of F/V compared with guidelines from the WHO and the United States. During the last decade, daily intake of meat and meat products in Korea has increased from 92.4 g to 104.6 g, whereas fruit intake has decreased from 208 g to 160 g. Daily vegetable intake in 2011 was 289 g, which is similar to the daily intake of 288 g in 2001.24 During the same period, the incidence of diabetes in adults older than 30 years old increased from 8.6% in 2001 to 9.8% in 2011, and the incidence of dyslipidemia increased from 10.1% in 2001 to 15% in 2011.24 It is assumed that decreased consumption of plant foods, including F/V, and increased consumption of animal products contribute to the development of lifestyle-related chronic diseases. This study also found that there are significant differences among age groups in terms of percentage of subjects who meet the F/V guidelines (P<0.001). In particular, adolescents (age 13 to 18 years) and young adults (age 19 to 39 years) had lower F/V intakes than other age groups. Although limited information is available for age-specific F/V consumption, a large European cross-sectional study reported that 6% to 24% of children met the WHO recommendations.7 However, the 2002-2003 WHO World Health Survey25 indicated that the prevalence of low F/V consumption tends to increase with age, which is different than the findings of the present study. This discrepancy may be due to rapid changes in lifestyle and dietary habits in more recent years. Estimates of major phytonutrient intake were calculated based on currently available data. Table 1 shows that carotenoid, flavonoid, and gallic acid intakes were significantly higher (P<0.001) in members of the study population who satisfied their recommended F/V intakes compared with those who did not. Both children and adults seemed to have similar consumption patterns except for beta carotene intake. Overall, estimates of phytonutrient intake in this study were similar to those reported by Murphy and colleagues.13 For example, in the present study, subjects who met the JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS
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Figure. Percentages of the study population consuming recommended daily intakes of fruits and vegetables by sex and age groups a 2 c test comparing the percentage of subjects within each sex and age group meeting and not meeting intake recommendations. recommended intake of F/V consumed 2.5 times more betacarotene than subjects who did not meet the recommended intake of F/V (7,763 mg/day vs 3,163 mg/day). This pattern was also observed by Murphy and colleagues13: men who met the recommended intake of F/V consumed an average of 4,679 mg/day of beta-carotene, whereas those who did not meet the F/V recommendations consumed an average of 2.6 times less beta-carotene, or 1,748 mg/day. This study also showed that members of the Korean population who met the recommended F/V intake consumed 12.0, 11.3, and 8.4 times more beta-cryptoxanthin, catechin, and anthocyanidins, respectively, compared to those who did not meet the recommended F/V intake. This indicates that dietary phytonutrients other than alpha and beta-carotene are affected even more significantly by fruit and vegetable intake. Smaller differences in alpha- and beta-carotene intake between the two groups may be due to the common consumption of carrots in the Korean population, which are a good source of alpha- and beta-carotene. The ranked contributions of each phytonutrient by food source are presented in Table 2. Carrots and squash are major sources of carotenoids, with the exception of lycopene. Koreans obtain 91% of their alpha carotene from carrots and 50% of their beta-carotene from sweet potatoes, a high-starch vegetable. High incidences of metabolic syndrome and hypertriglycemia in the Korean population have been attributed to the traditional high-starch Korean diet,25 and it thus may be necessary to encourage more diversity in F/V consumption.22 In particular, squash is a primary 1196
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source of major carotenoids and contributes 35.7% of lutein/ zeaxanthin intake. Watermelon and tomatoes contributed 52.2% and 38.6% of lycopene intake, respectively. In US populations, Murphy and colleagues13 reported that watermelon contributed 5.2% of lycopene intake, whereas tomatoes, tomato products, and tomato-based soup/stews comprised more than 90% of lycopene intake. Estimated daily lycopene intakes for these two populations were 2,575 mg/day for Koreans (data not shown) and between 4,242 mg/day and 11,834 mg/day for US adults.13 Because tomato-based foods are not a part of the traditional Korean diet, tomatoes and tomato products contribute far less to lycopene intake than in the US population. Major sources of flavonoids were fruits, onions, soybeans, and nuts. Because of differences in dietary habits of different countries, food sources of major flavonoids may vary widely. In this study, food sources for each flavonoid were diverse, although mandarins, persimmons, apples, grapes, and oranges accounted for at least two of the six flavonoids. Murphy and colleagues13 reported that tomatoes, carrots, oranges and orange juice, and strawberries accounted for more than two thirds of these phytonutrients in the US population. This suggests that Koreans may obtain phytonutrients from more diverse food sources compared with the US population. However, limited numbers of food items contributed to phytonutrient intake, indicating that a small number of foods account for a large proportion of total phytonutrient intake in Korea. In addition, the limited availability of a phytonutrient database may have contributed to September 2013 Volume 113 Number 9
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Table 1. Phytonutrient intakea in Korea in relation to fruit and vegetable consumption Total
Phytonutrients
Children (2-18 y)
Adults (‡19 y)
Meets Meets Meets Does Not Meet Does Not Meet Does Not Meet Recommendationb Recommendation Recommendationb Recommendation Recommendationb Recommendation (n[1,964) (n[6,538) P valuec (n[512) (n[1,716) P valuec (n[1,452) (n[4,822) P valuec meanSEd
meanSEd
meanSEd
Carotenoids (mg) <0.001
51553
30316
3,163175
<0.001
4,376723
2,715304
513
<0.001
33758
343
Alpha-carotene
47126
30012
Beta-carotene
7,763736 61282
Beta-cryptoxanthin
<0.001 0.066 <0.001
<0.001
45931
29914
8,666851
3,289184
<0.001
68594
553
<0.001
4,727199
2,39775
<0.001
3,136274
1,50480
<0.001
5,151232
2,64886
<0.001
6,611961
1,511142
<0.001
3,788800
1,292187
<0.001
7,3641091
1,573157
<0.001
<0.001
46.94.5
<0.001
79.95.4
Flavonoids (mg) Anthocyanidins
734.8
8.70.3
5.70.3
9.50.4
<0.001
Hesperitin
25.43.2
3.50.5
<0.001
33.55.2
40.6
<0.001
23.33.1
3.40.5
<0.001
Catechin
24.81.4
2.20.2
<0.001
20.12.2
1.90.2
<0.001
261.5
2.20.2
<0.001
Quercetin
9.10.3
2.90.1
<0.001
7.50.5
2.40.1
<0.001
9.60.4
30.1
<0.001
Isoflavones
25.82.8
5.40.5
<0.001
30.34.8
4.90.6
<0.001
24.62.7
5.60.5
<0.001
18.92.6
4.30.7
<0.001
14.14.1
3.10.9
<0.01
20.23.1
4.70.8
<0.001
Phenolics (mg) Gallic acid
a Estimates based on intakes by children (age 2-18 y) and adults (age19 y) obtained by 24-hour dietary recall as reported in the 2008 Korea National Health and Nutrition Examination Survey; phytonutrient concentration data based on The National Academy of Agricultural Science Ministry for Food, Agriculture, Forestry, and Fisheries data and data in the published literature.9 b Assessed using combined fruit and vegetable recommendations regardless of fruit-to-vegetable consumption ratio. c Two-sided Student’s t test comparison of the means. d Meanstandard error daily per capita. Weighted mean to be nationally representative.
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Lutein/zeaxanthin Lycopene
RESEARCH Table 2. Top five food sources of each phytonutrient based on the Korea National Health and Nutrition Examination Survey 2008a Alpha-Carotene
Beta-Carotene b
Food
%
Carrots
91.2
Beta-Cryptoxanthin
Food
%
b
Food
%
b
Lutein/Zeaxanthin b
Lycopene
Food
%
Food
%b
Sweet potatoes
48.0
Persimmon
63.0
Squash
35.7
Watermelon
53.6
Laver
1.6
Carrots
10.5
Squash
18.1
Spinach
22.9
Tomatoes
36.9
Squash
1.4
Squash
9.0
Peach
10.5
Cucumber
6.5
Tomato Ketchup
5.7
Banana
1.0
Watermelon
5.9
Orange
2.8
Tomatoes
6.2
Persimmon
3.3
1.0
Spinach
5.6
Spinach
1.5
Perilla, leaves
3.0
Grapefruit
Tomatoes Cumulative % of top five sources
96.2
Anthocyanidins
79.1
Hesperitin
95.9
Catechin
%b
Persimmon
24.8 Mandarin
87.2 Apple 79.4 Onion
Radish
23.2 Orange
12.7 Grape
Grape
22.7 Grapefruit
Pear
12.4 Lemon
0.1 Plum
Onion
10.2 Oats
0.0 Barley
Cumulative % of 93.3 top five sources
%b
Food
0.1 Peach
100.0
%b
Quercetin
Food
Food
74.3
Isoflavones %b
0.4 100.0
Gallic Acid Food
%b
51.5 Mandarin
66.9 Chestnuts
58.2
9.6 Apple
11.6 Soybean curd
15.4 Persimmon
39.1
3.4 Mandarin
11.0 Soybeans
10.6 Soybean sprout
0.9
2.7 Grape
9.2 Orange
3.2 Chicory, Leaves
0.6
2.6 Water dropwort
3.2 Soybean sprout
2.2 Apricot
0.4
Food
97.7
%b
Food
86.4
98.3
99.4
a Estimates based on intakes from subjects 2 y obtained by 24-hour dietary recall as reported in the 2008 Korea National Health and Nutrition Examination Survey; phytonutrient concentration data based on The National Academy of Agricultural Science Ministry for Food, Agriculture, Forestry, and Fisheries data and data in the published literature.9 b Contribution percent of intake per daily phytonutrient intake.
the apparently small number of food sources for phytonutrients in this study. That is, Koreans may be consuming more phytonutrients because some of the high-phytonutrient items such as tea or kimchi are not listed in an existing phytonutrient database. A Chinese study reported that the main food sources of flavonols and flavones are apples, potatoes, celery, eggplant, and actinidia.14 Otaki and colleagues26 found that the major food sources of isoflavones were processed soy foods, whereas onions, moroheiya (nalta jute), and Japanese radish leaves were the main sources of flavonols. In the same study, grapefruit and citrus fruit juices were the major sources of flavanones, whereas tsurumurasaki (malabar spinach), green pepper, and grapefruit were the main sources of flavones.26 A US study reported that the greatest daily mean intake of flavonoids was from tea, citrus fruit juices, wine, and citrus fruits.8 This study was the first to estimate phytonutrient intake relative to adherence to F/V intake recommendations in a representative Korean population. Currently, this study presents the only available data on phytonutrient intake estimates for Koreans. There are several limitations in this study. First, Koreans consume many different types of tea, yet a limited phytonutrient composition database is currently available, and therefore not all phytonutrients obtained from tea were accounted for in this study. Second, phytonutrient content for salted vegetables including kimchi is reported as zero in the database used in this study; because the Korean population 1198
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consumes a large amount of kimchi, the intake of phytonutrients may have been underestimated. This should be confirmed in future studies. In addition, the effects of food preparation on food phytonutrient content are not properly established, which may have caused overestimation or underestimation of certain phytonutrients. Lastly, the 24-hour diet recall method was used to estimate dietary phytonutrient intake of the study population, even though one day of dietary analysis is not a good representation of an individual’s diet. It is well established that 24-hour urine collection is the gold standard to estimate nutrient intake; however, this is impractical for use in field surveys. Future advances in dietary nutrient and phytonutrient intake measurement tools will support a better understanding of diet and related diseases.
CONCLUSIONS In this analysis, a small proportion of subjects consumed the recommended amounts of both F/V. Importantly, the proportion of adolescents (age 13 to 18 years) and young adults (age 19 to 39 years) satisfying the guidelines was significantly lower than other age groups. Both children and adults meeting the dietary recommendations for F/V consumption had phytonutrient intakes that were considerably higher than those who did not meet the recommendations for F/V consumption. However, it seems that a relatively limited number of foods contribute to phytonutrient intake. Therefore, the Korean population needs to consume more F/V from a larger variety of food sources. September 2013 Volume 113 Number 9
RESEARCH References
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AUTHOR INFORMATION H-S Lee is a head researcher, Department of Health Industry and Policy, Korea Health Industry Development Institute, Cheongwon-gun, Chungcheongbuk-do, Korea. Y-H Cho is an executive director, Technical Division, and J. Park is a scientific affairs team leader, Amway Korea Ltd, Daechi-dong, Kangnam-gu, Seoul, Korea. H-R Shin is a researcher and M-K Sung is a professor, Department of Food and Nutrition, Sookmyung Women’s University, Seoul, Korea. Address correspondence to: Mi-Kyung Sung, PhD, Department of Food and Nutrition, Sookmyung Women’s University, Cheongpa-ro 47-gil 100, Youngsan-gu, Seoul, 140-742, Korea. E-mail: [email protected]
STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors.
FUNDING/SUPPORT This project was financially supported by the Amway Korea Ltd.
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Dietary Intake of Phytonutrients in Relation to Fruit and Vegetable Consumption in Korea Haeng-Shin Lee, PhD; Yang-Hee Cho, PhD; Juyeon Park, PhD; Hye-Rim Shin, MS; Mi-Kyung Sung, PhD ARTICLE INFORMATION
ABSTRACT
Article history:
The purpose of this study was to provide baseline data for health policy creation by estimating phytonutrient intake and identifying major food sources of phytonutrients. Dietary recall data collected in the 2008 Korea National Health and Nutrition Examination Survey and phytonutrient database of the Korea National Academy of Agricultural Science were used in this study. The proportions of the population satisfying recommended dietary guidelines for fruits and vegetables were estimated, and phytonutrient intake was compared between populations who consumed the recommended intake and those who did not. The study found that 5.3% of subjects satisfied the recommended fruit and vegetable intake. In particular, the proportions of adolescents (13 to 18 years of age) and young adults (19 to 39 years of age) meeting the recommended fruit and vegetable intake were lower than other age groups (P<0.001). Intakes of major carotenoids (alpha-carotene, beta-carotene, beta-cryptoxanthin, lutein/ zeaxanthin, and lycopene), flavonoids (anthocyanidins, hesperitin, quercetin, catechin, and isoflavones), and one phenolic compound (gallic acid) were significantly higher (P<0.001) among subjects who met the recommendations for fruit and vegetable consumption compared with those who did not. Carrots, sweet potatoes, squash, tomatoes, and watermelons were found to be major sources of carotenoids. Flavonoids were mainly obtained from persimmons, mandarins, apples, grapes, onions, soybeans, and chestnuts. However, one or two food items contributed to nearly all intake of each phytonutrient, suggesting a lack of variety. In conclusion, the Korean population needs to consume a larger quantity and variety of fruits and vegetables.
Accepted 22 April 2013 Available online 3 July 2013
Keywords: Fruit Phytonutrient Vegetables Copyright ª 2013 by the Academy of Nutrition and Dietetics. 2212-2672/$36.00 doi:10.1016/j.jand.2013.04.022
J Acad Nutr Diet. 2013;113:1194-1199.
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ANY COUNTRIES HAVE ESTABLISHED A SET OF dietary guidelines that emphasize the importance of the sufficient intake of fruits and vegetables (F/V) as a component of good health. F/V intake has been inversely associated with many chronic diseases, including cardiovascular disease, cancer, and diabetes.1-3 F/V are rich in vitamins, minerals, and many other nutrients, including phytonutrients. Phytonutrients are not established nutrients but nevertheless seem to contribute substantially to preventing degenerative diseases.4,5 To date, many studies have explored population-based F/V consumption.6,7 However, few studies have focused on dietary phytonutrient intake using a representative national dataset.8,9 Only recently have specific phytonutrients been isolated, identified, and studied for their many specific nutritional properties and health benefits. Therefore, it is important to evaluate the association between the intake of each phytonutrient and its health benefits. The traditional Korean diet includes a wide variety of vegetables and fruits, with less food derived from animal sources. However, there have been dramatic changes in dietary habits in recent years, and, at the same time, mortality from noncommunicable diseases, including cancer, cardiovascular heart diseases, and diabetes, has increased. Therefore, this study attempted to 1194
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estimate phytonutrient intake of the Korean population using the Korea National Health and Nutrition Examination Survey (KNHANES) database.
METHODS Study Population This study used data collected from the 2008 KNHANES conducted by the Korea Centers for Disease Control and Prevention (KCDC).10 KNHANES is a cross-sectional health and nutrition examination survey using multistage, stratified area probability samples of noninstitutionalized Korean civilians age 1 year and older. A total of 8,502 subjects age 2 years and older who had completed a 24-hour dietary recall in the 2008 KNHANES were selected for this study. The KNHANES data collection was approved by the KCDC Institutional Review Board.
Dietary Intake Data Collection Trained dietitians collected recalled dietary intake data in person and also gathered recipes for each food item consumed by respondents in the previous 24-hour time period. For children younger than 8 years of age, one of the parents answered the dietary recall, and children older than ª 2013 by the Academy of Nutrition and Dietetics.
RESEARCH 8 years old were allowed to be assisted by their parents. Based on the recipes collected from each household, the weight of each ingredient was estimated from the volume of food ingested using the KNHANES Recipe Database.11
Assessment of Phytonutrient Intake The food composition table supplied by the Korea National Academy of Agricultural Science12 was used to quantify each carotenoid, flavonoid, and phenolic compound present in all foods. Dietary intake of 11 phytonutrients including five carotenoids (alpha-carotene, beta-carotene, beta-cryptoxanthin, lutein/zeaxanthin, and lycopene); five flavonoids (anthocyanidins, hesperitin, quercetin, catechin, and lycopene); three isoflavones (daidzein, genistein and glycitein); and one phenolic compound (gallic acid) were analyzed. These are the most commonly consumed phytonutrients according to previous phytonutrient intake studies13,14 and as compounds of health-related interests.15,16 The phytonutrient content for each food was calculated based on raw food weight. Food group categorization was based on food group criteria provided by the KCDC.17 The KNHANES 2008 reported that a total of 337 F/V foods were consumed. The percentage of F/V foods covered by the phytonutrient database were 96%, 65%, 87%, 90%, 85%, 75%, and 85% for carotenoids, anthocyanidins, hesperitin, catechin, quercetin, isoflavones, and gallic acid, respectively. These percentages were calculated using the same estimation method described by Yang and colleagues.18
Identification of Subjects Who Met or Did Not Meet the Recommended F/V Intake The energy contribution of F/V intake in the study population was estimated by adding the calories from each serving of F/V. Dietary guidelines for Koreans recommend one to three servings of fruits and five to seven servings of vegetables, depending on age and sex.19 Using these recommendations, individuals who satisfied the recommended energy intake from F/V were identified. The methods used to identify those who met the recommended intake and those who did not were based on a previous study by Murphy and colleagues.13
Statistical Analysis Percentages of the population who satisfied or did not satisfy the recommended daily intake of F/V for Koreans in different age and sex groups were compared using a c2 test. A t test was used to assess differences in the mean intake of phytonutrients between the respective populations. All means and percentages were weighted to be nationally representative. Weights indicating the probability of being sampled were assigned to each respondent, enabling the results to represent the entire Korean population using a sample weight developed by the Korea Centers for Disease Control to adjust for age and sex.20 All statistical analyses were done using SAS (release 9.2, 2010, SAS Institute Inc), and specified procedures (to account for the complex sampling design using variance estimation methods) were applied.21
RESULTS AND DISCUSSION The percentage of the population who consumed the recommended daily intake of F/V for Koreans is calculated according the method described in the Methods section September 2013 Volume 113 Number 9
(Figure). Of the total study population, 21.4% consumed the recommended amount of vegetables (five to seven servings per day) and 23.5% consumed the recommended amount of fruits (one to three servings). Only 5.3% of the study population complied with the guidelines for both F/V. A higher proportion of women than men met the recommended intake of F/V (P<0.001). A previous study reported that 25.7% of the Korean population meets the recommended intake of F/V when applying the WHO guidelines of 400 g/day.22 This estimation was based on the consumption of total number of servings (6 to 10 servings/day) supplied by either fruits or vegetables. Also, the WHO recommendation of 400 g/day is less than the recommended intake used in this study, and therefore a greater proportion of the population meets the WHO guidelines. In the present study, 20.9% of the population satisfied the recommended intake when proportions were calculated based on the WHO guidelines of 6 to 10 servings/day of either fruits or vegetables, which is similar to a previous report.22 Centers for Disease Control and Prevention (CDC) surveys reported that 33% of American adults consumed the recommended serving of fruits and 27% met the recommendation for vegetables.23 Despite the belief that Koreans consume enough F/V from traditional dietary patterns, the present study provides evidence that this may not be true, although Korean dietary guidelines recommend a greater intake of F/V compared with guidelines from the WHO and the United States. During the last decade, daily intake of meat and meat products in Korea has increased from 92.4 g to 104.6 g, whereas fruit intake has decreased from 208 g to 160 g. Daily vegetable intake in 2011 was 289 g, which is similar to the daily intake of 288 g in 2001.24 During the same period, the incidence of diabetes in adults older than 30 years old increased from 8.6% in 2001 to 9.8% in 2011, and the incidence of dyslipidemia increased from 10.1% in 2001 to 15% in 2011.24 It is assumed that decreased consumption of plant foods, including F/V, and increased consumption of animal products contribute to the development of lifestyle-related chronic diseases. This study also found that there are significant differences among age groups in terms of percentage of subjects who meet the F/V guidelines (P<0.001). In particular, adolescents (age 13 to 18 years) and young adults (age 19 to 39 years) had lower F/V intakes than other age groups. Although limited information is available for age-specific F/V consumption, a large European cross-sectional study reported that 6% to 24% of children met the WHO recommendations.7 However, the 2002-2003 WHO World Health Survey25 indicated that the prevalence of low F/V consumption tends to increase with age, which is different than the findings of the present study. This discrepancy may be due to rapid changes in lifestyle and dietary habits in more recent years. Estimates of major phytonutrient intake were calculated based on currently available data. Table 1 shows that carotenoid, flavonoid, and gallic acid intakes were significantly higher (P<0.001) in members of the study population who satisfied their recommended F/V intakes compared with those who did not. Both children and adults seemed to have similar consumption patterns except for beta carotene intake. Overall, estimates of phytonutrient intake in this study were similar to those reported by Murphy and colleagues.13 For example, in the present study, subjects who met the JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS
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Figure. Percentages of the study population consuming recommended daily intakes of fruits and vegetables by sex and age groups a 2 c test comparing the percentage of subjects within each sex and age group meeting and not meeting intake recommendations. recommended intake of F/V consumed 2.5 times more betacarotene than subjects who did not meet the recommended intake of F/V (7,763 mg/day vs 3,163 mg/day). This pattern was also observed by Murphy and colleagues13: men who met the recommended intake of F/V consumed an average of 4,679 mg/day of beta-carotene, whereas those who did not meet the F/V recommendations consumed an average of 2.6 times less beta-carotene, or 1,748 mg/day. This study also showed that members of the Korean population who met the recommended F/V intake consumed 12.0, 11.3, and 8.4 times more beta-cryptoxanthin, catechin, and anthocyanidins, respectively, compared to those who did not meet the recommended F/V intake. This indicates that dietary phytonutrients other than alpha and beta-carotene are affected even more significantly by fruit and vegetable intake. Smaller differences in alpha- and beta-carotene intake between the two groups may be due to the common consumption of carrots in the Korean population, which are a good source of alpha- and beta-carotene. The ranked contributions of each phytonutrient by food source are presented in Table 2. Carrots and squash are major sources of carotenoids, with the exception of lycopene. Koreans obtain 91% of their alpha carotene from carrots and 50% of their beta-carotene from sweet potatoes, a high-starch vegetable. High incidences of metabolic syndrome and hypertriglycemia in the Korean population have been attributed to the traditional high-starch Korean diet,25 and it thus may be necessary to encourage more diversity in F/V consumption.22 In particular, squash is a primary 1196
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source of major carotenoids and contributes 35.7% of lutein/ zeaxanthin intake. Watermelon and tomatoes contributed 52.2% and 38.6% of lycopene intake, respectively. In US populations, Murphy and colleagues13 reported that watermelon contributed 5.2% of lycopene intake, whereas tomatoes, tomato products, and tomato-based soup/stews comprised more than 90% of lycopene intake. Estimated daily lycopene intakes for these two populations were 2,575 mg/day for Koreans (data not shown) and between 4,242 mg/day and 11,834 mg/day for US adults.13 Because tomato-based foods are not a part of the traditional Korean diet, tomatoes and tomato products contribute far less to lycopene intake than in the US population. Major sources of flavonoids were fruits, onions, soybeans, and nuts. Because of differences in dietary habits of different countries, food sources of major flavonoids may vary widely. In this study, food sources for each flavonoid were diverse, although mandarins, persimmons, apples, grapes, and oranges accounted for at least two of the six flavonoids. Murphy and colleagues13 reported that tomatoes, carrots, oranges and orange juice, and strawberries accounted for more than two thirds of these phytonutrients in the US population. This suggests that Koreans may obtain phytonutrients from more diverse food sources compared with the US population. However, limited numbers of food items contributed to phytonutrient intake, indicating that a small number of foods account for a large proportion of total phytonutrient intake in Korea. In addition, the limited availability of a phytonutrient database may have contributed to September 2013 Volume 113 Number 9
September 2013 Volume 113 Number 9
Table 1. Phytonutrient intakea in Korea in relation to fruit and vegetable consumption Total
Phytonutrients
Children (2-18 y)
Adults (‡19 y)
Meets Meets Meets Does Not Meet Does Not Meet Does Not Meet Recommendationb Recommendation Recommendationb Recommendation Recommendationb Recommendation (n[1,964) (n[6,538) P valuec (n[512) (n[1,716) P valuec (n[1,452) (n[4,822) P valuec meanSEd
meanSEd
meanSEd
Carotenoids (mg) <0.001
51553
30316
3,163175
<0.001
4,376723
2,715304
513
<0.001
33758
343
Alpha-carotene
47126
30012
Beta-carotene
7,763736 61282
Beta-cryptoxanthin
<0.001 0.066 <0.001
<0.001
45931
29914
8,666851
3,289184
<0.001
68594
553
<0.001
4,727199
2,39775
<0.001
3,136274
1,50480
<0.001
5,151232
2,64886
<0.001
6,611961
1,511142
<0.001
3,788800
1,292187
<0.001
7,3641091
1,573157
<0.001
<0.001
46.94.5
<0.001
79.95.4
Flavonoids (mg) Anthocyanidins
734.8
8.70.3
5.70.3
9.50.4
<0.001
Hesperitin
25.43.2
3.50.5
<0.001
33.55.2
40.6
<0.001
23.33.1
3.40.5
<0.001
Catechin
24.81.4
2.20.2
<0.001
20.12.2
1.90.2
<0.001
261.5
2.20.2
<0.001
Quercetin
9.10.3
2.90.1
<0.001
7.50.5
2.40.1
<0.001
9.60.4
30.1
<0.001
Isoflavones
25.82.8
5.40.5
<0.001
30.34.8
4.90.6
<0.001
24.62.7
5.60.5
<0.001
18.92.6
4.30.7
<0.001
14.14.1
3.10.9
<0.01
20.23.1
4.70.8
<0.001
Phenolics (mg) Gallic acid
a Estimates based on intakes by children (age 2-18 y) and adults (age19 y) obtained by 24-hour dietary recall as reported in the 2008 Korea National Health and Nutrition Examination Survey; phytonutrient concentration data based on The National Academy of Agricultural Science Ministry for Food, Agriculture, Forestry, and Fisheries data and data in the published literature.9 b Assessed using combined fruit and vegetable recommendations regardless of fruit-to-vegetable consumption ratio. c Two-sided Student’s t test comparison of the means. d Meanstandard error daily per capita. Weighted mean to be nationally representative.
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Lutein/zeaxanthin Lycopene
RESEARCH Table 2. Top five food sources of each phytonutrient based on the Korea National Health and Nutrition Examination Survey 2008a Alpha-Carotene
Beta-Carotene b
Food
%
Carrots
91.2
Beta-Cryptoxanthin
Food
%
b
Food
%
b
Lutein/Zeaxanthin b
Lycopene
Food
%
Food
%b
Sweet potatoes
48.0
Persimmon
63.0
Squash
35.7
Watermelon
53.6
Laver
1.6
Carrots
10.5
Squash
18.1
Spinach
22.9
Tomatoes
36.9
Squash
1.4
Squash
9.0
Peach
10.5
Cucumber
6.5
Tomato Ketchup
5.7
Banana
1.0
Watermelon
5.9
Orange
2.8
Tomatoes
6.2
Persimmon
3.3
1.0
Spinach
5.6
Spinach
1.5
Perilla, leaves
3.0
Grapefruit
Tomatoes Cumulative % of top five sources
96.2
Anthocyanidins
79.1
Hesperitin
95.9
Catechin
%b
Persimmon
24.8 Mandarin
87.2 Apple 79.4 Onion
Radish
23.2 Orange
12.7 Grape
Grape
22.7 Grapefruit
Pear
12.4 Lemon
0.1 Plum
Onion
10.2 Oats
0.0 Barley
Cumulative % of 93.3 top five sources
%b
Food
0.1 Peach
100.0
%b
Quercetin
Food
Food
74.3
Isoflavones %b
0.4 100.0
Gallic Acid Food
%b
51.5 Mandarin
66.9 Chestnuts
58.2
9.6 Apple
11.6 Soybean curd
15.4 Persimmon
39.1
3.4 Mandarin
11.0 Soybeans
10.6 Soybean sprout
0.9
2.7 Grape
9.2 Orange
3.2 Chicory, Leaves
0.6
2.6 Water dropwort
3.2 Soybean sprout
2.2 Apricot
0.4
Food
97.7
%b
Food
86.4
98.3
99.4
a Estimates based on intakes from subjects 2 y obtained by 24-hour dietary recall as reported in the 2008 Korea National Health and Nutrition Examination Survey; phytonutrient concentration data based on The National Academy of Agricultural Science Ministry for Food, Agriculture, Forestry, and Fisheries data and data in the published literature.9 b Contribution percent of intake per daily phytonutrient intake.
the apparently small number of food sources for phytonutrients in this study. That is, Koreans may be consuming more phytonutrients because some of the high-phytonutrient items such as tea or kimchi are not listed in an existing phytonutrient database. A Chinese study reported that the main food sources of flavonols and flavones are apples, potatoes, celery, eggplant, and actinidia.14 Otaki and colleagues26 found that the major food sources of isoflavones were processed soy foods, whereas onions, moroheiya (nalta jute), and Japanese radish leaves were the main sources of flavonols. In the same study, grapefruit and citrus fruit juices were the major sources of flavanones, whereas tsurumurasaki (malabar spinach), green pepper, and grapefruit were the main sources of flavones.26 A US study reported that the greatest daily mean intake of flavonoids was from tea, citrus fruit juices, wine, and citrus fruits.8 This study was the first to estimate phytonutrient intake relative to adherence to F/V intake recommendations in a representative Korean population. Currently, this study presents the only available data on phytonutrient intake estimates for Koreans. There are several limitations in this study. First, Koreans consume many different types of tea, yet a limited phytonutrient composition database is currently available, and therefore not all phytonutrients obtained from tea were accounted for in this study. Second, phytonutrient content for salted vegetables including kimchi is reported as zero in the database used in this study; because the Korean population 1198
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consumes a large amount of kimchi, the intake of phytonutrients may have been underestimated. This should be confirmed in future studies. In addition, the effects of food preparation on food phytonutrient content are not properly established, which may have caused overestimation or underestimation of certain phytonutrients. Lastly, the 24-hour diet recall method was used to estimate dietary phytonutrient intake of the study population, even though one day of dietary analysis is not a good representation of an individual’s diet. It is well established that 24-hour urine collection is the gold standard to estimate nutrient intake; however, this is impractical for use in field surveys. Future advances in dietary nutrient and phytonutrient intake measurement tools will support a better understanding of diet and related diseases.
CONCLUSIONS In this analysis, a small proportion of subjects consumed the recommended amounts of both F/V. Importantly, the proportion of adolescents (age 13 to 18 years) and young adults (age 19 to 39 years) satisfying the guidelines was significantly lower than other age groups. Both children and adults meeting the dietary recommendations for F/V consumption had phytonutrient intakes that were considerably higher than those who did not meet the recommendations for F/V consumption. However, it seems that a relatively limited number of foods contribute to phytonutrient intake. Therefore, the Korean population needs to consume more F/V from a larger variety of food sources. September 2013 Volume 113 Number 9
RESEARCH References
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AUTHOR INFORMATION H-S Lee is a head researcher, Department of Health Industry and Policy, Korea Health Industry Development Institute, Cheongwon-gun, Chungcheongbuk-do, Korea. Y-H Cho is an executive director, Technical Division, and J. Park is a scientific affairs team leader, Amway Korea Ltd, Daechi-dong, Kangnam-gu, Seoul, Korea. H-R Shin is a researcher and M-K Sung is a professor, Department of Food and Nutrition, Sookmyung Women’s University, Seoul, Korea. Address correspondence to: Mi-Kyung Sung, PhD, Department of Food and Nutrition, Sookmyung Women’s University, Cheongpa-ro 47-gil 100, Youngsan-gu, Seoul, 140-742, Korea. E-mail: [email protected]
STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors.
FUNDING/SUPPORT This project was financially supported by the Amway Korea Ltd.
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