Osong Public Health Res Perspect 2016 7(3), 180e189

[Link]
pISSN 2210-9099 eISSN 2233-6052

- ORIGINAL ARTICLE -

Intake Trends of Red Meat, Alcohol, and Fruits

and Vegetables as Cancer-Related Dietary Factors
from 1998 to 2009
Min Kyung Park a, Hee Young Paik a,b,*, Yeonsook Lee a,b
a
Department of Food and Nutrition, Seoul National University, Seoul, Korea.
b
Research Institute of Human Ecology, Seoul National University, Seoul, Korea.

Received: December Abstract

26, 2015 Objectives: Cancer is the leading cause of death worldwide, and cancer inci-
Revised: April 17, 2016 dence and mortality have been increasing steadily in South Korea. This study
Accepted: April 20, aimed to examine the change in consumption of three cancer-related dietary
2016 factorsdred meat, alcohol, and fruits/vegetables, and to evaluate consumption
of these dietary factors among Koreans according to the criteria from the rec-
KEYWORDS: ommendations of the World Cancer Research Fund/American Institute of Cancer
alcoholic beverages, Research.
Methods: Consumption of red meat, alcoholic beverages, and fruits and vege-
cancer,
tables was calculated from the 24-hour recall data of 36,486 individuals older
fruit,
than 20 years who were selected from the Korea National Health and Nutrition
meat,
Examination Survey 1998e2009. The intake adequacy of these three factors was
risk factors, evaluated by the recommended criteria of the World Cancer Research Fund/
vegetables American Institute of Cancer Research report.
Results: The mean red meat intake in the men in their 20s increased sharply
(from 91.6 g to 111.3 g, p < 0.05). The mean alcohol intake increased continu-
ously in men (from 10.3 g to 20.0 g, p < 0.05) and women (from 1.5 g to 3.5 g,
p < 0.05). The mean fruit/vegetable intake decreased in the 21e29eyear age
group (from 349.4 g to 306.7 g in men; from 393.3 g to 292.5 g in women;
p < 0.05). The percentage of individuals who did not meet the intake criteria for
the three cancer-related dietary factors was especially high, and the percentage
increased over 10 years in those in their 20s (p < 0.05).
Conclusion: We confirmed that intakes of red meat, alcoholic drink, and fruits
and vegetables have moved toward a negative direction in both men and women
in their 20s.

*Corresponding author.
E-mail: hypaik@[Link] (H.Y. Paik).

Copyright ª 2016 Korea Centers for Disease Control and Prevention. Published by Elsevier Korea LLC. This is an open access article
under the CC BY-NC-ND license ([Link]
Intake trends of cancer-related dietary factors in Korea 181

1. Introduction would also be different by age groups and sex. There-

fore, it seems meaningful to evaluate the consumption of
Prevention of cancer is one of the most pressing cancer-related dietary factors for Koreans in order to
challenges faced by researchers and public health policy monitor risk groups for cancer prevention.
makers. Cancer is, however, preventable through In this study, we examined the change in consump-
modification of lifestyle and diet and by increasing tion of cancer-related dietary factorsdred meat, alcohol,
physical activity. The World Cancer Research Fund and fruits and vegetablesdand evaluated the con-
(WCRF) and the American Institute for Cancer sumption of these dietary factors according to the
Research (AICR) published the report “Food, Nutrition criteria from the recommendations of WCRF/AICR in
and the Prevention of Cancer: a Global Perspective” in Koreans, by comparing data from the first to the fourth
2007 [1]. The purpose of this report was to review all the Korea National Health and Nutrition Examination Sur-
relevant research to suggest comprehensive recommen- vey (KNHANES).
dations for food, nutrition, and physical activity to
prevent cancer. In this report, 10 dietary and physical
activity recommendations for cancer prevention were 2. Materials and methods
established, and six out of these 10 recommendations
are concerned with dietary factors: (1) limit consump- 2.1. Dataset for analysis
tion of energy-dense foods and avoid sugary drinks; (2) The intake levels of the selected factors were
eat mostly foods of plant origin; (3) limit intake of red analyzed in the 1998, 2001, 2005, and 2007e2009
meat and avoid processed meat; (4) limit intake of KNHANES, which is the national monitoring survey of
alcoholic drinks; (5) limit consumption of salt and avoid South Korea (a cross-sectional study). The KNHANES
moldy cereals (grains) or pulses (legumes); and (6) aim has been conducted with individuals selected by repre-
to meet nutritional needs through diet alone. sentative sampling of the household registries in the
Cancer is the leading cause of death worldwide, and National Census Registry since 1998. The KNHANES
cancer incidence and mortality have been increasing data have three components: a health interview, a health
steadily in South Korea [2]. According to Globocan examination, and a nutrition component. In this study,
2012, the incidence of all cancers is expected to increase we used 1-day 24-hour recall data from the nutrition
up to 25% in South Korea by 2020 [3]. Meanwhile, the survey in the KNHANES to calculate and evaluate the
dietary habits of Koreans may contribute to both pro- consumption of the selected cancer-related dietary fac-
tective factors against cancer and risk factors for cancer. tors. We selected participants who were over 21 years of
In general, Koreans consume a great deal of vegetable age in the KNHANES, since the intake criteria from the
dishes, such as salads and seasoned vegetables, which recommendations of the WCRF/AICR report were
are known through caseecontrol and cohort studies to applicable to adults older than 21 years.
be protective factors for colorectal cancer [4e7]. Meta-
analyses have reported that beans and soybean products
such as soybean paste, tofu, and soy milk reduce breast 2.2. Selection of cancer-related dietary factors
cancer risk [8e10]; these foods are frequently consumed and calculation of intake of cancer-related
in Korea. By contrast, barbecued meats, especially those dietary factors
barbecued with charcoal, are very popular in Korea and Three cancer-related dietary factorsdred meat,
significantly increase gastric cancer risk [11]. Tradi- alcohol, and fruits and vegetablesdwhich could be
tional Korean salted foods such as salted fish and salted analyzed quantitatively using the KNHANES data were
vegetables have been reported as risk factors for gastric selected to evaluate the consumption of cancer-related
cancer [12,13]. Koreans usually consume a large amount dietary factors. This is because only these three dietary
of salted vegetables such as kimchi. factors have recommended intake criteria, although the
In many studies, it has been found that food con- associations between > 40 dietary factors and cancer
sumption patterns are different by age groups and sex. were reviewed by panels in the WCRF/AICR report.
Bezerra et al [14] recently found differences in food This is due to the difficulty in determining the intake
intake by sex and age groups in a study comparing food criteria for all cancer-related dietary factors because of
intakes in Brazil and the United States. Differences in an insufficient number of reliable studies. Sodium
food consumption pattern by age groups and sex were intake, one of the cancer-related dietary factors in the
found in Canada and Lebanon as well [15,16]. In WCRF/AICR report, was excluded from this study
Taiwan and Spain, food consumption was different by because the average of the sodium intake of Koreans has
age groups [17,18]. In a cohort of young Brazilian exceeded the recommended limit of 2,400 mg/d; there-
adults, Arruda et al [19] found that sex is associated with fore, the evaluation of sodium intake in Koreans seemed
the dietary pattern. Considering these differences, con- meaningless. Ultimately, only three cancer-related di-
sumption patterns of cancer-related dietary factors etary factors with the intake criteriadred meat, alcohol,
182 M.K. Park, et al

and fruits and vegetablesdwere selected for the present day and women who consumed over one drink per day
study. were also classified as risk groups for cancer. The
The intakes of red meat, alcohol, and fruits and evaluation results were used to determine whether the
vegetables were calculated for each age or sex group. participants have risk factors, and the percentage of in-
All individuals were divided into five age groups ac- dividuals with risk factors was calculated.
cording to the age classification of Dietary Reference
Intakes for Koreans [20]. 2.3. Statistical analysis
Food items belonging to red meat, alcohol, and fruits The mean and median intakes of the three cancer-
and vegetables, according to the definitions in the WCRF/ related dietary factors of each year were calculated with
AICR report [21], were identified and combined to obtain the nutrition survey weight using the survey procedure.
the intake of each factor of each participant: (1) Red meat The mean intakes of the three cancer-related dietary
refers to beef, pork, lamb, and goat meat obtained from factors for subgroups such as sex, age groups, and
domesticated animals including that contained in pro- number of risk factors were calculated with the nutrition
cessed foods, and flesh from animals that have more red survey weight using the domain statement of survey
than white muscle fibers. Meat includes skeletal muscles procedure. The trends for mean intake of each cancer-
and the internal organs (offal, such as the brain, liver, related dietary factor were tested by regression analysis
heart, intestines, and tongue). (2) Alcoholic beverages using a generalized linear model. The trends for sex
include beer, wine, and spirits. Other alcoholic beverages ratio, percentages of individuals in each age group, and
that may be locally important include fermented milk, percentages of individuals who have three risk factors
fermented honey water (mead), and fermented apples were also tested by the two-sided CochraneArmitage
(cider). Since alcoholic beverages vary in their ethanol trend test. All statistical analyses were performed using
content, ethanol intake was calculated taking into SAS software (version 9.4; SAS Institute Inc., Cary, NC,
consideration alcoholicity and specific gravity of the USA); the level of significance was p < 0.05.
alcoholic drinks, and not their intake. The intake criterion
for ethanol was determined by assuming 10 g of ethanol
per “drink” because one glass of soju or beer, the most 3. Results
frequently consumed alcoholic beverage in Korea [22],
contains about 10 g of ethanol. Calculated ethanol con- Table 1 summarizes the general characteristics of the
tents were converted into number of “drinks,” with one participants. More female than male individuals older
drink being equivalent to 10 g of ethanol, to evaluate the than 21 years were in the four sets of KNHANES data
intake of alcoholic beverages. (3) Vegetables (nonstarch) from 1998 to 2009. The number of individuals in the
are the edible parts of plants, usually including fungi. fourth KNHANES (2007e2009) was more than twice
Nonstarch vegetables can be divided into green, leafy that who participated in any other previous KNHANES.
vegetables, and cruciferous vegetables. Fruits are the The number of individuals aged 30e49 years was the
seed-containing part of a plant, but only those that are highest and that of individuals older than 65 years was
eaten as fruits are included in the culinary definition, for the lowest in all KNHANES data. The percentage of
example, apples, bananas, berries, figs, grapes, mangoes, individuals in their 20s decreased, but the percentage of
and melons. These also include citrus fruits such as or- those older than 65 years increased. The mean intake of
anges, grapefruits, lemons, and limes, and dried fruits red meat slightly decreased from 63.0 g to 60.6 g
such as apricots, figs, and raisins. Judgments on vegeta- (p < 0.05). The mean alcohol intake consistently
bles and fruits do not include those preserved by salting increased (p < 0.05), and the mean intake of fruits and
and/or pickling (e.g., kimchi in Korea). vegetables decreased since 2001 (p < 0.05).
The consumption criteria for each factor were chosen Table 2 shows the changes in red meat, alcohol, and
from the 10 recommendations by WCRF/AICR [21]. fruit and vegetable intake by sex and age groups in the
Personal recommendations for each factor were as fol- KNHANES from 1998 to 2009. The mean intake of red
lows: (1) consumption of red meat should be limited meat for both sexes in their 20s was highest in 1998 and
to < 500 g/wk; (2) consumption of alcoholic beverages 2007e2009, while that for both sexes aged 30e49 years
should be limited to two drinks per day for men and one was highest in 2001. The mean intake of red meat in
drink per day for women; and (3) consumption of fruits men in their 20s increased sharply from 63.6 g in 2001
and vegetables should be at least 400 g/d. to 111.3 g in 2007e2009. The mean intake of red meat
We converted the intake criterion per week for red in women in their 20s also increased sharply from 2001
meat (500 g) to one per day (g) divided by 7 days to 2005. The mean alcohol intake increased from 9.2 g
because the KNHANES includes only 1-day 24-hour to 20.3 g, especially in men in their 20s, since 1998,
recall data. Individuals who consumed
71.4 g red although it was not statistically significant. Since 1998,
meat per day and/or < 400 g fruits and vegetables per the mean alcohol intake of men rapidly increased from
day were classified as risk groups for cancer. For alco- 10.6 g in 2001 to 20.3 g in 2007e2009 (p < 0.05). The
holic beverages, men who consumed over two drinks per mean alcohol intake of men aged 30e49 years was the
Intake trends of cancer-related dietary factors in Korea 183

Table 1. Distribution of selected individuals according to sex/age groups and the mean intake of red meat, alcohol, and fruits/
vegetables among selected individuals in the KNHANES.

1998 2001 2005 2007e2009

Total participants 7,292 6,880 6,384 15,930
Men (%)* 3,401 (46.6) 3,159 (45.9) 2,863 (44.9) 6,497 (40.8)
Age groups (y)
21e29* 1,341 (18.4) 1,158 (16.8) 903 (14.1) 1,783 (11.2)
30e49* 3,327 (45.6) 3,406 (49.5) 3,025 (47.4) 6,386 (40.1)
50e64* 1,650 (22.6) 1,400 (20.4) 1,452 (22.7) 3,970 (24.9)

65 * 974 (13.4) 916 (13.3) 1,004 (15.7) 3,791 (23.8)
Red meat intake* y,z
,

Mean  SE 63.0  1.3 53.6  1.4 64.8  1.5 60.6  1.1

Median (95% CL) 26.5 (25.1e27.9) 4.9 (1.3e8.6) 25.8 (23.5e28.2) 24.4 (22.8e26.0)
Alcohol intake* y,x
,

Mean  SE 5.7  0.3 6.4  0.3 9.1  0.5 11.7  0.4

Median (95% CL) 1.7 (e3.4 to 3.4) 0.0 (e3.4 to 3.4) 0.0 (e3.8 to 3.8) 0.0 (e3.5 to 3.5)
Fruit/vegetable intake* y,jj
,

Mean  SE 367.4  4.5 391.5  4.7 283.0  3.7 350.5  3.5

Median (95% CL) 277.5 (268.5e286.5) 307.8 (298.8e316.8) 219.2 (211.7e226.6) 254.7 (248.7e260.7)
*p for trend (p < 0.05). The p values are determined by the two-sided CochraneArmitage trend test for binominal variables and by a generalized linear model
for continuous variables; yWeighted with the nutrition survey weight; zOrgan meats, residual products, and processed meats were included; meat broth was
excluded; xAlcoholic drinks used for flavoring in the cooking process were excluded; jjFruit juices, fruit jams, and salted and picked foods were excluded.
CL Z confidence limits; KNHANES Z Korea National Health and Nutrition Examination Survey; SE Z standard error.

highest among all age groups from 1998 to 2009. In vegetables by the number of risk factors are presented in
women, alcohol intake increased continuously from Table 4. Individuals with one risk factor comprised 57%
1.5 g in 1998 to 3.5 g in 2007e2009 (p < 0.05). The of all participants, the highest percentage among groups
mean intake of fruits and vegetables for people of both with risk factors. Eighty-five percent of individuals with
sexes, aged 21e29 years, decreased from 1998 to one risk factor had a low intake of fruits and vegetables
2007e2009 (from 349.4 g to 306.7 g in men; from as their risk factor. In the group with two risk factors,
393.3 g to 292.5 g in women; p < 0.05). By contrast, the 89% of individuals had a risk factor for fruits and veg-
mean intake of fruits and vegetables for individuals of etables, 67% for red meat, and 44% for alcohol. The
both sexes, > 50 years of age, increased since 1998. For mean intake of red meat and alcohol increased as the
both sexes, the mean intake of fruits and vegetables number of risk factors increased (p < 0.05). By contrast,
decreased, but notably in women (from 375.4 g in 1998 the mean intake of fruits and vegetables decreased as the
to 346.5 g in 2007e2009, p < 0.05). Distribution of number of risk factors increased (p < 0.05).
individuals who did not meet each intake criterion for
red meat, alcohol, and fruits and vegetables is presented
in Table 3. The percentage of people in their 20s who 4. Discussion
consumed red meat over 71.4 g/d showed an increasing
tendency for both sexes and became the highest at This study is an important attempt to investigate the
47.2% for men in 2007e2009. The percentage of men changes in consumption of three cancer-related dietary
who drank more than two cups and that of women who factorsdred meat, alcohol, and fruits and vegeta-
drank more than one cup of alcoholic beverages blesdin the KNHANES data from 1998 to 2009. We
increased significantly with time, except for people over found that the mean red meat intake in men in their 20s
65 years of age. The percentage of men and women in increased sharply. The mean alcohol intake increased
their 20s who did not meet the intake criteria for alcohol continuously in men and women. The mean fruit/vege-
increased notably (from 13.4% in 1998 to 21.0% in table intake decreased notably in the 21e29-year age
2007e2009 in men; from 4.9% in 1998 to 12.9% in group. The percentage of individuals who did not meet
2007e2009 in women; p < 0.05). The percentages of the intake criteria for the three cancer-related dietary
individuals who consumed fruits and vegetables under factors was especially high, and the percentage
400 g/d in age groups 21e29 years and 30e49 years increased over 10 years in those in their 20s.
showed a tendency to increase significantly in both The three risk factors came from the WCRF/AICR
sexes from 1998 to 2009. recommendations for cancer prevention that were based
Distribution of individuals with risk factors and the on the reviews of numerous research findings from a
mean intake of red meat, alcohol, and fruits and variety of countries and ethnic backgrounds. Since these
184 M.K. Park, et al

Table 2. Changes in red meat, alcohol, and fruit/vegetable intake by gender and age groups in the KNHANES.

CRDF (g/d) Sex Age group (y) 1998 2001 2005 2007e2009
Red meat* Men 21e29y 91.6  5.9 63.6  5.1 92.9  6.4 111.3  6.2
30e49 88.7  3.4 81.8  4.0 94.0  3.6 88.6  2.8
50e64 61.9  4.0 50.8  3.9 56.5  3.9 61.2  3.0

65 35.3  3.2 40.5  4.8 35.4  4.3 33.4  2.1
Totaly 79.3  2.3 67.7  2.4 80.5  2.4 80.8  1.9
Women 21e29y 64.2  4.0 48.8  3.6 72.1  5.1 62.9  3.0
30e49y 54.5  2.3 51.5  2.6 55.2  2.4 45.7  1.4
50e64 32.5  2.2 29.5  2.4 34.8  2.9 29.8  1.4

65 23.9  2.2 20.4  2.2 20.9  2.4 18.0  1.1
Totaly 48.2  1.4 41.8  1.5 49.3  1.7 40.7  0.9
Alcoholz Men 21e29 9.2  1.4 10.6  1.3 15.9  2.3 20.3  2.2
30e49y 11.2  0.8 12.3  0.8 17.0  1.2 22.5  1.1
50e64y 11.1  1.2 11.2  1.2 15.5  2.0 19.9  1.9

65 5.7  0.9 6.5  0.9 8.2  1.3 9.2  0.7
Totaly 10.3  0.5 11.2  0.6 15.6  0.9 20.0  0.8
Women 21e29 1.9  0.4 2.8  0.8 5.1  1.2 6.7  0.8
30e49y 1.8  0.3 2.9  0.3 2.8  0.3 4.1  0.3
50e64 0.9  0.2 2.2  0.6 2.1  0.4 2.0  0.2

65 1.0  0.3 1.3  0.5 0.5  0.1 0.7  0.1
Totaly 1.5  0.2 2.5  0.3 2.7  0.3 3.5  0.2
Fruit/vegetablesx Men 21e29y 349.4  15.8 336.5  14.5 260.1  12.3 306.7  12.4
30e49y 382.6  8.8 392.5  10.0 315.8  7.8 379.9  8.1
50e64y 346.5  13.6 382.0  12.5 296.8  12.3 378.0  9.8

65y 264.5  16.6 341.6  18.9 235.2  11.5 286.8  8.8
Totaly 358.6  6.3 375.1  6.6 291.9  5.4 354.6  5.2
Women 21e29y 393.3  15.4 383.9  16.3 272.8  12.6 292.5  11.8
30e49y 414.5  9.8 435.9  9.3 297.7  7.8 374.7  7.2
50e64y 349.7  13.0 430.4  15.5 281.2  10.7 405.2  12.0

65y 244.5  11.5 294.4  11.9 192.7  8.9 247.1  7.6
Totaly 375.4  6.4 405.2  6.5 274.3  5.0 346.5  4.8
*Organ meats, residual products, and processed meats were included, meat broth was excluded; yp for trend (p < 0.05). The p values are determined by a
generalized linear model; zAlcoholic drinks used for flavoring in the cooking process were excluded; xFruit juices, fruit jams, and salted and picked foods
were excluded. Values are given as mean (g)  SE. All values were weighted with the nutrition survey weight. CRDF Z cancer-related dietary factors;
KNHANES Z Korea National Health and Nutrition Examination Survey; SE Z standard error.

recommendations were drawn from evidences that each breast cancer risk was reduced by 60% in women who
risk factor increases the risk for all cancers, we assumed met at least five recommendations compared with those
that the cancer risk for a person who has one risk factor who met none (the Vitamins and Lifestyle study cohort).
is higher than that for a person with no risk factors. It is They recently found that cancer-specific mortality was
also projected that the cancer risk for a person with three 61% lower in individuals who met at least five recom-
risk factors is higher than that for one with fewer risk mendations compared with those who met none, and
factors. With the data from European Prospective adherence to the recommendation of plant foods was
Investigation into Cancer and Nutrition Project (EPIC) strongly associated with lower cancer-specific mortality
study, Romaguera et al [23] found that concordance [26]. Consumption of < 500 g red meat per week was a
with WCRF/AICR recommendations may lower the risk statistically significant protective factor for prostate
for most types of cancer. Concordance with WCRF/ cancer [27]. Catsburg et al [28] found that adherence to
AICR recommendations was also associated with lower six or seven of the WCRF/AICR recommendations was
all-cause mortality among women cancer survivors, as associated with 31% reduction in breast cancer risk.
evident from the Iowa Women’s Health Study [24]. The consumption of red meat was similar to that in
Several studies assessed the associations between other countries but attention needs to be paid to red meat
WCRF/AICR recommendations and specific cancer consumption of men in their 20s. The mean intake of red
risks. Hastert et al [25] examined the association of six meat increased from 79.3 g/d in 1998 to 80.8 g/
recommendations, including three cancer-related dietary d 2007e2009 in men and from 48.2 g/d to 40.7 g/d in
factors that were selected in this study from the WCRF/ women (Table 2), which slightly exceeded other coun-
AICR report, with breast cancer risk and found that tries’ red meat intake. Linseisen et al [29] reported that
Intake trends of cancer-related dietary factors in Korea 185

Table 3. Distribution of participants who did not meet the intake criteria for red meat, alcohol, and fruits/vegetables from
recommendations of WCRF/AICR.

CRDF Sex Age group (y) 1998 2001 2005 2007e2009

Red meat* Men 21e29y 36.2 28.8 40.9 47.2
30e49y 36.9 31.1 41.8 39.2
50e64 27.9 23.5 27.6 28.0

65 16.9 17.8 16.7 15.7
Total 32.5 27.7 34.8 31.6
Women 21e29y 28.2 20.7 34.3 30.9
30e49 24.6 21.6 26.8 22.5
50e64 14.4 13.7 16.5 13.6

65 10.6 8.5 9.6 8.1
Total 20.8 17.9 22.7 17.8
Alcoholz Men 21e29y 13.4 16.3 18.9 21.0
30e49y 18.2 18.3 22.5 26.4
50e64y 20.7 19.0 21.0 25.7

65 12.2 13.6 14.6 16.3
Totaly 17.2 17.6 20.4 23.3
Women 21e29y 4.9 6.1 8.7 12.9
30e49y 4.4 7.5 8.6 10.8
50e64y 3.5 4.5 6.1 5.6

65 3.5 2.1 3.2 2.4
Totaly 4.1 5.8 7.0 7.8
Fruits/vegetablesx Men 21e29y 70.1 71.0 80.8 75.2
30e49y 65.3 63.1 72.1 67.0
50e64 70.3 60.7 74.8 64.6

65y 81.2 69.2 84.3 74.9
Totaly 69.0 64.6 75.7 69.2
Women 21e29y 66.2 64.5 79.9 75.2
30e49y 60.0 57.1 75.5 64.7
50e64 69.0 58.3 74.8 62.9

65 81.0 74.4 89.0 80.5
Totaly 66.4 61.2 78.3 69.3
*Percentages of participants who consumed red meat over 71.4 g/d; yp for trend (p < 0.05). The p values are determined by the two-sided CochraneArmitage
trend test; zPercentages of male participants who consumed more than two alcoholic drinks/d and female participants who consumed more than one alcoholic
drink/d; one drink Z 10 g of alcohol; xPercentages of participants who consumed fruits and vegetables < 400 g/d. Values are given as percentages.
CRDF Z cancer-related dietary factors; WCRF/AICR Z World Cancer Research Fund/American Institute of Cancer Research.

Table 4. Distribution of participants with risk factors and mean intake of red meat, alcohol, and fruits/vegetables by the
number of risk factors in the KNHANES 2007e2009.

Number of risk factors*

0 1 2 3
n (%)
Total 3,174 (19.9)y 9,107 (57.2) 3,049 (19.1) 600 (3.8)
Participants with risk factors
Red meat 0 (0.0)z 1,093 (12.0) 2,044 (67.0) 600 (100.0)
Alcohol 0 (0.0) 288 (3.2) 1,355 (44.4) 600 (100.0)
Fruits and vegetables 0 (0.0) 7,726 (84.8) 2,699 (88.5) 600 (100.0)
Mean intake Mean  SE (g)
Red meatx 16.6  0.5 37.5  1.1 122.7  2.9 200.0  6.6
Alcoholx,jj 0.4  0.0 2.4  0.2 30.0  1.3 74.0  2.8
Fruits/vegetablesx,{ 754.0  9.3 266.4  4.0 250.8  4.8 217.0  5.2
*Whether participants have risk factors was determined with the criteria in the WCRF/AICR report. Participants who consumed
71.4 g red meat per day
and/or < 400 g fruits and vegetables per day were classified as risk groups for cancer. For alcoholic drinks, men who consumed over two drinks and women
who consumed over one drink per day were also classified as risk groups for cancer; yProportions of total participants; zProportions of groups according to the
number of risk factors; xp for trend (p < 0.05). The p values are determined by a generalized linear model; jjThe intake of alcoholic drinks was converted into
alcohol content; {Salted vegetables were excluded. Mean intakes were weighted with the nutrition survey weight. KNHANES Z Korea National Health and
Nutrition Examination Survey; SE Z standard error; WCRF/AICR Z World Cancer Research Fund/American Institute of Cancer Research.
186 M.K. Park, et al

the intakes of red meat ranged from 40 g/d (UK) to 74 g/ The results from this study implied that intake of
d (Spain) in men and from 24.6 g/d (UK) to 44.1 g/ fruits and vegetables in most of Korean adults was not
d (Denmark) in women. The intake of red meat in the sufficient for cancer prevention, even though it is not
USA [30] ranged from 70.3 g/d (1994) to 76.0 g/ lower than the fruit and vegetable intake of other
d (2004). For the Fukuoka Colorectal Cancer Study in studies. The mean intake of fruits and vegetables in
Japan, the red meat intake ranged from 29 g/d to 61 g/ France was 424.4 g/d in men and 492.4 g/d in women
d [31]. Although the mean intake of red meat for all [41]. The median intakes of fruits and vegetables were
individuals decreased since 1998, that of men aged 346 g/d in The Netherlands [42] and 198 g/d in Sweden
21e29 years increased sharply from 88.4 g in 1998 to [43]. The median intakes obtained from the EPIC cohort
109.5 g in 2009 (p < 0.05). In addition, the mean intake were 150.9 g/d for vegetables and 163.9 g/d for fruits in
of red meat for men in their 20s has been the highest men, and 185.2 g/d for vegetables and 217.0 g/d for
since 1998 except for in 2001. By contrast, in the United fruits in women [44]. In this cohort, the median intake of
States and Brazil, meat intake was highest in the age fruits and vegetables in Greece was over 800 g/d, which
group of 40e59 years [14]. In Spain, meat intake was was more than twice that of the other participating
significantly decreased in the age group of 25e44 years countries. Kurahashi et al [45] reported the median fruit
from 1992 to 2003 [18]. and vegetable intake to be 120.3 g/d in Japan. In the
Alcohol intake for men in this study was similar to Shanghai women’s and men’s health studies, the median
that in other countries, while alcohol intake for women intakes for fruits were 238.3 g/d in women and 128.3 g/
was lower than that in other countries. However, alcohol d in men, and for vegetable were 261.3 g/d in women
consumption should be monitored with special interest and 307.2 g/d in men [46]. These results seem to show
because alcohol consumption for total population (in that the intake of fruits and vegetables in the KNHANES
both sexes) has shown a tendency to increase since was similar to that in other Western countries and China,
1998. In this study, alcohol intake for men 30e64 years but higher than that in Japan and Sweden. However,
of age has increased significantly since 1998 and for since our calculations for fruit and vegetable intake
women 30e49 years of age has been increasing since excluded pickled vegetables (e.g., kimchi), which were
1998 (p < 0.05; Table 2). Genkinger et al [32] reported important sources of vegetables among Koreans, and
that alcohol intake ranged from 7.9 g/d to 17.3 g/d in fruit juices, the fruit and vegetable intake of this study
men and from 1.6 g/d to 8.6 g/d in women, by the would seem to be low compared with the results from
assessment of alcohol intake from 13 cohort studies in other studies. The Korea Health Statistics 2014 reported
the USA. Weikert et al [33] reported alcohol intakes in that kimchi was the third most frequently consumed
European countries surveyed in the EPIC study. The food in Korea, and its mean intake was 62.5 g/d [47].
alcohol intake ranged from 10.1 g/d (UK) to 40.6 g/ Since the total vegetable intake was 304.9 g/d in the
d (Spain) in men and from 4.2 g/d (Italy) to 7.2 g/ report, the kimchi intake was > 20% of total vegetable
d (Denmark) in women. The mean alcohol intake intake. For Koreans, kimchi, a form of salted and fer-
observed in the Women’s Health Initiative was 5.6 g/ mented vegetables, is known as one of the healthy foods
d (range, 0e244.5 g/d) [34]. Compared with these because it is an important source of vitamins, minerals,
studies, alcohol intake for women in their 20s was and dietary fiber [48]. Kimchi has been studied for its
similar to those in other countries, which was 6.7 g in health-related effects, and many studies have reported
2007e2009, and the alcohol intake for this age group that kimchi has various lactic acid bacteria produced in
increased rapidly since 1998. A J- or U-shaped rela- the fermentation process [49]. In addition, some studies
tionship between alcohol consumption and chronic dis- reported that kimchi reduced body weight in obese pa-
eases has been demonstrated in many studies [35e38]. tients [50] and it had antioxidant functions [51]. How-
By contrast, Maraldi et al [39] found that the protective ever, little evidence supports the cancer-preventive
effect of moderate alcohol intake was strongly attenu- effects of kimchi. More research on kimchi and its effect
ated after adjustment for lifestyle indicators such as on cancer is needed in order to recommend kimchi
education, income, body mass index, and physical ac- consumption for cancer prevention. The most notable
tivity. In this respect, although alcohol intake in women results were that the intake of fruits and vegetables for
was not high enough to be classified as moderate intake, men and women aged 21e29 years showed a tendency
it should be noted that their alcohol intake increased of decreasing significantly over 10 years. In the study of
continuously from 1998 to 2007e2009. Furthermore, Bezerra et al [14] with the sample population of the
many studies have reported that alcohol intake is asso- United States and Brazil, fruit and vegetable consump-
ciated with colorectal cancer incidence [21]. In Korea, tion was lowest in the age group of 21e39 years for both
colorectal cancer incidence has increased in both sexes sexes, as individuals aged 21e29 years showed the
since 1999 [40]. While we calculated alcohol intake lowest intake of fruits and vegetables in 2007e2009,
using the 1998 KNHANES data, which are the oldest except for those over 65 years, in this study.
available data, there is a possibility that alcohol intake In addition, low intake of fruits and vegetables seems
had been increasing continuously before 1998. to be the major risk factor among the participants of the
Intake trends of cancer-related dietary factors in Korea 187

KNHANES from 1998 to 2009. As the number of risk research findings in the future, then consumption of
factors increased, distribution of risk factors and intakes other cancer-related dietary factors could be evaluated
of selected cancer-related dietary factors were changed. in further studies. The limitation of this study is that the
For the participants who had only one risk, it seems that KNHANES data are 1-day recall data, which do not
their risk came from low fruits and vegetables intake reflect usual intakes. To overcome this limitation, new
since intake of fruits and vegetables was sharply drop- statistical methods such as the multiple source method
ped down being compared to the participants who had [53] and the National Cancer Institute method [54] have
no risk. It is also supported by that 85% of the risk recently been suggested as alternatives. However, these
factors for individuals who had only one risk factor can methods require at least 2 days’ 24-hour recall data to
be attributed to the intake of fruits and vegetables. For convert 24-hour recall data into the usual intake. Thus, if
individuals who had two risk factors, intake of red meat the KNHANES could provide 2 days’ data, cancer-
massively increased compared with those who had one related dietary factor intake might be evaluated more
risk factor. This shows that risks of individuals with two precisely using statistical methods. In addition, dietary
risk factors were mostly from high red meat intake and factors such as selenium and quercetin could not be
low fruit and vegetable intake. Alcohol intake was analyzed in this study because no food composition ta-
multiplied in individuals who had three risk factors bles were available for these factors in Korea. Dietary
compared with those with two risk factors. As the supplements were also excluded because no supplement
number of risk factors increased, another type of risk database is open to the public in Korea.
factor was added one by one. Since individuals with one We confirmed that intakes of red meat, alcohol, and
risk factor are the majority, it seems that low intake of fruits and vegetables have changed toward a negative
fruits and vegetables that is the major source of the risk direction over 10 years, especially in the age group of
factor for individuals with one risk factor is the major 21e29 years. Overall, the percentage of individuals who
risk factor for all individuals from 1998 to 2009. did not meet the intake criteria for the three cancer-
The differences between fruit and vegetable intakes related dietary factors has increased over 10 years and
in 2005 and those at other times can partly be explained was especially high in those in their 20s. Therefore, it
by seasonal variation. The fruit and vegetable intake in seems necessary to monitor and educate individuals in
2005 was lower than that in other years. The KNHANES the age group of 21e29 years, based on the consumption
in 2005 was conducted in the spring (April and May), pattern of three cancer-related dietary factors, to reduce
whereas the surveys in 1998 and 2001 were conducted the risk of cancer and the increase of cancer incidence in
in the early winter (November and December). Since this age group in the future.
2007, the KNHANES has been a year-round survey.
Locke et al [52] found that consumption of fruits and
vegetables was highest in the fall harvest season. Conflicts of interest
As we assessed the consumption of three cancer-
related dietary factors in this study, the risk of cancer All authors have no conflicts of interest to declare.
might be underestimated. The percentages of individuals
with three risk factors have increased significantly since
1998 in all age groups except for in the age group of > Acknowledgments
65 years (data not shown). For both sexes in the age
group 21e29 years, notably, this percentage has This study was carried out with the support of
increased sharply since 1998 (data not shown). How- “Cooperative Research Program for Agricultural Sci-
ever, the actual cancer risk in Koreans could be higher ence & Technology Development” (Project No.
than shown by the results of this study, since sodium PJ007211), Rural Development Administration, Re-
intake was not counted as a cancer-related dietary factor public of Korea.
in this study although the mean intake of sodium in most
Koreans was much higher than the intake criteria in the References
WCRF/AICR report.
The strength of this study is that we used nationally 1. WCRF/AICR. Food, nutrition, physical activity, and the pre-
representative data with a large sample size, KNHANES vention of cancer: a global perspective. Washington D.C. (WA):
AICR; 2007.
data from 1998 to 2007e2009, spanning a period of 10 2. Korea National Statistical Office. Annual report on the cause of
years, for analysis. We examined the intake trends for death statistics; 2010.
cancer-related dietary factors reported in the most recent 3. Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012
WCRF/AICR report by chronological order. It should be v1.0, Cancer Incidence and Mortality Worldwide: IARC Can-
noted that this study has been primarily concerned with cerBase No. 11 [Internet]. Lyon (France): International Agency
for Research on Cancer; 2013. Available from: [Link]
cancer-related dietary factors that were included in goals [Link] [accessed 15.08.15].
and recommendations suggested by the WCRF/AICR. If 4. Vainio H, Weiderpass E. Fruit and vegetables in cancer pre-
the WCRF/AICR report is updated with more reliable vention. Nutr Cancer 2006 Jun;54(1):111e42.
188 M.K. Park, et al

5. Hu JF, Morrison H, Mery L, et al. Diet and vitamin or mineral 26. Hastert TA, Beresford SA, Sheppard L, et al. Adherence to the
supplementation and risk of colon cancer by subsite in Canada. WCRF/AICR cancer prevention recommendations and cancer-
Eur J Cancer Prev 2007 Aug;16(4):275e91. specific mortality: results from the Vitamins and Lifestyle
6. Butler LM, Wang R, Koh WP, et al. Prospective study of dietary (VITAL) Study. Cancer Causes Control 2014 May;25(5):
patterns and colorectal cancer among Singapore Chinese. Br J 541e52.
Cancer 2008 Nov;99(9):1511e6. 27. Arab L, Su J, Steck SE, et al. Adherence to World Cancer
7. Skjelbred CF, Saebo M, Hjartaker A, et al. Meat, vegetables and Research Fund/American Institute for Cancer Research lifestyle
genetic polymorphisms and the risk of colorectal carcinomas and recommendations reduces prostate cancer aggressiveness among
adenomas. BMC Cancer 2007 Dec;7:228. African and Caucasian Americans. Nutr Cancer 2013;65(5):
8. Qin LQ, Xu JY, Wang PY, et al. Soyfood intake in the prevention 633e43.
of breast cancer risk in women: a meta-analysis of observational 28. Catsburg C, Miller AB, Rohan TE. Adherence to cancer pre-
epidemiological studies. J Nutr Sci Vitaminol (Tokyo) 2006 Dec; vention guidelines and risk of breast cancer. Int J Cancer 2014
52(6):428e36. Nov;135(10):2444e52.
9. Wu AH, Yu MC, Tseng CC, et al. Epidemiology of soy expo- 29. Linseisen J, Kesse E, Slimani N, et al. Meat consumption in the
sures and breast cancer risk. Br J Cancer 2008 Jan;98(1):9e14. European Prospective Investigation into Cancer and Nutrition
10. Trock BJ, Hilakivi-Clarke L, Clarke R. Meta-analysis of soy (EPIC) cohorts: results from 24-hour dietary recalls. Public
intake and breast cancer risk. J Natl Cancer Inst 2006 Apr;98(7): Health Nutr 2002 Dec;5(6B):1243e58.
459e71. 30. National Cancer Institute. Average ounces of red meat consumed
11. Kim HJ, Chang WK, Kim MK, et al. Dietary factors and gastric per 1,000 calories by individuals aged 2 years and older, both
cancer in Korea: a caseecontrol study. Int J Cancer 2002 Feb; Sexes, 1994e2010 [Internet]. 2010 [updated 2012; cited 2015
97(4):531e5. Aug 1]. Available from: [Link]
12. Nan HM, Park JW, Song YJ, et al. Kimchi and soybean pastes are prevention/red_meat.
risk factors of gastric cancer. World J Gastroenterol 2005 Jun; 31. Kimura Y, Kono S, Toyomura K, et al. Meat, fish and fat intake in
11(21):3175e81. relation to subsite-specific risk of colorectal cancer: the Fukuoka
13. Takachi R, Inoue M, Shimazu T, et al. Consumption of sodium Colorectal Cancer Study. Cancer Sci 2007 Apr;98(4):590e7.
and salted foods in relation to cancer and cardiovascular disease: 32. Genkinger JM, Spiegelman D, Anderson KE, et al. Alcohol
the Japan Public Health Center-based Prospective Study. Am J intake and pancreatic cancer risk: a pooled analysis of fourteen
Clin Nutr 2010 Feb;91(2):456e64. cohort studies. Cancer Epidemiol Biomarkers Prev 2009 Mar;
14. Bezerra IN, Goldman J, Rhodes DG, et al. Difference in adult 18(3):765e76.
food group intake by sex and age groups comparing Brazil and 33. Weikert C, Dietrich T, Boeing H, et al. Lifetime and baseline
United States nationwide surveys. Nutr J 2014 Jul;13(1):74. alcohol intake and risk of cancer of the upper aero-digestive tract
15. Riediger ND, Shooshtari S, Moghadasian MH. The influence of in the European Prospective Investigation into Cancer and
sociodemographic factors on patterns of fruit and vegetable Nutrition (EPIC) study. Int J Cancer 2009 Jul;125(2):406e12.
consumption in Canadian adolescents. J Am Diet Assoc 2007 34. Duffy CM, Assaf A, Cyr M, et al. Alcohol and folate intake and
Sep;107(9):1511e8. breast cancer risk in the WHI Observational Study. Breast Cancer
16. Nasreddine L, Hwalla N, Sibai A, et al. Food consumption pat- Res Treat 2009 Aug;116(3):551e62.
terns in an adult urban population in Beirut, Lebanon. Public 35. Hines LM, Rimm EB. Moderate alcohol consumption and cor-
Health Nutr 2006 Apr;9(2):194e203. onary heart disease: a review. Postgrad Med J 2001 Dec;77(914):
17. Wu SJ, Chang YH, Wei IL, et al. Intake levels and major food 747e52.
sources of energy and nutrients in the Taiwanese elderly. Asia 36. Maraldi C, Volpato S, Kritchevsky SB, et al. Impact of inflam-
Pac J Clin Nutr 2005 Jul;14(3):211e20. mation on the relationship among alcohol consumption, mortal-
18. Ribas-Barba L, Serra-Majem L, Salvador G, et al. Trends in ity, and cardiac events: the health, aging, and body composition
dietary habits and food consumption in Catalonia, Spain study. Arch Intern Med 2006 Jul;166(14):1490e7.
(1992e2003). Public Health Nutr 2007 Nov;10(11A):1340e53. 37. Kim MK, Ko MJ, Han JT. Alcohol consumption and mortality
19. Arruda SP, da Silva AA, Kac G, et al. Socioeconomic and de- from all-cause and cancers among 1.34 million Koreans: the
mographic factors are associated with dietary patterns in a cohort results from the Korea National Health Insurance Corporation’s
of young Brazilian adults. BMC Public Health 2014 Jun;14:654. health examinee cohort in 2000. Cancer Causes Control 2010
20. The Korean Nutrition Society. Recommended dietary allowances Dec;21(12):2295e302.
for Koreans; 2000. 38. Bagnardi V, Randi G, Lubin J, et al. Alcohol consumption and
21. World Cancer Research Fund/American Institute for Cancer lung cancer risk in the Environment and Genetics in Lung Cancer
Research. Food, nutrition, physical activity, and the prevention of Etiology (EAGLE) study. Am J Epidemiol 2010 Jan;171(1):
cancer: a global perspective. Washington D.C. (WA): AICR; 2007. 36e44.
22. Korea Centers for Disease Control and Prevention. The report of 39. Maraldi C, Harris TB, Newman AB, et al. Moderate alcohol
fourth Korea ational Health and Nutrition Examination Survey. intake and risk of functional decline: the Health, Aging, and
Seoul: the Ministry of Health and Welfare; 2009. Body Composition study. J Am Geriatr Soc 2009 Oct;57(10):
23. Romaguera D, Vergnaud AC, Peeters PH, et al. Is concordance 1767e75.
with World Cancer Research Fund/American Institute for Cancer 40. National Cancer Information Center. Changes in age-
Research guidelines for cancer prevention related to subsequent standardized incidence rate of cancers [Internet]; 2015 [updated
risk of cancer? Results from the EPIC study. Am J Clin Nutr 2014 Dec 25; cited 2015 Aug 1]. Available from: [Link]
2012 Jul;96(1):150e63. [Link]/mbs/cancer/[Link]?idZcancer_
24. Inoue-Choi M, Robien K, Lazovich D. Adherence to the 040104000000.
WCRF/AICR guidelines for cancer prevention is associated with 41. Estaquio C, Druesne-Pecollo N, Latino-Martel P, et al. So-
lower mortality among older female cancer survivors. Cancer cioeconomic differences in fruit and vegetable consumption
Epidemiol Biomarkers Prev 2013 May;22(5):792e802. among middle-aged French adults: adherence to the 5 A Day
25. Hastert TA, Beresford SA, Patterson RE, et al. Adherence to recommendation. J Am Diet Assoc 2008 Dec;108(12):
WCRF/AICR cancer prevention recommendations and risk of 2021e30.
postmenopausal breast cancer. Cancer Epidemiol Biomarkers 42. Griep LMO, Geleijnse JM, Kromhout D, et al. Raw and pro-
Prev 2013 Sep;22(9):1498e508. cessed fruit and vegetable consumption and 10-year coronary
Intake trends of cancer-related dietary factors in Korea 189

heart disease incidence in a population-based cohort study in the 48. Cheigh HS, Park KY. Biochemical, microbiological, and nutri-
Netherlands. PloS One 2010 Oct;5(10):e13609. tional aspects of kimchi (Korean fermented vegetable products).
43. Lof M, Sandin S, Lagiou P, et al. Fruit and vegetable intake and Crit Rev Food Sci Nutr 1994 Sep;34(2):175e203.
risk of cancer in the Swedish women’s lifestyle and health 49. Yoon JH, Kang SS, Mheen TI, et al. Lactobacillus kimchii sp.
cohort. Cancer Causes Control 2011 Feb;22(2):283e9. nov., a new species from kimchi. Int J Syst Evol Microbiol 2000
44. Vrieling A, Verhage BA, van Duijnhoven FJ, et al. Fruit and Sep;50(Pt 5):1789e95.
vegetable consumption and pancreatic cancer risk in the Euro- 50. Kim EK, An SY, Lee MS, et al. Fermented kimchi reduces body
pean Prospective Investigation into Cancer and Nutrition. Int J weight and improves metabolic parameters in overweight and
Cancer 2009 Apr;124(8):1926e34. obese patients. Nutr Res 2011 Jun;31(6):436e43.
45. Kurahashi N, Inoue M, Iwasaki M, et al. Vegetable, fruit and 51. Park JM, Shin JH, Gu JG, et al. Effect of antioxidant activity in
antioxidant nutrient consumption and subsequent risk of hepa- kimchi during a short-term and over-ripening fermentation
tocellular carcinoma: a prospective cohort study in Japan. Br J period. J Biosci Bioeng 2011 Oct;112(4):356e9.
Cancer 2009 Jan;100(1):181e4. 52. Locke E, Coronado GD, Thompson B, et al. Seasonal variation in
46. Epplein M, Shu XO, Xiang YB, et al. Fruit and vegetable con- fruit and vegetable consumption in a rural agricultural commu-
sumption and risk of distal gastric cancer in the Shanghai nity. J Am Diet Assoc 2009 Jan;109(1):45e51.
Women’s and Men’s Health studies. Am J Epidemiol 2010 Aug; 53. Haubrock J, Nothlings U, Volatier JL, et al. Estimating usual
172(4):397e406. food intake distributions by using the multiple source method in
47. Korea Centers for Disease Control and Prevention. Korea health the EPIC-Potsdam Calibration Study. J Nutr 2011 May;141(5):
statistics 2014. Chungbuk: Korea Centers for Disease Control 914e20.
and Prevention; 2015. 54. Tooze JA, Kipnis V, Buckman DW, et al. A mixed-effects model
approach for estimating the distribution of usual intake of nu-
trients: the NCI method. Stat Med 2010 Nov;29(27):2857e68.