Time trends in dietary cadmium intake of Korean women

Abstract

Objectives: To examine the amount of daily dietary Cd intake (Cd-D) as the most influential non-occupational source of exposure to Cd for women among general populations in Korea. Design: Foci were placed on: 1. time trends in the amount of dietary Cd intake as the estimated values and instrumental analysis values; 2. the current trends in Cd-D and two biological exposure markers of Cd in blood (Cd-B) and in urine (Cd-U); 3. the Cd-D by food groups and their time trends. Method and Materials: Cd-D by instrumental analysis and Cd in blood (Cd-B) and urine (Cd-U) were cited from previous representative Korean reports. In addition, Cd-D was estimated from data on food intakes (by food groups) published in the Korea National Health and Nutrition Examination Survey and the Cd contents by each food group reported in previous representative publications. Results and Discussion: The estimated Cd-D for Korean women in 2007 was 14.82 μg per day, of which 9.74 μg per day was from plant foods and 5.09 μg per day was from animal foods. The Cd-D of plant origin accounted for 65.7%, indicating that Cd-D for Korean women is mostly from plant foods. Among the plant food groups, ‘potatoes and starch’ and ‘grains and cereals (including rice)’ were not only the major energy source in Korea but the largest Cd-D accounts among the food groups, followed by ‘seaweed’ as the third source. ‘Fish and shellfish’ were the largest Cd-D source among the food groups of animal origin. As for time trends, the estimated Cd-D decreased by 13% over a 10 year period, whereas no clear reduction was observed in Cd-B and Cd-U. Conclusion: The main Cd-D source for Korean women is foods of plant origin. ‘Grains and cereals’, and ‘potatoes and starch’, are the most influential sources of exposure to Cd. Overview of Cd-D exposure over 10 years showed a trend of a slight decrease, but there was no noteworthy reduction in Cd-B and Cd-U.

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Introduction

Cadmium (Cd) is a hazardous metal ubiquitous in the environment by nature as well as through human activities. The general population has long-term exposure to Cd, but mostly at low levels, and the main sources are foods and drinking water.^1–4

The background Cd exposure of the Korean population has been reported in the literature.^5–7 Oral intake via foods as background exposure may vary over time,^8–10 and periodical biological monitoring surveys are important, e.g., to clarify the time trends in exposure. Nationwide management of exposure to hazardous materials, in accordance with the Environmental Health Act in Korea, aims at well-being of the general population.¹¹ As part of an epidemiological survey by the Korean government, two nationwide surveys were conducted: one on the environmental exposure and body burden of residents living near industrial areas,¹² and the other on the impact on the health of residents living near abandoned mines.¹³

The background exposure in terms of Cd in diet (Cd-D), blood Cd concentration (Cd-B), and urinary Cd concentration (Cd-U) of the general population have been studied in many areas such as Japan.¹⁴ Few reports are available however on the time trends of Cd-D and the sources of Cd-D in terms of food groups in Korea.

The present study summarizes Cd-D in various food groups consumed by adult Korean women and elucidates the changes of Cd-D in each food group over a 10 year period. The time trend of Cd-B and Cd-U were also examined as biological markers of exposure to Cd-D.

Materials and methods

Consumption of food by food group and estimation of Cd-D in each food group

The Ministry for Health, Welfare and Family Affairs of the Korean government conducted in Korea the National Health and Nutrition Examination Surveys in 1998, 2001, 2005 and 2007.¹⁵ The survey results were recorded as databases. The average weight of food intake reported in the surveys for women were used as the primary data (Table 1). Cd concentrations in each of the food groups sold in markets were cited from previous reports.^{15,17–37,43} These reports were sorted out for each food group, and the median, minimum and maximum values were cited from the reported Cd concentrations for each food group (Table 2). The Cd content per gram of each food item was calculated. Then, the Cd intake from each food group was estimated by multiplication of the average food intake (by food group) with the median Cd-D in the food group.

Table 1 Daily intake in each food group

Food group	Intake (g per day) in the year of
	1998	2001	2005	2007
The values are cited from the National Health and Nutrition Survey.^15
Food of plant origin
Grains and cereals	303.9	265.3	286.2	248.7
Potatoes and starch	38.1	27.6	19.7	32.1
Sugars and sweet	6.5	10.5	6.4	5.8
Pulses	26.8	27.3	34.9	31.7
Nuts and seeds	3.0	2.8	3.7	3.1
Vegetables	257.6	269.6	292.5	243.3
Mushrooms	4.0	4.7	4.2	3.6
Fruits	218.3	235.3	97.9	195.0
Seaweed	7.4	9.2	9.0	6.2
Beverages	59.5	88.9	86.2	98.8
Seasonings	22.1	28.3	33.3	24.3
Oils and fats	4.9	8.9	6.7	5.6
Others (plant origin)	3.2	5.2	0	1.3
Subtotal	955.3	983.6	880.7	899.5
Food of animal origin
Fish and shellfish	58.4	56.3	57.6	40.8
Meats and poultry	53.7	74.8	74.5	67.0
Eggs	18.6	18.3	23.2	17.9
Milks and dairy products	79.5	78.3	94.2	90.6
Fats	1.9	0.1	1.2	0.2
Others	0.1	0.2	0.1	0
Subtotal	212.2	228.0	250.8	216.5
Total	1167.5	1211.6	1131.5	1116.0

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Table 2 Median and range of Cd levels in each food group

Food group	Median^a (μg g^−1)	Range^a (μg g^−1)	References
a The range and the median of the values reported in the references. b No value is reported.
Food of plant origin
Grains and cereals	0.01	0.001–0.023	Kim et al.^16; Kwon et al.^17
Potatoes and starch	0.1	0.017–0.185	Kim et al.^16; Kwon et al.^17
Sugars and sweet	0.01	0.01	Chung et al.^18
Pulses	0.01	0.004–0.017	Kim et al.^16; Kim et al.^19
Nuts and seeds	0.06	0.06	Kwon et al.^17
Vegetables	0	0.003–0.016	Kwon et al.^17; Chung et al.^20; Chun et al.^21; Yoo and Kim^22
Mushrooms	—^b	—
Fruits	0	0.000–0.004	Kwon et al.^17
Seaweed	0.22	0.144–0.304	Kwon et al.^17; Mok et al.^23
Beverages	0	0.001–0.007	Kwon et al.^17; Chun et al.^21; Chung et al.^24; Kim et al.^25
Seasonings	0.01	0.01	Kwon et al.^17
Oils	—^b	—
Others	—^b	—
Food of animal origin
Fish and shellfish	0.06	0.002–0.559	Chun et al.^21; Sheo et al.^26; Sung and Lee^27; Kim and Han^28; Kim and Han^29; Ham^30; Kim et al.^31; Ha et al.^33; Hwang and Park^34; Kim et al.^35; Mok et al.^36
Meats and poultry	0.03	0.03	Kim et al.^32
Eggs	—^b	—
Milks and dairy products	0.01	0.01	Park^37
Fats	—^b	—
Others	—^b	—

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Time trend in Cd-D, Cd-B and Cd-U

Previous publications on Cd-D, Cd-B and Cd-U^{5,6,12,15,31,38–43} were reviewed for time trends.

Results

Annual trends in food intake

The daily intake values in Table 1 were cited from the National Health and Nutrition Survey, Korea;¹⁵ the national surveys were conducted in 1998, 2001, 2005 and 2007 (4 times in 10 years) and a combined report was published in 2008. The data from these surveys were the basis for nationwide monitoring and management of public health by the Government of Korea. For this reason, the surveys were conducted by the governmental experts and the results should be taken as representative and reliable.

The food groups were divided into those of animal and plant origins (Table 1). The plant group was divided into 13 subgroups, and the animal group into six subgroups. The sum of the mean daily intake for all food subgroups made up the total intake by weight. The total food intake was 1116.0 g per day in 2007 (values for 1998 to 2007 in a range of 1167.5 to 1211.6 g per day), of which the intake from plant foods was 899.5 g per day (880.7 to 983.6 g per day) and that from animal foods was 216.5 g per day (212.2 to 250.8 g per day), respectively, or by 80.6% and 19.4% of the total intake. During the 10 year period of 1998 to 2007, the dietary intake of both plant origin such as grains and cereals, potatoes and starches and fruits decreased. In contrast, the intake of beverages of plant origin increased. In food groups of animal origin, the intake of ‘fish and shellfish’ decreased, and those of ‘meats and poultry’ and ‘milks and dairy products’ increased.

Daily intake of vegetables (243.3 g per day in 2007) was comparable to grains (248.7 g per day), the latter being the main energy source for Koreans. Other major groups by weight were fruits (195.0 g per day), beverages of vegetable origin (98.8 g per day), potatoes and starches (32.1 g per day), and pulses (31.7 g per day). In the food groups of animal origin, milks and dairy products were consumed by 90.6 g per day, being highest by intake weight. In a decreasing order of intake by weight, meats and poultry were 67.0 g per day, fish and shellfish 40.8 g per day, and eggs 17.9 g per day.

Cd levels in foods

Medians and ranges (i.e., the minimum and the maximum of the mean values given in reports cited) are summarized in Table 2. The median Cd content ranged from 0.002 to 0.224 μg g⁻¹ for food groups of plant origin and from 0.03 to 0.064 μg g⁻¹ for food groups of animal origin. Thus, the median Cd contents was in a range of 0.002 to 0.224 μg g⁻¹, respectively, for all food groups.

Annual trends in Cd intake

Table 3 shows the median and range of estimated dietary Cd intake (Cd-D) for each food group and the annual trend in Cd-D. The intake for each year was calculated as the intake of each food group (Table 1) multiplied by the median Cd content for each food group (Table 2), followed by summation. In 2007 for example, estimated dietary Cd intake (range) was 14.82 (5.73–45.15) μg per day. The estimated Cd-D was 9.74 μg per day for foods of plant origin and 5.09 μg per day for foods of animal origin. Therefore, 65.7% of the Cd-D came from plants. The leading Cd-D sources among those of plant origin were ‘potatoes and starch’ [3.25 (0.55–5.94) μg per day], followed by ‘grains and cereals’ [3.04 (0.35–5.72) μg per day]. Seaweed was the third largest source [1.39 (0.89–1.88) μg per day]. Among animal foods, the median and range were highest for fish and shellfish [2.62 (0.08–22.81) μg per day in 2007]. Thus, a half of the Cd intake of animal origin came from fish and shellfish. The next largest source of Cd intake was meats and poultry (2.01 μg per day).

Table 3 Time trend of estimated dietary Cd intake

Food group	Daily Cd intake (μg per day)
	1998		2001		2005		2007
	Median	Range^a	Median	Range^a	Median	Range^a	Median	Range^a
Values in the table are calculated from daily food intake in each year (Table 1) multiplied with median (minimum – maximum) Cd contents in each food group (Table 2).a The range of the minimum and the maximum.
Food of plant origin
Grains and cereals	3.71	0.43–6.99	3.24	0.38–6.10	3.49	0.41–6.58	3.04	0.35–5.72
Potatoes and starch	3.85	0.65–7.06	2.79	0.47–5.11	1.99	0.33–3.65	3.25	0.55–5.94
Sugars and sweet	0.03	0.03	0.05	0.05	0.03	0.03	0.03	0.03
Pulses	0.22	0.10–0.46	0.22	0.10–0.46	0.28	0.13–0.59	0.26	0.12–0.54
Nuts and seeds	0.19	0.19	0.18	0.18–0.18	0.23	0.23–0.23	0.19	0.19–0.19
Vegetables	0.88	0.77–4.12	0.92	0.81–4.31	0.99	0.88–4.68	0.83	0.73–3.89
Mushrooms	0	0	0	0	0	0	0	0
Fruits	0.44	0.00–0.85	0.47	0.00–0.92	0.2	0.00–0.38	0.39	0.00–0.76
Seaweed	1.66	1.07–2.25	2.06	1.32–2.79	2.01	1.30–2.73	1.39	0.89–1.88
Beverages	0.09	0.06–0.42	0.14	0.09–0.62	0.13	0.09–0.60	0.15	0.10–0.69
Seasonings	0.20	0.20	0.26	0.26	0.30	0.30	0.22	0.22
Oils	0	0	0	0	0	0	0	0
Others	0	0	0	0	0	0	0	0
Subtotal	11.26	3.50–22.56	10.32	3.66–20.81	9.67	3.70–19.79	9.74	3.18–19.88
Food of animal origin
Fish and shellfish	3.76	0.12–32.65	3.62	0.11–31.47	3.70	0.12–32.20	2.62	0.08–22.81
Meats and poultry	1.61	1.61	2.24	2.24	2.24	2.24	2.01	2.01
Eggs	0	0	0	0	0	0	0	0
Milks and dairy products	0.40	0.40	0.39	0.39	0.47	0.47	0.45	0.45
Fats	0	0	0	0	0	0	0	0
Others	0	0	0	0	0	0	0	0
Subtotal	5.76	2.13–34.65	6.26	2.75–34.11	6.41	2.82–34.90	5.09	2.54–25.27
Total	17.02	5.62–57.21	16.57	6.40–54.92	16.08	6.52–54.69	14.82	5.73–45.15

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As for a time trend, the dietary Cd intake decreased slightly (i.e., by 12.9%) during the 10 years, from 17.02 μg per day in 1998 to 14.82 μg per day in 2007. Similarly, the Cd intake from plant foods decreased (by 13.5%) from 11.26 μg per day in 1998 to 9.74 μg per day in 2007. The overall decrease of Cd-D in plant origin was mostly due to less Cd intake from ‘grains and cereals’ and ‘potatoes and starch’. Changes in Cd-D of animal origin were not clear; the Cd-D from’ fish and shellfish’ decreased whereas Cd-D from ‘meats and poultry’ increased, as dietary intake of these food items increased. It should be noted that the maximum Cd-D intake estimated for ‘fish and shellfish’ (22.81 μg per day) was greater than that for ‘potatoes and starch’ (5.94 μg per day) or ‘grains and cereals’ (5.72 μg per day).

Discussion

It seems that a slight decrease took place over the 10 year period (1998 to 2007) in total Cd-D intake, i.e., 17.02 μg per day to 14.82 μg per day (Table 3). Cd intake from grains and cereals, potatoes and starch, as well as fish and shellfish decreased. These results may be associated with moderate changes in dietary habits among Korean populations (Table 1).

Annual trends in Cd-B, Cd-U and Cd-D reported in the literature are summarized in survey date order in Table 4. It appears likely that Cd-B showed no clear increase or decrease over time. The lowest Cd blood concentration reported was 1.27 μg L⁻¹, as a geometric mean for general Korean populations in four sites in 1994.⁵ The highest value reported is 2.74 μg L⁻¹, which is the geometric mean for 20–30 year-old mothers in the Busan area in 2000.⁴⁰ The Cd-B in 2005 was 1.48 μg L⁻¹ as a geometric mean. Cd-U was 1.56 μg g⁻¹ creatinine in 2000⁴⁰ and 2.08 μg g⁻¹ creatinine in 2007,¹² based on the survey of exposure levels and the biological monitoring of environmental hazards for residents (in the Gwangyang area). Therefore, it is possible to summarize that Cd-D decreased slightly, whereas both Cd-B and Cd-U did not change clearly (being different from the case of Cd-D). It should be taken into account that the data referred to have a limitation for use in direct comparison, as some of them were estimated values whereas others were measured values. The data in Table 2 are representative as samples were collected nationwide under governmental sponsorship, and therefore the estimated Cd-D values in Table 3 can also be taken as representative for a whole country. In Table 4, however, some values are for local populations as specified in the remarks.

Table 4 Blood and urinary concentration and dietary intake of Cd

Year of survey	Cd-D (μg per day)	Cd-B (μg L^−1)	Cd-U (μg L^−1)	Reference	Remarks
a Unit: μg g^−1 creatinine.
1986	17.1	1.45		Watanabe et al.^38
1994	21.2	1.27		Moon et al.^5	4 sites in Korea
1994		1.39	1.86	Moon et al.^6	30–40yrs-old Korean women
			2.26^a
1995		2.1		Ohn et al.^39	AM
1998	17.02			Estimated Cd intake (the present study; see Table 3)
2000	16.7	2.74	1.23	Moon et al.^40	Large city (Busan)
			1.56^a
2000	18.55			Food and Drug Administration, Korea^41	Nation-wide field survey
2001	14.3			Food and Drug Administration, Korea^42	Nation-wide field survey
2001	16.57	1.66		Cd-D; Estimated Cd intake (the present study; see Table 3), Cd-B; Kim et al.^43	Large city (Seoul)
2001		1.68		Kim et al.^31	Men and women in a large city (Seoul)
2005	16.08	1.48		Cd-D; Estimated Cd intake (the present study; see Table 3), Cd-B; Ministry of Health, Welfare and Family affairs, Korea^15	Nationwide survey
2007			2.08^a	Ministry of Environment, Korea^12	Middle-sized city
2007	14.82			Estimated Cd intake (the present study; see Table 3)

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The major dietary sources of Cd in Korean foods deserve discussion in connection with time trends. The decreases from 1998 levels were clearer for those from ‘grains and cereals’, and ‘potatoes and starch’ than others. Furthermore, the intake of seaweed, which is a substantial Cd-D source, also decreased.

Two reports published by the Korean government are relevant to this result. One is on the dietary intake and risk assessment of heavy metals in Korean foods,⁴² which reported in 2001 that dietary Cd intake was 14.3 μg per day. The value is somewhat lower than the value obtained in the present study, i.e., 16.57 μg per day as estimated Cd intake for the same year (Tables 3 and 4). The report⁴² stated that roasted green seaweed was the most influential food for Cd intake in a typical Korean menu, followed by roasted anchovies, and kimchi (Korean pickles, or seasoned and fermented spinach, lettuce, and sliced white radish). The method employed in the study however appeared to be not sensitive enough; analytical values were given to only food items with high Cd contents, whereas values were not given to many other foods, e.g. ‘grains and cereals’ and ‘fish and shellfish’, even though they are known to be substantial sources as discussed above.

The other report⁴¹ published in 2000 was on the risk assessment of dietary intake of heavy metals in Korean foods. Namely, after the selection of one typical menu for each of six areas in Korea, the Cd-D were calculated based on the food material collection after a Korea National Health and Nutrition Examination Survey¹⁵ followed by instrumental analysis of the foods collected. The average dietary intake for Koreans was examined in six sampling sites; food samples were commonly collected in summer. In the report, the dietary Cd intake was lowest [1.39 μg kg⁻¹ body weight per week] in the Kyeongsang-do area and highest (3.16 μg kg⁻¹ body weight per week) in Gangwon-do area. The national average was 2.20 μg kg⁻¹ body weight per week. Assuming that the average body weight of a Korean woman is 59.0 kg,¹⁵ the range of the lowest (Gyeongsang-do) and the highest (Gangwon-do) is 11.72–26.64 μg per day with a national average of 18.55 μg per day. The results are close to that of the present study of estimated Cd-D for 2001 (16.57 μg per day; Table 3).

The estimation of Cd-D in the present study is based on 24 hour food intake which was reported in the nationwide surveys. Data for Cd-D in 2000 and earlier were based on the diet duplicate method coupled with instrumental analysis after acid wet-digestion. The estimated Cd-D value for 2001 (16.57 μg per day; Table 3) was very close to the values of instrumental analysis reported for 2000 (16.7 μg per day; Table 4), although no data were available for mushrooms, and oils of plant origin or eggs, and fats of animal origin in the estimation. However, the amounts of intake of these food items were generally small and no high Cd concentrations were ever reported. In addition, care should be taken in making comparison as the former is a nationwide estimate whereas the latter is for the city of Busan.

Among grains and cereals, cooked rice is the main Cd source. Median Cd intake from grains and cereals was 3.04 μg per day in 2007 (Table 3). Cooked rice is the major source of energy for everyday life in Korea as in Japan^3,5,44,45 and also the leading source of Cd burden in both countries. Potatoes and starch (3.25 μg Cd per day) and seaweed (1.39 μg Cd per day) are additional sources of Cd in foods in Korea. Cd contents in potatoes and starch (0.101 μg g⁻¹) were 10 times higher than that in grains and cereals (0.012 μg g⁻¹; Table 2). Seaweed contains 22 times Cd (0.224 μg g⁻¹) than ‘grains and cereals’. Therefore, as the Cd intake from grains and cereals is almost equal among people of various locations because they are staple foods, the intake of these two foods (potatoes and starch, and seaweed) should affect Cd intake substantially among the plant food group.

With regard to food groups of animal origin, ‘fish and shellfish’ provided 2.62 μg per day, which are the third highest Cd intake food group and the group with the widest variation in Cd content (Table 3). It has been reported that ‘fish and shellfish’ are the main source of Cd among food groups of animal origin.^46,47 When fish and shellfish were divided into two subgroups, fish does not contain Cd at high levels, but shellfish does. The median Cd intake from fish was 0.033 μg per day and the range was 0.002–0.073 μg per day.^{21,26–28,30,33–36} In contrast, the median and the range for Cd from shellfish were 0.120 μg per day and 0.120–0.559 μg per day,^28–31,33 respectively. Therefore, shellfish should be the most influential food item for the Cd-D from animal-based foods.

Comparing the changes over the 10 year period 1998–2007 it can be concluded that the estimated Cd-D intake in Korea decreased slightly (i.e., by 13%), while Cd-B and Cd-U did not show clear reductions. Cd-D for Korean comes mainly from foods of plant origin. ‘Grains and cereals’ and ‘potatoes and starch’ are the leading sources of dietary Cd.

Conflict of interest

The authors declare that they have no conflict of interest.

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