Open Access
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Dans une revue
Radioprotection
DOI https://doi.org/10.1051/radiopro/2021009
Publié en ligne 5 avril 2021

© The Authors, published by EDP Sciences 2021

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1 Introduction

137Cs, an isotope of Caesium (Cs), is produced by gamma (γ)-emission from artificial radiation resulting from nuclear weapons tests or nuclear facility accidents (UNSCEAR, 2000). 137Cs can be harmful to humans based on assessments of bodily exposure because it has a relatively long half-life (30.03 yr) and releases very strong gamma rays (662 keV) (Oh and Ryu, 2006). Furthermore, it is estimated that 15.2 ± 18.3 PBq 137Cs was introduced into the northern Pacific Ocean and deposited in the atmosphere by the recent Fukushima Nuclear Power Plant (NPP) accident in 2011 (Aoyama, 2018). This artificial Cs isotope has chemical characteristics similar to potassium (K), a significant nutrient present in nature, in that both Cs and K are alkali elements. Consequently, 137Cs released in the ocean is soluble in water and is therefore easily taken up by living organisms; furthermore, it known to affect the muscles and stomach (Koide et al., 1982).

239+240Pu is the alpha (α)-emitting isotope of Plutonium (Pu) that was released primarily during the 1950s and early 1960s by the atmospheric bomb tests of the Cold War period (Peirson et al., 1982; Clark and Smith, 1988; Donaldson et al., 1997). The half-lives of 239Pu and 240Pu are 24,100 and 6,561 years, respectively – much longer than other artificial radionuclides. 239+240Pu absorbed by marine organisms is known to pose significant health risks to humans via seafood consumption (Kim et al., 2020). Moreover, Pu is known to affect human liver and bone tissues, potentially causing cancer (Nielsen et al., 2012).

As of June 2020, the number of NPPs in South Korea has increased by 80.7% since the 1980s, with the amount of power generated by NPPs having increased to 25%–18% higher than the Organization for Economic Co-operation and Development (OECD) average (Korea Institute of Nuclear Safety, 2019). Hence, research on the potential impact of the release of artificial nuclides such as 137Cs and 239+240Pu on seawater surrounding the Korean Peninsula from NPP accidents, is needed.

However, studies on the effects of artificial radionuclide accumulation in marine products are rare, other than those conducted immediately following the Fukushima accident (Schiermeier, 2011; Kryshev et al., 2012; Fisher et al., 2013). More recently, Kim et al. (2019) reported that 137Cs in some fishes increased with increasing size (weight). However, this study categorized fishes into only two growth stages, limiting the evaluation of artificial nuclide accumulation patterns based on a lack of detail at various growth stages.

Anchovy (Engraulis japonicus) is a coastal migratory fish present along the entire coast of South Korea during the summer (Fig. 1) (Cha et al., 1990). Anchovy fisheries dominate the South Korean fishing industry, manifesting very high economic value because anchovies are commercially useful from the fry stage onward (Kim and Lo, 2001; Oh, 2018). Given that all body parts are edible and readily consumed (e.g., for broth in most Korean soups) in Korean food culture, investigation of the accumulation of artificial radionuclides in anchovies in the Korean seas is critical. Moreover, anchovies captured in the coastal waters of the Korean Peninsula are classified into four to six groups (within the same species) according to their growth stages, thereby rendering them a useful fish species for research on the accumulation of artificial radionuclides.

The purpose of this study was to determine the level of artificial radionuclides 137Cs and 239+240Pu in anchovies from Korean seas and to evaluate the accumulation patterns of these nuclides in anchovy – the fish most widely consumed by the people of South Korea in particular and East Asian countries in general.

thumbnail Fig. 1

The Korean seas, sampling region (yellow box), and locations of nuclear power plant facilities in South Korea (left). The migratory map of anchovy (right) around the Korean Peninsula. Arrows denote the direction of migration and the numbers denote the date (month) corresponding to the migration route of anchovy.

2 Methods

2.1 Sample collection and pretreatment

The dried anchovy samples were collected from seafood markets along the southeastern coast of South Korea in 2018. Each box of samples weighed approximately 5 kg. The samples were classified into smallest (1.6–3 cm, XS), small (4–5 cm, S), medium (5–6 cm, M), and large (6–7 cm, L) categories. Before analysis, the dried anchovies were further dried in a drying oven (60 °C) for more than 24 h, after which the dry weight was recorded. The samples were then homogenized and stored in a desiccator. The entire body of each anchovy was used. Here, we noted that the anchovies caught off the coast of Korea vary in size, but only one species (Engraulis japonicus) lives and is used as a food ingredient for Koreans. Thus, our study valid for the whole country (around the Korean Peninsula), not for a specific part of Korea.

2.2 Analytical procedure

2.2.1 137Cs measurements

Four to five hundred grams of anchovy dry-weight was placed in a γ-counter container (Marinelli beaker, Eckert & Ziegler, Germany) and gamma nuclide analysis was performed using a high-purity Ge (HPGe) detector (P-TYPE coaxial detector; Mirion Technologies (Canberra BNLS) NV, San Ramon, CA, USA). The γ-spectrometer used in this study was 39.7 mm in depth and 61.5 mm in diameter and the distance from the window was 5.51 mm. The relative efficiencies of the two detectors were 30% and > 50%, respectively. Prior to conducting sample measurements, the γ-spectrometer was calibrated using a mixed γ standard solution [Multinuclide Standard, Isotope Products Laboratories (IPL), Burbank, CA, USA] that was geometrically the same type as ours (Marinelli beaker). Samples were counted for more than 3 days and the average chemical yields were approximately 70%.

2.2.2 Pu isotope (239+240Pu) analyses

The homogenized samples (200–300 g) were incinerated in an electric furnace for 24 h at 600 °C. The temperature of the electric furnace was increased by 100 °C per hour for complete incineration, preventing carbonization. Next, the samples were spiked with the Pu tracer (242Pu; 4 mBq per sample) and acidified with a 1:3 mixture of nitric acid (HNO3) and hydrochloric acid (HCl), then heated at 80 °C to decompose the organic matter. If a white residue remained, concentrated HNO3 was added to complete the decomposition. After complete decomposition was verified visually, the samples were collected and evaporated to dryness.

The dried samples were dissolved with 50 mL of 8 N HNO3 and extracted upon passage through an anion-exchange resin column (AGI-X8, 100–200 mesh; Bio-Rad Laboratories, Hercules, CA, USA). Next, Pu isotopes were eluted using 0.1 N NH4I/9N HCl. The eluted samples were fully dried and subjected to one additional column extraction. The purified Pu-elution solutions were again dried with HNO3 and Na2SO4 to reduce Pu(VI) to Pu(IV) for electroplating by adsorption, then adjusted to a pH of 2.1–2.4 by adding sulfuric acid. The samples were transferred to an electrodeposition cell mounted with a stainless steel disc (16-mm diameter) and the Pu was separated under 1 Å for 1 h. Finally, the stainless steel discs electroplated with Pu were counted using α-spectrometry (PIPS detector with MCA, Mirion Technologies). Samples were counted for more than 5 days and the average chemical yields were approximately 80%. The measurement data were calibrated based on the chemical yields of spiked 242Pu.

2.2.3 Method validation

To validate our analysis methods, radionuclide certified reference material (CRM) IAEA-414 (mixed fish from the Irish and North Seas; IAEA, 2013) from the International Atomic Energy Agency (IAEA) was analyzed together with the samples. The analytical results of the CRM were in good agreement with the certified values for 137Cs and 239+240Pu (Tab. 1).

Table 1

Certified and measured values (Bq kg−1 based on dry mass) of radionuclide certified reference materials (CRMs).

3 Results and discussion.

3.1 Accumulation of 137Cs in anchovies

The 137Cs activity measured in each anchovy sample is listed in Table 2. The average 137Cs activity in the anchovies was 74 ± 11 mBq kg−1, 121 ± 16 mBq kg−1, 132 ± 16 mBq kg−1, and 137 ± 19 mBq kg−1, respectively, in the smallest (XS), small (S), medium (M), and large (L) anchovy. Overall, the 137Cs activity increased with increasing body size (length) (p < 0.05) (Fig. 2a). According to Kim et al. (2019), it was found that 137Cs accumulates as fish grow (for Spanish mackerel, mullet, and pollack, etc.) in the Korean seas. The higher 137Cs concentration in larger anchovies in this study also seems to be related to artificial radioactivity such as 137Cs accumulation in anchovy according to growth stage.

The 137Cs activity in anchovy was compared with that of other marine organisms collected in recent years (2015–2017) (Fig. 3a). The average 137Cs activity in anchovy was similar to that in other fishes. However, the average 137Cs activity was 1–2 times lower than that of microalgae and 2–3 times higher than that of crustaceans and mollusks (Kim et al., 2019) (Fig. 3a). Since 137Cs in seawater is soluble, it is easily taken up by living marine organisms. In this study, we did not determine the exact mechanism by which 137Cs accumulates in anchovy during growth, but we think it involves both: i) the uptake of seawater containing artificial nuclides from current NPP operations as well as past NPP accidents; and ii) elevated levels due to bioaccumulation by grazing.

Table 2

The body length of each anchovy sample group, activities of artificial radionuclides,137Cs and 239+240Pu, and calculated concentration factors (CFs) of these nuclides in this study. All uncertainties in this study are denoted as standard deviations for the measured values.

thumbnail Fig. 2

Activities of (a) 137Cs and (b) 239,240Pu in anchovy according to their size.

thumbnail Fig. 3

Comparisons of activities of (a) 137Cs and (b) 239,240Pu in anchovy (black bars) according to size with other groups of marine organisms such as other fish, crustaceans (Crus.), and mollusks (Moll.) (grey bars). The smallest-, small-, medium-, and large- anchovies are expressed as XS, S, M, and L, respectively, for convenience in visualization.

3.2 Accumulation of 239+240Pu in anchovy

The 239+240Pu activity measured in each anchovy sample is listed in Table 2. The mean 239+240Pu activity in anchovy was 0.27 ± 0.10 mBq kg−1, 1.58 ± 0.26 mBq kg−1, 3.21 ± 0.37 mBq kg−1, and 1.19 ± 0.23 mBq kg−1, respectively, in smallest (XS), small (S), medium (M), and large (L) anchovy. Overall, 239+240Pu activity increased with increasing body size, yet activity decreased noticeably in the large anchovy (Fig. 2b). The 239+240Pu activity in anchovy in this study was compared with that of other marine organisms collected in recent years (2015–2017) (Fig. 3b) in the same manner as 137Cs. The 239+240Pu activity in anchovy was 1–2 orders of magnitude higher than that in all other marine organisms observed, including fish, crustaceans, and mollusks (Kim et al., 2019) (Fig. 3b). This significantly higher 238+239Pu in anchovy is likely to be attributed to the anchovy’s unique migratory pattern that circulates the entire coastal area around the Korean Peninsula where several domestic NPPs are located (Fig. 1).

Pu is known to pose a significant health risk to humans via exposure through food or respiration. A previous study suggested that soluble Pu is associated with certain diseases, including tumors in bones, the liver, and other organs (Beyea and von Hippel, 2019).

In this study, improved food selectivity in anchovy following growth may be a more important mechanism of 239+240Pu accumulation (Fig. 2b) than seawater uptake because Pu(IV) (i.e., PuO2) is relatively insoluble in seawater, in contrast to 137Cs (Lindahl et al., 2010). In general, as an anchovy grows, feeding rate increases due to the increase in: i) mouth size, ii) swimming ability, and, above all, iii) food search ability. As a strategy to increase the survival rate, it has been known that the improvements of food selectivity of adult anchovy especially could lower the rate of empty stomach (Kim et al., 2013; Yoo and Jeong, 2016).

In contrast to 137Cs, 239+240Pu activity in adult (large, L) anchovies decreased 2–3-fold in this study, suggesting that certain in vivo mechanisms for reducing (artificial) radionuclides are at work in anchovies. Yue et al. (2018) reported that complexes of uranium (U), an actinide element similar to 239+240Pu, with chelating ligands constitute a common mechanism of U detoxification. In particular, metallothionein (synthesized in the liver and kidney) is often considered a significant biochemical antidote, complexing with metals and limiting the availability of toxic chemical substituents (e.g., metals or metalloids) in the cells and tissues of fish such as anchovy (Shi, 1990; King et al., 1997; Kang, 2006; Thompson and Bannigan, 2008; Annabi et al., 2013). Moreover, a recent study found that this low-molecular-weight protein shows efficient detoxifying effects based on acute depletion of U in land animals (Jiong et al., 2010). Therefore, we think that 239+240Pu accumulated in marine organisms can be sufficiently removed as a result of the metallothionein effect. Furthermore, a more recent study reported that the accumulation of 239+240Pu was more concentrated in the internal organs than in muscle or skin (or exoskeleton), unlike the accumulation 137Cs (mainly accumulated in muscle) (Kim et al., 2020). This implies that 239+240Pu can be more efficiently detoxified than 137Cs (as revealed in the present study) in adult fish because metallothionein metabolism mainly occurs in internal organs (e.g., the liver).

3.3 Accumulation rate of 137Cs in anchovies compared to other fishes

In order to compare and evaluate the enrichment pattern of the artificial radionuclide 137Cs according to the growth stage in anchovies and other fish species (Kim et al., 2019), 137Cs activity was plotted against the mean age of fish estimated from body length (data applied from the Korean Fisheries Life Resources Information Center, https://www.nifs.go.kr/frcenter/) (Fig. 4). The activity of 137Cs in other fish samples (anchovy, Spanish mackerel, pollack, mullet, and flounder; data from Kim et al. (2019)) increases as fish size increases. The activity of 137Cs in anchovy was lower than that in other fish species, except flounder. However, considering the accumulation rate and the coefficient of exponential growth (fitting) curve of anchovy (1.36) (Fig. 4), the accumulation rate of 137Cs in anchovy was significantly higher than that of Spanish mackerel (0.16), pollack (0.049), and mullet (0.0042) (Fig. 4). This relatively higher 137Cs accumulation rate considering the ages of each fish species seems to be due to the anchovy’s unique migratory pattern, circulating the entire coastal area around the Korean Peninsula where several domestic NPPs are located (Fig. 1).

thumbnail Fig. 4

The plot of mean 137Cs activities in anchovy against their age (months) and comparisons with other fish species. Note that the x-axis does not represent a linear scale but is instead an arbitrary scale.

3.4 Concentration factors of artificial nuclides in anchovy

The level of radioactive contamination in anchovy can be evaluated by quantifying the concentration factors (CFs) of nuclides in marine organisms based on mean activities in seawater. The CFs of the radioactive nuclides were determined as follow (IAEA, 2004):

The calculated CFs for 137Cs and 239+240Pu in anchovy used in this study are presented in Table 2. In this calculation, the average activities of 137Cs (1.64 ± 0.09 mBq kg−1) and 239+240Pu (4.78 ± 0.36 µBq kg−1) in the surface water of Korean sea (from the 5 stations in the East/Japan Sea) were measured in February 2018–the same period during which samples were collected for this study. In general, the CFs in the organisms have a wet weight-based value. However, the anchovy samples used in this study were dried; thus, we noted that our CF results were corrected by multiplying 0.2389 to convert to (estimated) wet weight, applying a previously reported value by Kim et al. (2017).

The quantified CFs of 137Cs and 239+240Pu by anchovy consumption are presented in Table 2. The calculated CFs of 137Cs were lowest in the smallest anchovy (10.9 ± 2.2) and highest in large anchovy (20.2 ± 3.9). The calculated CFs of 239+240Pu were also lowest in the smallest anchovy (14.0 ± 6.1) and highest in medium anchovy (162.8 ± 30.1) (Fig. 5). In order to evaluate the accumulation levels of 137Cs and 239+240Pu in anchovies, these results were compared with those of other marine products and their recommended CF values (IAEA, 2004) (Fig. 5). The calculated CFs of 137Cs in anchovies in this study were generally lower than those of other marine products (other fishes, crustaceans, mollusks, and algae) collected in 2015–2017 (Kim et al., 2019). The mean CF of 137Cs (16.82 ± 1.33) in anchovies were also an order of magnitude lower than the IAEA recommendations (100 for 137Cs in fish). On the other hand, the calculated CFs of 239+240Pu in anchovy is significantly higher than those in other fishes. In addition, the mean CFs of 239+240Pu in anchovies were comparable (61 and 80 in small- and large anchovy, respectively) or even higher (163 in medium anchovy) to the IAEA recommendations (100 for 239+240Pu in fish).

thumbnail Fig. 5

Comparisons of concentration factors (CFs) of 137Cs (black bar) and 239+240Pu (grey bar) in anchovy sample in this study and other marine organisms with IAEA-recommended CF values (red for 137Cs and blue for 239+240Pu). The smallest-, small-, medium-, and large- anchovies are expressed as XS, S, M, and L, respectively, for convenience in visualization.

3.5 Quantification of the effective dose rate from anchovy

In this study, we tried to assess the potential risk of radionuclides to humans by quantifying the annual effective dose rate (AED) (Sv yr−1) as follows:

where AAR is the average activity of an artificial radionuclide in anchovy (Bq kg−1) in this study, e(T) is an effective dose coefficient (Sv Bq−1) (1.30 × 10−8 and 2.50 × 10−7 Sv Bq−1 for 137Cs and 239+240Pu, respectively) (ICRP, 2012), and Iyr is the amount of intake per year for a person in South Korea (kg yr−1). The 2017 Food Balance Sheet from the Korea Rural Economic Institute (KREI) was applied to determine the amount of anchovy intake Iyr (assuming that anchovies at each growth stage were consumed equally).

The estimated AEDs of 137Cs and 239+240Pu by anchovy consumption are presented in Table 3. The estimated AED of 137Cs in anchovy was lowest in the smallest anchovy [(3.71 ± 0.55) × 10−6 mSv yr−1] and highest in large anchovy [(6.87 ± 0.95) × 10−6 mSv yr−1], showing an upward trend from smallest to largest anchovy (Tab. 3). The AED of 239+240Pu, estimated in the same manner as 137Cs, was lowest [(0.26 ± 0.09) × 10−6 mSv yr−1] in the smallest anchovy and highest [(3.10 ± 0.36) × 10−6 mSv yr−1] in the medium anchovy. Although other artificial radionuclides such as 90Sr were investigated in this study, the sum of the estimated AEDs of 137Cs and 239+240Pu by anchovy consumption (approximately 30 × 10−6 mSv yr−1) is significantly lower than that of 210Po (9.4 × 10−2 mSv yr−1) – a natural radionuclide – by entire seafood consumption for a person in South Korea. The total AED value by anchovy consumption in this study was also insignificant compared to the recommended AED limit of 1 mSv yr−1 suggested by the International Commission on Radiological Protection (ICRP, 2007).

Table 3

The estimated annual effective dose (AED) rate (× 10−6 mSv yr−1) of artificial radionuclides, 37Cs and 239+240Pu, for a person in South Korea by anchovy consumption.

4 Conclusion

We investigated the distribution and accumulation patterns of the artificial radionuclides 137Cs and 239+240Pu in anchovy, a major marine product in the Korean seas and the most popular fishery resource in Korean food culture. The concentration of 137Cs in anchovy increased with increasing body length, indicating that 137Cs accumulates in anchovy based on growth stages. The concentration of 239+240Pu in anchovy also increased with growth, but sharply decreased in the adult stage. It is not entirely clear why 239+240Pu decreased within a specific growth level, but we hypothesized that adult fish may have developed detoxification abilities against certain harmful radionuclides. The noticeably higher accumulation rate of 137Cs in anchovy was likely due to the relatively short migratory period of anchovies in coastal regions. The concentration factors (CFs) of 137Cs in anchovy were an order of magnitude lower than those in other marine organisms. However, the CFs of 239+240Pu in adult anchovy were significantly higher than those in other fishes and comparable (or even higher) to the IAEA recommendations. However, we do not yet understand the exact mechanisms involved in 239+240Pu depletion in adult anchovy; therefore, further research is needed. Moreover, further studies on the accumulation rate and detoxification of radionuclides in fishes are also necessary in the future to ensure that safe levels of harmful radionuclides are not exceeded in the typical Korean diet.

Acknowledgements

First, we especially appreciate our colleagues, Ms. Hyunmi Lee and Ms. Jaeun Lee, who helped us with lab experiments. We also thank Ms. Seunghyun Lee, who performed lots of official affairs for us. All datasets used in this paper are available upon request from the corresponding author (ikim@kiost.ac.kr). This work was supported by Korea Institute of Ocean Science and Technology (KIOST) under the project entitled “Biogeochemical cycling and marine environmental change studies” (PE99912).

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Cite this article as: Lee H, Kim I. 2021. Accumulations of artificial radionuclides 137Cs and 239+240Pu in anchovy from the Korean seas. Radioprotection, https://doi.org/10.1051/radiopro/2021009.

All Tables

Table 1

Certified and measured values (Bq kg−1 based on dry mass) of radionuclide certified reference materials (CRMs).

Table 2

The body length of each anchovy sample group, activities of artificial radionuclides,137Cs and 239+240Pu, and calculated concentration factors (CFs) of these nuclides in this study. All uncertainties in this study are denoted as standard deviations for the measured values.

Table 3

The estimated annual effective dose (AED) rate (× 10−6 mSv yr−1) of artificial radionuclides, 37Cs and 239+240Pu, for a person in South Korea by anchovy consumption.

All Figures

thumbnail Fig. 1

The Korean seas, sampling region (yellow box), and locations of nuclear power plant facilities in South Korea (left). The migratory map of anchovy (right) around the Korean Peninsula. Arrows denote the direction of migration and the numbers denote the date (month) corresponding to the migration route of anchovy.

In the text
thumbnail Fig. 2

Activities of (a) 137Cs and (b) 239,240Pu in anchovy according to their size.

In the text
thumbnail Fig. 3

Comparisons of activities of (a) 137Cs and (b) 239,240Pu in anchovy (black bars) according to size with other groups of marine organisms such as other fish, crustaceans (Crus.), and mollusks (Moll.) (grey bars). The smallest-, small-, medium-, and large- anchovies are expressed as XS, S, M, and L, respectively, for convenience in visualization.

In the text
thumbnail Fig. 4

The plot of mean 137Cs activities in anchovy against their age (months) and comparisons with other fish species. Note that the x-axis does not represent a linear scale but is instead an arbitrary scale.

In the text
thumbnail Fig. 5

Comparisons of concentration factors (CFs) of 137Cs (black bar) and 239+240Pu (grey bar) in anchovy sample in this study and other marine organisms with IAEA-recommended CF values (red for 137Cs and blue for 239+240Pu). The smallest-, small-, medium-, and large- anchovies are expressed as XS, S, M, and L, respectively, for convenience in visualization.

In the text

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