Ewha Med J 2018;41(1):1-7 Original https://doi.org/10.12771/emj.2018.41.1.1 Article eISSN 2234-2591 Systematic Review of Heavy Metal Concentrations in Fish and Shellfish in Korea Shinhee Ye, Jiyoung Shin, Jueun Lee, Eun Mi Jung, Jeongsook Lee1, Eunsun Yun1, Yeosook Kim1, Younghee Oh1, Eun-Hee Ha Department of Occupational and Environmental Medicine, Ewha Womans University College of Medicine, 1Seoul Metropolitan Government Research Institute of Public Health and Environment, Seoul, Korea Objectives: Heavy metals ingested through the consumption of aquatic products can Received November 1, 2017 accumulate in the human body over the long-term and cause various health problems. Revised December 29, 2017 Accepted January 3, 2018 This study aims to present comprehensive data on the amount of heavy metals found in fish and shellfish in Korea using a systematic review of studies that report on that issue. Corresponding author Methods: The study used the following databases: PubMed, Korean Studies Informa- Eun-Hee Ha tion Service System, and Research Information Sharing Service. The search terms for Department of Occupational and Environmental PubMed included fish OR shellfish OR seafood AND mercury OR cadmium OR lead Medicine, Ewha Womans University College of Medicine, 1071 Anyangcheon-ro, Yangcheon-gu, OR heavy metal AND Korea. The search terms for Korean Studies Information Service Seoul 07985, Korea System and Research Information Sharing Service included eoryu sueun, eoryu kadeu- Tel: 82-2-2650-5757, Fax: 82-2-2653-1086 myum, eoryu nab, eoryu jung-geumsog, paeryu sueun, paeryu kadeumyum, paeryu E-mail: [email protected] nab, paeryu jung-geumsog, eopaeryu sueun, eopaeryu kadeumyum, eopaeryu nab, and eopaeryu jung-geumsog. Results: A total of 32 articles were selected for review. The total mercury, lead, and cad- mium concentrations in fish and shellfish reported in each of the articles are summa- rized, as are the species of fish and shellfish with relatively high concentrations of heavy metals. Total mercury concentrations tended to be higher in predatory fish species, such as sharks, billfishes, and tuna, while lead and cadmium concentrations tended to be higher in shellfish. Conclusion: This paper is the first to report a comprehensive summary of the concen- trations of heavy metals in fish and shellfish. This data could be used as evidence to pro- tect Koreans from exposure to heavy metals due to the consumption of highly polluted Key Words aquatic products. (Ewha Med J 2018;41(1):1-7) Metals, heavy; Fishes; Shellfish Introduction humans such as neurophysiological dysfunction, kidney dysfunc- tion, and decreases in bone mineral density, even at low con- Due to heavy metal pollution across the globe, aquatic prod- centrations [3-5]. Heavy metal contamination of aquatic prod- ucts contain heavy metals. Mercury (Hg), cadmium (Cd), and ucts is transmitted to humans through food, so the heavy metal lead (Pb) are the primary heavy metals contained in aquatic content of aquatic products has a significant impact on human products [1]. These heavy metals are reported to accumulate in health. living organisms [2] and cause various harmful health effects to In Korea, 30% of all food containing protein and 80% of all This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. THE EWHA MEDICAL JOURNAL 1 Ye S, et al animal proteins are consumed as aquatic products [6]. Aquatic exclusion criteria, and then they extracted the data. The follow- products also contain various nutrients, such as selenium and ing exclusion criteria were used to screen the articles: 1) did not omega-3 fatty acids [7]. However, since aquatic products are report the three heavy metals concentrations; 2) heavy metal one of the largest sources of human exposure to hazardous concentration unit is not convertible to ppm; 3) did not report heavy metals [1], there is a social concern about heavy metal the heavy metal concentration based on the type of fish and contamination of marine products, and various studies have re- shellfish species; and 4) did not report the numbers or mean ported on the heavy metal concentrations in fish and shellfish. values of the analytical samples. Although several studies [6,8,9] have reported on the amount of heavy metals in fish and shellfish in Korea, it is difficult for 3. Data extraction researchers or the general public to obtain integrated information In the selected articles, the number of species samples exam- on the heavy metal content in fish and shellfish in Korea due to ined, the means, the standard deviation, and the minimum and data is not found in one source. maximum values were extracted and summarized. After unify- Therefore, this study aims to present comprehensive data ing the fish and shellfish species on the basis of Korean names, on the amount of heavy metals in fish and shellfish in Korea scientific names, or English names, the average of each heavy through a systematic review of studies that have investigated and metal concentration in the same species was calculated from the reported on that issue. data collected from several articles using the number of samples and mean values (formula 1). When recalculating the averages Methods using formula 1, undetectable values were considered as zero. 1 1. Search strategy � ∑���� ��������� � To search for articles written in English and Korean, we ��������������� = ∑��� �� conducted comprehensive database searches of the literature 2 Results published from January 1998 to September 2017 using three da- tabases: PubMed, Korean Studies Information Service System, After removing duplicate records, 398 bibliographic records and Research Information Sharing Service. The search terms for were identified. Among these records, 345 articles did not meet PubMed included fish OR shellfish OR seafood AND mercury the inclusion criteria at the first screening, 53 full-text ar- OR cadmium OR lead OR heavy metal AND Korea. The search ticles were selected for full-text screening, and 32 articles were terms for Korean Studies Information Service System and Re- obtained and screened. Information about the searching and search Information Sharing Service included eoryu sueun, eoryu screening process, and the study inclusion criteria are summa- kadeumyum, eoryu nab, eoryu jung-geumsog, paeryu sueun, rized in the PRISMA (Preferred Reporting Items for Systematic paeryu kadeumyum, paeryu nab, paeryu jung-geumsog, eopae- Reviews and Meta-Analyses) flow diagram presented in Fig. 1. ryu sueun, eopaeryu kadeumyum, eopaeryu nab, and eopaeryu Studies that examined the concentrations of three heavy met- jung-geumsog. The bibliographic records were imported, du- als, Hg, Pb, and Cd, in fish and shellfish in Korea are sum- plicates were removed, and the articles were screened to ensure marized in Supplementary Table 1. The number of samples that they met the inclusion criteria. analyzed, and the mean, standard deviation, and minimum and maximum values of the total Hg, Pb, and Cd concentrations 2. Article screening and inclusion and exclusion criteria in fish and shellfish reported in the selected literature are sum- The titles and abstracts of the articles were screened by marized in Supplementary Tables 2, 3, and 4, respectively. Of one investigator (SY) to ensure that they included English or the 32 articles that reported on the concentrations of heavy Korean-language studies that reported original data on the three metals in fish and shellfish, 15 reported Hg concentrations [10- heavy metals (total Hg, Pb, and Cd) concentrations in fish and 24], 12 reported heavy metal concentrations for Hg, Pb, and shellfish in Korea. Reviews were included at this level. Two in- Cd [6,8,9,25-33], and 5 reported Pb and Cd concentrations vestigators (SY and JS) independently screened the studies using [34-38]. The mean values for each of the heavy metal con- 2 THE EWHA MEDICAL JOURNAL 1 Heavy Metal in Fish and Shellfish 683 Records identified through 1 Additional records identified database searching through other sources Identification 398 Records after duplicates removed Screening 398 Records screened 345 Records excluded 53 Full-text articles 21 Full-text articles assessed for eligibility excluded, with reasons Eligibility 1 Study did not report heavy metal concentration 9 Studies did not report mean value or sample number 9 Studies did not report Included mean values by species 2 Studies did not use Fig. 1. PRISMA (Preferred Reporting Items ppm unit for Systematic Reviews and Meta-Anal- 32 Studies included yses) flow diagram of database search evidence and inclusion inclusion criteria. centrations for the same species were calculated using the data 2). Concentrations of Pb and Cd were higher than the KFDA collected from several articles (Supplementary Tables 5-7). standard in Mediterranean mussels (Figs. 3, 4). Therefore, Figs. 2, 3, and 4 present information on 30 kinds of fish among the fish and shellfish with relatively high concentrations and shellfish with high total Hg, Pb, and Cd concentrations, of heavy metals it is necessary to be particularly careful about respectively. The concentration of total Hg tended to be higher consuming those that exceed the KFDA standards. in predatory fish, such as sharks, billfishes, and tuna, while the Figs. 5, 6, and 7 illustrate 30 kinds of fish and shellfish with concentrations of Pb and Cd tended to be higher in shellfish. low total concentrations of Hg, and low Pb and CD concentra- The criteria for heavy metal concentrations in fish and shell- tions, respectively. Among the 30 kinds of fish and shellfish fish used by the Korea Food and Drug Administration (KFDA) with low total concentrations of Hg, oysters and gizzard shads are as follows: total Hg concentration should be below 0.5 are known to contain high levels of omega-3 fatty acids (Fig.