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Origin and organ-specific bioaccumulation pattern of perfluorinated alkyl substances in crabs
Journal Pre-proof Origin and organ-specific bioaccumulation pattern of perfluorinated alkyl substances in crabs Seogyeong Choi, Jeong-Jae Kim, Min-Hyuk Kim, Yong-Sung Joo, Myung-Sub Chung, Younglim Kho, Kwang-Won Lee PII:
S0269-7491(19)33753-4
DOI:
https://doi.org/10.1016/j.envpol.2020.114185
Reference:
ENPO 114185
To appear in:
Environmental Pollution
Received Date: 11 July 2019 Revised Date:
22 November 2019
Accepted Date: 11 February 2020
Please cite this article as: Choi, S., Kim, J.-J., Kim, M.-H., Joo, Y.-S., Chung, M.-S., Kho, Y., Lee, K.W., Origin and organ-specific bioaccumulation pattern of perfluorinated alkyl substances in crabs, Environmental Pollution (2020), doi: https://doi.org/10.1016/j.envpol.2020.114185. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Credit author statement Seogyeong Choi: Investigation, Writing-Original Draft. Jeong-Jae Kim: Visualization. MinHyuk Kim: Validation. Yong-Sung Joo: Formal analysis, Data Curation. Myung-Sub Chung: Resources. Younglim Kho: Methodology. Kwang-Won Lee: Conceptualization, WritingReview & Editing, Supervision.
Graphical abstracts
1
Research Article
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Origin and organ-specific bioaccumulation pattern of perfluorinated alkyl substances in
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crabs
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Seogyeong Choi1, Jeong-Jae Kim2, Min-Hyuk Kim1, Yong-Sung Joo2, Myung-Sub Chung3,
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Younglim Kho4, and Kwang-Won Lee *
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1
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Seoul 02841, Republic of Korea
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2
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Republic of Korea
1,
Department of Biotechnology, College of Life Sciences & Biotechnology, Korea University,
Department of Statistics, College of Natural Science, Dongguk University, Seoul 04620,
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do 17546, Republic of Korea
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4
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Republic of Korea
Department of Food Science and Technology, Chung-Ang University, Anseong, Gyeonggi-
Department of Health, Environment & Safety, Eulji University, Sungnam, Gyeonggi, 461-713,
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*Corresponding author:
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Prof. Kwang-Won Lee, Department of Biotechnology, College of Life Sciences &
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Biotechnology, Korea University, 145 Anam-ro, Seongbuk-gu, Seoul 02841, Republic of
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Korea
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Tel: +82-2-3290-3473
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Fax: +82-2-927-1970
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E-mail: [email protected] 1
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Abstract
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Consumption of seafood is a major contributor to perfluorinated alkyl substances (PFASs)
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exposure. Crabs contain high levels of PFASs, and different PFASs are concentrated in their
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tissues depending on their habitat. Despite South Korea importing huge quantities of crabs,
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no investigation has been conducted on the effect of PFAS exposure. This study investigated
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the risk of exposure to PFASs when ingesting crab. To determine the risk of exposure, 19
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different PFASs species were measured in the edible parts (body, legs, offal, and eggs) of
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crabs originating from South Korea (n=17), China (n=14), India (n=7), and Pakistan (n=31),
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which were distributed in the fish markets of South Korea. The results revealed that, in
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contrast to short-chain PFASs, long-chain PFASs (PFCAs≥8, PFSAs≥6, and perfluorooactane
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sulfonamidoacetic acids (FOSAAs)≥8) were detected in crab samples from all four countries
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of origin, and in all the edible parts except for the legs. Perfluorooctanoic acid (PFOA; 16.9
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ng/g in South Korea, 9.42 ng/g in China) and perfluoro-n-tridecanoic acid (PFTrDA; 5.35
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ng/g in South Korea, 2.40 ng/g in China) were the predominant perfluoroalkyl carboxylic
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acids (PFCAs) detected in the crabs originating from South Korea and China, and
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perfluorooctane sulfonic acid (PFOS; 7.02 ng/g in Pakistan, 5.88 ng/g in India) was the
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predominant perfluoroalkyl sulfonic acids (PFSAs) detected in crabs originating from
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Pakistan and India. These results indicate that PFASs that are accumulated in crabs differ
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depending on the ocean from which they originate. The concentrations of PFOA and PFOS
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were significantly higher in the eggs and offal than in the legs and body of the crab. The
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average daily intake of PFOA and PFOS in Koreans ranges from 0.01% to 0.07% based on 2
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the tolerable daily intake of EFSA and MFDS. These results establish the PFAS profiles and
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risk assessment of crabs that are distributed in South Korea.
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Keywords: perfluorinated alkyl substances; crab; organ-specific; long-chain PFASs; risk
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assessment
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Introduction
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Perfluorination implies that the hydrogen atoms in a molecular chain are converted to
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fluorine atoms (OECD, 2012). The two most widely known PFASs are perfluoroalkyl
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sulfonic acids (PFSAs, e.g., perfluorooctane sulfonic acid (PFOS)), and perfluoroalkyl
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carboxylic acids (PFCAs, e.g., perfluorooctanoic acid (PFOA))(OECD, 2012). PFASs are
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man-made chemicals (Lehmler, 2005) and characterized by a hydrophobic tail and a water-
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soluble anionic head group (Prevedouros et al., 2006). Strong carbon-fluorine bonds make
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PFASs resistant to hydrolysis, photodegradation, and microbial degradation (Giesy and
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Kannan, 2002). Due to their unique properties, PFASs have been used for the last 60 years in
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the manufacture of fire-fighting equipment, paper, cookware, automotive components, and
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cosmetics, with roles as surfactants, coatings, and polishes (Jogsten et al., 2012; Key et al.,
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1997; Lehmler, 2005; Taylor and Johnson, 2016). PFOA and PFOS that have eight carbon
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atoms are known to be the most abundant substances released into the environment through
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applications such as metal plating, use in the semiconductor industry, firefighting foams, and
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textile treatment (Giesy and Kannan, 2001; Wang et al., 2015). PFASs are distributed
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globally through the movement of air and water (Lehmler, 2005).
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The toxic effects of PFASs depend on the fluorinated chain length but also on their functional
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groups (Lau et al., 2007). Numerous studies have indicated that PFOA and PFOS cause
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endocrine disorders in humans (Grün and Blumberg, 2006; Preston et al., 2018). Human
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exposure to PFASs is usually through consumption of contaminated food and water
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(D’Hollander et al., 2010; Kärrman et al., 2009; Su et al., 2017). At the 2009 Stockholm
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Convention, PFOS and its salts were included in the category of persistent organic pollutants
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(POPs) due to their persistence and toxicity in the environment and the human body (UNEP, 4
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2009). Furthermore, PFOA, perfluorohexane sulfonate (PFHxS), and their salts were
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presented as POPs at the Stockholm conventions in 2015 and 2017 (Ripley, 2018; Wang and
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Sun, 2016). The United States and Europe have agreed to phase out certain types of PFAS
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production (Bergman et al., 2013). Canada has already phased out the sale of PFOA and other
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long-chain PFASs, and prohibited the illegal sale and import of long-chain PFASs (EPA,
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2012). Nonetheless, PFOA and PFOS are still problematic because they can persist and
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accumulate in the environment or in organisms over long periods of time (Fromme et al.,
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2009). The half-life of PFOA and PFOS in the human body is estimated to be 3.5 and 4.8
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years, respectively (Olsen et al., 2007).
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Several studies have detected PFASs in aquatic organisms. PFASs have been observed at
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high levels in shellfish, especially crabs, due to the specificity of the species (Habibullah-Al-
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Mamun et al., 2017; Ip et al., 2005; Yang et al., 2007). In addition, demersal organisms have
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higher levels of PFASs compared to pelagic organisms due to environmental pollution of the
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water, sediments, and soil (Zareitalabad et al., 2013). Crabs are prone to PFAS exposure as
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they are a scavenger (Ip et al., 2005). In addition, crabs accumulate PFASs relatively well as
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they have gills with a relatively large surface area that continuously transport organic
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contaminants and suspended particles from the water (Yang et al., 2007). Our review paper
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reported that crabs contain relatively high levels of PFOA and PFOS compared to fish (Jeong
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et al., 2019). Likewise, mean PFOA and PFOA concentrations were found to be higher in
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Giant Mud Crab than in Mulloway and Dusky Flathead (Taylor, 2019). Despite these studies,
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there are few studies on the levels of PFASs, especially with respect to the varied origins of
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the crabs that are distributed in East Asia.
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The purpose of this study was to analyze 19 species of PFASs in the edible body parts of
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crabs (the body, offal, legs, and eggs) from different countries of origin that were distributed
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in South Korean markets. We aimed to assess the profile distribution of short-chain and long-
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chain PFASs, and the accumulation of PFOA and PFOS in the different edible parts of the
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crabs. We then assessed the risks of PFOA and PFOS exposure due to the consumption of
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crabs.
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2. Materials and Methods
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2.1 Chemicals and reagents
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Details on the standards and, structure, and their corresponding internal standard used to
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analysis are described in Table S1. The 19 species of PFASs were purchased from
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Wellington Laboratories (Guelph, ON, Canada). In addition, protease, lipase, tetra butyl
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ammonium hydrogen sulfate (TBAHS), sodium bicarbonate (NaHCO3), and sodium
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carbonate anhydrous (Na2CO3) were used in the pretreatment process and were purchased
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from Sigma-Aldrich Chemical Co. (St. Louis, MO, USA) at a purity of 99%. The analytical
111
solvent, methanol, distilled water, acetonitrile, methyl-t-butyl ether (MTBE), and hexane
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were purchased from Burdick and Jackson (Muskegon, MI, USA) as HPLC grade. A blender
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(BL-1401 KR) was used for sample homogenization, and an O2 Incubator (Vision Scientific,
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Daejeon, Korea) was used for enzyme activity. An ultrasonic extractor (5510R-DTH,
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Bransonic, Danbury, CT, USA) and rotary stirrer (model AG, FinePCR, Korea) were used for
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material extraction. A PLC-05 (Gemmy Industrial Corp., Taiwan) was used for centrifugal
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separation, and an Eyela Centrifugal Evaporator (CVE3100; Tokyo, Japan) was used for 6
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concentrating samples. The equipment that comes into contact with the samples must not
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contain or be coated with Teflon, polytetrafluoroethylene, or ethylene tetrafluoroethylene,
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and must not contact the external environment.
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2.2 Sampling collection and sample extraction
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The blank tests of the analytical solvent, methanol, distilled water, acetonitrile, MTBE,
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hexane, blender, and nitrile gloves were performed to control potential contamination during
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sample extraction and analysis. A total of 69 crab samples (Origin: South Korea (n = 17),
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China (n = 14), India (n = 7), and Pakistan (n = 31)) were purchased from two fish markets
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and five supermarkets in South Korea in November 2017. In accordance with the Republic of
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Korea Act on the indication of origin of agricultural and fishery products, the crabs were
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purchased after verifying that the indication of the country of origin was correct. All samples
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were transported to the laboratory in iceboxes. The samples were dissected to collect the
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body, offal, legs, and eggs for analysis. Each dissected sample was mixed with distilled water
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at a 1:1 ratio (weight by volume), and homogenized using a blender (BL142 KR, Tefal,
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France). During this time, the gizzard and gills were removed separately as they are not
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edible. All the samples were collected in high density polyethylene wide-mouth bottles,
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which were unlined (no Teflon) and had polypropylene screw cap, and stored in a -20°C
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freezer (model WS-1244DF, Woosung, Seoul, South Korea) until further analysis.
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Most of the analytes was quantitatively examined with the introduction of internal standards
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substituted with isotopes before pretreatment, with the exception of some analytes. The edible
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parts (body, legs, offal, and eggs) are more easily homogenized than other solid foods, so
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there is little risk of underestimating the PFAS exposure levels. For PFASs that were non-
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extractable due to protein and fat binding, we used protease and lipase to hydrolyze the fats
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and protein-bound PFASs, respectively, in samples in the presence of spiked internal
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standards. The detailed sample extraction procedure is described in Supporting Information
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(SI) Section 1. Sample extraction procedure. Additionally, the schematic flow diagram of the
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pretreatment procedure for crab samples is provided in SI Fig. S1.
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2.3 Instrument analysis
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Concentrations of PFASs were determined using High-Performance Liquid Chromatography
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(HPLC) (Agilent 1100 LC series, Agilent Technologies, Palo Alto, CA, USA) and Tandem
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Mass Spectrometry (API 4000, Applied Biosystems, Foster City, CA, USA), equipped with a
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electrospray ionization (ESI) source in the negative ion mode with multiple reaction
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monitoring modes. The instrument and quantification details are given in SI Table S2, and
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Table S3.
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2.4 Quality assurance and quality control (QA/QC)
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To reflect the sample characteristics for validation, the pooled QC sample was prepared by
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mixing samples according to their country of origin (South Korea, China, India, and Pakistan)
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and parts (body, offal, legs, and eggs). Ten concentration levels (0.01, 0.02, 0.05, 0.1, 0.2, 0.5,
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1, 2, 5, and 10 ng/mL) were spiked in the pooled sample, and the calibration curves were
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obtained. The mean PFAS value of the pooled QC sample was subtracted from the calculated
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calibration standard concentration. Detailed methodologies used for QA/QC of PFASs are
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described in SI Section 2.
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Accuracy was evaluated using recovery (%) and precision was evaluated using relative
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standard deviation (RSD) (%). The coefficient of determination (r2) of the calibration curve
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showed excellent linearity of 0.99 or more (Table 1). The MLOD ranged from 0.06 to 0.1
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ng/g (Table 1). The intra-day accuracy ranged from 82.6 to 120% and the inter-day accuracy
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ranged from 84.8 to 118.4% (Table S4). AOAC (2002) recommends a recovery range of 70–
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125% when the analytes are present in ng/g concentration. Also, the intra-day precision and
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the inter-day precision were 19.7% RSD and 18.6% RSD, respectively (Table S4). The
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concentrations of 0.2 ng/g (low level) and 1 ng/g (medium level) of PFASs were analyzed for
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every 20 samples for QA/QC. Detailed methodologies used for quality assurance and quality
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control of PFASs are described in the supplementary data.
173 174
2.5 Potential exposure assessment
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To assess the potential health risks to humans, tolerable daily intake (TDI), reference dose
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(RfD), and disability-adjusted life-years (DALY) were used. In the case of RfD, the criteria
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are mainly set for animal experiments, not humans, and DALY is rarely used for risk
178
assessment of PFASs. In this study, the potential health risks associated with PFOA and
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PFOS with human intake were evaluated by comparison with the TDI standards of the
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European Food Safety Authority (EFSA) (2008) and South Korea's Ministry of Food and
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Drug Safety (MFDS) (2010). EFSA has established TDI to be 150 ng/kg b.w./d for PFOS and
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1.5 µg/kg b.w./d for PFOA (EFSA, 2008). MFDS set the TDI to be 150 ng/kg b.w./d for
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PFOS and 1 µg/kg b.w./d for PFOA. Detailed methodologies used to calculate the PFOA and
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PFOS dietary intakes and risk (%) are described in SI Section 3.
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For risk assessment of PFOA and PFOS caused due to consumption of crabs, we used the
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National Health and Nutrition Survey (Kweon et al., 2014) published by the Korea Center for
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Disease Control and Prevention. As a risk assessment procedure, a random number was
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generated from a lognormal distribution using the mean and SD of PFOAs and PFOSs. Then,
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the random number was multiplied by the value of the crab intake recorded in the National
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Health and Nutrition Survey. The estimated daily intake (EDI) was calculated using two
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scenarios that assumed average intake and an extreme amount of intake.
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2.6 Statistical Analysis
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A two-way ANOVA with multiple comparisons using the least squares means test were
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conducted to determine the significant differences among the PFAS concentrations in the
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crab samples. Since the distribution of both PFOAs and PFOS were skewed to the right, the
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natural logarithmic transformation was applied to their concentrations before conducting the
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ANOVA, to obtain a valid result. Values of p < 0.05 were considered statistically significant.
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For statistical analyses, concentrations that were lower than the MLOD were assigned a value
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that was half of the MLOD (WHO, 1995).
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3. Results and discussion
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3.1 PFASs distribution pattern in crab 10
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The detailed concentrations and detection frequency of individual PFASs in each country of
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origin, and each crab part, are shown in SI Table S5. Table S5 shows the average (detection
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rate) and the range (median value) of 19 PFASs. The concentration of ΣPFASs (ΣPFASs =
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ΣPFCAs + ΣPFSAs + Σperfluorooactane sulfonamidoacetic acids (FOSAAs)) was compared
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for each edible body part of the crab samples, belonging to each country of origin.
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The contributions of long-chain PFASs (PFCAs≥8, PFSAs≥6, and FOSAAs≥8) and short-
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chain PFASs in crabs are shown in Fig. 1 (a). Long-chain and short-chain PFASs differ in
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toxicity and bioaccumulation (OECD, 2013). Martin et al. reported that longer carbon chains
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lead to higher carcinogenicity and bioaccumulation (2003, 2004). Fig. 1 (a) shows that,
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regardless of the country of origin, long-chain PFASs containing PFOA and PFOS are
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dominant over short-chain PFASs, including PFBA, PFPeA, PFHxA, PFHpA, and PFBS in
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the body, offal, and eggs, but not the legs. The distribution of long-chain and short-chain
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carbons in the leg varied depending on the country of origin. Long-chain PFASs were
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dominant in the legs of Pakistani female crabs, Korean crabs, and Chinese male crabs. In the
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legs of male crabs originating from Pakistan and crabs from India, the percentage of short-
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chain PFASs were 66% and 53% (of the total PFASs), respectively, which was similar to or
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higher than the percentage of long-chain PFASs, that were 34% and 47%, respectively. In
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case of the body, the percentage of long-chain PFASs were as follows: Korean male crabs
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(82%) > Korean female crab (80%) > Pakistani male crab (80%) > Chinese male crab (76%)
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> Pakistani female crab (68%) > Indian female crab (51%). In the offal, the percentage of
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long-chain PFASs were as follows: Chinese male crab (90%) > Pakistani male crab (85%) >
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Korean female crab (83%) > Korean male crab (80%), Indian female crab (80%) > Pakistani
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female crab (70%). In the eggs, the percentage of long-chain PFASs were as follows: Indian 11
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female crab (84 %) > Korean male crab (80%) > Pakistani female crab (52%). On the other
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hand, the long-chain PFASs in the legs were 82% (Korean male crab), 78% (Korean female
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crab), 78% (Chinese male crab), 51% (Pakistani female crab), 47% (Indian female crab), and
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34% (Pakistani male crab).
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The contributions of PFCAs, PFSAs, and FOSAAs, depending on the crab parts and country
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of origin, are shown in Fig. 1 (b). There was a definite difference in the concentration
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tendency of PFASs depending on the origin of the crabs. The contribution of ΣPFCAs was
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dominant among the total PFASs in Korean and Chinese crab samples, that is 58%−76%. In
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contrast, in the Pakistani and Indian crab samples, the ΣPFSA among the total PFASs, were
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45%−91%. These results suggest that the concentrations of PFASs differ depending on the
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country of origin, even if they are the same species. This variation may be due to the
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difference in sediment, water, and diet of the habitat to which the crab is exposed (Hong et al.,
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2015).
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Fig. 2 shows the distribution of 19 individual PFASs. In Korean and Chinese crab samples,
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PFOA is the most dominant compound among the PFCAs, regardless of the body part of the
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crab, with a concentration of 32−54%, followed by PFTrDA (9−16%), and PFOS (5−18%)
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(Figs. 2 (a) and (b)). In the case of Indian and Pakistani crab samples, PFOS is the most
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dominant compound among the PFSAs, regardless of the body part of the crab, with a
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concentration of 33−85%, followed by PFBA (2−15%) and PFPeA (1−27%) (Figs. 2 (c) and
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(d)). Fifty samples of the coastal waters of the central and eastern Pacific and of the South
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China Sea of Korea, Japan, and China showed PFOA as the major pollutant in marine waters
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(So et al., 2004; Yamashita et al., 2005). According to the Yeung et al., (2009), PFOS was the
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most dominant PFAS in most samples from the Ganges River flowing into the Bay of Bengal 12
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and the Indian Ocean. This result implies that there may be differences in the PFASs
252
component, according to the country of origin.
253
Bioconcentration factor (BCF) is a measure of the accumulation, in a living organism, of a
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chemical substance from the ambient environment through its respiratory and dermal surfaces
255
(at steady state), and will be the concentration of the test substance in the organism (as mg/kg)
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divided by the concentration of the chemical substance in the surrounding medium (as mg/L)
257
(Arnot and Gobas, 2006). Although BCF can only be calculated under controlled conditions,
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we estimated BCF of PFASs in crabs, using the reported concentration and our data of PFASs
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in crabs and its concentration in the water, in Table S6. In the Indian ocean, the estimated
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BCF values of PFOS were remarkably higher than those in the East and South China Sea,
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whereas the estimated BCF values of PFOA were higher in the East and South China Sea
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compared with those in the Indian Ocean. These results suggest that the accumulation of
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PFOA and PFOS in crabs may be an indicator for the level of PFASs in the water where
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those crabs originated.
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3.2 Comparison of the trend of PFASs in crab with other international studies
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Table 2 summarizes the previously reported preliminary results on PFASs. The distribution
268
of PFASs can be affected by geographical features or by aquatic climatic conditions
269
(Habibullah-Al-Mamun et al., 2017). According to Hong et al. (2015), the highest detected
270
levels of PFOA in the samples of grapsid crabs, penicillate shore crabs, and beach crabs
271
collected from the west coast of South Korea were 6.6 ng/g, 12.76 ng/g, and 2.52 ng/g,
272
respectively. The mean concentration of PFOA detected in the domestic (Korean) crabs in
273
this study was 16.6 ng/g, which was similar or higher than the value observed in the Hong et 13
274
al. (2015) study. In addition, Hong et al. (2015) reported that PFOS was the analyte with the
275
highest concentration, that is 2.3 ng/g and 4.2 ng/g in the hermit crab and the flat shore crab
276
respectively, which is found on the western coast of South Korea. These values are similar or
277
lower than the result obtained in this study, which was 4.27 ng/g.
278
The mean concentration of PFOA (9.42 ng/g), which was the most prevalent in the Chinese
279
crabs in this study, was similar to that of PFOA (9.5 ng/g) detected in the crabs
280
(hepatopancreas) on the western coast of the Ariake Sea, Japan (Nakata et al., 2006).
281
However, this value was much lower than the PFOA concentration in the gills (36.6 ng/g)
282
and viscera (28.4 ng/g) of crabs from Bohai Bay, China, as Yang et al. (2012) reported.
283
According to their report, PFOA was predominantly detected in crab gills. Clarke et al. (2010)
284
reported that the concentration of PFOA in spider crabs, cromer crabs, and dressed crabs
285
found in the UK were 5 ng/g, 4 ng/g, and 9 ng/g, respectively.
286
Moreover, PFUnDA (31.7 ng/g), PFOS (17.9 ng/g), and PFDoDA (13 ng/g) were also
287
detected at high levels. In the case of crab viscera, PFOS (105 ng/g) had the highest
288
concentration, followed by PFOA. According to a report by Taylor and Johnson (2016),
289
among all the PFASs, PFOS was present in the highest concentration in the mud crab (0.0021
290
ng/g) and eastern king mud crab (0.0042 ng/g) of Australia. These values are significantly
291
lower than the results obtained in our study. In the case of PFOS, we obtained lower values
292
for crabs originating from Korea and China, and higher values for crabs originating from
293
Pakistan and India. In addition, the PFOS concentrations of spider crabs, brown crabs, and
294
crab originating from the UK were 13 ng/g, 3 ng/g, and 4 ng/g, respectively, similar to the
295
PFOS results of this study.
296 14
297
3.3 Correlation between PFASs concentration and edible parts of the crab
298
To determine whether the accumulation of PFOA and PFOS were related to the crab parts
299
(body, legs, offal, and eggs), significance tests were performed using data from all the
300
countries of origin of the crabs (Fig. 3). The result revealed that the accumulation of PFOA
301
and PFOS was significantly different depending on the body part of the crab. In the case of
302
the female crabs, PFOA levels were in the order of eggs >offal>body>legs, and in the case of
303
male crabs, PFOA levels were in the order of legs, offal> body (P<0.05). For PFOS, which is
304
known to have the highest bioaccumulation among PFASs, high concentrations were detected
305
in the order of offal> eggs> body> legs in female crabs (P <0.05) and offal> body> legs in
306
male crabs (P<0.05). This is consistent with previous studies, which showed that high levels
307
of PFASs were detected in the blood, liver, intestines, and eggs of guillemot, rainbow trout,
308
and other water organisms (Berger, 2008; Hong et al., 2015; Martin et al., 2003). Unlike most
309
persistent organic contaminants, PFAS chemicals accumulate higher in the kidney and liver
310
than in the blubber/fat or skeletal muscle due to their surfactant-like composition, and in a
311
study on harbor seals from the Dutch Wadden Sea, there was increasing concentrations of
312
PFOS in the order kidney > liver > blubber > skeletal muscle (Van de Vijver et al., 2005).
313
PFOS has a different pattern of accumulation as it binds preferentially to blood proteins and
314
accumulates in various tissues, such as liver and kidney (Jones et al., 2003). In addition,
315
Holmström and Berger (2008) reported a 3-fold higher concentration of PFOS in common
316
guillemot eggs relative to the livers of female birds sampled in the same year. They discussed
317
that most of the PFOS in bird eggs was found in the yolk, primarily in combination with very
318
low density lipoproteins, but to some degree also associated with phosvitin and vitellogenin
319
proteins, and such proteins of egg yolk are produced in the mother bird's liver and transferred 15
320
to the forming egg. These results suggest that PFOA and PFOS are detected at relatively high
321
concentrations in the offal of both male and female crabs and the eggs of female crabs due to
322
the unique bio-specificity of PFASs, which are both hydrophobic and oleophobic.
323 324
3.4 Potential exposure assessment of PFASs in humans
325
In this study, exposure to PFOA and PFOS was calculated by multiplying the concentration
326
of the compound in crabs by their intake. Then, this exposure of the compound was compared
327
with the TDI to calculate the risk (%) of exposure. EFSA has established TDI to be 150 ng/kg
328
b.w./d for PFOS and 1.5 µg/kg b.w./d for PFOA (EFSA, 2008). MFDS also recognized the
329
TDI to be 150 ng/kg b.w./d for PFOS and 1 µg/kg b.w./d for PFOA (MFDS, 2010). Most
330
common intake frequency level of the South Korean population on PFOA occurs at level of
331
less than 200 ng of PFOA/kg bw/d through the consumption of domestic and imported crabs,
332
and the frequency for PFOS takes place below 20 ng of PFOS/kg bw/d (Fig. 4).
333
In Scenario 1 we show the average daily intake of PFOA for South Koreans of all ages
334
through female crabs, using the average consumption value of 27.3 ng/person/d was 0.467
335
ng/kg b.w./d, assuming that the average body weight is 58.5 kg (Kweon et al., 2014). These
336
values corresponded to 0.03% of the EFSA TDI and 0.05% of the MFDS TDI. Also, the
337
average daily intake of PFOA for South Koreans of all ages through male crabs using the
338
average consumption value of 43.3 ng/person/d was 0.739 ng/kg b.w./d, which is 0.05% of
339
the EFSA TDI (1.5 µg/kg b.w.) and 0.07% of the MFDS TDI (1.5 µg/kg b.w.). Additionally,
340
the average daily intake of PFOS for South Koreans of all ages through female crabs (using
341
the average consumption value of 2.73 ng/person/d) was 0.0470 ng/kg b.w./d. The risk of
16
342
PFOS exposure is also found to be negligible, corresponding to 0.03% of both EFSA and
343
MFDS TDI (150 µg/kg b.w.). The average PFOS intake per day for South Koreans of all ages
344
through male crabs (using an average consumption value of 1.12 ng/person/d) was 0.153
345
ng/kg b.w./d, which is 0.01% of the EFSA TDI and MFDS TDI. Therefore, the risk of PFOA
346
and PFOS to South Koreans through the average food intake was evaluated to be very low
347
compared to the TDI of EFSA and MFDS.
348
In Scenario 2, using the 99th percentile consumption, it was demonstrated that the daily
349
intake of PFOA through female crabs was 148 ng/person/d, and the intake per body weight
350
was 2.52 ng/kg b.w./d, which is 0.16% of the EFSA TDI and 0.25% of the MFDS TDI. The
351
daily intake of PFOA through male crabs was 193 ng/person/d, and the intake per body
352
weight was 3.31 ng/kg b.w./d, which is 0.22% of the EFSA TDI and 0.33% of the MFDS
353
TDI. Furthermore, the daily intake of PFOS through female crabs was 58.4 ng/person/d, and
354
the intake per body weight was 0.10/ ng/kg b.w./d, which is 0.67% of the EFSA and MFDS
355
TDI. The daily intake of PFOS through male crabs was 30.6 ng/person/d, and the intake per
356
body weight was 0.52/ ng/kg b.w./d, which is 0.35% of the EFSA and MFDS TDI. Thus, the
357
level of overall exposure to PFOA and PFOS for South Koreans through crab intake was
358
below the EFSA and MFDS levels, making it a low risk.
359 360
4. Conclusion
361
This is the first study to monitor 19 species of PFASs in the body, offal, legs, and eggs of
362
crabs distributed in South Korean markets from four different countries of origin. The results
363
revealed that different PFAS species were detected in the crabs, depending on the country of
364
origin. With respect to the concentration of PFASs, PFOA was the most dominant among 17
365
PFCAs in South Korean and Chinese crabs, and PFOS was the most dominant among PFSAs
366
in Pakistani and Indian crabs. Furthermore, the accumulation of PFOA and PFOS differed
367
depending on the part of the crab that was studied (body, legs, offal, and eggs). PFOA and
368
PFOS were detected at significantly higher concentrations in the offal of both male and
369
female crabs and eggs of females. In addition, the dietary exposure levels of PFOA and PFOS
370
through crab consumption were considered too low to pose a risk to humans.
371 372
Source of funding
373
This work was supported by a Korea University Grant (K1617111)
374 375
Conflicts of interest
376
The authors have no other potential conflicts of interest to declare.
377 378
Acknowledgment
379
This work was supported by a Korea University Grant (K1617111) and School of Life
380
Sciences & Biotechnology of Korea University for BK21PLUS. The authors would also like
381
to thank the Institute of Biomedical Science & Food Safety, CJ-Korea University Food Safety
382
Hall (Seoul, South Korea) for providing the equipment and facilities.
18
383
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21
499
Figure legend
500
Figure 1. (a) The sum of perfluoroalkyl carboxylates (ΣPFCAs), perfluoroalkane sulfonates
501
(ΣPFSAs), and perfluorooactane sulfonamidoacetic acids (ΣFOSAAs), and (b) relative
502
abundance (%) of short chain and long chain (PFCAs≥8, PFSAs≥6, FOSAAs≥8) according to
503
the organ specificity of crabs.
504 505
Figure 2. Distribution profiles of PFASs concentration in crabs originating from (a) South
506
Korea, (b) China, (c) India, and (d) Pakistan.
507 508
Figure 3. Comparison of the concentrations of PFOA and PFOS according to the organ
509
specificity of crabs, (a) female crab; (b) male crab; (c) female crab; (d) male crab.
510 511
Figure 4. Dietary intake histogram of the South Korean general population on PFOA (a and b)
512
and PFOS (c and d) based on the gender of domestic and imported crabs.
22
Table 1. Linear regression data of method limits of detection (MLOD) and method limit of quantification (MLOQ) of the investigated perfluorinated alkyl substances (PFASs). b
Compounds
Regression equation
a
2
MLOD
r
-1
(ng g )
c
MLOQ -1
(ng g )
PFBA
y=0.13x+0.00587
0.9998 0.1
0.30
PFPeA
y=0.0438x+0.00388
0.9998 0.09
0.27
PFHxA
y=0.144x+0.00901
0.9994 0.09
0.27
PFHpA
y=0.0471x+0.0016
0.9998 0.1
0.29
PFOA
y=0.075x+0.00636
0.9999 0.1
0.29
PFNA
y=0.141x+0.00962
0.9998 0.09
0.26
PFDA
y=0.132x+0.00422
0.9999 0.1
0.30
PFUnDA
y=0.0864x+0.00456
0.9997 0.06
0.18
PFDoDA
y=0.0761x+0.00436
0.9998 0.08
0.23
PFTrDA
y=0.0287x+0.00134
0.9999 0.06
0.17
PFTeDA
y=0.0425x+0.00236
0.9998 0.09
0.27
PFBS
y=0.073x+0.00429
0.9996 0.09
0.27
PFHxS
y=0.0872x+0.00758
0.9999 0.09
0.27
PFHpS
y=0.0448x+0.000817
1
0.21
PFOS
y=0.0779x+0.00433
0.9995 0.1
0.3
PFDS
y=0.0858x+0.000937
0.999
0.1
0.32
PFOSA
y=0.0854x+0.000914
0.9992 0.1
0.30
MePFOSAA
y=0.0322x+0.00142
0.9996 0.08
0.26
0.07
y=0.037x+0.000647 0.9991 0.09 0.28 EtPFOSAA a y refers to the peak area, and x refer to counts per second (CPS) value; b MLOD refers to the method limit of detection, (S/σ)x3.3; c MLOQ refers to the method limit of quantification, (S/σ)x10
Table 2. Mean concentration (ng/g) of PFASs in crab samples reported in published literature.
Crab Crab Crab Crab
Origin of country South Koreab Chinab Pakistanb Indiab
Giant Mud Crab
Australia
Blue Swimmer Crab
Australia
Sampling
PFOA 16.90 9.42 0.01 0.49
PFNA 2.33 1.43 0.34 0.14
PFDA 1.01 0.35 0.00 0.00
PFUnDA 2.66 0.80 0.03 0.00
PFDoDA 0.76 0.16 0.01 0.00
PFTrDA 5.35 2.40 0.03 0.07
PFTeDA 1.15 0.35 0.07 0.00
ΣPFSAs PFBS PFHxS 0.10 1.37 0.03 0.26 0.03 0.13 0.02 0.53
PFHpS 0.01 0.01 0.01 0.02
PFOS 4.52 1.60 7.02 5.88
PFDS 11.58 0.01 1.46 0.03
This study This study This study This study
-
nac
na
na
na
0.73
na
na
na
na
na
na
na
12.42
na
12.95
na
(Taylor 2019)
2015
na
na
0.15
0.21
na
na
na
0.11
ndd
na
na
na
na
na
na
na
-
Australia
9
Australia
8
Grapsid crabd
South Korea
1
Penicillate shore crabd
South Korea
5
Hermit crabd
South Korea
4
Beach crabd
South Korea
2
Flat shore crabe
South Korea
1
Crab soft tissue Crab gill Crab viscera
China China China
70 70 70
Spider crab
UK
1
Brown crab
UK
1
Crab
UK
1
Japan
2
a
PFHpA 0.35 0.18 0.00 0.00
20 14 37 6 2040
Eastern king mud crab
Crab (hepatopancreas)
2017 2017 2017 2017
PFHxA 0.07 0.22 0.00 0.16
Year
Mud crab
Reference
ΣPFCAs PFBA PFPeA 1.93 0.62 0.57 0.06 0.52 0.51 0.59 0.02
Na
(Taylor et al. 2019) (Taylor and Johnson 2016) (Taylor and Johnson 2016)
2015
na
na
na
na
<0.0003
na
na
na
na
na
na
na
na
na
0.0021
na
2015
na
na
na
na
<0.0003
na
na
na
na
na
na
na
na
na
0.0042
na
1.90
5.10
0.08
0.08
6.60
0.45
0.26
0.36
na
na
na
3.40
0.55
na
4.10
0.25
(Hong et al. 2015)
0.96
0.80
0.27
0.25
12.76
0.98
0.72
1.00
na
na
na
1.57
0.65
na
8.22
0.20
(Hong et al. 2015)
2.08
16.18
0.22
0.18
1.00
0.29
0.20
0.51
na
na
na
0.75
0.23
na
2.30
0.23
(Hong et al. 2015)
1.67
4.11
0.25
0.15
2.52
0.34
0.14
0.48
na
na
na
0.55
0.43
na
1.24
0.25
(Hong et al. 2015)
1.00
1.00
0.25
0.33
0.42
0.85
0.10
0.19
na
na
na
1.30
0.51
na
4.20
0.25
(Hong et al. 2015)
na na na
na na na
na na na
6.07 <0.05 <0.05
1.15 36.60 28.40
<0.01 <0.05 <0.05
<0.01 6.94 <0.05
<0.01 31.70 <0.05
<0.01 13.00 <0.05
na na na
na na na
<0.02 <0.1 <0.1
<0.02 <0.1 <0.1
na na na
1.17 17.90 105.00
<0.01 <0.05 <0.05
(Yang et al. 2012) (Yang et al. 2012) (Yang et al. 2012)
na
na
<1
<1
6.00
1.00
<1
<1
<1
na
na
<1
<1
na
13.00
na
(Clarke et al. 2010)
na
na
<1
<1
6.00
3.00
<1
<1
<1
na
na
<1
<1
na
3.00
na
(Clarke et al. 2010)
na
na
<1
<1
5
1
<1
1
1
na
na
<1
<1
na
4
na
(Clarke et al. 2010)
na
na
na
na
9.5
<1.5
na
na
na
na
na
na
<1.5
na
<0.3
na
(Nakata et al. 2006)
20102012 20102012 20102012 20102012 20102012 2010 2010 2010 20072008 20072008 20072008 2004
b
c
d
e
N is the number of samples analyzed in each group; body + legs + offal + eggs; na=not analyzed; nd=not detected; data less than
method limit of detection (MLOD) and method limit of quantitation (MLOQ) were set as equal to half of the MLOD and MLOQ respectively (when calculating the mean values).
Eggs Legs
Eggs
Legs
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Highlights • PFOA was dominant among the PFCAs in Korean and Chinese crabs, and PFOS was dominant among the PFSAs in Pakistani and Indian crabs • PFOA and PFOS were detected at significantly higher concentrations in the offal and egg of in crabs • The dietary exposure levels of PFOA and PFOS through crab consumption are considered too low to pose a risk
Declaration of interests √☐ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:
The authors have no other potential conflicts of interest to declare.
S0269-7491(19)33753-4
DOI:
https://doi.org/10.1016/j.envpol.2020.114185
Reference:
ENPO 114185
To appear in:
Environmental Pollution
Received Date: 11 July 2019 Revised Date:
22 November 2019
Accepted Date: 11 February 2020
Please cite this article as: Choi, S., Kim, J.-J., Kim, M.-H., Joo, Y.-S., Chung, M.-S., Kho, Y., Lee, K.W., Origin and organ-specific bioaccumulation pattern of perfluorinated alkyl substances in crabs, Environmental Pollution (2020), doi: https://doi.org/10.1016/j.envpol.2020.114185. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Credit author statement Seogyeong Choi: Investigation, Writing-Original Draft. Jeong-Jae Kim: Visualization. MinHyuk Kim: Validation. Yong-Sung Joo: Formal analysis, Data Curation. Myung-Sub Chung: Resources. Younglim Kho: Methodology. Kwang-Won Lee: Conceptualization, WritingReview & Editing, Supervision.
Graphical abstracts
1
Research Article
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Origin and organ-specific bioaccumulation pattern of perfluorinated alkyl substances in
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crabs
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Seogyeong Choi1, Jeong-Jae Kim2, Min-Hyuk Kim1, Yong-Sung Joo2, Myung-Sub Chung3,
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Younglim Kho4, and Kwang-Won Lee *
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1
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Seoul 02841, Republic of Korea
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2
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Republic of Korea
1,
Department of Biotechnology, College of Life Sciences & Biotechnology, Korea University,
Department of Statistics, College of Natural Science, Dongguk University, Seoul 04620,
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do 17546, Republic of Korea
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4
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Republic of Korea
Department of Food Science and Technology, Chung-Ang University, Anseong, Gyeonggi-
Department of Health, Environment & Safety, Eulji University, Sungnam, Gyeonggi, 461-713,
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*Corresponding author:
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Prof. Kwang-Won Lee, Department of Biotechnology, College of Life Sciences &
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Biotechnology, Korea University, 145 Anam-ro, Seongbuk-gu, Seoul 02841, Republic of
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Korea
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Tel: +82-2-3290-3473
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Fax: +82-2-927-1970
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E-mail: [email protected] 1
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Abstract
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Consumption of seafood is a major contributor to perfluorinated alkyl substances (PFASs)
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exposure. Crabs contain high levels of PFASs, and different PFASs are concentrated in their
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tissues depending on their habitat. Despite South Korea importing huge quantities of crabs,
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no investigation has been conducted on the effect of PFAS exposure. This study investigated
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the risk of exposure to PFASs when ingesting crab. To determine the risk of exposure, 19
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different PFASs species were measured in the edible parts (body, legs, offal, and eggs) of
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crabs originating from South Korea (n=17), China (n=14), India (n=7), and Pakistan (n=31),
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which were distributed in the fish markets of South Korea. The results revealed that, in
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contrast to short-chain PFASs, long-chain PFASs (PFCAs≥8, PFSAs≥6, and perfluorooactane
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sulfonamidoacetic acids (FOSAAs)≥8) were detected in crab samples from all four countries
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of origin, and in all the edible parts except for the legs. Perfluorooctanoic acid (PFOA; 16.9
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ng/g in South Korea, 9.42 ng/g in China) and perfluoro-n-tridecanoic acid (PFTrDA; 5.35
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ng/g in South Korea, 2.40 ng/g in China) were the predominant perfluoroalkyl carboxylic
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acids (PFCAs) detected in the crabs originating from South Korea and China, and
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perfluorooctane sulfonic acid (PFOS; 7.02 ng/g in Pakistan, 5.88 ng/g in India) was the
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predominant perfluoroalkyl sulfonic acids (PFSAs) detected in crabs originating from
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Pakistan and India. These results indicate that PFASs that are accumulated in crabs differ
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depending on the ocean from which they originate. The concentrations of PFOA and PFOS
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were significantly higher in the eggs and offal than in the legs and body of the crab. The
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average daily intake of PFOA and PFOS in Koreans ranges from 0.01% to 0.07% based on 2
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the tolerable daily intake of EFSA and MFDS. These results establish the PFAS profiles and
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risk assessment of crabs that are distributed in South Korea.
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Keywords: perfluorinated alkyl substances; crab; organ-specific; long-chain PFASs; risk
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assessment
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Introduction
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Perfluorination implies that the hydrogen atoms in a molecular chain are converted to
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fluorine atoms (OECD, 2012). The two most widely known PFASs are perfluoroalkyl
53
sulfonic acids (PFSAs, e.g., perfluorooctane sulfonic acid (PFOS)), and perfluoroalkyl
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carboxylic acids (PFCAs, e.g., perfluorooctanoic acid (PFOA))(OECD, 2012). PFASs are
55
man-made chemicals (Lehmler, 2005) and characterized by a hydrophobic tail and a water-
56
soluble anionic head group (Prevedouros et al., 2006). Strong carbon-fluorine bonds make
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PFASs resistant to hydrolysis, photodegradation, and microbial degradation (Giesy and
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Kannan, 2002). Due to their unique properties, PFASs have been used for the last 60 years in
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the manufacture of fire-fighting equipment, paper, cookware, automotive components, and
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cosmetics, with roles as surfactants, coatings, and polishes (Jogsten et al., 2012; Key et al.,
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1997; Lehmler, 2005; Taylor and Johnson, 2016). PFOA and PFOS that have eight carbon
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atoms are known to be the most abundant substances released into the environment through
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applications such as metal plating, use in the semiconductor industry, firefighting foams, and
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textile treatment (Giesy and Kannan, 2001; Wang et al., 2015). PFASs are distributed
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globally through the movement of air and water (Lehmler, 2005).
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The toxic effects of PFASs depend on the fluorinated chain length but also on their functional
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groups (Lau et al., 2007). Numerous studies have indicated that PFOA and PFOS cause
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endocrine disorders in humans (Grün and Blumberg, 2006; Preston et al., 2018). Human
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exposure to PFASs is usually through consumption of contaminated food and water
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(D’Hollander et al., 2010; Kärrman et al., 2009; Su et al., 2017). At the 2009 Stockholm
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Convention, PFOS and its salts were included in the category of persistent organic pollutants
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(POPs) due to their persistence and toxicity in the environment and the human body (UNEP, 4
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2009). Furthermore, PFOA, perfluorohexane sulfonate (PFHxS), and their salts were
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presented as POPs at the Stockholm conventions in 2015 and 2017 (Ripley, 2018; Wang and
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Sun, 2016). The United States and Europe have agreed to phase out certain types of PFAS
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production (Bergman et al., 2013). Canada has already phased out the sale of PFOA and other
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long-chain PFASs, and prohibited the illegal sale and import of long-chain PFASs (EPA,
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2012). Nonetheless, PFOA and PFOS are still problematic because they can persist and
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accumulate in the environment or in organisms over long periods of time (Fromme et al.,
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2009). The half-life of PFOA and PFOS in the human body is estimated to be 3.5 and 4.8
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years, respectively (Olsen et al., 2007).
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Several studies have detected PFASs in aquatic organisms. PFASs have been observed at
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high levels in shellfish, especially crabs, due to the specificity of the species (Habibullah-Al-
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Mamun et al., 2017; Ip et al., 2005; Yang et al., 2007). In addition, demersal organisms have
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higher levels of PFASs compared to pelagic organisms due to environmental pollution of the
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water, sediments, and soil (Zareitalabad et al., 2013). Crabs are prone to PFAS exposure as
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they are a scavenger (Ip et al., 2005). In addition, crabs accumulate PFASs relatively well as
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they have gills with a relatively large surface area that continuously transport organic
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contaminants and suspended particles from the water (Yang et al., 2007). Our review paper
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reported that crabs contain relatively high levels of PFOA and PFOS compared to fish (Jeong
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et al., 2019). Likewise, mean PFOA and PFOA concentrations were found to be higher in
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Giant Mud Crab than in Mulloway and Dusky Flathead (Taylor, 2019). Despite these studies,
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there are few studies on the levels of PFASs, especially with respect to the varied origins of
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the crabs that are distributed in East Asia.
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The purpose of this study was to analyze 19 species of PFASs in the edible body parts of
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crabs (the body, offal, legs, and eggs) from different countries of origin that were distributed
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in South Korean markets. We aimed to assess the profile distribution of short-chain and long-
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chain PFASs, and the accumulation of PFOA and PFOS in the different edible parts of the
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crabs. We then assessed the risks of PFOA and PFOS exposure due to the consumption of
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crabs.
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2. Materials and Methods
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2.1 Chemicals and reagents
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Details on the standards and, structure, and their corresponding internal standard used to
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analysis are described in Table S1. The 19 species of PFASs were purchased from
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Wellington Laboratories (Guelph, ON, Canada). In addition, protease, lipase, tetra butyl
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ammonium hydrogen sulfate (TBAHS), sodium bicarbonate (NaHCO3), and sodium
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carbonate anhydrous (Na2CO3) were used in the pretreatment process and were purchased
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from Sigma-Aldrich Chemical Co. (St. Louis, MO, USA) at a purity of 99%. The analytical
111
solvent, methanol, distilled water, acetonitrile, methyl-t-butyl ether (MTBE), and hexane
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were purchased from Burdick and Jackson (Muskegon, MI, USA) as HPLC grade. A blender
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(BL-1401 KR) was used for sample homogenization, and an O2 Incubator (Vision Scientific,
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Daejeon, Korea) was used for enzyme activity. An ultrasonic extractor (5510R-DTH,
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Bransonic, Danbury, CT, USA) and rotary stirrer (model AG, FinePCR, Korea) were used for
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material extraction. A PLC-05 (Gemmy Industrial Corp., Taiwan) was used for centrifugal
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separation, and an Eyela Centrifugal Evaporator (CVE3100; Tokyo, Japan) was used for 6
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concentrating samples. The equipment that comes into contact with the samples must not
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contain or be coated with Teflon, polytetrafluoroethylene, or ethylene tetrafluoroethylene,
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and must not contact the external environment.
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2.2 Sampling collection and sample extraction
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The blank tests of the analytical solvent, methanol, distilled water, acetonitrile, MTBE,
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hexane, blender, and nitrile gloves were performed to control potential contamination during
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sample extraction and analysis. A total of 69 crab samples (Origin: South Korea (n = 17),
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China (n = 14), India (n = 7), and Pakistan (n = 31)) were purchased from two fish markets
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and five supermarkets in South Korea in November 2017. In accordance with the Republic of
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Korea Act on the indication of origin of agricultural and fishery products, the crabs were
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purchased after verifying that the indication of the country of origin was correct. All samples
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were transported to the laboratory in iceboxes. The samples were dissected to collect the
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body, offal, legs, and eggs for analysis. Each dissected sample was mixed with distilled water
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at a 1:1 ratio (weight by volume), and homogenized using a blender (BL142 KR, Tefal,
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France). During this time, the gizzard and gills were removed separately as they are not
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edible. All the samples were collected in high density polyethylene wide-mouth bottles,
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which were unlined (no Teflon) and had polypropylene screw cap, and stored in a -20°C
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freezer (model WS-1244DF, Woosung, Seoul, South Korea) until further analysis.
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Most of the analytes was quantitatively examined with the introduction of internal standards
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substituted with isotopes before pretreatment, with the exception of some analytes. The edible
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parts (body, legs, offal, and eggs) are more easily homogenized than other solid foods, so
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there is little risk of underestimating the PFAS exposure levels. For PFASs that were non-
141
extractable due to protein and fat binding, we used protease and lipase to hydrolyze the fats
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and protein-bound PFASs, respectively, in samples in the presence of spiked internal
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standards. The detailed sample extraction procedure is described in Supporting Information
144
(SI) Section 1. Sample extraction procedure. Additionally, the schematic flow diagram of the
145
pretreatment procedure for crab samples is provided in SI Fig. S1.
146 147
2.3 Instrument analysis
148
Concentrations of PFASs were determined using High-Performance Liquid Chromatography
149
(HPLC) (Agilent 1100 LC series, Agilent Technologies, Palo Alto, CA, USA) and Tandem
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Mass Spectrometry (API 4000, Applied Biosystems, Foster City, CA, USA), equipped with a
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electrospray ionization (ESI) source in the negative ion mode with multiple reaction
152
monitoring modes. The instrument and quantification details are given in SI Table S2, and
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Table S3.
154 155
2.4 Quality assurance and quality control (QA/QC)
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To reflect the sample characteristics for validation, the pooled QC sample was prepared by
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mixing samples according to their country of origin (South Korea, China, India, and Pakistan)
158
and parts (body, offal, legs, and eggs). Ten concentration levels (0.01, 0.02, 0.05, 0.1, 0.2, 0.5,
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1, 2, 5, and 10 ng/mL) were spiked in the pooled sample, and the calibration curves were
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obtained. The mean PFAS value of the pooled QC sample was subtracted from the calculated
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calibration standard concentration. Detailed methodologies used for QA/QC of PFASs are
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described in SI Section 2.
163
Accuracy was evaluated using recovery (%) and precision was evaluated using relative
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standard deviation (RSD) (%). The coefficient of determination (r2) of the calibration curve
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showed excellent linearity of 0.99 or more (Table 1). The MLOD ranged from 0.06 to 0.1
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ng/g (Table 1). The intra-day accuracy ranged from 82.6 to 120% and the inter-day accuracy
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ranged from 84.8 to 118.4% (Table S4). AOAC (2002) recommends a recovery range of 70–
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125% when the analytes are present in ng/g concentration. Also, the intra-day precision and
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the inter-day precision were 19.7% RSD and 18.6% RSD, respectively (Table S4). The
170
concentrations of 0.2 ng/g (low level) and 1 ng/g (medium level) of PFASs were analyzed for
171
every 20 samples for QA/QC. Detailed methodologies used for quality assurance and quality
172
control of PFASs are described in the supplementary data.
173 174
2.5 Potential exposure assessment
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To assess the potential health risks to humans, tolerable daily intake (TDI), reference dose
176
(RfD), and disability-adjusted life-years (DALY) were used. In the case of RfD, the criteria
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are mainly set for animal experiments, not humans, and DALY is rarely used for risk
178
assessment of PFASs. In this study, the potential health risks associated with PFOA and
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PFOS with human intake were evaluated by comparison with the TDI standards of the
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European Food Safety Authority (EFSA) (2008) and South Korea's Ministry of Food and
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Drug Safety (MFDS) (2010). EFSA has established TDI to be 150 ng/kg b.w./d for PFOS and
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1.5 µg/kg b.w./d for PFOA (EFSA, 2008). MFDS set the TDI to be 150 ng/kg b.w./d for
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PFOS and 1 µg/kg b.w./d for PFOA. Detailed methodologies used to calculate the PFOA and
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PFOS dietary intakes and risk (%) are described in SI Section 3.
185
For risk assessment of PFOA and PFOS caused due to consumption of crabs, we used the
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National Health and Nutrition Survey (Kweon et al., 2014) published by the Korea Center for
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Disease Control and Prevention. As a risk assessment procedure, a random number was
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generated from a lognormal distribution using the mean and SD of PFOAs and PFOSs. Then,
189
the random number was multiplied by the value of the crab intake recorded in the National
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Health and Nutrition Survey. The estimated daily intake (EDI) was calculated using two
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scenarios that assumed average intake and an extreme amount of intake.
192 193
2.6 Statistical Analysis
194
A two-way ANOVA with multiple comparisons using the least squares means test were
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conducted to determine the significant differences among the PFAS concentrations in the
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crab samples. Since the distribution of both PFOAs and PFOS were skewed to the right, the
197
natural logarithmic transformation was applied to their concentrations before conducting the
198
ANOVA, to obtain a valid result. Values of p < 0.05 were considered statistically significant.
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For statistical analyses, concentrations that were lower than the MLOD were assigned a value
200
that was half of the MLOD (WHO, 1995).
201 202
3. Results and discussion
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3.1 PFASs distribution pattern in crab 10
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The detailed concentrations and detection frequency of individual PFASs in each country of
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origin, and each crab part, are shown in SI Table S5. Table S5 shows the average (detection
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rate) and the range (median value) of 19 PFASs. The concentration of ΣPFASs (ΣPFASs =
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ΣPFCAs + ΣPFSAs + Σperfluorooactane sulfonamidoacetic acids (FOSAAs)) was compared
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for each edible body part of the crab samples, belonging to each country of origin.
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The contributions of long-chain PFASs (PFCAs≥8, PFSAs≥6, and FOSAAs≥8) and short-
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chain PFASs in crabs are shown in Fig. 1 (a). Long-chain and short-chain PFASs differ in
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toxicity and bioaccumulation (OECD, 2013). Martin et al. reported that longer carbon chains
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lead to higher carcinogenicity and bioaccumulation (2003, 2004). Fig. 1 (a) shows that,
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regardless of the country of origin, long-chain PFASs containing PFOA and PFOS are
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dominant over short-chain PFASs, including PFBA, PFPeA, PFHxA, PFHpA, and PFBS in
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the body, offal, and eggs, but not the legs. The distribution of long-chain and short-chain
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carbons in the leg varied depending on the country of origin. Long-chain PFASs were
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dominant in the legs of Pakistani female crabs, Korean crabs, and Chinese male crabs. In the
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legs of male crabs originating from Pakistan and crabs from India, the percentage of short-
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chain PFASs were 66% and 53% (of the total PFASs), respectively, which was similar to or
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higher than the percentage of long-chain PFASs, that were 34% and 47%, respectively. In
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case of the body, the percentage of long-chain PFASs were as follows: Korean male crabs
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(82%) > Korean female crab (80%) > Pakistani male crab (80%) > Chinese male crab (76%)
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> Pakistani female crab (68%) > Indian female crab (51%). In the offal, the percentage of
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long-chain PFASs were as follows: Chinese male crab (90%) > Pakistani male crab (85%) >
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Korean female crab (83%) > Korean male crab (80%), Indian female crab (80%) > Pakistani
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female crab (70%). In the eggs, the percentage of long-chain PFASs were as follows: Indian 11
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female crab (84 %) > Korean male crab (80%) > Pakistani female crab (52%). On the other
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hand, the long-chain PFASs in the legs were 82% (Korean male crab), 78% (Korean female
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crab), 78% (Chinese male crab), 51% (Pakistani female crab), 47% (Indian female crab), and
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34% (Pakistani male crab).
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The contributions of PFCAs, PFSAs, and FOSAAs, depending on the crab parts and country
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of origin, are shown in Fig. 1 (b). There was a definite difference in the concentration
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tendency of PFASs depending on the origin of the crabs. The contribution of ΣPFCAs was
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dominant among the total PFASs in Korean and Chinese crab samples, that is 58%−76%. In
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contrast, in the Pakistani and Indian crab samples, the ΣPFSA among the total PFASs, were
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45%−91%. These results suggest that the concentrations of PFASs differ depending on the
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country of origin, even if they are the same species. This variation may be due to the
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difference in sediment, water, and diet of the habitat to which the crab is exposed (Hong et al.,
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2015).
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Fig. 2 shows the distribution of 19 individual PFASs. In Korean and Chinese crab samples,
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PFOA is the most dominant compound among the PFCAs, regardless of the body part of the
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crab, with a concentration of 32−54%, followed by PFTrDA (9−16%), and PFOS (5−18%)
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(Figs. 2 (a) and (b)). In the case of Indian and Pakistani crab samples, PFOS is the most
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dominant compound among the PFSAs, regardless of the body part of the crab, with a
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concentration of 33−85%, followed by PFBA (2−15%) and PFPeA (1−27%) (Figs. 2 (c) and
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(d)). Fifty samples of the coastal waters of the central and eastern Pacific and of the South
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China Sea of Korea, Japan, and China showed PFOA as the major pollutant in marine waters
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(So et al., 2004; Yamashita et al., 2005). According to the Yeung et al., (2009), PFOS was the
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most dominant PFAS in most samples from the Ganges River flowing into the Bay of Bengal 12
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and the Indian Ocean. This result implies that there may be differences in the PFASs
252
component, according to the country of origin.
253
Bioconcentration factor (BCF) is a measure of the accumulation, in a living organism, of a
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chemical substance from the ambient environment through its respiratory and dermal surfaces
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(at steady state), and will be the concentration of the test substance in the organism (as mg/kg)
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divided by the concentration of the chemical substance in the surrounding medium (as mg/L)
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(Arnot and Gobas, 2006). Although BCF can only be calculated under controlled conditions,
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we estimated BCF of PFASs in crabs, using the reported concentration and our data of PFASs
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in crabs and its concentration in the water, in Table S6. In the Indian ocean, the estimated
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BCF values of PFOS were remarkably higher than those in the East and South China Sea,
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whereas the estimated BCF values of PFOA were higher in the East and South China Sea
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compared with those in the Indian Ocean. These results suggest that the accumulation of
263
PFOA and PFOS in crabs may be an indicator for the level of PFASs in the water where
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those crabs originated.
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3.2 Comparison of the trend of PFASs in crab with other international studies
267
Table 2 summarizes the previously reported preliminary results on PFASs. The distribution
268
of PFASs can be affected by geographical features or by aquatic climatic conditions
269
(Habibullah-Al-Mamun et al., 2017). According to Hong et al. (2015), the highest detected
270
levels of PFOA in the samples of grapsid crabs, penicillate shore crabs, and beach crabs
271
collected from the west coast of South Korea were 6.6 ng/g, 12.76 ng/g, and 2.52 ng/g,
272
respectively. The mean concentration of PFOA detected in the domestic (Korean) crabs in
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this study was 16.6 ng/g, which was similar or higher than the value observed in the Hong et 13
274
al. (2015) study. In addition, Hong et al. (2015) reported that PFOS was the analyte with the
275
highest concentration, that is 2.3 ng/g and 4.2 ng/g in the hermit crab and the flat shore crab
276
respectively, which is found on the western coast of South Korea. These values are similar or
277
lower than the result obtained in this study, which was 4.27 ng/g.
278
The mean concentration of PFOA (9.42 ng/g), which was the most prevalent in the Chinese
279
crabs in this study, was similar to that of PFOA (9.5 ng/g) detected in the crabs
280
(hepatopancreas) on the western coast of the Ariake Sea, Japan (Nakata et al., 2006).
281
However, this value was much lower than the PFOA concentration in the gills (36.6 ng/g)
282
and viscera (28.4 ng/g) of crabs from Bohai Bay, China, as Yang et al. (2012) reported.
283
According to their report, PFOA was predominantly detected in crab gills. Clarke et al. (2010)
284
reported that the concentration of PFOA in spider crabs, cromer crabs, and dressed crabs
285
found in the UK were 5 ng/g, 4 ng/g, and 9 ng/g, respectively.
286
Moreover, PFUnDA (31.7 ng/g), PFOS (17.9 ng/g), and PFDoDA (13 ng/g) were also
287
detected at high levels. In the case of crab viscera, PFOS (105 ng/g) had the highest
288
concentration, followed by PFOA. According to a report by Taylor and Johnson (2016),
289
among all the PFASs, PFOS was present in the highest concentration in the mud crab (0.0021
290
ng/g) and eastern king mud crab (0.0042 ng/g) of Australia. These values are significantly
291
lower than the results obtained in our study. In the case of PFOS, we obtained lower values
292
for crabs originating from Korea and China, and higher values for crabs originating from
293
Pakistan and India. In addition, the PFOS concentrations of spider crabs, brown crabs, and
294
crab originating from the UK were 13 ng/g, 3 ng/g, and 4 ng/g, respectively, similar to the
295
PFOS results of this study.
296 14
297
3.3 Correlation between PFASs concentration and edible parts of the crab
298
To determine whether the accumulation of PFOA and PFOS were related to the crab parts
299
(body, legs, offal, and eggs), significance tests were performed using data from all the
300
countries of origin of the crabs (Fig. 3). The result revealed that the accumulation of PFOA
301
and PFOS was significantly different depending on the body part of the crab. In the case of
302
the female crabs, PFOA levels were in the order of eggs >offal>body>legs, and in the case of
303
male crabs, PFOA levels were in the order of legs, offal> body (P<0.05). For PFOS, which is
304
known to have the highest bioaccumulation among PFASs, high concentrations were detected
305
in the order of offal> eggs> body> legs in female crabs (P <0.05) and offal> body> legs in
306
male crabs (P<0.05). This is consistent with previous studies, which showed that high levels
307
of PFASs were detected in the blood, liver, intestines, and eggs of guillemot, rainbow trout,
308
and other water organisms (Berger, 2008; Hong et al., 2015; Martin et al., 2003). Unlike most
309
persistent organic contaminants, PFAS chemicals accumulate higher in the kidney and liver
310
than in the blubber/fat or skeletal muscle due to their surfactant-like composition, and in a
311
study on harbor seals from the Dutch Wadden Sea, there was increasing concentrations of
312
PFOS in the order kidney > liver > blubber > skeletal muscle (Van de Vijver et al., 2005).
313
PFOS has a different pattern of accumulation as it binds preferentially to blood proteins and
314
accumulates in various tissues, such as liver and kidney (Jones et al., 2003). In addition,
315
Holmström and Berger (2008) reported a 3-fold higher concentration of PFOS in common
316
guillemot eggs relative to the livers of female birds sampled in the same year. They discussed
317
that most of the PFOS in bird eggs was found in the yolk, primarily in combination with very
318
low density lipoproteins, but to some degree also associated with phosvitin and vitellogenin
319
proteins, and such proteins of egg yolk are produced in the mother bird's liver and transferred 15
320
to the forming egg. These results suggest that PFOA and PFOS are detected at relatively high
321
concentrations in the offal of both male and female crabs and the eggs of female crabs due to
322
the unique bio-specificity of PFASs, which are both hydrophobic and oleophobic.
323 324
3.4 Potential exposure assessment of PFASs in humans
325
In this study, exposure to PFOA and PFOS was calculated by multiplying the concentration
326
of the compound in crabs by their intake. Then, this exposure of the compound was compared
327
with the TDI to calculate the risk (%) of exposure. EFSA has established TDI to be 150 ng/kg
328
b.w./d for PFOS and 1.5 µg/kg b.w./d for PFOA (EFSA, 2008). MFDS also recognized the
329
TDI to be 150 ng/kg b.w./d for PFOS and 1 µg/kg b.w./d for PFOA (MFDS, 2010). Most
330
common intake frequency level of the South Korean population on PFOA occurs at level of
331
less than 200 ng of PFOA/kg bw/d through the consumption of domestic and imported crabs,
332
and the frequency for PFOS takes place below 20 ng of PFOS/kg bw/d (Fig. 4).
333
In Scenario 1 we show the average daily intake of PFOA for South Koreans of all ages
334
through female crabs, using the average consumption value of 27.3 ng/person/d was 0.467
335
ng/kg b.w./d, assuming that the average body weight is 58.5 kg (Kweon et al., 2014). These
336
values corresponded to 0.03% of the EFSA TDI and 0.05% of the MFDS TDI. Also, the
337
average daily intake of PFOA for South Koreans of all ages through male crabs using the
338
average consumption value of 43.3 ng/person/d was 0.739 ng/kg b.w./d, which is 0.05% of
339
the EFSA TDI (1.5 µg/kg b.w.) and 0.07% of the MFDS TDI (1.5 µg/kg b.w.). Additionally,
340
the average daily intake of PFOS for South Koreans of all ages through female crabs (using
341
the average consumption value of 2.73 ng/person/d) was 0.0470 ng/kg b.w./d. The risk of
16
342
PFOS exposure is also found to be negligible, corresponding to 0.03% of both EFSA and
343
MFDS TDI (150 µg/kg b.w.). The average PFOS intake per day for South Koreans of all ages
344
through male crabs (using an average consumption value of 1.12 ng/person/d) was 0.153
345
ng/kg b.w./d, which is 0.01% of the EFSA TDI and MFDS TDI. Therefore, the risk of PFOA
346
and PFOS to South Koreans through the average food intake was evaluated to be very low
347
compared to the TDI of EFSA and MFDS.
348
In Scenario 2, using the 99th percentile consumption, it was demonstrated that the daily
349
intake of PFOA through female crabs was 148 ng/person/d, and the intake per body weight
350
was 2.52 ng/kg b.w./d, which is 0.16% of the EFSA TDI and 0.25% of the MFDS TDI. The
351
daily intake of PFOA through male crabs was 193 ng/person/d, and the intake per body
352
weight was 3.31 ng/kg b.w./d, which is 0.22% of the EFSA TDI and 0.33% of the MFDS
353
TDI. Furthermore, the daily intake of PFOS through female crabs was 58.4 ng/person/d, and
354
the intake per body weight was 0.10/ ng/kg b.w./d, which is 0.67% of the EFSA and MFDS
355
TDI. The daily intake of PFOS through male crabs was 30.6 ng/person/d, and the intake per
356
body weight was 0.52/ ng/kg b.w./d, which is 0.35% of the EFSA and MFDS TDI. Thus, the
357
level of overall exposure to PFOA and PFOS for South Koreans through crab intake was
358
below the EFSA and MFDS levels, making it a low risk.
359 360
4. Conclusion
361
This is the first study to monitor 19 species of PFASs in the body, offal, legs, and eggs of
362
crabs distributed in South Korean markets from four different countries of origin. The results
363
revealed that different PFAS species were detected in the crabs, depending on the country of
364
origin. With respect to the concentration of PFASs, PFOA was the most dominant among 17
365
PFCAs in South Korean and Chinese crabs, and PFOS was the most dominant among PFSAs
366
in Pakistani and Indian crabs. Furthermore, the accumulation of PFOA and PFOS differed
367
depending on the part of the crab that was studied (body, legs, offal, and eggs). PFOA and
368
PFOS were detected at significantly higher concentrations in the offal of both male and
369
female crabs and eggs of females. In addition, the dietary exposure levels of PFOA and PFOS
370
through crab consumption were considered too low to pose a risk to humans.
371 372
Source of funding
373
This work was supported by a Korea University Grant (K1617111)
374 375
Conflicts of interest
376
The authors have no other potential conflicts of interest to declare.
377 378
Acknowledgment
379
This work was supported by a Korea University Grant (K1617111) and School of Life
380
Sciences & Biotechnology of Korea University for BK21PLUS. The authors would also like
381
to thank the Institute of Biomedical Science & Food Safety, CJ-Korea University Food Safety
382
Hall (Seoul, South Korea) for providing the equipment and facilities.
18
383
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21
499
Figure legend
500
Figure 1. (a) The sum of perfluoroalkyl carboxylates (ΣPFCAs), perfluoroalkane sulfonates
501
(ΣPFSAs), and perfluorooactane sulfonamidoacetic acids (ΣFOSAAs), and (b) relative
502
abundance (%) of short chain and long chain (PFCAs≥8, PFSAs≥6, FOSAAs≥8) according to
503
the organ specificity of crabs.
504 505
Figure 2. Distribution profiles of PFASs concentration in crabs originating from (a) South
506
Korea, (b) China, (c) India, and (d) Pakistan.
507 508
Figure 3. Comparison of the concentrations of PFOA and PFOS according to the organ
509
specificity of crabs, (a) female crab; (b) male crab; (c) female crab; (d) male crab.
510 511
Figure 4. Dietary intake histogram of the South Korean general population on PFOA (a and b)
512
and PFOS (c and d) based on the gender of domestic and imported crabs.
22
Table 1. Linear regression data of method limits of detection (MLOD) and method limit of quantification (MLOQ) of the investigated perfluorinated alkyl substances (PFASs). b
Compounds
Regression equation
a
2
MLOD
r
-1
(ng g )
c
MLOQ -1
(ng g )
PFBA
y=0.13x+0.00587
0.9998 0.1
0.30
PFPeA
y=0.0438x+0.00388
0.9998 0.09
0.27
PFHxA
y=0.144x+0.00901
0.9994 0.09
0.27
PFHpA
y=0.0471x+0.0016
0.9998 0.1
0.29
PFOA
y=0.075x+0.00636
0.9999 0.1
0.29
PFNA
y=0.141x+0.00962
0.9998 0.09
0.26
PFDA
y=0.132x+0.00422
0.9999 0.1
0.30
PFUnDA
y=0.0864x+0.00456
0.9997 0.06
0.18
PFDoDA
y=0.0761x+0.00436
0.9998 0.08
0.23
PFTrDA
y=0.0287x+0.00134
0.9999 0.06
0.17
PFTeDA
y=0.0425x+0.00236
0.9998 0.09
0.27
PFBS
y=0.073x+0.00429
0.9996 0.09
0.27
PFHxS
y=0.0872x+0.00758
0.9999 0.09
0.27
PFHpS
y=0.0448x+0.000817
1
0.21
PFOS
y=0.0779x+0.00433
0.9995 0.1
0.3
PFDS
y=0.0858x+0.000937
0.999
0.1
0.32
PFOSA
y=0.0854x+0.000914
0.9992 0.1
0.30
MePFOSAA
y=0.0322x+0.00142
0.9996 0.08
0.26
0.07
y=0.037x+0.000647 0.9991 0.09 0.28 EtPFOSAA a y refers to the peak area, and x refer to counts per second (CPS) value; b MLOD refers to the method limit of detection, (S/σ)x3.3; c MLOQ refers to the method limit of quantification, (S/σ)x10
Table 2. Mean concentration (ng/g) of PFASs in crab samples reported in published literature.
Crab Crab Crab Crab
Origin of country South Koreab Chinab Pakistanb Indiab
Giant Mud Crab
Australia
Blue Swimmer Crab
Australia
Sampling
PFOA 16.90 9.42 0.01 0.49
PFNA 2.33 1.43 0.34 0.14
PFDA 1.01 0.35 0.00 0.00
PFUnDA 2.66 0.80 0.03 0.00
PFDoDA 0.76 0.16 0.01 0.00
PFTrDA 5.35 2.40 0.03 0.07
PFTeDA 1.15 0.35 0.07 0.00
ΣPFSAs PFBS PFHxS 0.10 1.37 0.03 0.26 0.03 0.13 0.02 0.53
PFHpS 0.01 0.01 0.01 0.02
PFOS 4.52 1.60 7.02 5.88
PFDS 11.58 0.01 1.46 0.03
This study This study This study This study
-
nac
na
na
na
0.73
na
na
na
na
na
na
na
12.42
na
12.95
na
(Taylor 2019)
2015
na
na
0.15
0.21
na
na
na
0.11
ndd
na
na
na
na
na
na
na
-
Australia
9
Australia
8
Grapsid crabd
South Korea
1
Penicillate shore crabd
South Korea
5
Hermit crabd
South Korea
4
Beach crabd
South Korea
2
Flat shore crabe
South Korea
1
Crab soft tissue Crab gill Crab viscera
China China China
70 70 70
Spider crab
UK
1
Brown crab
UK
1
Crab
UK
1
Japan
2
a
PFHpA 0.35 0.18 0.00 0.00
20 14 37 6 2040
Eastern king mud crab
Crab (hepatopancreas)
2017 2017 2017 2017
PFHxA 0.07 0.22 0.00 0.16
Year
Mud crab
Reference
ΣPFCAs PFBA PFPeA 1.93 0.62 0.57 0.06 0.52 0.51 0.59 0.02
Na
(Taylor et al. 2019) (Taylor and Johnson 2016) (Taylor and Johnson 2016)
2015
na
na
na
na
<0.0003
na
na
na
na
na
na
na
na
na
0.0021
na
2015
na
na
na
na
<0.0003
na
na
na
na
na
na
na
na
na
0.0042
na
1.90
5.10
0.08
0.08
6.60
0.45
0.26
0.36
na
na
na
3.40
0.55
na
4.10
0.25
(Hong et al. 2015)
0.96
0.80
0.27
0.25
12.76
0.98
0.72
1.00
na
na
na
1.57
0.65
na
8.22
0.20
(Hong et al. 2015)
2.08
16.18
0.22
0.18
1.00
0.29
0.20
0.51
na
na
na
0.75
0.23
na
2.30
0.23
(Hong et al. 2015)
1.67
4.11
0.25
0.15
2.52
0.34
0.14
0.48
na
na
na
0.55
0.43
na
1.24
0.25
(Hong et al. 2015)
1.00
1.00
0.25
0.33
0.42
0.85
0.10
0.19
na
na
na
1.30
0.51
na
4.20
0.25
(Hong et al. 2015)
na na na
na na na
na na na
6.07 <0.05 <0.05
1.15 36.60 28.40
<0.01 <0.05 <0.05
<0.01 6.94 <0.05
<0.01 31.70 <0.05
<0.01 13.00 <0.05
na na na
na na na
<0.02 <0.1 <0.1
<0.02 <0.1 <0.1
na na na
1.17 17.90 105.00
<0.01 <0.05 <0.05
(Yang et al. 2012) (Yang et al. 2012) (Yang et al. 2012)
na
na
<1
<1
6.00
1.00
<1
<1
<1
na
na
<1
<1
na
13.00
na
(Clarke et al. 2010)
na
na
<1
<1
6.00
3.00
<1
<1
<1
na
na
<1
<1
na
3.00
na
(Clarke et al. 2010)
na
na
<1
<1
5
1
<1
1
1
na
na
<1
<1
na
4
na
(Clarke et al. 2010)
na
na
na
na
9.5
<1.5
na
na
na
na
na
na
<1.5
na
<0.3
na
(Nakata et al. 2006)
20102012 20102012 20102012 20102012 20102012 2010 2010 2010 20072008 20072008 20072008 2004
b
c
d
e
N is the number of samples analyzed in each group; body + legs + offal + eggs; na=not analyzed; nd=not detected; data less than
method limit of detection (MLOD) and method limit of quantitation (MLOQ) were set as equal to half of the MLOD and MLOQ respectively (when calculating the mean values).
Eggs Legs
Eggs
Legs
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Highlights • PFOA was dominant among the PFCAs in Korean and Chinese crabs, and PFOS was dominant among the PFSAs in Pakistani and Indian crabs • PFOA and PFOS were detected at significantly higher concentrations in the offal and egg of in crabs • The dietary exposure levels of PFOA and PFOS through crab consumption are considered too low to pose a risk
Declaration of interests √☐ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:
The authors have no other potential conflicts of interest to declare.