Relationship between crustacean consumption and serum perfluoroalkyl substances (PFAS): the Korean National Environmental Health Survey (KoNEHS) cycle 4
Article information
Abstract
Background
Perfluoroalkyl substances (PFASs) are non-aromatic organic compounds, whose hydrogen atoms in the carbon chain substituted by fluorine atoms. PFASs exhibit developmental toxicity, carcinogenicity, hepatotoxicity, reproductive toxicity, immunotoxicity, and hormone toxicity. PFASs are used in the production of disposable food packages, aircraft and automobile devices, cooking utensils, outdoor gear, furniture and carpets, aqueous film forming foam (AFFF), cables and wires, electronics, and semiconductors. This study aimed to determine the association between crustacean consumption and serum PFASs.
Methods
Adult participants (2,993) aged ≥ 19 years were extracted from the 4th cycle data of the Korean National Environmental Health Survey (KoNEHS). Based on the 50th percentile concentrations of serum PFASs, participants were divided into the low-concentration group (LC) and the high-concentration group (HC). General characteristics, dietary factors, coated product usage, and personal care product usage, an independent t-test and χ2 test were analyzed. The odds ratio (OR) of serum PFAS concentration against crustacean consumption was estimated via logistic regression analysis adjusting for general characteristics, dietary factors, coated product usage, and personal care product usage.
Results
The OR for the HC of serum PFASs was higher in individuals with ≥once a week crustacean consumption than in those with < once a week crustacean consumption. Estimated ORs were perfluorohexanesulfonic acid 2.15 (95% confidence interval [CI]: 1.53–3.02), perfluorononanoic acid (PFNA) 1.23 (95% CI: 1.07–1.41), and perfluorodecanoic acid (PFDeA) 1.42 (95% CI: 1.17–1.74) in males, and perfluorooctanoic acid 1.48 (95% CI: 1.19–1.84), perfluorooctanesulfonic acid 1.39 (95% CI: 1.27–1.52), PFNA 1.70 (95% CI: 1.29–2.26) and PFDeA 1.43 (95% CI: 1.32–1.54) in females.
Conclusions
This study revealed the association between the crustacean consumption and concentrations of serum PFASs in general Korean population.
BACKGROUND
Perfluoroalkyl substances (PFASs) are non-aromatic organic chemical compounds, in which hydrogen atoms within the carbon chain are substituted by fluorine atoms.1 PFASs are highly stable based on the strong binding between carbon and fluorine, and their non-stick and surface tension-lowering properties allow application in many fields.12 The main uses include disposable food packages, aircraft and automobile devices, cooking utensils, outdoor gear, furniture and carpets, aqueous film forming foam (AFFF), cables and wires, electronics, and semiconductors.3 The high stability of PFASs prevents degradation, continuously affecting the marine environment.4
Crustaceans include shrimps, crayfish, crabs, krill, and etc., and they feed on seaweeds, plankton, small fish, and organic matter in sediments.567 High concentrations of PFASs are detected in crustaceans due to high PFAS exposure from food and habitat conditions.8 Crustaceans are abundantly found in the marine environment and can be used to quantitatively assess the level of marine pollution, so they are used as biomonitors for PFAS contamination.910
The PFAS exposure pathways in the human body include oral intake, dust inhalation, and skin contact, while the main pathway is through food intake.11 The elimination half-life of PFASs in the human body is 2.7 years for perfluorooctanoic acid (PFOA), 3.4 years for perfluorooctanesulfonic acid (PFOS), and 5.3 years for perfluorohexanesulfonic acid (PFHxS), which is considerably long.12 Various symptoms may be induced with long-term persistence of PFASs in the body, from developmental toxicity to carcinogenicity, hepatotoxicity, reproductive toxicity, immunotoxicity, and hormone toxicity.1314
South Korea’s seafood consumption is one of the highest in Asia, and like ganjang-gejang (soy sauce marinated crab), there is a recipe for eating the intestines of crustaceans.1516 So far, few large-scale studies in South Korea have investigated the association between crustacean consumption and serum PFAS. Thus, this study aimed to determine the association between crustacean consumption and serum concentrations of PFASs in the Korean population using the 4th cycle data (2018–2020) of the Korean National Environmental Health Survey (KoNEHS).
METHODS
Study participants
This study used the KoNEHS data collected between 2018 and 2020. 4,239 participants, who were aged ≥ 19 years were selected. The KoNEHS is a national monitoring program that has been conducted by the Ministry of Environment and the National Institute of Environmental Research in 3-year intervals since 2009.17 Those with missing values on the main variables of this study were excluded. After excluding 1,246 participants, 2,993 individuals were included in the analysis (Fig. 1).
Serum PFAS concentration
Investigated in KoNEHS data were 5 PFAS types: PFOA, PFOS, PFHxS, perfluorononanoic acid (PFNA), and perfluorodecanoic acid (PFDeA). Blood samples were collected in a container and stored in a −70°C freezer.17 After protein precipitation via centrifugation and removal of, and using the Q-sight Triple Quad High-Performance Liquid Chromatography/Mass Spectrometer (PerkinElmer, Waltham, MA, USA), serum PFASs were isolated and quantitatively analyzed.17 The limit of detection (LOD) in this study was as follows: PFOA 0.071 μg/L, PFOS 0.056 μg/L, PFHxS 0.071 μg/L, PFNA 0.019 μg/L, and PFDeA 0.017 μg/L.17 In this way, serum PFAS concentration was divided into quartiles, and participants were divided into the low-concentration group (LC) and the high-concentration group (HC) based on the 50th percentile concentration.18
Consumption of crustaceans
The question on crustacean consumption in the KoNEHS is on the following frequency scale: rarely, once a month, 2 to 3 times a month, once a week, 2 to 3 times a week, 4 to 6 times a week, once a day, twice a day, and 3 times a day. The survey about crustacean consumption was conducted from year 2018 to 2020.17 In this study, responses of rarely, once a month, and 2 to 3 times a month were grouped as < once a week consumption, and those of once a week, 2 to 3 times a week, four to 6 times a week, once a day, twice a day, and 3 times a day were grouped as ≥ once a week consumption.19
Potential confounders
The confounders in this study were set as follows: general characteristics, including age, body mass index (BMI), marital status, smoking, the usage of products containing PFASs, food and water intake, and ventilation time. To exclude additional PFAS exposure other than crustacean consumption, the usage of products known to contain PFASs for waterproofing or anti-stick purposes, which leads to exposure via oral or dermal was included.1120 Those are, coated frying pans, coated pots, coated electric cookers, coated containers, hiking suits, hiking boots and sneakers, disposable paper cups, hair products, make-up products, and ultraviolet (UV) block sunscreen.2112021 The food and water intake items included seafood, the type of indoor or outdoor water drinking, and the average ventilation time per day. 211 Consumption of grilled meat and grilled fish was included because frying or grilling can increase the total PFAS, while popcorn and hamburger-pizza-chicken consumption was included because PFAS is used in packages.2223
Statistical analysis
Since previous studies recommended separating the analysis of males and females, we stratified the analysis according to the sex of the participants.24 An independent t-test and χ2 test were employed to compare serum PFAS concentrations, general characteristics, dietary factors, coated product usage, and personal care product usage. The odds ratio (OR) of serum PFAS concentration against crustacean consumption was estimated via logistic regression analysis after adjustments for general characteristics, dietary factors, coated product usage, and personal care product usage. In this study, a complex sample analysis was performed, including stratification, clustering, and weighting.17 In all analyses, IBM SPSS version 28 for Windows (IBM Corp., Armonk, NY, USA) was used, and statistical significance was set at p < 0.05.
Ethics statement
This study received approval from the Institutional Review Board of Soonchunhyang University Gumi Hospital (IRB No.2023-12-02).
RESULTS
Table 1 describes the general characteristics of the study participants. Among 2,993 participants, 1,298 (43%) were males, and 1,695 (57%) were females. The mean concentrations of PFOA, PFOS, PFHxS, PFNA, and PFDeA were consistently higher in males than in females. Males exhibited higher consumption of large fish and tuna, fish, and seaweeds, and disposable paper cups. Conversely, females showed higher usage frequency of hair products, make-up products, and UV block sunscreen.
Tables 2 and 3 show the distribution of serum PFASs according to the tested variables, with the participants divided into the HC and LC based on the 50th percentile concentrations of serum PFOA, PFOS, PFHxS, PFNA, and PFDeA. For all PFASs; PFOA, PFOS, PFHxS, PFNA, and PFDeA, the average age of males was higher in the HC. Males in the HC had higher percentages when frequently using a coated frying pan or with ≥ once a week crustaceans, shellfish, or seaweed consumption than those with < once a week consumption. Females in the HC had higher percentages when using a coated agent or polish or hiking suit or boots once or more in 1 week and those with ≥ once a week consumption of fish, shellfish, or seaweeds. In both males and females, HC percentages were higher for those consuming groundwater or tap water for drinking compared to those drinking purified or mineral water.
Table 4 describes the results of multiple logistic regression analysis, indicating the association between crustacean consumption and serum PFAS concentration in males and females. The OR was higher in males with ≥once a week crustacean consumption than those with < once a week consumption: PFOA 1.57 (95% CI: 0.85–2.90), PFOS 0.94 (95% CI: 0.71–1.25), PFHxS 2.15 (95% CI: 1.53–3.02), PFNA 1.23 (95% CI: 1.07–1.41), and PFDeA 1.42 (95% CI: 1.17–1.74). The OR was higher in females with ≥ once a week crustacean consumption: PFOA 1.48 (95% CI: 1.19–1.84), PFOS 1.39 (95% CI: 1.27–1.52), PFHxS 1.56 (95% CI: 0.68–3.57), PFNA 1.70 (95% CI: 1.29–2.26), and PFDeA 1.43 (95% CI: 1.32–1.54).
DISCUSSION
This study demonstrated that the OR for the HC of serum PFASs was higher in individuals with ≥once a week crustacean consumption than in those with < once a week crustacean consumption. PFASs exhibit developmental toxicity, carcinogenicity, hepatotoxicity, reproductive toxicity, immunotoxicity, neurotoxicity, and hormone toxicity.132526 PFOS, PFOA, PFHxS, PFNA, and PFDeA decrease neonatal antibody concentration;27 PFOA, PFNA, and PFDeA cause congenital hypothyroidism;28 PFOA and PFOS increase LDL cholesterol, total cholesterol, and ALT while suppressing antibody responses t, vaccines.25 PFOA and PFOS are associated with testicular cancer, kidney cancer, and low birth weight infants.2930 Furthermore, PFOA is associated with ulcerative colitis, thyroid disease, and pregnancy-induced hypertension, and PFHxS is associated with developmental disability.31323334
PFASs are mainly released to the marine environment from industrial and urban wastewater treatment plants.35 From the treatment plants, wastewater with incomplete removal of PFASs is released to river and ultimately flows into seawater.36 For this reason, rivers are considered the main source of PFASs in the marine environment.37 Among different PFASs, PFOA, PFOS, PFNA, PFHxS, and PFDeA (C ≥ 6) which has a linear isomer or long carbon chain exhibit high hydrophobicity to be present abundantly in seawater sediments.3839 With thermal and chemical stability conferred by the strong C-F bond, PFASs are not readily degraded in the natural environment.1 The half-life of PFOS in underwater environment is 41 years and that of PFOA is 92 years, which is considerably longer in comparison.40 Hence, PFASs, once released into seawater, can persist for a long time without degradation to continuously exert negative effects on marine ecosystems.
A study on marine organisms collected from an urban estuary and a nearby coastal area in Rhodes Island, U.S., revealed a high concentration of PFASs found in crustaceans.41 In Tunisia, it was found that the sum of 8 kinds of PFAS was the highest in crustaceans (2.24 ng/g dry weight [dw]), followed by fish (0.751 ng/g dw), and mollusk (0.510 ng/g dw).42 In a study on seafood in a coastal area on the northeastern side of Brazil, PFOS concentration was the highest in shrimps.43 In a study examining the Bohai Sea in China, the total PFAS was 4.64 μg/kg in crustaceans, 1.82 μg/kg in fish, and 1.40 μg/kg in cephalopods.8 Total PFAS concentration varies where the habitat is, for example, Mexican crab shows 0.16–0.37 μg/kg, while Indonesian crab shows 0.6–2.2 μg/kg of total PFAS concentration.44 Crustaceans feed on PFAS-contaminated sediments, resulting in a higher level of PFAS exposure.1044
Once absorbed through the gill and food intake by crustaceans, PFASs accumulate in the hepatopancreas, which is responsible for absorbing and storing nutrients.4546 Long-chain PFASs accumulate at a high density in hepatopancreas due to high affinity to liver fatty acid binding proteins.945 In a study on Chinese mitten crab, high levels of perfluorododecanoic acid, perfluorotridecanoic acid, and perfluorotetradecanoic acid were observed in the hepatopancreas compared to muscle or shell tissues.9 In a study on PFOS in the crabs of the Bohai Sea in China, the PFOS concentration was higher in the intestines at 105 ng/g than in other parts at 1.17 ng/g.4748 In a study conducted in Spain, the total concentration of PFASs was higher in the head of crustaceans, where the hepatopancreas is located.49 In previous study, the correlation between crustacean intestine consumption and blood cadmium level was already shown.15 For humans, PFAS exposure increases as the consumption of flesh and intestines of crustaceans increases.
The PFAS exposure pathways in the human body include oral intake, dust inhalation, and skin contact, while the main pathway is through food intake.11 A study analyzing the statistical data of the National Health and Nutrition Examination Survey in the U.S. reported that the concentrations of serum PFOA, PFOS, PFHxS, perfluoroundecanoic acid, PFNA, and PFDeA increased after crab consumption.50 A study conducted in Japan verified the association between crab or shrimp consumption and increased levels of PFOS and PFOA in blood.51 The largest proportion of PFASs (86%) absorbed via food intake is through seafood, especially fish and crustaceans which are the main causes of PFAS exposure.52 Currently, the European Food Safety Authority set the tolerable weekly intake of 4.4 ng/kg bw per week.25
PFASs consist of 2 parts: the anionic head and the aliphatic tail.53 These 2 parts exhibit strong binding with albumin, while they migrate to various organs via blood.4547 As they reach the liver, PFASs accumulate inside hepatocytes through binding with liver fatty acid binding proteins.4554 In the kidney, PFASs released in urine are reabsorbed by the organic anion transporter 4, and in the small intestine, PFASs are reabsorbed by organic anion transporting polypeptide, sodium taurocholate co-transporting polypeptide, and apical sodium-dependent bile acid transporter to remain in the body for long.45555657 The elimination half-life of PFASs in the human body is 2.7 years for PFOA, 3.4 years for PFOS, and 5.3 years for PFHxS.12 As a result, continuous consumption of crustaceans can cause prolonged effects of PFASs in the human body. Additionally, PFOA, PFOS, PFHxS, PFNA, and PFDeA can serve as key indicators in assessing PFAS exposure associated with crustacean consumption.
This study has limitations. First, the causality remains unidentified as this study was a cross-sectional study. Second, due to the COVID-19 pandemic, the KoNEHS in 2020 had been conducted using non-face-to-face methods and the number of participants in blood analysis was small. Third, the possibility of occupational exposure, such as work environment and use of protective gear, had not been taken into account. Fourth, since the data has only 5 kinds of PFASs in the KoNEHS 4th cycle, other types of PFAS frequently used nowadays were not accounted for.58 Fifth, it was impossible to identify the total PFAS concentration of crustacean in the KoNEHS 4th cycle. Finally, the comparison in this study was based on the frequency of crustacean consumption, the data of which were obtained through recall, implying potential recall bias.
So far, few large-scale studies have been conducted on the association between crustacean consumption and serum PFASs in the Korean population. This study is significant in exploring the association between crustacean consumption and concentrations of serum PFASs by analyzing the data of samples representing the general population of South Korea. Considering that the toxicity of PFASs in the human body is well-known, research on the amount of crustacean consumption which can affect human health, and periodic monitoring is necessary regarding the PFAS concentration in crustaceans.
CONCLUSIONS
This study revealed the association between crustacean consumption and concentrations of serum PFASs in general Korean population. Periodic monitoring of PFAS concentration in crustaceans is needed due to toxicity of PFAS on human.
Acknowledgements
This study used the Korean National Environmental Health Survey cycle 4 (2018–2020), made by National Institute of Environmental Research (NIER-2020-01-01-016). We appreciate National Institute of Environmental Research for making the raw data of Korean National Environmental Health Survey available.
Notes
Funding: This research was supported by the Soonchunhyang University Research Fund and Inha University Hospital’s Environmental Health Center for Training Environmental Medicine Professional funded by the Ministry of Environment, Republic of Korea (2024).
Competing interests: The authors declare that they have no competing interests.
Author contributions:
Conceptualization: Huh SW, Cho SY.
Data curation: Huh SW, Kim KW, Kang JS.
Formal analysis: Huh SW, Park HW.
Investigation: Cho SY.
Methodology: Yoon SY.
Software: Huh SW, Cho SY, Kang JS.
Validation: Huh SW, Cho SY, Kim DH Writing - original draft.
Writing - review & editing: Huh SW, Cho SY.
Abbreviations
AFFF
aqueous film forming foam
BMI
body mass index
CI
confidence interval
dw
dry weight
HC
high-concentration group
KoNEHS
Korean National Environmental Health Survey
LC
low-concentration group
LOD
limit of detection
OR
odds ratio
PFAS
perfluoroalkyl substance
PFDeA
perfluorodecanoic acid
PFHxS
perfluorohexanesulfonic acid
PFNA
perfluorononanoic acid
PFOA
perfluorooctanoic acid
PFOS
perfluorooctanesulfonic acid
UV
ultraviolet