Abstract
Red swamp crayfish (Procambarus clarkia) is an exposed species to heavy metals due to their lifestyle of direct contact with sediments. Based on the complete crayfish industry, we focus on the presence of heavy metals in crayfish from different circulation links, which provides a new idea for the investigation of heavy metals in food. To analyze the exposure levels of heavy metals in crayfish during aquaculture and circulation, the five elements (Cd, Pb, Hg, Cr, Cu) in crayfish from 126 sampling sites were investigated. Cultured environmental samples were collected for Spearman correlation analysis. Monte Carlo simulation was used to analyze the uncertain health risks of heavy metals in crayfish. The results indicated that the average heavy metal concentrations in crayfish were all below the limit threshold values. The hepatopancreas was the main target organ for heavy metal accumulation (Cd: 0.3132 mg/kg; Pb: 0.0258 mg/kg; Hg: 0.0072 mg/kg; Cr: 0.1720 mg/kg; Cu: 10.6816 mg/kg). The positive correlation of heavy metal content between crayfish and sediments was not significant under the crayfish-rice coculture model. The 95th HI values for adults and children ranged from 0.022 to 0.042 and 0.071 to 0.137, well below 1, indicating that heavy metals do not pose a noncarcinogenic risk to humans. The potential carcinogenic risk of Cd and Cr in crayfish should be taken seriously, as the 95th CR values for children have reached 4.299 × 10−5 and 6.509 × 10−5, respectively.
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The data presented in this study are available on request from the corresponding author.
References
Yue GH, Li J, Bai Z, Wang CM, Feng F (2010) Genetic diversity and population structure of the invasive alien red swamp crayfish. Biol Invasions 12(8):2697–2706. https://doi.org/10.1007/s10530-009-9675-1
Barbaresi S, Santini G, Tricarico E, Gherardi F (2004) Ranging behaviour of the invasive crayfish, Procambarus clarkii (Girard). J Nat Hist 38(22):2821–2832. https://doi.org/10.1080/00222930410001663308
Li Y, Guo X, Cao X, Deng W, Luo W, Wang W (2012) Population genetic structure and post-establishment dispersal patterns of the red swamp crayfish Procambarus clarkii in China. Plos One. 7(7):e40652. https://doi.org/10.1371/journal.pone.0040652
MARA (2022) China crayfish industry development report. Ministry of Agriculture and Rural Affairs of the People’s Republic of China 990(12)
Tan Y, Peng B, Wu Y, **ong L, Sun J, Peng G, Bai X (2021) Human health risk assessment of toxic heavy metal and metalloid intake via consumption of red swamp crayfish (Procambarus clarkii) from rice-crayfish co-culture fields in China. Food Control. 128:108181. https://doi.org/10.1016/j.foodcont.2021.108181
Yi S, Li Y, Shi L, Zhang L, Li Q, Chen J (2018) Characterization of population genetic structure of red swamp crayfish, Procambarus clarkii. China Scientific Reports 8(1):5586. https://doi.org/10.1038/s41598-018-23986-z
Colin N, Maceda-Veiga A, Flor-Arnau N, Mora J, Fortuño P, Vieira C, Prat N, Cambra J, de Sostoa A (2016) Ecological impact and recovery of a Mediterranean river after receiving the effluent from a textile dyeing industry. Ecotoxicol Environ Saf 132:295–303. https://doi.org/10.1016/j.ecoenv.2016.06.017
Devi M, Thomas DA, Barber JT, Fingerman M (1996) Accumulation and physiological and biochemical effects of cadmium in a simple aquatic food chain. Ecotoxicol Environ Saf 33(1):38–43. https://doi.org/10.1006/eesa.1996.0004
Kouba A, Buřič M, Kozák P (2010) Bioaccumulation and effects of heavy metals in crayfish: a review. Water Air Soil Pollut 211(1):5–16. https://doi.org/10.1007/s11270-009-0273-8
Kim J-J, Kim Y-S, Kumar V (2019) Heavy metal toxicity: an update of chelating therapeutic strategies. J Trace Elem Med Biol 54:226–231. https://doi.org/10.1016/j.jtemb.2019.05.003
AtiqueUllah AKM, Akter M, Musarrat M, Quraishi SB (2019) Evaluation of possible human health risk of heavy metals from the consumption of two marine fish species Tenualosa ilisha and Dorosoma cepedianum. Biol Trace Elem Res 191(2):485–494. https://doi.org/10.1007/s12011-018-1616-3
Pigna M, Caporale AG, Cavalca L, Sommella A, Violante A (2015) Arsenic in the soil environment: mobility and phytoavailability. Environ Eng Sci 32(7):551–563. https://doi.org/10.1089/ees.2015.0018
Zhang M, He P, Qiao G, Huang J, Yuan X, Li Q (2019) Heavy metal contamination assessment of surface sediments of the Subei Shoal, China: spatial distribution, source apportionment and ecological risk. Chemosphere. 223:211–222. https://doi.org/10.1016/j.chemosphere.2019.02.058
Jia Y, Wang L, Qu Z, Wang C, Yang Z (2017) Effects on heavy metal accumulation in freshwater fishes: species, tissues, and sizes. Environ Sci Pollut Res 24(10):9379–9386. https://doi.org/10.1007/s11356-017-8606-4
Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Med Toxicol 1(1):22. https://doi.org/10.1186/1745-6673-1-22
Sundseth K, Pacyna JM, Pacyna EG, Pirrone N, Thorne RJ (2017) Global sources and pathways of mercury in the context of human health. Int J Environ Res Public Health 14(1):105
Lippert J, Montgomery J, DeMarco C (2020) Lead health fairs: a community-based approach to addressing lead exposure in Chicago. Health Educ Behav 48(6):758–768. https://doi.org/10.1177/1090198120954359
Mo A, Huang Y, Gu Z, Liu C, Wang J, Yuan Y (2022) Health risk assessment and bioaccumulation of heavy metals in Procambarus clarkii from six provinces of China. Environ Sci Pollut Res 29(2):2539–2546. https://doi.org/10.1007/s11356-021-15855-6
Ni L, Chen D, Fu H, **e Q, Lu Y, Wang X, Zhao Y, Chen L (2021) Residual levels of antimicrobial agents and heavy metals in 41 species of commonly consumed aquatic products in Shanghai, China, and cumulative exposure risk to children and teenagers. Food Control. 129:108225. https://doi.org/10.1016/j.foodcont.2021.108225
Liu Y, Fu Q, Gao J, Xu WG, Yin B, Cao YQ, Qin WH (2013) Concentrations and safety evaluation of heavy metals in aquatic products of Yancheng, Jiangsu Province. Huan **g Ke Xue 34(10):4081–4089
Wang X, Wu J, Yu B, Dong KF, Ma D, **ao G, Zhang C (2020) Heavy metals in aquatic products and the health risk assessment to population in China. Environ Sci Pollut Res 27(18):22708–22719. https://doi.org/10.1007/s11356-020-08685-5
Ariano A, Scivicco M, D’Ambola M, Velotto S, Andreini R, Bertini S, Zaccaroni A, Severino L (2021) Heavy metals in the muscle and hepatopancreas of red swamp crayfish (Procambarus clarkii) in Campania (Italy). Animals 11(7):1933
Antón A, Serrano T, Angulo E, Ferrero G, Rallo A (2000) The use of two species of crayfish as environmental quality sentinels: the relationship between heavy metal content, cell and tissue biomarkers and physico-chemical characteristics of the environment. Sci Total Environ 247(2):239–251. https://doi.org/10.1016/S0048-9697(99)00493-3
Nakayama SMM, Ikenaka Y, Muzandu K, Choongo K, Oroszlany B, Teraoka H, Mizuno N, Ishizuka M (2010) Heavy metal accumulation in lake sediments, fish (Oreochromis niloticus and Serranochromis thumbergi), and crayfish (Cherax quadricarinatus) in Lake Itezhi-tezhi and Lake Kariba, Zambia. Arch Environ Contam Toxicol 59(2):291–300. https://doi.org/10.1007/s00244-010-9483-8
Shui Y, **e J, Zhou Y, Li J, Gan J (2020) Molecular characterization of p38 MAPK and tissue-specific expression under cadmium stress in red swamp crayfish (Procambarus clarkii). Sci Total Environ. 720:137325. https://doi.org/10.1016/j.scitotenv.2020.137325
Zhang Y, Li Z, Kholodkevich S, Sharov A, Feng Y, Ren N, Sun K (2019) Cadmium-induced oxidative stress, histopathology, and transcriptome changes in the hepatopancreas of freshwater crayfish (Procambarus clarkii). Sci Total Environ 666:944–955. https://doi.org/10.1016/j.scitotenv.2019.02.159
Peng F, Li J, Gong Z, Yue B, Wang X, Manyande A, Du H (2022) Investigation of bioaccumulation and human health risk assessment of heavy metals in crayfish (Procambarus clarkii) farming with a rice-crayfish-based coculture breeding modes. Foods 11(3). https://doi.org/10.3390/foods11030261
**ong B, Xu T, Li R, Johnson D, Ren D, Liu H, ** Y, Huang Y (2020) Heavy metal accumulation and health risk assessment of crayfish collected from cultivated and uncultivated ponds in the Middle Reach of Yangtze River. Sci Total Environ 739:139963. https://doi.org/10.1016/j.scitotenv.2020.139963
Ning K, Ji L, Zhang L, Zhu X, Wei H, Han M, Wang Z (2022) Is rice-crayfish co-culture a better aquaculture model: From the perspective of antibiotic resistome profiles. Environ Pollut 292:118450. https://doi.org/10.1016/j.envpol.2021.118450
**ong B, Xu T, Li R, Johnson D, Ren D, Liu H, ** Y, Huang Y (2020) Heavy metal accumulation and health risk assessment of crayfish collected from cultivated and uncultivated ponds in the Middle Reach of Yangtze River. Sci Total Environ. 739:139963. https://doi.org/10.1016/j.scitotenv.2020.139963
Karami MA, Fakhri Y, Rezania S, Alinejad AA, Mohammadi AA, Yousefi M, Ghaderpoori M, Saghi MH, Ahmadpour M (2019) Non-carcinogenic health risk assessment due to fluoride exposure from tea consumption in iran using Monte Carlo simulation. Int J Environ Res Public Health 16(21):4261
FAOSTAT: https://www.fao.org/faostat/en/#data/CL.
Adebiyi FM, Ore OT, Ogunjimi IO (2020) Evaluation of human health risk assessment of potential toxic metals in commonly consumed crayfish (Palaemon hastatus) in Nigeria. Heliyon. 6(1):e03092. https://doi.org/10.1016/j.heliyon.2019.e03092
USEPA (2000) Guidance for assessing chemical contaminant data for use in fish advisories volume 3, overview of risk management. United States Environmental Protection Agency. https://www.epa.gov/fish-tech/epa-guidance-develo**-fish-advisories
Bonsignore M, Salvagio Manta D, Mirto S, Quinci EM, Ape F, Montalto V, Gristina M, Traina A, Sprovieri M (2018) Bioaccumulation of heavy metals in fish, crustaceans, molluscs and echinoderms from the Tuscany coast. Ecotoxicol Environ Saf 162:554–562. https://doi.org/10.1016/j.ecoenv.2018.07.044
Liu X, Han H, Xu H, Zhang H, Fang M, Wang Q, Li J, Wu Y, Gong Z (2022) Integration of probabilistic exposure assessment and risk characterization for perchlorate in infant formula and supplementary food. Food Chem Toxicol 168:113347. https://doi.org/10.1016/j.fct.2022.113347
WHO (1989) Environmental health criteria. World Health Organization. https://www.who.int/publications/i/item/9789241572408
Mo A, Dang Y, Wang J, Liu C, Yang H, Zhai Y, Wang Y, Yuan Y (2022) Heavy metal residues, releases and food health risks between the two main crayfish culturing models: rice-crayfish coculture system versus crayfish intensive culture system. Environ Pollut. 305:119216. https://doi.org/10.1016/j.envpol.2022.119216
Peng Q, Nunes LM, Greenfield BK, Dang F, Zhong H (2016) Are Chinese consumers at risk due to exposure to metals in crayfish? A bioaccessibility-adjusted probabilistic risk assessment. Environ Int 88:261–268. https://doi.org/10.1016/j.envint.2015.12.035
Gedik K, Kongchum M, DeLaune RD, Sonnier JJ (2017) Distribution of arsenic and other metals in crayfish tissues (Procambarus clarkii) under different production practices. Sci Total Environ 574:322–331. https://doi.org/10.1016/j.scitotenv.2016.09.060
Li J, Du H, Peng F, Manyande A, **ong S (2022) Evaluation of the effect of different cooking methods on the heavy metal levels in crayfish muscle. Biol Trace Elem Res. https://doi.org/10.1007/s12011-022-03476-0
Ashraf W (2005) Accumulation of heavy metals in kidney and heart tissues of epinephelus microdon fish from the Arabian gulf. Environ Monit Assess 101(1):311–316. https://doi.org/10.1007/s10661-005-0298-4
Nędzarek A, Czerniejewski P, Tórz A (2019) Macro- and trace elements in Chinese mitten crabs (Eriocheir sinensis) from Szczecin Lagoon, Poland – implications for human health. Aquaculture. 506:229–237. https://doi.org/10.1016/j.aquaculture.2019.03.042
Nędzarek A, Czerniejewski P, Tórz A (2020) Macroelements and trace elements in invasive signal crayfish (Pacifastacus leniusculus) from the Wieprza River (Southern Baltic): human health implications. Biol Trace Elem Res 197(1):304–315. https://doi.org/10.1007/s12011-019-01978-y
Çoğun HY, Firat Ö, Aytekin T, Firidin G, Firat Ö, Varkal H, Temiz Ö, Kargin F (2017) Heavy metals in the blue crab (Callinectes sapidus) in Mersin Bay, Turkey. Bull Environ Contam Toxicol 98(6):824–829. https://doi.org/10.1007/s00128-017-2086-6
Karar S, Hazra S, Das S (2019) Assessment of the heavy metal accumulation in the Blue Swimmer Crab (Portunus pelagicus), northern Bay of Bengal: Role of salinity. Mar Pollut Bull 143:101–108. https://doi.org/10.1016/j.marpolbul.2019.04.033
Alcorlo P, Otero M, Crehuet M, Baltanás A, Montes C (2006) The use of the red swamp crayfish (Procambarus clarkii, Girard) as indicator of the bioavailability of heavy metals in environmental monitoring in the River Guadiamar (SW, Spain). Sci Total Environ 366(1):380–390. https://doi.org/10.1016/j.scitotenv.2006.02.023
Mistri M, Munari C, Pagnoni A, Chenet T, Pasti L, Cavazzini A (2020) Accumulation of trace metals in crayfish tissues: is Procambarus clarkii a vector of pollutants in Po Delta inland waters? Eur Zool J 87(1):46–57. https://doi.org/10.1080/24750263.2020.1717653
Ling MP, Wu CC, Yang KR, Hsu HT (2013) Differential accumulation of trace elements in ventral and dorsal muscle tissues in tilapia and milkfish with different feeding habits from the same cultured fishery pond. Ecotoxicol Environ Saf 89:222–230. https://doi.org/10.1016/j.ecoenv.2012.12.002
Baki MA, Hossain MM, Akter J, Quraishi SB, HaqueShojib MF, AtiqueUllah AKM, Khan MF (2018) Concentration of heavy metals in seafood (fishes, shrimp, lobster and crabs) and human health assessment in Saint Martin Island Bangladesh. Ecotoxicol Environ Saf 159:153–163. https://doi.org/10.1016/j.ecoenv.2018.04.035
Tian Y, Xu H, Liu S, Fang M, Wu Y, Gong Z (2020) Study on the bioaccessibility and bioavailability of perchlorate in different food matrices in vitro. Food Chem 333:127470. https://doi.org/10.1016/j.foodchem.2020.127470
**ao X, Zhang J, Wang H, Han X, Ma J, Ma Y, Luan H (2020) Distribution and health risk assessment of potentially toxic elements in soils around coal industrial areas: a global meta-analysis. Sci Total Environ 713:135292. https://doi.org/10.1016/j.scitotenv.2019.135292
Varol M (2019) Arsenic and trace metals in a large reservoir: seasonal and spatial variations, source identification and risk assessment for both residential and recreational users. Chemosphere 228:1–8. https://doi.org/10.1016/j.chemosphere.2019.04.126
Li Y, Wang X, Du H, **ao G, Guo L (2021) Heavy metal accumulation and health risk assessment of crayfish in the middle and lower reaches of Yangtze River during 2015–2017. Environ Monit Assess 194(1):24. https://doi.org/10.1007/s10661-021-09652-4
Hwang IM, Ha J-H (2021) Human health risk assessment of toxic elements in South Korean cabbage, Kimchi, using Monte Carlo simulations. J Food Compos Anal 102:104046. https://doi.org/10.1016/j.jfca.2021.104046
Shi H, Zeng M, Peng H, Huang C, Sun H, Hou Q, Pi P (2022) Health risk assessment of heavy metals in groundwater of Hainan Island using the Monte Carlo simulation coupled with the APCS/MLR model. Int J Environ Res Public Health 19(13). https://doi.org/10.3390/ijerph19137827
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This study was supported by the National Natural Science Foundation of China (Grant No. 32001772), the Hubei Key Laboratory for Processing and Transformation of Agricultural Products (Wuhan Polytechnic University) (Grant No. 2018HBSQGDKFA02), and the “Thirteenth Five-Year” National Key Research and Development Program of China (No. 2019YFC1606003).
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Bingjie Zhou: collected the samples, analyzed the data, and wrote and edited the draft. **aoyu Zeng: collected the samples, and analyzed the data. Qiao wang: collected the samples. Yan Liu: designed research. **n Liu: designed research. Yongning Wu: contributed to the design of the study. Zhiyong Gong: contributed to the design of the study, and revised the manuscript. Min Fang: contributed to the design of the study, and revised the manuscript.
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Zhou, B., Zeng, X., Wang, Q. et al. Exposure and Health Risk Assessment of Heavy Metal in Crayfish from the Middle and Lower Reaches of the Yangtze River. Biol Trace Elem Res 202, 332–345 (2024). https://doi.org/10.1007/s12011-023-03672-6
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DOI: https://doi.org/10.1007/s12011-023-03672-6