Tissue Distribution and Whole Body Burden of the Chlorinated Polyfluoroalkyl Ether Sulfonic Acid F-53B in Crucian Carp (Carassius carassius): Evidence for a Highly Bioaccumulative Contaminant of Emerging Concern

Environmental Science and Technology

Volumn 49, Issue 24, 2015, Pages 14156-14165

  Shi, Yali ^a   Vestergren, Robin ^b   Zhou, Zhen ^c   Song, Xiaowei ^a   Xu, Lin ^a   Liang, Yong ^c   Cai, Yaqi ^a,c  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c JIANGHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BARIUM COMPOUNDS; BIOACCUMULATION; BIOCHEMISTRY; ETHERS; LAKE POLLUTION; TISSUE;

BIOACCUMULATION FACTOR; BIOLOGICAL SAMPLES; CARASSIUS CARASSIUS; MEDIAN CONCENTRATION; POLYFLUOROALKYL SUBSTANCES; REGULATORY ACTIONS; TISSUE DISTRIBUTIONS; XIAOQING RIVERS;

RIVER POLLUTION;

POLYFLUOROALKYL ETHER SULFONIC ACID; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG; 2-((6-CHLORO-1,1,2,2,3,3,4,4,5,5,6,6-DODECAFLUOROHEXYL)OXY)-1,1,2,2-TETRAFLUOROETHANESULFONIC ACID; ALKANESULFONIC ACID; WATER POLLUTANT;

BIOACCUMULATION; CYPRINID; ECOTOXICOLOGY; ORGANOFLUORINE; PERSISTENT ORGANIC POLLUTANT;

ADULT; ANIMAL TISSUE; ARTICLE; BILE; BIOACCUMULATION; BLADDER; BODY BURDEN; BRAIN; CHLORINATION; CRUCIAN CARP; GILL; GONAD; HEART; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; KIDNEY; LIVER; MASS SPECTROMETRY; MUSCLE; NONHUMAN; TANDEM MASS SPECTROMETRY; TISSUE DISTRIBUTION; TISSUE SPECIFICITY; ANALYSIS; ANIMAL; CARP; CHEMISTRY; CHINA; FEMALE; LAKE; MALE; METABOLISM; PHARMACOKINETICS; PROCEDURES; RIVER; WATER POLLUTANT;

CHINA; HUBEI; SHANDONG; TANGXUN LAKE; XIAOQING RIVER;

CARASSIUS; CARASSIUS CARASSIUS;

ALKANESULFONATES; ANIMALS; BODY BURDEN; CARPS; CHINA; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FEMALE; LAKES; MALE; RIVERS; TANDEM MASS SPECTROMETRY; TISSUE DISTRIBUTION; WATER POLLUTANTS, CHEMICAL;

EID: 84950115712     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b04299     Document Type: Article

References (55)

1. Paul, A. G.; Jones, K. C.; Sweetman, A. J. A. First global production, emission, and environmental inventory for perfluorooctane sulfonate Environ. Sci. Technol. 2009, 43 (2) 386-392 10.1021/es802216n
2. Wang, Z.; Cousins, I. T.; Scheringer, M.; Buck, R. C.; Hungerbühler, K. Global emission inventories for C4-C14 perfluoroalkyl carboxylic acid (PFCA) homologues from 1951 to 2030, Part I: production and emissions from quantifiable sources Environ. Int. 2014, 70, 62-75 10.1016/j.envint.2014.04.013
3. Buck, R. C.; Franklin, J.; Berger, U.; Conder, J. M.; Cousins, I. T.; de Voogt, P.; Jensen, A. A.; Kannan, K.; Mabury, S. A.; van Leeuwen, S. P. J. Perfluoroalkyl and polyfluoroalkyl substances in the environment: terminology, classification, and origins Integr. Environ. Assess. Manage. 2011, 7 (4) 513-541 10.1002/ieam.258
4. Bowman, J. S. Fluorotechnology is critical to modern life: The FluoroCouncil counterpoint to the Madrid Statement Environ. Health Perspect. 2015, 123 (5) A112-A113 10.1289/ehp.1509910
5. Giesy, J. P.; Kannan, K. Global distribution of perfluorooctane sulfonate in wildlife Environ. Sci. Technol. 2001, 35 (7) 1339-1342 10.1021/es001834k
6. Hansen, K. J.; Clemen, L. A.; Ellefson, M. E.; Johnson, H. O. Compound-specific, quantitative characterization of organic fluorochemicals in biological matrices Environ. Sci. Technol. 2001, 35 (4) 766-770 10.1021/es001489z
7. Lindstrom, A. B.; Strynar, M. J.; Libelo, E. L. Polyfluorinated compounds: Past, present, and future Environ. Sci. Technol. 2011, 45 (19) 7954-7961 10.1021/es2011622
8. 3M Company. 3M Phasing Out Some of its Specialty Materials; 2000. http://www.fluoridealert.org/wp-content/pesticides/3m.may16.2000.press.release.pdf.
9. United Nations Environment Programme. Governments unite to step-up reduction on global DDT reliance and add nine new chemicals under international treaty; UNEP, 2009. http://chm.pops.int/Convention/PressreleaseCOP4Geneva8May2009/tabid/542/language/en-US/Default.aspx.
10. U.S. Environmental Protection Agency. 2010/15 PFOA Stewardship Program; 2006. http://www.epa.gov/opptintr/pfoa/pubs/pfoastewardship.htm.
11. Calafat, A. M.; Wong, L. Y.; Kuklenyik, Z.; Reidy, J. A.; Needham, L. L. Polyfluoroalkyl chemicals in the US population: Data from the national health and nutrition examination survey (NHANES) 2003-2004 and comparisons with NHANES 1999-2000 Environ. Health Perspect. 2007, 115 (11) 1596-1602 10.1289/ehp.10598
12. Glynn, A.; Berger, U.; Bignert, A.; Ullah, S.; Aune, M.; Lignell, S.; Darnerud, P. O. Perfluorinated alkyl acids in blood serum from primiparous women in Sweden: Serial sampling during pregnancy and nursing, and temporal trends 1996-2010 Environ. Sci. Technol. 2012, 46 (16) 9071-9079 10.1021/es301168c
13. Gomis, M. I.; Wang, Z.; Scheringer, M.; Cousins, I. T. A modeling assessment of the physicochemical properties and environmental fate of emerging and novel per- and polyfluoroalkyl substances Sci. Total Environ. 2015, 505, 981-991 10.1016/j.scitotenv.2014.10.062
14. Wang, S.; Huang, J.; Yang, Y.; Hui, Y.; Ge, Y.; Larssen, T.; Yu, G.; Deng, S.; Wang, B.; Harman, C. First report of a Chinese PFOS alternative overlooked for 30 years: Its toxicity, persistence, and presence in the environment Environ. Sci. Technol. 2013, 47 (18) 10163-10170 10.1021/es401525n
15. Ruan, T.; Lin, Y.; Wang, T.; Liu, R.; Jiang, G. Identification of novel polyfluorinated ether sulfonates as PFOS alternatives in municipal sewage sludge in China Environ. Sci. Technol. 2015, 49 (11) 6519-6527 10.1021/acs.est.5b01010
16. Conder, J. M.; Hoke, R. A.; Wolf, W. D.; Russell, M. H.; Buck, R. C. Are PFCAs bioaccumulative? A critical review and comparison with regulatory criteria and persistent lipophilic compounds Environ. Sci. Technol. 2008, 42 (4) 995-1003 10.1021/es070895g
17. Ng, C. A.; Hungerbuhler, K. Bioconcentration of perfluorinated alkyl acids: How important is specific binding? Environ. Sci. Technol. 2013, 47 (13) 7214-7223 10.1021/es400981a
18. Armitage, J. M.; Arnot, J. A.; Wania, F. Potential role of phospholipids in determining the internal tissue distribution of perfluoroalkyl acids in biota Environ. Sci. Technol. 2012, 46 (22) 12285-12286 10.1021/es304430r
19. Armitage, J. M.; Arnot, J. A.; Wania, F.; Mackay, D. Development and evaluation of a mechanistic bioconcentration model for ionogenic organic chemicals in fish Environ. Toxicol. Chem. 2013, 32 (1) 115-128 10.1002/etc.2020
20. Schmitt, W. General approach for the calculation of tissue to plasma partition coefficients Toxicol. In Vitro 2008, 22 (2) 457-467 10.1016/j.tiv.2007.09.010
21. Ng, C. A.; Hungerbuhler, K. Bioaccumulation of perfluorinated alkyl acids: Observations and models Environ. Sci. Technol. 2014, 48 (9) 4637-4648 10.1021/es404008g
22. Roche, H.; Buet, A.; Jonot, O.; Ramade, F. Organochlorine residues in european eel (Anguilla anguilla), crucian carp (Carassius carassius) and catfish (Ictalurus nebulosus) from Vaccarès lagoon (French National Nature Reserve of Camargue)-effects on some physiological parameters Aquat. Toxicol. 2000, 48, 443-459 10.1016/S0166-445X(99)00061-2
23. Zhou, Z.; Shi, Y.; Vestergren, R.; Wang, T.; Liang, Y.; Cai, Y. Highly elevated serum concentrations of perfluoroalkyl substances in fishery employees from Tangxun Lake, China Environ. Sci. Technol. 2014, 48 (7) 3864-3874 10.1021/es4057467
24. Zhou, Z.; Liang, Y.; Shi, Y.; Xu, L.; Cai, Y. Occurrence and transport of perfluoroalkyl acids (PFAAs), including short-chain PFAAs in Tangxun Lake, China Environ. Sci. Technol. 2013, 47 (16) 9249-9257 10.1021/es402120y
25. 51Cr- erythrocyte tracers Fish Physiol. Biochem. 1989, 6 (1) 39-47 10.1007/BF01875602
26. 109Cd in female zebrafish, Brachydanio rerio J. Fish Biol. 1985, 27 (5) 571-581 10.1111/j.1095-8649.1985.tb03202.x
27. Inoue, Y.; Hashizume, N.; Yakata, N.; Murakami, H.; Suzuki, Y.; Kikushima, E.; Otsuka, M. Unique physicochemical properties of perfluorinated compounds and their bioconcentration of common carp Cyprinus carpio L Arch. Environ. Contam. Toxicol. 2012, 62, 672-680 10.1007/s00244-011-9730-7
28. Martin, J. W.; Mabury, S. A.; Solomon, K. R.; Muir, D. C. G. Bioconcentration and tissue distribution of perfluorinated acids in rainbow trout (Oncorhynchus mykiss) Environ. Toxicol. Chem. 2003, 22 (1) 196-204 10.1002/etc.5620220126
29. Berger, U.; Kaiser, M. A.; Karrman, A.; Barber, J. L.; van Leeuwen, S. P. J. Recent developments in trace analysis of poly- and perfluoroalkyl substances Anal. Bioanal. Chem. 2011, 400 (6) 1625-1635 10.1007/s00216-011-4823-8
30. Benskin, J. P.; Ikonomou, M. G.; Woudneh, M. B.; Cosgrove, J. R. Rapid characterization of perfluoralkyl carboxylate, sulfonate, and sulfonamide isomers by high-performance liquid chromatography-tandem mass spectrometry J. Chromatogr. A 2012, 1247, 165-170 10.1016/j.chroma.2012.05.077
31. Wang, Z.; Cousins, I. T.; Scheringer, M.; Hungerbühler, K. Fluorinated alternatives to long-chain perfluoroalkyl carboxylic acids (PFCAs), perfluoroalkane sulfonic acids (PFSAs) and their potential precursors Environ. Int. 2013, 60, 242-248 10.1016/j.envint.2013.08.021
32. Shi, Y.; Vestergren, R.; Xu, L.; Song, X.; Niu, X.; Zhang, C.; Cai, Y. Characterizing direct emissions of perfluoroalkyl substances from ongoing fluoropolymer production sources: A spatial trend study of Xiaoqing River, China Environ. Pollut. 2015, 206, 104-112 10.1016/j.envpol.2015.06.035
33. Han, X.; Snow, T. A.; Kemper, R. A.; Jepson, G. W. Binding of perfluorooctanoic acid to rat and human plasma proteins Chem. Res. Toxicol. 2003, 16 (6) 775-781 10.1021/tx034005w
34. Bischel, H. N.; Macmanus-Spencer, L. A.; Luthy, R. G. Noncovalent interactions of long-chain perfluoroalkyl acids with serum albumin Environ. Sci. Technol. 2010, 44 (13) 5263-5269 10.1021/es101334s
35. Hebert, P. C.; MacManus-Spencer, L. A. Development of a fluorescence model for the binding of medium- to long-chain perfluoroalkyl acids to human serum albumin through a mechanistic evaluation of spectroscopic evidence Anal. Chem. 2010, 82 (15) 6463-6471 10.1021/ac100721e
36. Zhang, X.; Chen, L.; Fei, X. C.; Ma, Y. S.; Gao, H. W. Binding of PFOS to serum albumin and DNA: Insight into the molecular toxicity of perfluorochemicals BMC Mol. Biol. 2009, 10, 16 10.1186/1471-2199-10-16
37. Luebker, D. J.; Hansen, K. J.; Bass, N. M.; Butenhoff, J. L.; Seacat, A. M. Interactions of flurochemicals with rat liver fatty acid-binding protein Toxicology 2002, 176 (3) 175-185 10.1016/S0300-483X(02)00081-1
38. Zhang, L.; Ren, X. M.; Guo, L. H. Structure-based investigation on the interaction of perfluorinated compounds with human liver fatty acid binding protein Environ. Sci. Technol. 2013, 47 (19) 11293-11301 10.1021/es4026722
39. Lehmler, H.-J.; Bummer, P. M. Mixing of perfluorinated carboxylic acids with dipalmitoylphosphatidylcholine Biochim. Biophys. Acta, Biomembr. 2004, 1664 (2) 141-149 10.1016/j.bbamem.2004.05.002
40. Xie, W.; Ludewig, G.; Wang, K.; Lehmler, H. Model and cell membrane partitioning of perfluorooctanesulfonate is independent of the lipid chain length Colloids Surf., B 2010, 76 (1) 128-136 10.1016/j.colsurfb.2009.10.025
41. Xie, W.; Bothun, G. D.; Lehmler, H.-J. Partitioning of perfluorooctanoate into phosphatidylcholine bilayers is chain length-independent Chem. Phys. Lipids 2010, 163 (3) 300-308 10.1016/j.chemphyslip.2010.01.003
42. Pazos, A. J.; Román, G.; Acosta, C. P.; Sánchez, J. L.; Abad, M. Lipid classes and fatty acid composition in the female gonad of pecten maximus in relation to reproductive cycle and environmental variables Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 1997, 117, 393-402 10.1016/S0305-0491(97)00135-1
43. Patton, S.; Thomas, A. J. Composition of lipid foams from swim bladders of two deep ocean fish species J. Lipid Res. 1971, 12, 331-335
44. Johnson, J. D.; Gibson, S. J.; Ober, R. E. Cholestyramine-enhanced fecal elimination of carbon-14 in rats after administration of ammonium [14C]perfluorooctanoate or potassium [14C]perfluorooctanesulfonate Toxicol. Sci. 1984, 4 (6) 972-976 10.1093/toxsci/4.6.972
45. Dobrinska, M. R. Enterohepatic circulation of drugs J. Clin. Pharmacol. 1989, 29 (7) 577-580 10.1002/j.1552-4604.1989.tb03385.x
46. Ankley, G. T.; Kuehl, D. W.; Kahl, M. D.; Jensen, K. M.; Linnum, A.; Leino, R. L.; Villeneuve, D. A. Reproductive and developmental toxicity and bioconcentration of perfluorooctanesulfonate in a partial life-cycle test with the fathead minnow (Pimephales promelas) Environ. Toxicol. Chem. 2005, 24, 2316-2324 10.1897/04-634R.1
47. Becker, A. M.; Gerstmann, S.; Frank, H. Perfluorooctanoic acid and perfluorooctane sulfonate in two fish species collected from the Roter Main River, Bayreuth, Germany Bull. Environ. Contam. Toxicol. 2010, 84 (1) 132-135 10.1007/s00128-009-9896-0
48. Zhang, L. Z.; Zhang, T.; Zhuang, P.; Zhao, F.; Wang, B.; Feng, G. P.; Song, C.; Wang, Y.; Xu, S. J. Discriminant analysis of blood biochemical parameters at different developmental gonad stages and gender identification for controlled breeding of Amur sturgeon (Acipenser schrenckii, Brandt, 1869) J. Appl. Ichthyol. 2014, 30 (6) 1207-1211 10.1111/jai.12584
49. Kudo, N.; Sakai, A.; Mitsumoto, A.; Hibino, Y.; Tsuda, T.; Kawashima, Y. Tissue distribution and hepatic subcellular distribution of perfluorooctanoic acid at low dose are different from those at high dose in rats Biol. Pharm. Bull. 2007, 30 (8) 1535-1540 10.1248/bpb.30.1535
50. Liu, C.; Gin, K. Y.; Chang, V. W. C.; Goh, B. P. L.; Reinhard, M. Novel perspectives on the bioaccumulation of PFCs - the concentration dependency Environ. Sci. Technol. 2011, 45 (22) 9758-9764 10.1021/es202078n
51. Arnot, J. A.; Gobas, F. A. P. C. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms Environ. Rev. 2006, 14 (4) 257-297 10.1139/a06-005
52. Beesoon, S.; Martin, J. W. Isomer-Specific binding affinity of perfluorooctanesulfonate (PFOS) and perfluorooctanoate (PFOA) to serum proteins Environ. Sci. Technol. 2015, 49 (9) 5722-5731 10.1021/es505399w
53. Loi, E. I. H.; Yeung, L. W. Y.; Taniyasu, S.; Lam, P. K. S.; Kannan, K.; Yamashita, N. Trophic magnification of poly- and perfluorinated compounds in a subtropical food web Environ. Sci. Technol. 2011, 45 (13) 5506-5513 10.1021/es200432n
54. Taniyasu, S.; Senthilkumar, K.; Yamazaki, E.; Yeung, L. W. Y.; Guruge, K. S.; Kannan, K.; Yamashita, N. Perfluoroalkyl substances in the blood of wild rats and mice from 47 prefectures in Japan: use of samples from nationwide specimen bank Arch. Environ. Contam. Toxicol. 2013, 65 (1) 149-170 10.1007/s00244-013-9878-4
55. Yeung, L. W. Y.; Miyake, Y.; Taniyasu, S.; Wang, Y.; Yu, H.; So, M. K.; Jiang, G.; Wu, Y.; Li, J.; Giesy, J. P.; Yamashita, N.; Lam, P. S. Perfluorinated Compounds and Total and Extractable Organic Fluorine in Human Blood Samples from China Environ. Sci. Technol. 2008, 42 (21) 8140-8145 10.1021/es800631n