Progress toward understanding the bioaccumulation of perfluorinated alkyl acids

Abstract

Environmental Toxicology and ChemistryVolume 32, Issue 11 p. 2421-2423 ET&C Impact PapersFree Access Progress toward understanding the bioaccumulation of perfluorinated alkyl acids Jonathan W. Martin, Jonathan W. Martin Department of Chemistry, University of Toronto, ON, CanadaSearch for more papers by this authorScott A. Mabury, Scott A. Mabury School of Environmental Sciences, University of Guelph, ON, CanadaSearch for more papers by this authorKeith R. Solomon, Keith R. Solomon Environment Canada, Aquatic Contaminants Research Division, Burlington, ON, CanadaSearch for more papers by this authorDerek C.G. Muir, Corresponding Author Derek C.G. Muir Environment Canada, Aquatic Contaminants Research Division, Burlington, ON, CanadaAddress correspondence to derek.muir@ec.gc.ca.Search for more papers by this author Jonathan W. Martin, Jonathan W. Martin Department of Chemistry, University of Toronto, ON, CanadaSearch for more papers by this authorScott A. Mabury, Scott A. Mabury School of Environmental Sciences, University of Guelph, ON, CanadaSearch for more papers by this authorKeith R. Solomon, Keith R. Solomon Environment Canada, Aquatic Contaminants Research Division, Burlington, ON, CanadaSearch for more papers by this authorDerek C.G. Muir, Corresponding Author Derek C.G. Muir Environment Canada, Aquatic Contaminants Research Division, Burlington, ON, CanadaAddress correspondence to derek.muir@ec.gc.ca.Search for more papers by this author First published: 07 October 2013 https://doi.org/10.1002/etc.2376Citations: 34AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat The discovery of the global distribution and biomagnification of perfluorooctane sulfonate (PFOS) in wildlife 1 as well as the presence of perfluorooctanoate (PFOA) and PFOS in humans 2 came as a surprise to many bioaccumulation scientists 3. These chemicals were nonvolatile anions at neutral pH, and the prevailing wisdom was that apart from a few organometallics such as methylmercury and tributyltin, only recalcitrant neutral halogenated organics such as polychlorinated biphenyls (PCBs) would biomagnify. Further monitoring revealed that, while PFOS was the predominant perfluoroalkyl substance in most biotic samples, there were also quantifiable perfluoroalkyl sulfonates (PFSAs) with 4 to 10 carbons 4, 5, and PFOA was generally only detected near detection limits. Unexpectedly, a study on the fate of polyfluoroalkyl and perfluoroalkyl substances (PFASs) after a spill of aqueous film forming foam on a small creek revealed the presence of a range of perfluorocarboxylates (PFCAs) with 5 to 14 carbons in fish liver, with perfluorodecanoate predominating 6. The source of all of the PFCA/PFSAs being measured in environmental and human samples at the time was puzzling. The production of PFOS and PFOA was relatively small compared with the total production of PFASs in commerce such as those based on perfluoroalkylsulfonamide, perfluoroalkyl phosphates/phosphonates, and corresponding polyfluoro-telomer–based compounds and their polymers (e.g., fluorotelomer-based polymer and phosphate surfactants) 7. Therefore, the bioaccumulation properties of the PFASs, and the potential contribution to body burdens of precursor compounds that might degrade to form PFCAs and PFSAs, emerged as important research and risk assessment questions 3. We set out to study the bioconcentration and dietary bioaccumulation of a suite of PFCAs and PFSAs to address the question of how their bioaccumulation potential varied with fluorinated chain length. The results were reported in 2 papers published in Environmental Toxicology and Chemistry in 2003 8, 9. No published studies existed on fish bioaccumulation of PFCAs and PFSAs, and we were concerned about the unusual properties of these chemicals such as the ability to bind to glass surfaces as well as possible contamination from polytetrafluoroethylene (e.g., Teflon) polymers. We chose a relatively standard experimental design for both studies involving flow-through exposures of juvenile rainbow trout (Oncorhynchus mykiss), a well-known test species. The bioconcentration study used plastic-lined aquaria to limit glass adsorption of the test chemicals. Fish were exposed for 12 d to a mixture of 8 PFCAs (C5–C14) and 3 PFSAs (C4–C8), followed by a 33-d depuration period in clean water. Dietary accumulation was studied separately in a 34-d uptake period on food spiked with the same chemicals followed by a 41-d depuration phase using clean food. Analysis of the PFCAs and PFSAs in the fish tissues was also challenging because very few electrospray liquid chromatography/mass spectrometry instruments were available in academic or government laboratories at the time, and also because no mass-labeled analytical standards existed to control for matrix effects. We used perfluorononanoate (PFNA) as an internal standard, which worked well but sacrificed bioaccumulation data for this key PFCA. We found that PFCAs and PFSAs with perfluoroalkyl chain lengths shorter than 7 and 6 carbons, respectively, had insignificant bioconcentration factors (BCFs) and low bioaccumulation factors (BAFs) in rainbow trout; that is, levels were below detection limits in all tissues (liver, muscle, blood). However, both BCFs and BAFs increased with increasing length of the perfluoroalkyl chain. Bioconcentration factors increased by a factor of 8 for each additional carbon in the perfluoroalkylchain between 8 and 12 carbons, but this relationship deviated from linearity for the longest PFCA tested, possibly because of decreased gill permeability. Sulfonates had greater BCFs and BAFs, half-lives, and rates of uptake than the corresponding carboxylate of equal perfluoroalkyl chain length, indicating that chain length was not the only determinant of PFA bioaccumulation potential and that the acid functional group must also be considered. The BCF data identified perfluorotetradecanoate as the most bioaccumulative of the suite of PFCA/PFSAs with BCF of 23 000 and BAF = 1 based on concentrations in the fish carcass (liver and gastrointestinal tract removed from the fish). None of the chemicals had BAFs statistically greater than 1, which demonstrates the limitations of short-term laboratory bioaccumulation exposures with small fish for assessing biomagnification. Many subsequent field studies have shown that C9–C14 PFCAs as well as C6–C10 PFSAs have whole-body predator/prey biomagnification greater than 1 10, 11. Also, many studies of marine and freshwater food webs have shown trophic magnification factors, which represent an average biomagnification factor, were greater than 1 for C8 to C12 PFCAs, PFOS, and perfluorooctanesulfonamide (FOSA) in food webs that include homeotherms as top predators 11. Trophic magnification factors greater than 1 for C8 to C12 PFCAs and PFOS have also been demonstrated in the lichen-caribou-wolf terrestrial food web 12. Recent bioconcentration measurements of PFCAs in carp (Cyprinus carpio) 13 have largely confirmed the BCFs reported by Martin et al 9 and demonstrated that long chain PFCAs are highly bioaccumulative. The assessment of aquatic bioaccumulation of PFASs using laboratory exposures has moved on to the precursor chemicals, including 8:2 fluorotelomer alcohol and FOSA 14, 8:2 fluorotelomer acrylate 15, and perfluorophosphonates and perfluorophosphinates 16. The results of these studies have underlined the rapid biotransformation of precursors and the persistence of the PFCA and PFSA terminal metabolites in both fish and mammals (Butt et al., Duke University, Durham, NC, USA, unpublished manuscript). For example, studies with the 8:2 fluorotelomer alcohol universally show metabolism to PFOA, and, to a more limited extent, PFNA and lower-chain-length PFCAs. Progress has also been made on understanding the fundamental aspects of bioaccumulation of perfluoroalkyl anions. The inclusion of protein interactions has been shown to predict tissue-specific PFCA/PFSA bioconcentration 17 and food web biomagnification 18. Association of PFCA/PFSAs with phospholipids rather than just proteins and carbohydrates has been identified as a potentially important contributor to bioaccumulation of these anionics 19. Did this research have an impact on the regulatory and industry decisions related to PFASs? Decisions on PFOS-related chemistry had largely been made by the time our bioaccumulation papers were published because the 3M Company announced a phaseout of PFOS and PFOA chemistry in 2001, and the US Environmental Protection Agency (USEPA) issued a significant new use ruling in 2002 banning future uses of PFOS-related chemistry in the United States 20. However, the observation of low aquatic bioaccumulation potential for perfluorobutane sulfonate in our studies contributed to the assessment of the replacement chemistry adopted by 3M. The work was also cited in the Stockholm Convention risk profile for PFOS 21. The many exemptions for PFOS under the Stockholm Convention (listed in Part III of Annex B of the Convention) resulted in PFOS and related compounds remaining in global commerce with significant production in China and Brazil. Our work on PFCAs, along with that of many other research groups, contributed to the science underlying decisions related to long-chain polyfluorinated chemicals. In 2006, the USEPA announced a stewardship agreement with 8 leading fluorotelomer manufacturers to reduce emissions and product content of PFOA and related chemicals by 95% by 2010 and to work toward their elimination by 2015 22. Fluorotelomer manufacturers have announced products based on short-chain (C4, C6) perfluoro chains 23. The United Nations Environment Program Strategic Approach for International Chemicals Management includes an initiative to reduce emissions of long-chain “fluorochemicals” and encourages use of short-chain perfluoro chemistry globally 24. Many gaps in our knowledge of bioaccumulation of perfluoro- and polyfluoroalkyl substances remain. Limited laboratory or field bioaccumulation data are available for a wide range of PFASs, particularly for terrestrial food webs. The bioaccumulation and biotransformation of PFAS polymers is also of interest given the large quantities produced. For modeling of PFCA/PFSA bioaccumulation, additional information is needed on the apparent octanol–water and membrane–water partition coefficients, as well as protein–water and protein–air partition coefficients 17-19. SUPPLEMENTAL DATA Table S1. (49 KB PDF). Supporting Information All Supplemental Data may be found in the online version of this article. See Table S1 for the number of citations and rank of all the “Top 100” papers, which in this essay are references [8,9]. Filename Description etc2376-sm-0001-SuppTab-S1.pdf44.9 KB Supplementary Table S1. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. REFERENCES 1 Giesy JP, Kannan K. 2001. Global distribution of perfluorooctane sulfonate in wildlife. Environ Sci Technol 35: 1339– 1342. CrossrefCASPubMedWeb of Science®Google Scholar 2 Hansen KJ, Clemen LA, Ellefson ME, Johnson HO. 2001. Compound-specific, quantitative characterization of organic fluorochemicals in biological matrices. Environ Sci Technol 35: 766– 770. CrossrefCASPubMedWeb of Science®Google Scholar 3 Renner R. 2001. Growing concern over perfluorinated chemicals. Environ Sci Technol 35: 154A– 160A. CrossrefCASPubMedWeb of Science®Google Scholar 4 Kannan K, Newsted J, Halbrook RS, Giesy JP. 2002. Perfluorooctanesulfonate and related fluorinated hydrocarbons in mink and river otters from the United States. Environ Sci Technol 36: 2566– 2571. CrossrefCASPubMedWeb of Science®Google Scholar 5 Kannan K, Corsolini S, Falandysz J, Oehme G, Focardi S, Giesy JP. 2002. Perfluorooctanesulfonate and related fluorinated hydrocarbons in marine mammals, fishes, and birds from coasts of the Baltic and the Mediterranean Seas. Environ Sci Technol 36: 3210– 3216. CrossrefCASPubMedWeb of Science®Google Scholar 6 Moody CA, Martin JW, Kwan WC, Muir DCG, Mabury SA. 2002. Monitoring perfluorinated surfactants in biota and surface water samples following an accidental release of fire-fighting foam into Etobicoke Creek. Environ Sci Technol 36: 545– 551. CrossrefCASPubMedWeb of Science®Google Scholar 7 Buck RC, Franklin J, Berger U, Conder JM, Cousins IT, Voogt PD, Jensen AA, Kannan K, Mabury SA, van Leeuwen SPJ. 2011. Perfluoroalkyl and polyfluoroalkyl substances in the environment: Terminology, classification, and origins. Integr Environ Assess Manage 7: 513– 541. Wiley Online LibraryCASPubMedGoogle Scholar 8 Martin JW, Mabury SA, Solomon KR, Muir DCG. 2003. Dietary accumulation of perfluorinated acids in juvenile rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 22: 189– 195. Wiley Online LibraryCASPubMedWeb of Science®Google Scholar 9 Martin JW, Mabury SA, Solomon KR, Muir DCG. 2003. Bioconcentration and tissue distribution of perfluorinated acids in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 22: 196– 204. Wiley Online LibraryCASPubMedWeb of Science®Google Scholar 10 Houde M, Martin JW, Letcher RJ, Solomon K, Muir DCG. 2006. Biological monitoring of polyfluoroalkyl substances: A review. Environ Sci Technol 40: 3463– 3473. CrossrefCASPubMedWeb of Science®Google Scholar 11 Houde M, De Silva AO, Muir DCG, Letcher RJ. 2011. Monitoring of perfluorinated compounds in aquatic biota: An updated review. Environ Sci Technol 45: 7962– 7973. CrossrefCASPubMedWeb of Science®Google Scholar 12 Müller CE, De Silva AO, Small J, Williamson M, Wang X, Morris A, Katz S, Gamberg M, Muir DCG. 2011. Biomagnification of perfluorinated compounds in a remote terrestrial food chain: Lichen-caribou-wolf. Environ Sci Technol 45: 8665– 8673. CrossrefCASPubMedWeb of Science®Google Scholar 13 Inoue Y, Hashizume N, Yakata N, Murakami H, Suzuki Y, Kikushima E, Otsuka M. 2012. Unique physicochemical properties of perfluorinated compounds and their bioconcentration in common carp Cyprinus carpio L. Arch Environ Contam Toxicol 62: 672– 680. CrossrefCASPubMedWeb of Science®Google Scholar 14 Brandsma SH, Smithwick M, Solomon K, Small J, de Boer J, Muir DCG. 2011. Dietary exposure of rainbow trout to 8:2 and 10:2 fluorotelomer alcohols and perfluorooctanesulfonamide: Uptake, transformation and elimination. Chemosphere 82: 253– 258. CrossrefCASPubMedWeb of Science®Google Scholar 15 Butt CM, Muir DCG, Mabury SA. 2010. Biotransformation of the 8:2 FTOH acrylate in rainbow trout. I. In vivo dietary exposure. Environ Toxicol Chem 29: 2726– 2735. Wiley Online LibraryCASPubMedWeb of Science®Google Scholar 16 Lee H, De Silva AO, Mabury SA. 2012. Dietary bioaccumulation of perfluorophosphonates and perfluorophosphinates in juvenile rainbow trout: Evidence of metabolism of perfluorophosphinates. Environ Sci Technol 46: 3489– 3497. CrossrefCASPubMedWeb of Science®Google Scholar 17 Ng CA, Hungerbühler K. 2013. Bioconcentration of perfluorinated alkyl acids: How important is specific binding? Environ Sci Technol 47: 7214– 7223. CrossrefCASPubMedWeb of Science®Google Scholar 18 Kelly BC, Ikonomou MG, Blair JD, Surridge B, Hoover D, Grace R, Gobas FAPC. 2009. Perfluoroalkyl contaminants in an arctic marine food web: Trophic magnification and wildlife exposure. Environ Sci Technol 43: 4037– 4043. CrossrefCASPubMedWeb of Science®Google Scholar 19 Armitage JM, Arnot JA, Wania F, Mackay D. 2013. Development and evaluation of a mechanistic bioconcentration model for ionogenic organic chemicals in fish. Environ Toxicol Chem 32: 115– 128. Wiley Online LibraryCASPubMedWeb of Science®Google Scholar 20 US Environmental Protection Agency. 2002. Perfluoroalkyl sulfonates, significant new use rule: Final rule and supplemental proposed rule. Fed Regist 67: 11007– 11013. Google Scholar 21 United Nations Environment Programme. 2006. Risk profile on perfluorooctane sulfonate UNEP/POPS/POPRC.2/17/Add.5. Geneva, Switzerland. Google Scholar 22 US Environmental Protection Agency. 2006. PFOA Stewardship Program docket ID number EPA-HQ-OPPT-2006-0621. Washington, DC. Google Scholar 23 Ritter SK. 2010. Fluorochemicals go short. Chem Eng News 88: 12– 17. CrossrefWeb of Science®Google Scholar 24 United Nations Environment Programme. 2012. Progress report on managing perfluorinated chemicals and the transition to safer alternatives (SAICM/ICCM.3/18). Geneva, Switzerland. Google Scholar Citing Literature Volume32, Issue11November 2013Pages 2421-2423 ReferencesRelatedInformation