Progress toward understanding the bioaccumulation of perfluorinated alkyl acids

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 BAF1⁄4 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, 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]. * Address correspondence to derek.muir@ec.gc. ca. Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/etc.2376 Environmental Toxicology and Chemistry, Vol. 32, No. 11, pp. 2421–2423, 2013 # 2013 SETAC Printed in the USA