ARTICLE pubs.acs.org/est
Novel Perspectives on the Bioaccumulation of PFCs the Concentration Dependency Changhui Liu,† Karina Y. H. Gin,‡ Victor W. C. Chang,†,* Beverly P. L. Goh,§ and Martin Reinhard|| †
School of Civil and Environmental Engineering, Nanyang Technological University, 50 Nanyang Avenue, Singapore 639798 Department of Civil and Environmental Engineering, National University of Singapore § Natural Sciences and Science Education, National Institute of Education, Singapore Civil and Environmental Engineering, Stanford University, California, United States
)
‡
bS Supporting Information ABSTRACT: The effects of exposure concentration on the bioaccumulation of four perfluorinated chemicals (PFCs): perfluorooctanesulfonate (PFOS), perfluoroocanoic acid (PFOA), perfluorononanoic acid (PFNA), and perfluorodecanoic acid (PFDA), was investigated using green mussels, Perna viridis. Mussels were exposed to concentrations of 1 μgL1 and 10 μgL1 of each PFC for 56 days, and the bioaccumulation factors (BAF) were found to range from 15 to 859 L/kg and from 12 to 473 L/kg at 1 μgL1 and 10 μgL1, respectively. For all compounds, the BAF was larger at the lower dosage. Results suggest that the bioaccumulation of PFCs is concentration dependent. This concentration dependency can be explained by a nonlinear adsorption mechanism, which was further supported by the experimental results. The sensitivity of BAF to exposure concentration was found to be positively related to perfluorinated chain length and the binding affinity of the compounds. Bioaccumulation of long chain carboxylates and sulfonates are more easily affected by concentration changes. The validity of the conventional kinetic method was examined by comparing the results with the fundamental steady-state method: in addition to the above-mentioned batch test, mussels were also subject to 24-day exposure (1 μgL1 and 10 μgL1) followed by 24-day depuration. Contradictions were found in the resulting kinetic BAF and model curving fittings. A new kinetic model based on adsorption mechanism was proposed, which potentially provide more accurate description of the bioaccumulation process of PFCs.
’ INTRODUCTION In recent years, there has been growing concern in perfluorinated chemicals (PFCs). PFCs are synthetic compounds that have been applied in a broad spectrum of commercial products and industrial processes in the past few decades. Due to their unique water and fat repellent properties, PFCs are widely used as surfactants, refrigerants and as components of pharmaceuticals, lubricants, paints, fire fighting foams, cosmetics, and food packaging. 13 PFCs are released to the environment either through usage of the PFCs-containing products or by degradation of their precursors. Due to the high energy of carbonfluorine covalent bonds, PFCs are thermally and chemically stable, and are also resistant to biodegradation. Hence, they are extremely persistent in the environment,48 and have been found extensively in wildlife and human bodies worldwide, even in remote regions such as the Arctic.917 A number of studies have also demonstrated that PFCs have adverse effects on human and animals including possible carcinogenic effects.3,1822 Both monitoring and controlled laboratory studies have demonstrated the potential of PFCs to bioaccumulate.1,9,23,24 Studying the bioaccumulation of PFCs requires approaches that are different from those used for other persistent organic pollutants r 2011 American Chemical Society
(POPs), such as polychlorinated biphenyls (PCBs) because PFCs are not only hydrophobic but also oleophobic. They possess a high affinity to protein albumin, and are sometimes referred to as “proteinophilic”.5,15 Both monitoring and laboratory studies have demonstrated that PFCs tend to accumulate preferentially in protein-rich tissues, such as the liver, and in blood.17,19 The accumulation mechanism and exposure routes of PFCs are therefore different from other hydrophobic POPs. Thus, the commonly used octanolwater partition coefficient, Kow, to predict bioaccumulation is inappropriate and inaccurate. Current bioaccumulation data shows discrepancies between different laboratory studies.3,19 A possible explanation for these discrepancies is that the test species contained different amounts of protein or that environmental conditions maintained during the tests differed.25 Most studies adopted a kinetic approach that involved approximation and estimation in curve fitting.19,2427 As the relative contribution of each of the affecting factors of Received: April 4, 2011 Accepted: September 19, 2011 Revised: September 13, 2011 Published: October 11, 2011 9758
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Figure 1. Bioaccumulation of PFCs in green mussels at exposure concentrations of 1 μgL1 and 10 μgL1 during 56 day exposure (n = 12). Data points are results from the steady-state experiment. Error bars represent standard deviation. Curves are the proposed kinetic model fitted to eq 9.
PFCs bioaccumulation is still unclear, direct measurement of the bioaccumulation factor or the steady-state approach may elicit greater accuracy. Recent reviews suggested that PFCs bioaccumulation is concentration dependent,4,19 that is, it is a function of concentration. However, data that shows exposure concentration is a significant parameter in the bioaccumulation assessment seems to be lacking. The purpose of this study was to examine the bioaccumulation mechanism of PFCs, and in particular, to characterize the effects of exposure concentration on the bioaccumulation process. The validity of the commonly used approach to model bioaccumulation kinetics was evaluated and a new model was proposed. A local species of green mussels, Perna viridis, was chosen as the test organism. Bivalves, in particular mussels, have been commonly used as bioindicators in pollution monitoring because they are filter-feeding, sessile organisms and therefore can accumulate relatively large concentrations of pollutants.
’ MATERIALS AND METHODS Chemicals and Standards. Potassium perfluorooctanesulfonate (PFOS, 98%), perfluoroocanoic acid (PFOA, 96%), perfluorononanoic acid (PFNA, 97%), perfluorodecanoic acid (PFDA, 98%) were purchased from Sigma-Aldrich (St. Louis, MO).
The internal standards, perfluoro-n-[1,2,3,4- 13 C 4 ]octanoic acid (MPFOA, 99%), perfluoro-n-[1,2,3,4,5-13C5]nonanoic acid (MPFNA, 99%), perfluoro-n-[1,2-13C2]decanoic acid (MPFDA, 99%) and sodium perfluoro-1-[1,2,3,4-13C4]octanesulfonate (MPFOS, 99%) were purchased from Wellington Laboratories (Guelph, ON). The stock solutions were prepared with PFOS, PFOA, PFNA, and PFDA at 1000 mg L1 and 100 mg L1 in optima grade methanol. The stock solutions were stored at 4 °C. Experiment Set-Up. To examine the effects of exposure concentration on bioaccumulation, mussels were exposed to 1 μgL1 and 10 μgL1 of PFOS, PFOA, PFNA, and PFDA (total PFC concentration of the mixtures were 4 μgL1 and 40 μgL1, respectively). These concentrations were below the lowest no observed effect concentration (NOEC) of marine invertebrates,28 so as not to affect the general well-being of the test organisms. Seventy-liter polypropylene (PP) tanks were used as the test chambers. 6065 mussels with similar size were raised in artificial seawater. For each exposure concentration, two sets of duplicate tanks were used: in one set, mussels were exposed to PFCs for up to 56 days; in the other set, mussels were subject to a 24-day exposure followed by a 24-day depuration. The purpose of this experimental design was to determine and compare the bioaccumulation factors through both steady-state 9759
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Figure 2. Depuration kinetic of PFCs after exposure to concentrations of (a)1 μgL1 and (b)10 μgL1.
(former set) and kinetic approaches (latter set). Another tank was also engaged as a control, where no PFCs were present. All tanks were cleaned and refilled every two days. Four mussels were sampled from each tank at each sampling time. 100 mL aqueous samples were also taken every four or eight days for PFCs concentration analysis. Additional information on experiment setup and mussel rearing is available in the Supporting Information (SI). Sample Preparation and Extraction. A few extraction methods have been described in the literature.11,29,30 In order to validate the precision and accuracy of PFC determination in mussel tissues, two commonly used extraction methods, the acetonitrile extraction30 and alkaline digestion with SPE11 were tested and compared. The latter (recovery 95110%) was selected in this experiment. Details of the extraction method and recovery tests are available in the SI. Briefly, homogenized dry mussel tissues was extracted using 30 mL of potassium hydroxide solvent (KOH 0.01 mol/L in methanol) in 50 mL PP tubes. The mixture was vortexed, shaken (300 rpm, 25 °C, 18 h), and centrifuged (4000 rpm, 15 min). 0.5 mL of supernatant was diluted (1:100 with Milli-Q water) and extracted by using Oasis HLB cartridges (0.2 g, 6 cm3; Waters). Prior to loading, cartridges were preconditioned by eluting with 5 mL methanol followed by 5 mL Milli-Q water. Cartridges were vacuum-dried before elution using 15 mL methanol. Elutes were dried by nitrogen gas and reconstituted to 2 mL with methanol. Prior to analysis, 200 mL of final extracts were transferred to the sample vial with 20 μL of internal standards. Instrumental Analysis. Details of analytical method and sample analysis are available in the SI. Briefly, concentrations of PFCs in mussel tissues were determined using high-performance liquid chromatography coupled with tandem mass spectrometry (LC MS/MS). The MS/MS was operated in negative electrospray ionization multiple reaction monitoring (MRM) mode. A volume injection of 20 μL was injected into a Targa Sprite C18 column (3.5 μm pore size, 40 mm 2.1 mm ID, Higgins Analytical, CA) using methanol gradient (initial and final eluent condition of 35% methanol) at a flow rate of 0.25 mL min1 with 2 mM ammonium acetate as the second mobile phase.27,30
Data Analysis. The bioaccumulation factor (BAF) was calculated according to
BAF ¼
Co Cw
ð1Þ
where Co is the PFC concentration in the organism at steady state(ng/g); Cw is the PFC concentration in water (μg/L); BAF is in L/kg. Steady state was determined using a previous apporach19 modified as follows: steady state was assumed when three or more consecutive measurements were not statistically different, or when the normalized slope of the fitted line of three or more consecutive measurements was less than 0.005 (1/day). One-way ANOVA was applied to determine the statistical significance.
’ RESULTS AND DISCUSSION Bioaccumulation Results. Among the tested compounds, the long-chain perfluorocarboxylate and perfluorosulfonate were found to have the highest bioaccumulation potential. PFDA possess the largest BAF followed by PFOS (Figure 1). PFOA, on the other hand, is the least accumulative compound with a steady state concentration about 20 times lower than PFOS. This is consistent with the observation that PFOS is generally detected at higher level in wildlife than PFOA, although the environmental concentrations of the two are comparable.16,31 Compounds with higher BAF take longer to reach steady state, which is also consistent with previous studies,4,24,26 and their depuration is generally slower too. PFC depuration follows a first-order (exponential) model with rates increasing in the order of PFDA < PFOS < PFNA < PFOA (Figure 2). The fast elimination may be facilitated by the presence of PFCs in the circulating blood, coupled with extensive blood-water exchange at mussel gills during respiration.15 It also implies that there should be a continuous exposure of PFCs at a certain level to maintain an observed tissue concentration. Concentration Dependency of Bioaccumulation. Figure 1 shows that when exposure concentration (Cw) changes from low (1 μgL1) to high (10 μgL1), steady state organism concentrations (Co) do not increase proportionally. The BAF values (eq 1) 9760
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965 ( 297
Highlight that data in the columns with the same superscript are significantly different at p < 0.01. b A:ke estimated from elimination phase where Co = A 3 exp(ket); B: BAFss was the average of steady-state results; D: nku and (kuCw + ke) are directly obtained from curve fitting results; E: k0 u estimated from initial uptake phase;25 n = 12; All curve fittings were carried out by Matlab. Data are provided with standard error ((SE) and R2 in parentheses. a
473 ( 40 (0.96) 464 ( 25 9 PFDA
0.05 ( 0.01 (0.93) 0.04 ( 0.01 (0.95) 838 ( 66
0.10 ( 0.03
859 ( 93 (0.97)
112 ( 50
146 ( 64
18 ( 7
13.1 ( 0.0 (1.0) 10.4 ( 0.0 (1.0) 105 ( 7 (0.96) 149 ( 12 (0.97) 109 ( 14 8 PFNA
0.09 ( 0.04 (0.92) 0.09 ( 0.04 (0.93) 144 ( 14
0.05 ( 0.02
12 ( 1 (0.94) 15 ( 1 (0.97)
62.1 ( 16.8 (0.98) 40.6 ( 3.5 (0.99) 1375 ( 569
384 ( 126
1.9 ( 0.4 (0.99) 1.9 ( 0.4 (0.99)
236 ( 17 (0.97) 386 ( 37 (0.96)
12 ( 0
0.07 ( 0.02 235 ( 13
0.10 ( 0.04 (0.95) 0.10 ( 0.04 (0.96) 15 ( 1 7 PFOA
0.05 ( 0.01 (0.95) 0.05 ( 0.01 (0.96) 378 ( 29 8 PFOS
10 ppb perfluorinated chain length
1 ppb
10 ppb
1 ppb
0.03 ( 0.01
10 ppba#
19 ( 8
25.4 ( 22.9 (0.77) 19.3 ( 3.9 (0.99) 472 ( 447
10 ppba# 1 ppba*
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1 ppba*
(BAFkinetic = nku/(kuCw+ke)) (L/kg) BAFss = Co/Cw (L/kg) ke (1/d)
α (L/kg)
B A
Table 1. Bioaccumulation Factors and Parameters
C
D - proposed model
1 ppb
10 ppb
BAF0 kinetic = k0 u/ke (L/kg) k0 u (L/kg/d)
E - old model 25
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of each compound are different at the two exposure concentrations (p < 0.01, t test) and decrease with increasing exposure by a factor of 1.3 for PFOA and 1.8 for PFDA (Figure 1, Table 1-B). For each compound, the time to reach steady state is longer under the lower exposure concentration where the BAF is also higher. These results show that the bioaccumulation of PFCs is concentration dependent. Although the concentration dependency of PFCs bioaccumulation has been mentioned in previous studies,14,19 insight into the underlying factors have been lacking. A possible explanation of the observed results is that bioaccumulation of PFCs is an adsorption-like process in which PFC molecules adsorb to the surface of quasi-solid materials, and the rationale is that PFC molecules are surface active chemicals.4 The conventional bioaccumulation model only views tissues as a “bulk phase” and the biological uptake as simple partitioning process. The mechanism of chemical adsorption is shown as follows:32 ku
M þ Sf s s MS r
ð2Þ
ke
M = chemicals, S = free binding sites, MS = bonded chemicals, ku = uptake rate constant, ke = elimination rate constant For PFCs, the binding sites are most likely at the surface of hemocytes and liver cells. As mentioned previously, PFCs tend to accumulate in these protein-rich compartments. In adsorption, The binding sites limit the amount of adsorbate, and the fractional surface coverage of adsorbent, θ, depends on the concentration of adsorbate: θ¼
MS αM ku ¼ where α ¼ MS þ S 1 þ αM ke
ð3Þ
Therefore the amount of adsorption depends on the chemical concentration. From this adsorption model, the major findings in this experiment can be well explained: (1) exposure concentration dependency of BAF, (2) correlation between BAF sensitivity to exposure concentration and perfluorinated chain length, and (3) discrepancy between the kinetic and the steady-state approach. Additional information on derivations and calculations are available in the SI. (1) Concentration Dependency of BAF. As illustrated in Figure 1, the BAF decreases as the exposure concentration Cw increases. If n is the number of total binding sites per gram organism, Co is equivalent to nθ; Cw is equivalent to M. By substituting Co and eq 3 into the eq 1, we obtain BAF ¼
Co nθ nα ¼ ¼ Cw 1 þ αCw Cw
ð4Þ
Eq 4 shows that the BAF is an inverse function of the exposure concentration Cw. An increase in Cw will lead to a decrease in BAF. Therefore, when concentration Cw increased from 1 μgL1 to 10 μgL1, the BAF decreased from nα/(1+α 3 1 μgL1) to nα/(1+α 3 10 μgL1), which explains the observed results that BAF became lower at the higher exposure concentration. (2) Chain Length Effect. Binding Affinity Vs Chain Length. In eq 3, the constant α is determined by, and directly proportional to, the binding energy.32 The α value of each compound can be calculated by eq 3 when Co and Cw are known. The results obtained follow the order of PFDA > PFOS > PFNA > PFOA (Table 1-C). A linear relationship was found between α, the binding affinity, and perfluorinated chain length (Figure 3). This is 9761
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Figure 3. Relationship between binding affinity and perfluorinated chain length. Error bars represent standard deviation.
consistent with the previous conclusion that long chain PFCs have enhanced binding energy.8,13 Bioaccumulation of PFCs was shown to be related to the chemical’s hydrophobicity.24,26 Being the hydrophobic portion in the PFC molecule, the longer the perfluorinated chain, the stronger the hydrophobic interaction, and thus the higher the binding energy. In addition, it is also believed that bioaccumulation is governed to some degree by the contribution of ionic interactions of functional groups,33 which explains the higher binding affinity by sulfonate than carboxylate with the same perfluorinated chain (Figure 3: PFNA and PFOS). Concentration Sensitivity Vs Chain Length. The correlation of the exposure concentration induced change in log BAF (Δlog BAF) and chain length was demonstrated in Figure 4: among the carboxylates, BAF of long chain PFC is affected more significantly by concentration change. The magnitude of Δlog BAF follows the order of increasing chain length. The Δlog BAF of sulfonate is larger than that of carboxylate with the same perfluorinated chain length (Figure 4: PFNA and PFOS). These results can be well explained by involving the binding affinity α. In eq 4, dividing both the denominator and the numerator by α we have n BAF ¼ 1 þ Cw α
ð5Þ
As the number of total binding sites, n, is constant, the effect of Cw on BAF, or in other words the BAF’s sensitivity to Cw, depends on α value. When αv, 1/αV, therefore Cw will have greater influence on the BAF. Hence the larger the α value, the more sensitive the BAF to changes in Cw (i.e., the larger concentration induced change in log BAF). From a physio-chemical point of view, when concentration increases, compounds possessing higher binding affinity are more likely to be adsorbed than those with low binding affinity. Thus, the amount of accumulation with respect to concentration change is more significant. The concentration-induced change in log BAF was found to be linearly correlated with α, too (Figure 4). Since the binding affinity α is closely related with chain length as discussed earlier, it is feasible to relate chain length with Δlog BAF through α, that is, longer chain f larger α f greater influence by Cw.
Figure 4. Relationship between Δlog BAF with binding affinity (lower curve, left axis); and with perfluorinated chain length (upper curve, right axis). Error bars represent standard deviation.
(3) Comparison of Kinetic Approach and Steady-State Approach. Besides the fundamental steady-state approach (eq 1) to determine BAF, the kinetic approach has been popular in laboratory bioaccumulation studies.2426 The kinetic BAF is estimated as the quotient of uptake and elimination rate constants (eq 7), with the assumption that both uptake and elimination of chemicals are first order reactions (eq 6).34 dCoðtÞ ¼ k0u Cw ke CoðtÞ dt BAF0kinetic ¼
k0u ke
ð6Þ
ð7Þ
Controlled laboratory studies have shown that the kinetic approach can generate similar results as the steady-state method for many POPs.34 However, the validity of the kinetic approach had never been verified for PFCs before it was applied in several laboratory studies.13,2426 In this study, the kinetic method was for the first time compared with the steady-state method and the result shows that it is not suitable for the assessment of bioaccumulation of PFCs. As discussed previously, the BAF is exposure concentration dependent. However, the expression of eq 7 itself suggests that the kinetic BAF (BAF0 kinetic) should be a constant value independent of concentration. This fundamentally contradicts the experimental results. Moreover, if following the above-mentioned kinetic approach as described in a previous study,25 the resulting uptake rate constant in eq 7, k0 u, varies for the two exposure concentrations (Table 1-E), which suggests that k0 u here is not a constant as defined. Hence, the previous assumption of “first order uptake reaction” is inappropriate in the case of PFCs bioaccumulation. Even though two kinetic BAF values can be calculated from the variant k0 u, the results were still shown to deviate from the steady-state BAF (BAFss) (Table 1-B and E, SI Figure S1). Based on the experimental results and the special surfactant property of PFCs we hereby propose a new kinetic equation (eq 8) to describe the bioaccumulation of PFCs, incorporating the adsorption model (eq 2). Compared with the old kinetic model (eq 6), accumulation is no longer first order reaction: the rate of accumulation of PFCs depends on both the exposure 9762
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concentration and free binding sites: dCoðtÞ ¼ ku Cw SðtÞ ke CoðtÞ dt
ð8Þ
where S(t) is the free binding sites at time t (eq 2). The expression for organism concentration at time t (Co(t)) can be obtained by solving eq 8 as CoðtÞ ¼
nku Cw f1 exp½ ðku Cw þ ke Þtg ku Cw þ ke
ð9Þ
And the kinetic BAF can be obtained as BAFkinetic ¼
nku ku Cw þ ke
ð10Þ
Compared with eq 7, the exposure concentration effect is incorporated in eq 10. This proposed expression of the kinetic BAF is consistent with the one obtained from the steady-state approach (eq 4). Curve fittings using eq 9 show agreement with the steady-state experimental results with good reliability, and so does the resulted BAFkinetic with the steady-state BAF, the BAFss (R2 g 0.94; p < 0.01, F test) (Figure 1; Table 1-B and D). Time to Reach Steady State. As mentioned previously, the time to reach the steady state, tss, varies between the two exposure concentrations. Therefore, tss also appears to be concentration dependent. Mathematically the time to reach steady state is infinity. However, the time for Co to reach 95% of steady state concentration, t95% ss , can be used as a performance metric and derived from eq 9 as tss95% ¼
1 lnð1 0:95Þ ku Cw þ ke
ð11Þ
Equation 11 shows that when exposure concentration Cw increases, tss will decrease accordingly, which explains the observed results of longer tss at lower exposure. However, if the old kinetic method (eq 6) is followed, the t95% ss will be t 095% ¼ ss
1 lnð1 0:95Þ ke
ð12Þ
where tss depends only on ke and thus, is a constant value for each compound. Taken together, the bioaccumulation of PFC appears to follow an adsorption model. In consideration of the special partitioning behavior of PFCs, the conventionally used kinetic model appears to be inaccurate for this group of chemicals. The fundamental assumption that both uptake and elimination of PFCs are first order reactions merits further scrutiny.
’ IMPLICATIONS To our knowledge, this is the first study that demonstrates the concentration dependency of the bioaccumulation of perfluorinated compounds, and describes the relationships among various factors using mathematical models. Examination of the concentration dependency reveals the inadequacy of the conventional kinetic model and a new model based on the adsorption mechanism is accordingly proposed. This model may provide more accurate description of the bioaccumulation process and thus, the fate of PFCs. It is also noted that protein binding and adsorption have similar mechanisms, both of which can be described by eq 2.35 Protein-water partitioning has been suggested to be useful in
evaluating the bioaccumulation of PFCs.15 As proteins have been considered as major reservoirs for PFCs, it is expected that protein binding could dominate the bioaccumulation process. It is therefore also possible that the observed results in our study are attributed to this predominant process. Partitioning coefficients used to predict the environmental distribution of chemicals, such as Kow, are independent of concentration. Although more species- and environmental factordependent, the BAF in many ways is similar to these partitioning coefficients. Hence, in previous studies, the BAF of perfluorochemicals were always treated as a constant, regardless of the exposure concentration.13,2426 In other words, bioaccumulation was assessed without considering concentration as an influencing parameter. The unique properties of PFCs, however, suggest that this approach may not be appropriate. This argument is further supported by the results of this study which has shown the importance of specifying the environmental concentration. Literature reviews indicate that BAF data from both laboratory and field studies are inconsistent, a fact that may possibly be explained by the concentration dependence of PFC. Although further research work is still needed to fully understand the mechanisms of bioaccumulation of PFCs, the concentration factor should be taken into consideration in this process and also in ecotoxicological assessment.
’ ASSOCIATED CONTENT
bS
Supporting Information. Additional information regarding the method, equation derivation, and model comparison. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Phone: (65)6790 4773; e-mail:
[email protected].
’ ACKNOWLEDGMENT Funding support for this study was provided by the Environment and Water Industry Development Council (EWI) (0601IRIS-031000). We also thank Nguyen Viet Tung for his assistance in PFCs analysis. ’ REFERENCES (1) Houde, M.; Martin, J. W.; Letcher, R. J.; Solomon, K. R.; Muir, D. C. G. Biological monitoring of polyfluoroalkyl substances: A review. Environ. Sci. Technol. 2006, 40 (11), 3463–3473. (2) Suja, F.; Pramanik, B. K.; Zain, S. M. Contamination, bioaccumulation and toxic effects of perfluorinated chemicals (PFCs) in the water environment: A review paper. Water Sci. Technol. 2009, 60 (6), 1533–1544. (3) Lau, C.; Anitole, K.; Hodes, C.; Lai, D.; Pfahles-Hutchens, A.; Seed, J. Perfluoroalkyl acids: A review of monitoring and toxicological findings. Toxicol. Sci. 2007, 99 (2), 366–394. (4) Conder, J. M.; Hoke, R. A.; De Wolf, W.; Russell, M. H.; Buck, R. C. Are PFCAs bioaccumulative? A critical review and comparison with regulatory lipophilic compounds. Environ. Sci. Technol. 2008, 42 (4), 995–1003. (5) Rayne, S.; Forest, K. Perfluoroalkyl sulfonic and carboxylic acids: A critical review of physicochemical properties, levels and patterns in waters and wastewaters, and treatment methods. J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2009, 44 (12), 1145–1199. 9763
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