Fate and redistribution of perfluoroalkyl acids through ...

Science of the Total Environment 596–597 (2017) 360–368

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Fate and redistribution of perfluoroalkyl acids through AFFF-impacted groundwater Jennifer Bräunig a,⁎, Christine Baduel a,1, Amy Heffernan a,2, Anna Rotander a,3, Eric Donaldson b, Jochen F. Mueller a a b

Queensland Alliance for Environmental Health Sciences (QAEHS), The University of Queensland, 39 Kessels Rd, 4108 Coopers Plains, QLD, Australia Aviation Medical Specialist, Oakey, QLD, Australia

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• Widespread PFAA groundwater contamination originating from a point source • PFAAs detected in eight biotic and abiotic matrices. • Redistribution of PFAAs occurring from the point source through water usage • Creation of secondary sources and human relevant exposure pathways

a r t i c l e

i n f o

Article history: Received 11 February 2017 Received in revised form 12 April 2017 Accepted 12 April 2017 Available online xxxx Editor: Adrian Covaci Keywords: Groundwater contamination Aqueous film-forming foams (AFFF) Human blood serum Creation of secondary sources

a b s t r a c t Leaching of perfluoroalkyl acids (PFAAs) from a local point source, a fire-fighting training area, has led to extensive contamination of a groundwater aquifer which has spread underneath part of a nearby town, Oakey, situated in the State of Queensland, Australia. Groundwater is extracted by residents from privately owned wells for daily activities such as watering livestock and garden beds. The concentration of 10 PFAAs in environmental and biological samples (water, soil, grass, chicken egg yolk, serum of horses, cattle and sheep), as well as human serum was investigated to determine the extent of contamination in the town and discuss fate and redistribution of PFAAs. Perfluorooctane sulfonate (PFOS) was the dominant PFAA in all matrices investigated, followed by perfluorohexane sulfonate (PFHxS). PFOS concentrations measured in water ranged between b0.17–14 μg/L, concentrations of PFHxS measured between b0.07–6 μg/L. PFAAs were detected in backyards (soil, grass), livestock and chicken egg yolk. Significant differences (p b 0.01) in PFOS and PFHxS concentrations in two groups of cattle were found, one held within the contamination plume, the other in the vicinity but outside of the contamination plume. In human serum PFOS concentrations ranged from 38 to 381 μg/L, while PFHxS ranged from 39 to 214 μg/L. Highest PFOS concentrations measured in human serum were N 30-fold higher compared to the general Australian population. Through use of contaminated groundwater secondary sources of PFAA contamination are created on private property, leading to further redistribution of contamination and creation of additional human exposure pathways. © 2017 Elsevier B.V. All rights reserved.

⁎ Corresponding author. E-mail address: [email protected] (J. Bräunig). University Lyon, CNRS, Université Claude Bernard Lyon 1, Ens de Lyon, Institut des Sciences Analytiques, UMR 5280, 5 rue de la Doua, F-69100 Villeurbanne, France. 2 The Florey Institute of Neuroscience and Mental Health, The University of Melbourne, Parkville, VIC, Australia. 3 Man-Technology-Environment (MTM) Research Centre, 702 81 Örebro University, Örebro, Sweden. 1

http://dx.doi.org/10.1016/j.scitotenv.2017.04.095 0048-9697/© 2017 Elsevier B.V. All rights reserved.

J. Bräunig et al. / Science of the Total Environment 596–597 (2017) 360–368

1. Introduction Perfluoroalkyl substances (PFAAs) have been used widely in the past 50 years in a variety of applications and consumer goods, as well as being key ingredients in aqueous film-forming foams (AFFFs) (Buck et al., 2012). The strong carbon-fluorine bonds make PFAAs highly persistent and today they are found ubiquitously in the environment on a global scale (Buck et al., 2012; Giesy and Kannan, 2001; Prevedouros et al., 2006). Some PFAAs have the potential to bioaccumulate and biomagnify (Ahrens and Bundschuh, 2014; Martin et al., 2013) and together with their persistence, has raised concerns regarding their environmental fate. The most studied and frequently detected PFAAs are the 8-carbon perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS), and the 6-carbon perfluorohexane sulfonate (PFHxS). PFAA toxicity has predominantly been assessed for PFOA and PFOS. Some of the observed effects in laboratory animals include hepatotoxicity, developmental effects and immunotoxicity (reviewed in Lau et al., 2007). Due to their widespread environmental occurrence and the increasing concern regarding the toxicological effects of PFAAs, measures have been taken to reduce exposure to these chemicals, including the addition of PFOS to the Stockholm Convention in 2009 (UNEP, 2009). Background exposure of humans to PFAAs occurs primarily though dietary intake of fish, dairy products, meat and drinking water, as well as through household dust (Ericson et al., 2008; Fromme et al., 2009; Haug et al., 2011). Human serum-elimination half-lives have been estimated to be around 3.8 years for PFOA, 5.4 years for PFOS and 8.5 years for PFHxS (Olsen et al., 2007). As a result PFOS and PFOA can be detected in serum of the general population (Calafat et al., 2007; Kato et al., 2011; Schröter-Kermani et al., 2013; Toms et al., 2014). PFAA levels above those of the general population have been found in occupationally exposed populations such as firefighters (Rotander et al., 2015) and fluorochemical production workers (Olsen et al., 2007). Exposure to contaminated groundwater has also resulted in elevated levels of serum PFAA concentrations in communities in Sweden, Germany and the U.S. (Gyllenhammar et al., 2015; Hoffman et al., 2011; Weiß et al., 2012). In these cases, the key conclusion was that the drinking water directly resulted in elevated exposure and associated increased serum concentrations. Oakey is a small community west of the Great Dividing Range in Queensland, Australia. Since the 1970s PFAA-containing AFFF was used at a nearby fire training facility on a military airfield (AECOM, 2016b). The historical use, as well as spillages and leakages from underground storage tanks of AFFF concentrate and waste have led to point sources of PFAAs located on the military base (AECOM, 2015). From there, they have leached into the ground and contaminated a groundwater aquifer. The hydrogeological setting has favoured the spread of the contamination plume to the South-West by several kilometres and it has spread underneath parts of the nearby town (AECOM, 2016b). The local community has in parts relied on the extraction of groundwater from private wells for various purposes, such as irrigation and live-stock watering. Only very limited personal consumption of groundwater has been reported by most residents. No records are available about the history of the contamination plume prior to the start of the investigations led by the Department of Defence in 2010. The aim of this pilot study was to evaluate the concentration and distribution of PFAAs in environmental samples from within the contamination plume. Furthermore, we assessed the bioaccumulation of PFAAs in grass, various terrestrial animals and animal products in the broader area. Redistribution of PFAAs through the local groundwater extraction, resulting in off-site transport, widespread contamination of the environment and the creation of secondary contamination sources is further discussed. Lastly, we evaluated the concentration and pattern of PFAAs in a few participants that live within the contamination plume and have used the groundwater on their personal properties to assess the impact on local residents. To our knowledge this is the first peer-

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reviewed research study investigating abiotic as well as biotic compartments in an area where contaminated groundwater is used resulting in the spread of contamination into terrestrial ecosystems.

2. Material and methods 2.1. Site history The main AFFF formulation used at the Army Aviation Centre Oakey (AACO) from the 1970s was 6% Light Water™ produced by 3M (AECOM, 2015). Light Water is known to contain PFAAs, especially high concentrations of PFOS and PFHxS, as well as PFAA precursors (3M Company, 1997; Backe et al., 2013; Houtz et al., 2013). Concentrations of PFOS in different formulations of 3M Light Water occur at levels approximately 8–12 times greater than those of PFHxS (Backe et al., 2013). The product was replaced by Ansulite® around 2005, a fluorotelomer-based product which also contains precursors to PFCAs (ANSUL, 2016; Houtz et al., 2013; Place and Field, 2012). Ansulite is still in use to date. PFAA precursors present in AFFF formulations have been shown to transform to stable short-chain PFAAs under environmental conditions and may thus add to environmental PFAA contamination (Houtz et al., 2013). The use of these products, especially 3M Light Water, has caused legacy contamination in soil and concrete at sites where the product was used and has from there migrated into the surrounding environment (AECOM, 2016b). In recent years, Defence Australia became aware of the contamination of the groundwater with PFASs and started a series of investigations to determine the extent of contamination. Fig. 1 shows an overview of the study area and also includes the outline of the estimated PFOS contamination plume as determined by Defence Australia through hydrogeological modelling (AECOM, 2016a). The local residents have been advised not to drink the groundwater sourced from private wells but may continue to use the water for irrigation of lawns and garden beds and other household uses such as laundry and washing of cars.

2.2. Sample collection Environmental and biological samples (groundwater, top 10 cm of surface soil, grass, chicken eggs (yolk), cow, sheep, and horse serum) were collected from the area known to have elevated concentrations of PFAAs in groundwater originating from a nearby fire-fighting training facility (Fig. 1). Serum samples of 10 residents living within the boundaries of the plume were additionally sampled. Samples were collected between March 2015 and March 2016. Table 1 gives an overview of the samples collected. Water, surface soil (top 10 cm) and grass samples were taken in private backyards situated in the plume of PFAAs contamination and in areas that are known to flood with surface water draining from the airfield. Sampled egg yolk were taken from one privately owned chicken coop, while serum samples of cows, sheep and horses were taken from animals raised either within the boundaries of the plume or just outside of the plume. All serum samples were taken by qualified personnel (UQ Ethical Clearance #ANRFA/ENTOX/153/16). Ten residents (six male and four female) voluntarily took part in our study after conferring with their local healthcare practitioner. All of the participants have lived within the present boundaries of the contamination plume for at least more than a decade and operate groundwater bores for everyday activities. Of these ten people only one person reported to have consumed groundwater regularly. Ethical approval was obtained from the Human Research Ethics Committee at the University of Queensland (UQ Ethical Clearance # 2014001211) and all study participants gave informed consent. Serum samples were collected by a private pathology company, Sullivan Nicolaides Pathology, and analysed for their PFAA content at our laboratoy.

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Fig. 1. Sampling sites for water, soil, grass, eggs, horse, sheep and cattle serum samples analysed in this study. Map and estimated PFOS groundwater concentration ranges are indicative only, and do not represent the full extent of borewater and/or aquifer impacts (redrawn from AECOM (2016a)).

2.3. Standards and reagents The target analytes in this study were perfluorobutanoic acid (PFBA), perfluoropentanoic acid (PFPeA) perfluorohexanoate (PFHxA), perfluoroheptanoate (PFHpA), perfluorooctanoate (PFOA), perfluorononanoate (PFNA), perfluorodecanoate (PFDA),

perfluorobutane sulfonate (PFBS), perfluorohexanesulfonate (PFHxS), perfluorooctane sulfonate (PFOS). A mix of isotopically labelled standards used included 13C4-PFBA, 13C2-PFHxA, 13C4-PFOA, 13 C5-PFNA, 13C2-PFDA, 18O2-PFHxS and 13C4-PFOS. Labelled instrument performance internal standards 13C8-PFOA and 13C8-PFOS were used for recovery calculation. All standards were purchased from

Table 1 Overview of samples collected to investigate PFAA exposure in Oakey. Sample

Date sampled

Sample Sample description size

Groundwater Surface water Pond/drinking trough Surface soil (top 10 cm) Grass Cow serum

March 2015 March 2015 March 2015 March 2015

10 1 2 10

Private groundwater bores Lake Pond used for bathing horses and drinking trough Private yards/fields

March 2015 August 2015 to March 2016 March 2016 April 2015 December 2014 June 2015 October 2014

7 15

Private yards Cattle kept within contamination plume until February 2016

12 4 9 7 10

Cattle kept on paddock outside of the contamination plume for most of their lives. Privately owned sheep, kept in backyards Stabled racehorses Private chicken coop, within plume Residents of the town who own and operate a groundwater bore. Six male and four female, aged between 40 and 77 years.

Cow serum Sheep serum Horse serum Egg yolk Human serum


Wellington Laboratories (Guelph, Ontario, Canada). Solvents and reagents used were of analytical grade. 2.4. Sample extraction and analysis All samples were extracted according to matrix specific methods adapted in our laboratory and validated for each matrix separately. Isotopic dilution mass spectrometry was used to determine PFAA concentrations. Further information on extraction protocols can be found in the Supplementary material. Water samples were either directly injected onto an LC-MS/MS system or extracted according to previously published protocols (Gallen et al., 2014; Thompson et al., 2011). Briefly, 50 mL of sample were spiked with 13C8-labelled internal standard and extracted on a solid phase extraction (SPE) manifold using 100 mg Strata™ weak anion exchange (X-AW) cartridges (Phenomenex). Dried soil was spiked with 13C8-labelled internal standard and extracted twice by sonication with methanol/NH3(aq) (99/1). The sample was neutralized, reduced in volume to 1 mL and cleaned up using a 100 mg BondElut Carbon cartridge (Agilent Technologies). Homogenized grass was spiked with 13C8-labelled internal standard, digested overnight with methanol/NaOH and then extracted using ultrasonification. The sample was reduced in volume to 1 mL and cleaned up using a 250 mg BondElut Carbon cartridge (Agilent Technologies). Water, soil and grass samples were made up to a final volume of 1 mL (2:3 methanol/5 mM ammonium acetate in water) and spiked with 13C8-PFOA and 13C8-PFOS labelled performance standards before analysis. Egg yolk (1 g wet weight (ww)) was extracted with acetonitrile according to a published protocol (Baduel et al., 2014). Sample clean-up consisted of liquid-liquid extraction with n-hexane and a 100 mg BondElut carbon cartridge (Agilent Technologies). The final volume of the extract was 1 mL, consisting of 400 μL sample in methanol and 600 μL 5 mM ammonium acetate in water. Serum samples were extracted according to a previously published protocol (Rotander et al., 2015). Briefly, mass labelled internal standards were added to 200 μL of serum and PFAAs were extracted with 1.5 mL acetonitrile using ultrasonication, followed by centrifugation. The supernatant was filtered (Phenomenex RC membrane 0.2 μm syringe filter) and the sample volume reduced to 200 μL. Ammonium acetate in water (5 mM) was added to the sample to a final volume of 500 μL. PFAAs were analysed using high performance liquid chromatography (Nexera HPLC, Shimadzu Corp., Kyoto Japan) coupled to a tandem mass spectrometer (QTrap 5500 AB-Sciex, Concord, Ontario, Canada) operating in negative electrospray ionisation mode and multiple reaction monitoring (MRM) mode. A volume of 5 μL was injected onto a Gemini NX C18 column (50 × 2 mm, 3 μm, 110 Å, Phenomenex, Lane Cove, Australia) held at a constant temperature of 50 °C, and separation of PFAAs was achieved by gradient elution from the column using mobile phases 10% (A) and 90% (B) methanol, respectively, with 5 mM ammonium acetate. A pre-column (C18, 50 × 4.6 mm, 5 μm, Phenomenex, Lane Cove, Australia) was installed between the solvent reservoirs and the injector to trap and delay the background of PFAAs originating from the HPLC system. Identification and confirmation of peaks was done using retention times and comparing the ratios of MRM transition area between the samples and the calibration standards in the same batch of analysis. Quantification was conducted using labelled PFAAs. Calibration standards were made up in 1000 μL (400 μL methanol and 600 μL 5 mM ammonium acetate in water). The concentration range of the eight prepared calibration standards was 0.1–100 μg/L (0.1; 0.4; 1; 4; 10; 20; 40; 100). 2.5. Analytical quality assurance Calibration standards were injected three times in each batch of samples. Quality control standards, including duplicate samples, native

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spikes, and procedural blanks were added to the batch and treated in the same way as the real samples. No PFAA contamination was found in procedural or instrument blanks. Quantification of PFAAs was performed using a linear regression fit analysis weighted by 1/x of the calibration curve. Limits of quantification (LOQ) were set at 10 times the standard deviation of the lowest standard with a signal-to-noise higher than 10 after 8 injections as well as a minimum signal-to-noise ratio of 10 in the matrix. Matrix specific LOQs and average recoveries for each matrix are listed in Table S1 and S4 of the Supplementary Information and are based on extraction mass of each sample matrix. All values reported are corrected for recovery of the surrogate standards. The authors have successfully taken part in two interlaboratory studies run by the National Measurement Institute of Australia targeting PFOA, and linear and total PFOS in water, soil and biota. 3. Results and discussion PFAAs were detected in all biological and environmental matrices investigated in this study. Table 2 gives an overview of the average concentrations as well as ranges of PFAAs measured, and frequencies of detection for each matrix are shown in Table S1 (Supplementary Information). Varying concentration patterns can be observed for each matrix, reflecting the different accumulation potentials as well as different exposure pathways. In all matrices PFOS was generally the most abundant PFAA, followed by PFHxS, making these the chemicals of greatest concern in this study. The presence of mainly PFOS and PFHxS in environmental and biological samples further supports the fact that the main AFFF formulation used at the AACO site was 3M Light Water™ (Backe et al., 2013). 3.1. Concentrations and patterns of PFAAs in environmental matrices PFOS and PFHxS were detected in most water samples and at the highest concentrations of all PFAAs investigated. Other PFAAs detected in over 50% of the water samples include PFBA (64%), PFPA (57%), PFHxA (79%), PFOA (79%) and PFBS (79%). Although detected frequently, concentrations of these were generally below 1 μg/L. PFNA was not detected above the LOQ in any water samples. Highest PFOS concentrations measured in groundwater were 13 μg/L, with an average of 4.3 μg/L and generally agreed with the contamination ranges determined by Defence Australia for groundwater bores in the respective areas (cf. Fig. 1); and were comparable to concentrations measured in contaminated private wells in the vicinity of a fire training area in Cologne, Germany Weiß et al. (2012). The maximum PFOS concentration detected in groundwater was N800-fold higher compared to the highest concentrations measured in Australian drinking water (Thompson et al., 2011). The Environmental Health Standing Committee (enHealth) of the Australian Health Protection Principal Committee has set interim national guideline values for the sum of PFOS and PFHxS in drinking water at 0.5 μg/L (enHealth, 2016). With the exception of a single bore, all groundwater bores tested substantially exceeded the guideline value for combined PFOS/PFHxS, supporting Defence Australia's advice to residents to not drink the bore water and instead supply alternate drinking water sources. In addition to groundwater, surface water from a lake and water samples from a horse dip and an animal drinking trough (originally sourced from groundwater) were analysed. The lake lies directly south of the airfield, with one of the above ground drain lines originating at the airfield feeding into it. PFOS concentrations measured here were 0.4 μg/L, which was lower compared to groundwater concentrations measured in the vicinity. While the lake does not serve as a drinking water source to humans it is accessible to native wildlife. The horse dip and animal drinking trough are periodically refilled with groundwater. Through evaporation and refilling PFAA concentrations may increase over time. Both, the horse dip and drinking trough, showed concentrations 1 μg/L higher than the respective groundwater


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Table 2 PFAA concentrations measured each matrix. Mean values with standard deviation and range.

PFBA PFPeA PFHxA PFHpA PFOA PFNA PFDA PFBS PFHxS L-PFOS T-PFOS

Water (n = 13) μg/L

Soil (n = 10) μg/kg dw

Grass (n = 7) μg/kg ww

Egg yolk (n = 7) ng/g yolk

Cow ‘inside plume’ (n = 15) μg/L serum

Cow ‘outside plume’ (n = 12) μg/L serum

Sheep (n = 4) μg/L serum

Horse (n = 9) μg/L serum

Human (n = 10) μg/L serum

0.2 ± 0.1 (b0.08–0.3) 0.2 ± 0.1 (b0.08–0.3) 0.6 ± 0.5 (b0.08–1.4) 0.2 ± 0.1 (0.1–0.2) 0.2 ± 0.2 (b0.05–0.6) 0.15 N.C. 0.12 N.C. 0.5 ± 0.3 (b0.05–1) 2.4 ± 1.9 (b0.07–6) 2.6 ± 2.4 (b0.17–7.2) 4.6 ± 4.4 b0.17–13

0.8 ± 0.9 (b0.1–3) 1.7 ± 1.6 (0.2–5.2) 8.4 ± 8.2 (b0.2–26) 1 ± 0.6 (b0.2–2) 1.6 ± 2.3 (b0.1–7) 0.55 N.C. 0.4 ± 0.2 (b0.1–0.7) 2.1 ± 1.8 (b0.1–6) 13 ± 23 (b0.1–74) 183 ± 429 (2–1388) 227 ± 522 (2–1692)

11 ± 8 (3–27) 4± 5 (b0.3–14) 3± 2 (0.5–6) b0.4 N.C. 0.6 ± 0.3 (b0.2–0.8) b0.3 N.C. b0.2 N.C. 7± 8 (0.4–24) 10 ± 8 (1–26) 23 ± 21 (1–53) 32 ± 28 (2–68)

0.25 ± 0.07 (0.12–0.36) b0.08 N.C. b0.08 N.C. b0.1 N.C. 0.53 ± 0.24 (b0.05–0.68) 0.12 ± 0.06 (b0.09–0.13) 0.24 ± 0.1 (0.12–0.39) 0.07 ± 0.04 (b0.05–0.09) 13 ± 2.2 (10–16) 48 ± 8 (39–60) 70 ± 10 (57–84)

0.55 N.C. b0.5 N.C. b0.5 N.C. b0.1 N.C. 0.24 ± 0.1 (b0.12–0.44) 4 ± 3.2 (b0.2–11.5) 9.7 ± 8.6 (b0.2–31) b0.2 N.C. 52 ± 37 (2–125) 383 ± 347 (18–1167) 509 ± 490 (24–1583)

b0.5 N.C. b0.5 N.C. b0.5 N.C. b0.1 N.C. 0.22 ± 0.11 (b0.12–0.21) 1.92 N.C. 6.9 N.C. b0.2 N.C. 7 ± 5.6 (0.5–18) 56 ± 22 (25–95) 118 ± 51 (56–215)

1 ± 0.6 (b0.5–1.3) b0.5 N.C. b0.5 N.C. b0.1 N.C. 0.2 ± 0.1 (0.1–0.3) b0.2 N.C. 0.3 ± 0.2 (b0.2–0.3) 0.2 ± 0.1 (b 0.2–0.23) 63 ± 45 (32–129) 86 ± 21 (68–116) 180 ± 54 (137–259)

N.A. N.C. N.A. N.C. N.A. N.C. b0.1 N.C. b0.1 N.C. b0.2 N.C. 0.21 N.C. b0.2 N.C. 33 ± 17 (18–74) 36 ± 15 (18–58) 83 ± 31 (43–129)

b0.5 N.C. 0.8 ± 0.4 (b0.5–0.9) b0.5 N.C. b0.1 N.C. 4.7 ± 1.9 (2–9) 0.6 ± 0.3 (b0.2–1) 0.4 ± 0.2 (b0.2–0.5) b0.2 N.C. 93 ± 49 (39–214) 136 ± 107 (27–303) 172 ± 133 (38–381)

N.A. = not analysed. N.C. = not calculated.

concentration at the sites from which they are refilled. However, it was not determined if this difference was statistically significant. Soil samples were taken from residential back yards and fields around the town. Detection frequencies of the 10 investigated PFAAs were comparable to those observed in the water samples. Only one soil sample had all 10 PFAAs detected above the LOQ. PFOS was detected at the highest concentration compared to other PFAAs, with concentrations between 2.3 and N1600 μg/kgdw. In water samples the ratio between PFOS and PFHxS was 0.3 to 2.8 (linear PFOS:PFHxS, c.f. Fig. S1, Supporting Information); the ratio in soil varied from 4 and 46 for the different sites (Fig. S1, Supporting Information). Generally, sorption to soil increases with increasing carbon chain length; sulfonic acids are sorbed stronger than carboxylic acids of the same chain length; and sorption increases with increasing organic carbon content and decreasing pH (Higgins and Luthy, 2006). In the topsoil investigated in this study the shorter chain PFHxS may have already leached further down in the soil column compared to PFOS, thereby increasing the ratio between the two compared to initial ratios in groundwater. Soil contamination is thought to have occurred primarily through watering of yards/crops with bore water, and occasional flooding of drains originating at the airfield after heavy rainfalls in few locations. No national guideline values exist for residential soil in Australia, but the Government of Western Australia proposed an interim health based screening value of 4000 μg/kg of PFOS in residential soil (Government of Western Australia, 2016) and advises that further assessment of risks and a conservative management approach should be adopted if levels exceeding the screening value are found. All tested soils were below this limit. However, scientific literature indicates that accumulation of PFAAs into edible vegetables, for example, can occur readily at low PFAA levels (Blaine et al., 2014a; Lechner and Knapp, 2011; Wen et al., 2014), indicating a potential entry point into the human food chain. Blaine et al. (2014b) further determined uptake of PFAAs into lettuce and strawberry fruit watered with PFAA spiked water at concentrations representative of contaminated groundwater and showed high uptake potential for PFAAs. While the uptake and accumulation potential into plants is highest for very short chain PFAAs, it is possible for longer chain PFAAs such as PFOS and PFHxS to be taken up, especially into leafy vegetables (Blaine et al., 2014b; Felizeter et al., 2012).

3.2. Concentrations and patterns of PFAAs in biological samples 3.2.1. Grass analysis PFAAs were measured in all grass samples taken in backyards with PFOS concentrations ranging between 2 and 68 μg/kggrass, ww, and confirmed that a translocation of PFAAs had taken place from the contaminated groundwater and/or soil into grass. Higher detection frequencies and concentrations of short chain PFAAs were measured in grass compared to any other matrix investigated. However, despite the lower accumulation potential of longer chain PFAAs in plants (Blaine et al., 2014b; Stahl et al., 2009) absolute concentrations of PFHxS and PFOS in grass were still highest, due to initially high concentrations of these chemicals in soil and water. 3.2.2. Livestock serum analysis Serum was analysed in cattle (n = 27), horses (n = 9) and sheep (n = 4), all of which were kept either within the contamination plume or close by (cf. Fig. 1). Sheep were kept in enclosures within the contamination plume and were watered with groundwater. Average concentrations of PFOS and PFHxS measured in sheep serum (n = 4) were 151 μg/L and 63 μg/L, respectively, and were the major contributors to total PFAAs measured in sheep. PFBA was the only short chain PFAA detected in two of the sheep, while other PFAAs detected were PFOA, PFBS and PFDA. Race horses, kept mostly in stables within the contamination plume and fed groundwater, showed overall lower concentrations compared to sheep. PFOS and PFHxS concentrations averaged 83 and 33 μg/L, respectively. Different concentrations and patterns of PFAAs measured in livestock species can be attributed to different initial source concentrations of PFAAs, species-specific uptake and metabolism/excretion patterns, as well as varying food and water sources. The average ratios of linear PFOS to PFHxS among most sample matrices were similar, ranging between 1 and 4 (Fig. S1, Supporting Information). Solely soil and cattle had higher ratios (linear PFOS:PFHxS) and may in part reflect dietary uptake of soil in cattle. However, this would have to be confirmed in future studies. PFAA concentrations in animals of two cattle herds, mixed female cows and calves (both male and female), kept in separate areas (c.f. Fig. 1) were investigated. One herd was kept in paddocks in between


the township and the airfield and is from hereon called ‘inside plume’. These animals grazed on paddocks south of the airfield along drains running off from the base, and on areas that had periodically flooded after heavy rainfalls. The second herd (referred to as ‘outside plume’) was kept on paddocks outside of the plume (marked in Fig. 1) for most of their lives. However, the older cows in the herd were kept within the contaminated area for a short period of time during their younger years. It was unfortunately not possible to reconstruct the exact whereabouts of the herd. Furthermore, the borders of the plume are based on hydrogeological modelling and are only indicative, therefore the herd ‘outside of the plume’ may still be kept in a more diluted part of the plume. Nonetheless, a clear difference in the contamination pattern of the two herds was visible. The short chain PFBA was detected in 7% of cattle inside the plume and none outside of the plume. Other short chain PFAAs were not detected in either group. PFOA (range b0.12– 0.21 μg/L), PFNA and PFDA were all detected in 93% of the cattle serum from inside the plume, while in cattle kept outside of the plume PFOA (range b0.12–0.44 μg/L) was detected in 100% of the samples and PFNA and PFDA only in each 8% of samples. PFHxS and PFOS were detected in 100% of samples, both inside and outside of the plume. Concentrations of PFOS ranged from 24 to 1283 μg/L and PFHxS from 2 to 125 μg/L in cattle kept inside the plume. In cattle outside of the plume PFOS concentrations ranged from 56 to 215 μg/L and PFHxS concentrations from 0.55 to 18 μg/L (Fig. 2). The median PFOS (303 μg/L) and PFHxS (52 μg/L) concentrations in cattle serum from cows pastured inside the plume was higher than the 95th percentile of the ones pastured outside of the plume. For both PFOS and PFHxS concentrations measured for the two groups (Inside and Outside of the plume) were statistically different from each other (Unpaired ttest with Welch's correction, p b 0.01). The cows outside of the plume still had concentrations of PFOS and PFHxS in the same order of magnitude as the sheep living inside the plume, a potential reason for this may be access to groundwater from a more dilute part of the groundwater plume or early exposure of the mothers during a time when they were kept inside the plume and subsequent transfer of PFAAs to calves through milk (Kowalczyk et al., 2013). Cattle living inside the plume could have been exposed to PFAAs through multiple routes: either directly through drinking of contaminated groundwater and surface water, or indirectly through the consumption of contaminated soil and grass. A combination of both is the most likely scenario. The paddock in which the herd was kept inside the plume flooded periodically after large rainfalls from the drain leading away from the airfield. A soil sample taken on this paddock showed concentrations of PFOS and PFHxS of 280 μg/kgd.w and 7 μg/kgd.w, respectively. A transfer of PFAAs from soil to grass is likely and could represent a concentrated source of PFAAs for cattle grazing in the area. Furthermore, cattle are known to ingest

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between 1% and 18% of soil as a percentage of total daily dry matter intake while foraging, and thus direct ingestion of contaminated soil could be a major exposure source of PFAAs for cattle (Thornton and Abrahams, 1983). The similarly high ratios of PFOS:PFHxS found in soil and cattle serum (Fig. S1) may be an indication of this dietary exposure to soil. 3.3. Chicken egg analysis Egg yolks (n = 7) of chickens kept in a coop inside the PFOS contamination plume and fed groundwater were analysed for their PFAA content. PFBA was detected in all samples analysed, together with PFDA, PFOS and PFHxS. Other PFAAs detected included PFOA, PFNA and PFBS. Only PFOS and PFHxS were detected at concentrations above 1 ng/gyolk ww, at average concentrations of 70 and 13 ng/gyolk ww, respectively. PFOS concentrations were above levels measured in yolk from chickens in the Netherlands and from Greece, where average concentrations were 3.5 and 1.1 ng/gyolk, ww, respectively (Zafeiraki et al., 2016). D'Hollander et al. (2011) measured yolk concentrations ranging between 53 and 3885 ng/gyolk, ww in home-produced chicken eggs which were kept in the vicinity (b1 km) of a perfluorochemical production plant in Zwijndrecht, Belgium. 3.4. Human serum analysis PFOS, PFHxS and PFOA were detected in 100% of blood serum samples analysed. Concentrations measured ranged from 38 to 381 μg/L for PFOS (average of 172 μg/L) and 39 to 214 μg/L for PFHxS (average of 93 μg/L). Average PFOA concentrations measured were 4.6 μg/L (ranging from 2 to 9 μg/L). Other long chain PFAAs, PFNA and PFDA, were detected in 80 and 70% of samples analysed, respectively, although concentrations of these ≤1 μg/L in all cases. The only short chain PFAA detected was PFPeA, with concentrations below 1 μg/L. However, short chain PFAAs are known to have a relatively short half-life in human serum (Chang et al., 2008; Olsen et al., 2007), and detection of PFPeA may therefore be indicative of recent PFAA exposure in some of the study participants. A comparison of the serum levels measured in the present study to those measured elsewhere is shown in Fig. 3. Toms et al. (2014) derived a median concentration of PFOS of 9.4 μg/L serum for the general Australian population from 24 pools of blood serum containing 2400 individual samples. Upper boundaries (95th percentiles) for these pooled datasets were derived by Aylward et al. (2014) for the 2011/2012 cohorts of pooled samples of the general Australian population, divided into age groups. For the highest age group investigated (N 66 years) the 95th percentile was 37.8 μg/L serum. All PFOS concentrations

Cattle: PFHxS

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Fig. 2. Concentrations of PFOS (μg/Lserum) and PFHxS (μg/Lserum) of cattle kept within the contamination plume compared to cattle kept mostly outside the contamination plume. Box extends from 25th to 75th percentile, line shows median, whiskers show 5th and 95th percentile. For both PFOS and PFHxS statistical difference found between ‘Inside plume’ and ‘Outside plume’ (t-test with Welch's correction, p b 0.01).

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3.5. Creation of secondary sources and implications for human exposure pathways

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Fig. 3. Comparison of human serum PFOS concentrations in this study (n = 10), the general Australian population (Toms et al., 2014), the general US American population (Kato et al., 2011), and two occupationally exposed cohorts (Olsen et al., 2007; Rotander et al., 2015). The bars indicate median values in this study, AUS, 3M and fire fighters and geometric mean in USA. Whiskers show 95th percentile in USA and range in this study, AUS, 3M and fire fighters.

measured in the present study exceeded this 95th percentile for the Australian (Aylward et al., 2014) and the 95th percentile for the US American general populations (Kato et al., 2011). The median PFOS serum concentration in the present study (123 μg/L) showed a 3-fold increase above these 95th percentiles. Median PFOS levels measured in this study were 5-fold lower compared to an exposed cohort of 3M workers from a fluorochemical production facility (Olsen et al., 2007). A comparison to another occupationally exposed cohort (Rotander et al., 2015) showed that serum levels measured in this study were comparable to levels measured in 149 Australian firefighters who had direct exposure to AFFF. However, their exposure to AFFF had ceased approximately 10 years prior to sampling, so serum concentrations directly after exposure would have been higher. Additionally, Rotander et al. (2015) measured biochemical markers (serum cholesterol, triglycerides, high-density lipoproteins, low density lipoproteins, and uric acid) in serum collected of the firefighter cohort, but found no statistically significant associations between these and PFAA exposure. Comparison of serum concentrations measured in this study to the above mentioned studies clearly show that exposure of residents has occurred at levels above what would be expected from normal day-to-day exposure. PFOA concentrations were comparable to those reported by Toms et al. (2014) for the general Australian population (average of 4.5 ± 0.8, range of 3.1 to 6.5). This, as well as the relatively low concentrations of PFOA measured in all other matrices, suggests that PFOA-based AFFF was not used at the fire training ground, or only in very low quantities, and the exposure seen in residents is likely due to every day background exposure. A wider study of community members at the here investigated site was initiated by Defence Australia, in which 75 residents participated (Heffernan, 2015, as reported by AECOM, 2016a). Mean concentrations reported were 69 μg/L and 46 μg/L, for PFOS and PFHxS, respectively. These results, although lower than those reported here, are also elevated above the 95th percentile of the Australian general population (Aylward et al., 2014). However, it is not clear if the participants of the Defence study were all current residents of the community, or if they had lived within the contamination plume and for what duration. The results from our study population are biased towards higher concentrations, as we samples serum from residents known to have exposure to groundwater through the use of bores on their private property.

The continuous use of contaminated groundwater in a relatively dry environment can create new ‘hotspots’ of contamination. Concentrations of PFAAs in soil will likely increase in areas where yards are continuously irrigated, especially around groundwater bores where dripping and spillages of the contaminated water may occur more frequently. Thus, over time, secondary sources of PFAAs are created, from where they are once again cycled through the environment. PFAAs can migrate back into the groundwater over time, dependant on their hydrophobicity and local soil characteristics, and accumulate into plants and vegetables. Multiple entry points into terrestrial food-webs are thus created from an original point source that lies several kilometres away. Many residents of the community have privately owned groundwater bores on their properties that are currently or historically used for everyday activities. Major uses include irrigation of gardens, indoor use for cooking and laundry, washing of cars and animals and in certain cases the now ceased use of groundwater as a drinking water source. With these uses come a multitude of direct human exposure pathways to PFAAs, connected to exposure to contaminated water. In addition, it is not uncommon for residents to consume home-grown produce such as eggs, vegetables, dairy and meat. Kowalczyk et al. (2012) investigated the uptake and tissue distribution of PFOS and PFOA in dairy sheep fed with contaminated corn silage for 21 days. Concentrations of linear PFOS measured in blood plasma by Kowalczyk (n = 2, 168 and 240 μg/L) were higher compared to serum concentrations measured in this study (n = 4, range 68–116). Muscle tissue concentrations of the sheep sacrificed directly following the exposure period were 35 ng/g PFOS, the second sheep was allowed a 21-day depuration period but it was found that PFOS concentrations did not decrease markedly during this time. A similarly controlled study was conducted by Lupton et al. (2015) in beef cattle fed a single oral dose of PFOS to determine tissue distribution and half-life in plasma and muscle PFOS was distributed to all major organs, including the most commonly consumed meatcuts, and half-lives were estimated as 106–120 days and 110– 150 days for plasma and muscle tissue, respectively. Vestergren et al. (2013) investigated bioaccumulation of PFAAs in dairy cows in a naturally contaminated environment and concluded that based on derived biotransfer factors for meat and milk long chain PFAAs have a relatively high potential to transfer from contaminated feed to meat and milk. Combined with accumulation of PFAAs from the water phase into livestock, as shown in this study, consumption of meat and other animal products produced locally may be a major dietary source of PFAAs to humans. The tolerable daily intake (TDI) of PFOS that has been adopted in many countries around the world is set at 150 ng/kg body weight per day (EFSA, 2008). Australia has very recently (April 2017) revised the adoption of this value and derived updated TDIs which are substantially lower than the ones derived by EFSA. The health-based guidance values for PFOS and PFHxS were released by Food Standards Australia and New Zealand (FSANZ, 2016) and are set at 20 ng/kg body weight per day for the sum of PFOS and PFHxS. The TDI could be exceeded in residents living in the contaminated area through uptake of PFAAs through multiple exposure routes, leading to an accumulation of PFOS above that of the general Australian population. With the newly released health-based guidance values by FSANZ there may be a need to revise the risk of secondary sources of contamination to humans and provisions of maximum allowable concentrations in foods such as meat, dairy and eggs from contaminated areas may become a necessity. 3.6. Future perspectives Baduel et al. (2015) showed that a point source such as a concrete fire training pad can be an ongoing source of PFOS contamination for several decades, while Filipovic et al. (2015) showed the extent of PFAA contamination in soil and water surrounding a fire training


ground point source. Effective remediation and management of these highly-contaminated areas should therefore be a priority. However, remediation of the already contaminated groundwater is a challenge, and this study has shown how the continuous use of contaminated groundwater can further the spread of contamination even into terrestrial ecosystems, which can increase human exposure. Granular activated carbon (GAC) filtration has been shown to remove the longer chain PFAAs from contaminated water (Lampert et al., 2007; Yu et al., 2009) and has been an effective and affordable technology in lowering exposure of residents in PFOA contaminated areas (Bartell et al., 2010; Brede et al., 2010). Application of GAC filtrations directly on residential groundwater bores at the location investigated in this study may lower direct exposure of residents. Further exposure from contaminated soils in backyards and pastures should be prevented, soil capping or exchange in cases of high contamination may be an option. Groundwater plays a significant role in providing water for domestic, recreational, rural and industrial use, and serves to maintain wetlands and streams during dry periods. Across Australia groundwater accounts for 30% of the total water consumption and yearly N5000 GL of groundwater are used (Harrington and Cook, 2014). Groundwater is a resource of major importance, particularly for arid rural communities, and needs to be protected, especially from poorly-reversible contamination such as PFAAs. Acknowledgements JFM acknowledges funding by an ARC future fellowship (FF120100546). JB receives a University of Queensland International Scholarship. The authors would like to thank residents of the study site for participating in this research, Sullivan Nicolaides Pathology for processing of blood samples and Darling Downs Vets for sample collection. The Queensland Alliance for Environmental Health Sciences, The University of Queensland gratefully acknowledges the financial support of the Queensland Department of Health. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2017.04.095. References 3M Company, 1997. Material Safety Data Sheet for FC-203CF Light Water Brand Aqueous Film Forming Foam St. Paul, MN. AECOM, 2015. PFC Background Review and Source Study. Army Aviation Centre, Oakey Available from:. http://www.defence.gov.au/id/oakey/Documents.asp. AECOM, 2016a. Stage 2C Environmental Site Assessment. Oakey, Army Aviation Centre. AECOM, 2016b. Stage 2C Environmental Site Assessment. Oakey, Army Aviation Centre. Ahrens, L., Bundschuh, M., 2014. Fate and effects of poly- and perfluoroalkyl substances in the aquatic environment: a review. Environ. Toxicol. Chem. 33 (9), 1921–1929. ANSUL, 2016. Data Sheet: Ansulite A364 3%x6% AR-AFFF Concentrate, Marinette, WI, USA. Aylward, L.L., Green, E., Porta, M., Toms, L.-M., Den Hond, E., Schulz, C., Gasull, M., Pumarega, J., Conrad, A., Kolossa-Gehring, M., Schoeters, G., Mueller, J.F., 2014. Population variation in biomonitoring data for persistent organic pollutants (POPs): an examination of multiple population-based datasets for application to Australian pooled biomonitoring data. Environ. Int. 68, 127–138. Backe, W.J., Day, T.C., Field, J.A., 2013. Zwitterionic, cationic, and anionic fluorinated chemicals in aqueous film forming foam formulations and groundwater from U.S. military bases by nonaqueous large-volume injection HPLC-MS/MS. Environ. Sci. Technol. 47 (10), 5226–5234. Baduel, C., Lai, F.Y., Townsend, K., Mueller, J.F., 2014. Size and age–concentration relationships for perfluoroalkyl substances in stingray livers from eastern Australia. Sci. Total Environ. 496, 523–530. Baduel, C., Paxman, C.J., Mueller, J.F., 2015. Perfluoroalkyl substances in a firefighting training ground (FTG), distribution and potential future release. J. Hazard. Mater. 296, 46–53. Bartell, S.M., Calafat, A.M., Lyu, C., Kato, K., Ryan, P.B., Steenland, K., 2010. Rate of decline in serum PFOA concentrations after granular activated carbon filtration at two public water systems in Ohio and West Virginia. Environ. Health Perspect. 118 (2), 222–228. Blaine, A.C., Rich, C.D., Sedlacko, E.M., Hundal, L.S., Kumar, K., Lau, C., Mills, M.A., Harris, K.M., Higgins, C.P., 2014a. Perfluoroalkyl acid distribution in various plant compartments of edible crops grown in biosolids-amended soils. Environ. Sci. Technol. 48 (14), 7858–7865.

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