Article pubs.acs.org/JAFC
Perfluorooctane Sulfonate Plasma Half-Life Determination and LongTerm Tissue Distribution in Beef Cattle (Bos taurus) Sara J. Lupton,*,† Kerry L. Dearfield,‡ John J. Johnston,§ Sarah Wagner,⊥ and Janice K. Huwe†,¶ †
Biosciences Research Laboratory, Agricultural Research Service, USDA, 1605 Albrecht Boulevard, Fargo, North Dakota 58102, United States ‡ Office of Public Health Science, Food Safety and Inspection Service, USDA, 1400 Independence Avenue SW, Washington, DC 20250, United States § Office of Public Health Science, Food Safety and Inspection Service, USDA, 2150 Centre Avenue, Building D, Suite 320, Fort Collins, Colorado 80526, United States ⊥ Department of Veterinary Technology, North Dakota State University, Hultz Hall Rm 165, Fargo, North Dakota 58102, United States S Supporting Information *
ABSTRACT: Perfluorooctane sulfonate (PFOS) is used in consumer products as a surfactant and is found in industrial and consumer waste, which ends up in wastewater treatment plants (WWTPs). PFOS does not breakdown during WWTP processes and accumulates in the biosolids. Common practices include application of biosolids to pastures and croplands used for feed, and as a result, animals such as beef cattle are exposed to PFOS. To determine plasma and tissue depletion kinetics in cattle, 2 steers and 4 heifers were dosed with PFOS at 0.098 mg/kg body weight and 9.1 mg/kg, respectively. Plasma depletion half-lives for steers and heifers were 120 ± 4.1 and 106 ± 23.1 days, respectively. Specific tissue depletion half-lives ranged from 36 to 385 days for intraperitoneal fat, back fat, muscle, liver, bone, and kidney. These data indicate that PFOS in beef cattle has a sufficiently long depletion half-life to permit accumulation in edible tissues. KEYWORDS: perfluorooctane sulfonate, PFOS, plasma, half-life, beef cattle, residue, food safety
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INTRODUCTION Perfluorooctane sulfonate (PFOS) is an industrial surfactant used in the manufacturing of numerous consumer products due to its chemical and thermal stability.1−3 PFOS may also occur as a breakdown product from other polyfluoroalkyl and perfluoroalkyl compounds used in plastics, textiles, and electronics.1−4 Numerous investigators have documented that PFOS is ubiquitous in the environment, bioaccumulates in biota, and is of toxicological concern. 1−3,5−10 Several toxicological end points associated with PFOS include hepatocellular hypertrophy observed in monkeys (chronic dose of 0.75 mg/kg/day) and neonatal mortality from utero exposure in rats at 1.6−3.2 mg/kg/day.1−3,5−10 Human exposures to PFOS are mainly through the consumption of contaminated food animal products.2,7,10 The estimated half-life of PFOS in humans is 5.4 years,1 indicating that prolonged exposures and possible toxic outcomes could occur after singular point exposures or with chronic accumulation of lowlevel PFOS exposures. Half-lives of PFOS have been determined in other animals including rats (>90 days),6 birds (chickens, 125 days; mallard ducks, 6.9 days),11 monkeys (200 days),8 and food animals (116 days)12 from previous studies. PFOS residues have been measured in biosolids from wastewater treatment plants (WWTPs) and as a result is a major contributor to the intake of PFOS by cattle from contaminated soil and/or contaminated plant material due to use as fertilizer on pastures and croplands.13−17 The transfer of PFOS from biosolid amended soils and fields to crop and © 2015 American Chemical Society
forage plants (e.g., wheat, maize, rye grass, tall fescue, Bermuda grass, and Kentucky bluegrass) has been demonstrated in previous studies.13−19 Specifically, studies by Kowalczyk et al.18,20 and Numata et al.21 examined contaminated feed (grown on contaminated fields) fed to ewes, dairy cows, and fattening pigs, respectively, and provided evidence of the bioavailability and transfer of PFOS from plant material to food-producing animals. Determining the half-lives of chemical residues in food animals after exposure is important to establish potential concentrations in animal food products that may be consumed by humans. In a short-term 28 day study, we previously demonstrated that a single dose of PFOS is well absorbed by beef cattle and remains in systemic circulation through 28 days.12 From the concentrations of PFOS in urine and feces, a body burden depletion half-life for PFOS was estimated to be 116 days. Due to the limited data obtained from the 28 day study, estimating a terminal plasma PFOS elimination half-life was not possible. In addition, plasma data indicated that PFOS concentrations increased a second time 15 days after initial dosing, strongly suggesting that in cattle PFOS is redistributed from another body compartment.12 To better define plasma PFOS kinetics and generate additional tissue distribution data, a Received: Revised: Accepted: Published: 10988
September 18, 2015 November 23, 2015 December 6, 2015 December 18, 2015 DOI: 10.1021/acs.jafc.5b04565 J. Agric. Food Chem. 2015, 63, 10988−10994
Article
Journal of Agricultural and Food Chemistry
10 mL MTBE aliquots were added to each tube and capped tubes were shaken horizontally for 20 min using a shaking water bath (100 rpm). Separation of the MTBE layer was achieved by centrifugation (1160g for 20 min). The top layer (MTBE) was removed with a Pasteur pipet, and the MTBE extraction was repeated twice, with 8 and 6 mL additions. MTBE extracts were concentrated to 0.5 mL under nitrogen and transferred into 1.5 mL snap-cap tubes. To each extract was added 0.5 mL of HFP. Samples were vortex mixed and allowed to stand in a −20 °C freezer for 10 min to aid particle formation. Samples were then centrifuged at 17 000g for 15 min. Supernatant was syringe filtered through a 0.45 μm nylon filter and filtered extract was evaporated to dryness under nitrogen, reconstituted in 0.5 mL HPLCgrade MeOH, and syringe filtered a second time through a 4 mm, 0.2 μm nylon filter. An internal standard of PFOA (final concentration 100 pg/μL) was added before liquid chromatography tandem mass spectrometry (LC-MS/MS) analysis. Skin samples were digested in 12.5 mL of a 2.5% sodium hydroxide solution (w/v). Each sample was vortex mixed and placed into a shaking (100 rpm) water bath at 65 °C for 24 h. Tubes were removed, allowed to cool, and 1.5 mL of 0.5 M TBAHS (pH 10) was added to each tube. Tubes were vortex mixed, 6 mL of MTBE was added, and horizontally shaken (100 rpm) in a water bath for 20 min, and centrifuged at 1160g for 20 min. The MTBE layer was removed with a Pasteur pipet, and the extraction was repeated twice with 5 and 4 mL additions of MTBE. Sample extracts were then processed similar to bone samples above using HFP, centrifugation, and syringe filtering. The LC-MS/MS method, standard curve preparation, and QA/QC protocols were described previously in Lupton et al.12 For skin and bone, matrix-matched standard curves were prepared because of ion enhancement during mass spectrometric analysis. Other tissues, however, had minimal matrix effects and were quantified with respect to a standard curve prepared in solvent. All heifer extracts needed to be diluted (1:2 to 1:20) due to the high PFOS concentrations. All samples were quantified using internal standard added before LC-MS/ MS analysis as stated above. Kinetic Parameter Estimates. Elimination parameters (E and α) for PFOS were estimated using the mean concentrations from plasma versus time data (105−343 days) by noncompartmental methods (PKSolutions; Summit Research Services; Montrose, CO). Data from 105 to 343 days were used to describe the plasma elimination phase and to estimate the plasma elimination half-life. For predictive purposes, plasma concentrations at each time point were averaged across all animals within the same dose level, and least-squares parameter estimates were calculated after curve-stripping. Predicted plasma PFOS concentrations (Ct) were calculated using
year-long disposition study was completed using high and environmentally relevant PFOS doses in Angus cattle. The study provided PFOS half-life data in cattle and also provided long-term tissue distribution data. Half-life and distribution data are very useful for risk assessments and determining potential dietary PFOS exposure levels in humans.
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MATERIALS AND METHODS
Chemicals. Ammonium acetate, perfluorooctane sulfonate (purity ≥98%), and tetrabutyl ammonium sulfate (TBAHS) were purchased from Sigma-Aldrich (St. Louis, MO). Other chemicals included 1,1,1,3,3,3-hexafluoroisopropanol (HFP; TCI, Portland, OR), HPLCgrade methanol (MeOH; Honeywell Burdick and Jackson, Morristown, NJ), sodium carbonate (Fisher, Pittsburgh, PA), and methyl tertbutyl ether (MTBE; BDH, Radnor, PA). Experimental Design and Sample Collection. Eight Angus steers (n = 4) and heifers (n = 4) were purchased and held at North Dakota State University (NDSU) animal pasture facilities during the summer of 2011 (May 31−September 1) and in indoor pens from September 1, 2011 to May 10, 2012. When housed indoors, cattle were provided ad libitum access to water and grass hay with a daily allotment of 2.3 kg of rolled corn. Drinking water was analyzed for PFOS and was not detected. Pasture land was not tested for PFOS, but no biosolids have been applied prior to use for animals. Three steers (307.3 kg ±11.1 kg) were given a single oral bolus dose of PFOS at 0.098 mg/kg body weight (bw), and four heifers (308.1 kg ±29.9 kg) were given single oral bolus doses at 9.09 mg/kg bw. Bolus doses consisted of a gelatin capsule containing ground corn and the PFOS dose. All animals were dosed in a single day after a 0 time point blood sample was drawn. A single steer was supposed to serve as a control animal. However, during dosing, one of the dosed steers ejected its dose, which went unnoticed until the blood analysis revealed no detectable PFOS. Presumably, due to their proximity to dosed cattle (housing in pasture and indoor pens), control steers had low levels of contamination through ingestion or dermal contact. The misdosed animal must have disgorged its dose very soon after dosing because the PFOS concentrations were similar or lower than the actual control steer. Animals were weighed at the end of each month to ascertain healthy growth. Blood (10 mL) was drawn via the jugular vein at intervals of 0, 4, 12, and 24 h and 2, 3, 6, 9, 15, 22, 30, 42, 56, 77, 105, 119, 133, 161, 175, 203, 238, 266, 294, 329, and 343 days relative to dosing. After placing cattle into head gates, blood was drawn into heparinized polypropylene Vacutainer tubes (BD, Franklin Lakes, NJ) using 21 gauge needles and centrifuged at 1160g for 15 min at 5 °C to separate plasma and cells. Plasma was removed from the cell layer, transferred to labeled 15 mL Sarstedt polypropylene tubes (Newton, NC), and stored at −20 °C until analysis. After a period equivalent to an approximate body burden half-life for PFOS in cattle (114 days12), two heifers from the high-dose group were humanely slaughtered22 and bone, liver, kidney, tenderloin, ribeye, shoulder (also known as chuck), rump (also known as round), intraperitoneal fat, and back fat samples were harvested for analysis of PFOS residues. The remaining animals were held for a period approximating two or more additional half-lives (343 days) and slaughtered. Tissues were collected as described above with the addition of skin. All tissue samples were ground twice through a LEM meat grinder (West Chester, OH) and stored at −20 °C until analysis. Sample Preparation, Cleanup, and LC-MS/MS Analysis. Methods used for plasma and tissue extractions of PFOS were described previously.12,23 Bone was broken into small pieces of approximately equal size, and skin with hair was initially cut into 0.5−1 cm2 pieces with subsequent mincing using scalpels. Bone and skin aliquots were weighed (5.00 ± 0.05 g) into 50 mL Sarstedt tubes. Aliquots of a 1 M sodium hydroxide solution (25 mL) were added to each bone sample and were vortex mixed. Tubes were incubated in a shaking water bath at 65 °C and 100 rpm for a minimum of 24 h, removed, and allowed to cool. A 5.0 mL aliquot of 0.5 M TBAHS (pH 10) was added to each tube and tubes were again vortex mixed. Then
C t = Ee−αt where t is time (in hours) and E is the Y intercept of the line having a slope of α (rate). For tissue depletion half-lives, data from the previous 28 day study12 and the data from the two heifer time points (105 and 343 days) were used to obtain an equation as above. Using the α term from the above equation as the rate in the below equation
half‐life = 0.693/α the tissue depletion half-life can be estimated. Statistical Analysis. One-way analysis of variance (ANOVA) was performed for the tissue depletion half-life from the 28 day study,12 the low-dose steer half-life, and the high-dose heifer half-life to determine if they were significantly different. To determine if there were any significant differences in PFOS concentrations between muscle cuts (n = 4) and muscle cuts versus fat, ANOVA was calculated within slaughter time point 343 days for steers and heifers within muscle cut (tenderloin, ribeye, shoulder, and rump) and between muscle cut and fat PFOS concentrations, that is, steers (343 days) and heifers (343 days). When ANOVA analyses were significant (p ≤ 0.05), a Bonferroni t test was performed on all pairs. All analyses were completed using SigmaPlot 12. 10989
DOI: 10.1021/acs.jafc.5b04565 J. Agric. Food Chem. 2015, 63, 10988−10994
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Journal of Agricultural and Food Chemistry
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RESULTS AND DISCUSSION Plasma PFOS Concentrations and Elimination HalfLife Estimations. Low-Dose Steers. Plasma PFOS concen-
Table 1. Average PFOS Tissue Concentrations (μg/g ww) with Standard Deviations for Low-Dose Steers (0.098 mg/kg bw) and High-Dose Heifers (9.1 mg/kg bw) tissue liver kidney back fat IP fat skin shoulder tenderloin ribeye rump bone
steersa
heifers (105 days)b
± ± ± ± ± ± ± ± ± ±
8.76 ± 3.54 3.96 ± 0.16 1.26 ± 0.14 0.93 ± 0.08 NCg 1.20 ± 0.46 0.36 ± 0.04 0.86 ± 0.19 0.92 ± 0.30 0.46 ± 0.05
0.149 0.082 0.037 0.014 0.008 0.004 0.007 0.004 0.004 0.003
0.015d 0.024d 0.009f 0.002 0.010 0.001 0.001 0.000 0.001 0.001
heifers (343 days)c 4.74 2.36 0.87 0.33 0.69 0.27 0.30 0.17 0.39 0.23
± ± ± ± ± ± ± ± ± ±
0.56d 0.57e 0.11f 0.05 0.86 0.01 0.01 0.10 0.03 0.19
a
Average tissue concentration (n = 2 steers) with low dose of 0.098 mg/kg bw and slaughtered at 343 days. bAverage tissue concentration (n = 2 heifers) with high dose of 9.1 mg/kg bw and slaughtered at 105 days. cAverage tissue concentration (n = 2 heifers) with high dose of 9.1 mg/kg bw and slaughtered at 343 days. dSignificantly different (Bonferroni t test, p < 0.05) from all other tissues. eSignificantly different (Bonferroni t test, p < 0.05) from all tissues except skin and back fat. fSignificantly different (Bonferroni t test, p < 0.05) from all muscle cuts and IP fat. gNot collected.
Figure 1. Plasma PFOS concentrations in individual steers (a) and heifers (b). SC stands for steer control; S stands for steer; and H stands for heifer. Box around 1−111 days is time animals were in pasture.
Figure 2. Average tissue concentrations for steers and heifers with standard deviations. Heifer data are at 105 and 343 days. No skin concentration for heifers at 105 days. Data presented on a log scale.
trations (μg/mL) for individual steers dosed with 0.098 mg PFOS/kg bw are presented in Figure 1a, as well as Table S1. As suggested by the data, there appeared to be residual contamination occurring in the control animals (SC-184; SC186; Figure 1a) during the 343 day study period. Steer control 184, which was misdosed, did not have higher residual concentrations than the true control animal and apparently expelled the dosing capsule prior to any PFOS absorption. Because all animals were pastured together (May−August) and subsequently penned together (September−May), contamination could have occurred orally and/or dermally through urine and/or fecal contamination of pasture and pen. Transmission through forage contamination with urine and feces seems probable because PFOS burdens of control animals seemed to stop accumulating approximately 120 days into the study or just after the animals were removed from pasture. In test animals, PFOS appearance in plasma increased rapidly after oral dosing and appeared to peak (0.61 ± 0.053 μg/mL) on study day 6; thereafter, a long distribution period occurred
(between 6 and 105 days) with variable plasma PFOS concentrations (0.37−0.61 μg/mL). A long depletion period (105−343 days) occurred thereafter. From a previous 28 day study conducted in our laboratory, a similar trend was observed in steers provided a high dose (8 mg PFOS/kg bw) of PFOS;12 that is, plasma PFOS levels peaked initially, appeared to undergo a distribution phase, and a secondary plasma peak occurred weeks after dosing. Kowalczyk et al.18,20 also observed a second peak of PFOS plasma concentrations subsequent to the initiation of a depuration period, after the PFOS feeding period had stopped. Collectively, these data suggest that PFOS equilibration among body compartments is a complex and lengthy process. High-Dose Heifers. Plasma PFOS concentrations (μg/mL) for individual heifers dosed with a single 9.1 mg PFOS/kg bw oral dose are shown in Figure 1b, as well as Table S2. The high PFOS dose was absorbed and PFOS concentrations increased 10990
DOI: 10.1021/acs.jafc.5b04565 J. Agric. Food Chem. 2015, 63, 10988−10994
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and humans are >90 days, 200 days, and 5.4 years, respectively.1,6,8 Numata et al.21 determined the half-life of PFOS in chronically exposed fattening pigs to be 634 days, which is 4−5 times that of the cattle that received a single oral dose for this study. The differences observed for the half-life of fattening pigs compared to that of cattle could be due to the chronic dose and differences in anatomy. The similarity of pig anatomy to that of humans could explain the much longer halflife observed in fattening pigs.21 PFOS Tissue Distribution and Depletion Half-Life Estimations. PFOS Tissue Concentrations. Average tissue concentrations for the low-dose steers slaughtered at 343 days, high-dose heifers slaughtered at 105 days, and the high-dose heifers slaughtered at 343 days are shown in Table 1 and Figure 2. For both dose levels, liver concentrations were the highest at 1.5 ± 0.01 μg PFOS/g wet weight (ww) for steers and 8.8 ± 3.54 and 4.7 ± 0.56 μg/g for 105 day heifers and 343 day heifers, respectively. Liver concentrations were significantly different from all other tissues. These liver concentrations are consistent with the previous 28 day study (17.9 ± 2.25 μg/g), especially when considering the longer time points when liver samples were taken in this study at 105 and 343 days (Table 1). The higher liver PFOS residues in this study and the previous 28 day study indicated that liver has the potential to accumulate PFOS.12 Also, from the previous 28 day study, it was observed that very small amounts of PFOS (∼0.5% of total dose) were eliminated via urine, whereas larger amounts of PFOS were eliminated via feces (∼11% of total dose).12 The continual low elimination via feces, high liver concentrations, and the long half-life suggest that PFOS has the potential to undergo enterohepatic circulation, which can sustain levels of contaminants within the body for longer periods of time and increases a chemical’s elimination half-life, which has been observed in other studies.5,24 Kidney PFOS residues (0.08 ± 0.02 μg/g) in steers and heifers (4.0 ± 0.16 and 2.4 ± 0.57 μg/g at 105 and 343 days, respectively) ranked second with respect to liver in total PFOS concentration. Kidney concentrations at 343 days for steers were significantly different from all other tissue concentrations and for 343 day heifers were significantly different from all tissues with the exception of skin and back fat. Again, these residue levels were consistent with the previous 28 day study where kidney residue was 3.7 ± 0.87 μg/g. The ranked tissue concentrations (based on low-dose steer values) for all other tissues were back fat > intraperitoneal fat ≥ skin ≥ tenderloin ≥ shoulder muscle ≥ ribeye muscle ≥ rump muscle ≥ bone. Back fat concentrations for 343 day steers and heifers were significantly different from IP fat and all muscle cuts; however, IP fat was not significantly different from muscle cuts. This trend was similar to the previous 28 day study except back fat had slightly higher residues than kidney.12 The trend was also consistent with the Kowalcyzk et al.18,20 studies in which liver > kidney > muscle.18,20 Considering that back fat PFOS concentrations were significantly different from muscle, we cannot pool muscle and fat concentrations together as did Numata et al.21 The fat concentrations could be attributed to the similar fluorinated fatty acid chain that the PFOS chemical structure has. As Numata et al.21 discussed, PFOS is 100 times more lipophilic25 than the nonfluorinated version, and physiologically, PFOS would be deprotonated, which provides evidence to support finding PFOS in fat tissue. Different muscle cuts were sampled to determine if there were different distribution patterns of PFOS throughout the
Figure 3. Comparison of average PFOS concentrations with standard deviations in various meat cuts for steers (low dose) and heifers (high dose). Data presented on a log scale.
rapidly in plasma, by day 3, plasma PFOS concentrations peaked (64.7 ± 11.6 μg/mL); thereafter, PFOS was distributed to the body and reabsorbed into the plasma (3−105 days) and finally distributed back into the tissues and/or eliminated via feces (105−343 days). Similar to steers, a second peak in plasma PFOS concentrations occurred at 42 days (71.5 ± 5.3 μg/mL) after the distribution from and during the reabsorption into the plasma. The plasma concentration difference between the low dose for the steers and the high dose for the heifers was roughly 100-fold, which is consistent with the difference between dose levels, suggesting little to no dose dependency on percent accumulated but should be further investigated. As discussed for the steer data, a similar trend was observed in a previous study using steers dosed with 8 mg/kg bw but slaughtered after 28 days.12 Similar initial absorption phases (3−4.7 days) were observed between the short- (steers, 28 days) and long-term (heifers, 343 days) studies. Also, the same order of magnitude of the plasma PFOS concentrations was observed between the high dosed animals of both studies.12 Plasma Elimination Half-Life Estimations. A plasma elimination half-life could not be calculated from data derived from our previous 28 day study; however, a whole body depletion half-life of 116 ± 12.7 days was estimated.12 For this study, a period of 343 days allowed a plasma elimination halflife for PFOS to be estimated. Using 105 to 343 day plasma PFOS residue data and noncompartmental pharmacokinetic modeling, the estimated plasma elimination half-life for PFOS in steers was 120 ± 4.1 days. There seemed to be little to no dose dependency when the steer plasma elimination half-life for the 343 day study (0.098 mg/kg bw dose) was compared to the whole body depletion half-life from the previous 28 day study. For the high-dose heifers, the depletion phase started at 105 days and a plasma elimination half-life was estimated for data from 105 to 343 days. For the heifers, the average plasma elimination half-life was 106 ± 23.1 days, compared to the lowdose steers in this same study at 120 days and the high-dose steers from the 28 day study at 116 days.12 Comparing these three half-lives (116, 120, and 106 days), there were no significant differences by ANOVA between plasma depletion of different dose levels or between steers (altered bulls) or heifers; however, there could be differences between unaltered bulls and heifers. Estimated half-lives for PFOS in rodents, monkeys, 10991
DOI: 10.1021/acs.jafc.5b04565 J. Agric. Food Chem. 2015, 63, 10988−10994
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Figure 4. Exponential decay plots for PFOS tissue concentrations (μg/g ww) of 28 day high-dose (8 mg/kg bw) steers,12 105 day high-dose (9.1 mg/kg bw) heifers, and 343 day high-dose (9.1 mg/kg bw) heifers.
animal and if this would affect exposure through consumption. Muscle samples (tenderloin, shoulder, ribeye, and rump) were the lowest PFOS residue samples analyzed, except for bone, and had similar PFOS concentrations (Table 1 and Figure 3). There were only slight variations between PFOS residues observed in the different cuts of meat (tenderloin, shoulder, ribeye, and rump), with no significant differences between the concentrations. Consuming different meat cuts (tenderloin, shoulder, ribeye, and rump), except for liver, would not likely result in different exposure levels considering that they are not statistically different. Tissue Depletion Half-Life Estimations. Assuming no large dose dependency between 8 and 9.1 mg/kg bw, the observed tissue concentrations from the previous 28 day study (steers, 8 mg/kg bw), and the time points at 105 days (n = 2) and 343
days (n = 2, heifers, 9.1 mg/kg bw) in this study can be graphically compared. Figure 4 shows the decreasing tissue levels (observed values) between the different time points from the previous 28 day study and the two slaughter time points for the heifers in this study (105 and 343 days) with exponential decay equations, correlation coefficients (r2), and estimated half-lives for each tissue.12 An adjustment was made to tissue concentrations for differences in doses at 28 days and a change in animal weight between 105 and 343 days. These changes to the tissue concentrations at 28 days and body weight at 343 days did not significantly change the half-lives or 95% confidence intervals for the rates, so depletion plots used observed values. A declining trend in tissue concentrations from 28 to 343 days can be observed between the two studies. Performing an exponential curve fit on the data results in an 10992
DOI: 10.1021/acs.jafc.5b04565 J. Agric. Food Chem. 2015, 63, 10988−10994
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Journal of Agricultural and Food Chemistry equation for which the rate can be obtained from the α term. The depletion half-life for each tissue can be calculated using the half-life equation provided above. Kidney had the longest estimated PFOS depletion half-life at 385 days, followed by muscle at 165 days. The other tissue depletion half-lives in rank order were bone > liver > IP fat > back fat. Most of the PFOS depletion half-lives for tissues are longer than that for the plasma depletion half-life, suggesting that PFOS residues in plasma could distribute to other tissues, thus extending their depletion half-life. Considering the much shorter half-lives from IP fat (41 days) and back fat (36 days), this suggested that fat could be a reservoir for initial distribution but depletes PFOS more rapidly back into the blood. Longer tissue depletion especially seems true when the slow elimination via urine and feces is considered.12 These halflives could be even longer if animals were to receive chronic exposure to PFOS. Considerations for Food Safety. The tissue depletion half-lives for beef are long (∼110−150 days), however, with regard to the lifetime of the animal (1.5−2 years), the half-lives are shorter, with maybe the exception of kidney (>300 days). If animals were to be fed uncontaminated feed during finishing on the feedlot or taken off pasture before slaughter, there might be declines in PFOS levels, especially for fat and muscle tissues. As for consumer exposure, the United States has no established tolerable daily intake (TDI) for PFOS in humans; however, the European Food Safety Authority (EFSA) has established a TDI for PFOS at 0.15 μg/kg bw/day.26 Based on the highest observed muscle concentration (0.007 μg/g) from the environmentally relevant PFOS dose, a person would need to consume 2.14 g of meat/kg bw/day to reach the TDI set by EFSA.26 However, on average,Americans only consume 0.77 g of meat/kg bw on a daily basis,27 which equates to an intake of 0.005 μg/kg bw/day and a third of the recommended EFSA TDI.26
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Research Service, or the Food Safety and Inspection Service of any product or service to the exclusion of others that may be suitable. USDA is an equal opportunity provider and employer.
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(1) 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 criteria and persistent lipophilic compounds. Environ. Sci. Technol. 2008, 42, 995−1003. (2) Noorlander, C. W.; van Leeuwen, S. P. J.; te Biesebeek, J. D.; Mengelers, M. J. B.; Zeilmaker, M. J. Levels of perfluorinated compounds in food and dietary intake of PFOS and PFOA in The Netherlands. J. Agric. Food Chem. 2011, 59, 7496−7505. (3) Committee on Toxicity.. COT statement on the tolerable daily intake for perfluorooctane sulfonate. COT of Chemicals in Food, Consumer Products and the Environment. 2006, 1−21. (4) Beach, S. A.; Newsted, J. L.; Coady, K.; Giesy, J. P. Ecotoxicological evaluation of perfluorooctanesulfonate (PFOS). Rev. Environ. Contam. Toxicol. 2006, 186, 133−174. (5) Lau, C.; Butenhoff, J. L.; Rogers, J. M. The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicol. Appl. Pharmacol. 2004, 198, 231−241. (6) European Food Safety Authority (EFSA).. Opinion of the scientific panel on contaminants in the food chain on perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA) and their salts. EFSA J. 2008, 653, 1−131. (7) Tittlemier, S. A.; Pepper, K.; Seymour, C.; Moisey, J.; Bronson, R.; Cao, X. L.; Dabeka, R. W. Dietary exposure of Canadians to perfluorinated carboxylates and perfluorooctane sulfonate via consumption of meat, fish, fast foods, and food items prepared in their packaging. J. Agric. Food Chem. 2007, 55, 3203−3210. (8) Seacat, A. M.; Thomford, P. J.; Hansen, K. J.; Olsen, G. W.; Case, M. T.; Butenhoff, J. L. Subchronic toxicity studies on perfluorooctanesulfonate potassium salt in Cynomolgus monkeys. Toxicol. Sci. 2002, 68, 249−264. (9) Luebker, D. J.; Case, M. T.; York, R. G.; Moore, J. A.; Hansen, K. J.; Butenhoff, J. L. Two-generation reproduction and cross-foster studies of perfluorooctanesulfonate (PFOS) in rats. Toxicology 2005, 215, 126−148. (10) van Asselt, E. D.; Rietra, R. P. J. J.; Römkens, P. F. A. M.; van der Fels-Klerx, H. J. Perfluorooctane sulphonate (PFOS) throughout the food production chain. Food Chem. 2011, 128, 1−6. (11) Yoo, H.; Guruge, K. S.; Yamanaka, N.; Sato, C.; Mikami, O.; Miyazaki, S.; Yamashita, N.; Giesy, J. P. Depuration kinetics and tissue disposition of PFOA and PFOS in white leghorn chickens (Gallus gallus) administered by subcutaneous implantation. Ecotoxicol. Environ. Saf. 2009, 72, 26−36. (12) Lupton, S. J.; Huwe, J. K.; Smith, D. J.; Dearfield, K. L.; Johnston, J. J. Distribution and excretion of perfluoroctane sulfonate (PFOS) in Beef Cattle (Bos taurus). J. Agric. Food Chem. 2014, 62, 1167−1173. (13) Loganathan, B. G.; Sajwan, K. S.; Sinclair, E.; Kumar, K. S.; Kannan, K. Perfluoroalkyl sulfonates and perfluorocarboxylates in two wastewater treatment facilities in Kentucky and Georgia. Water Res. 2007, 41, 4611−4620. (14) Clarke, B. O.; Smith, S. R. Review of ’emerging’ organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids. Environ. Int. 2011, 37, 226−247. (15) Sepulvado, J. G.; Blaine, A. C.; Hundal, L. S.; Higgins, C. P. Occurrence and fate of perfluorochemicals in soil following the land application of municipal biosolids. Environ. Sci. Technol. 2011, 45, 8106. (16) Washington, J. W.; Yoo, H.; Ellington, J. J.; Jenkins, T. M.; Libelo, E. L. Concentrations, distribution, and persistence of perfluoroalkylates in sludge-amended soils near Decatur, Alabama, USA. Environ. Sci. Technol. 2010, 44, 8390−8396.
ASSOCIATED CONTENT
* Supporting Information S
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.5b04565. Tables S1 and S2 (PDF)
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REFERENCES
AUTHOR INFORMATION
Corresponding Author
*Tel: (701) 239-1236. Fax: (701) 239-1430. E-mail: sara.
[email protected]. Notes
The authors declare no competing financial interest. ¶ Retired from Biosciences Research Laboratory, ARS, USDA.
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ACKNOWLEDGMENTS The authors acknowledge Andrew Thompson, Dillon Hofsommer, Dee Ellig, Jason Holthusen, Theresa Goering, and Erin Loeb for their help with blood draws, sample collection, and sample analysis. We would also like to acknowledge Terry Skunberg and Justin Gilbertson form North Dakota State University (NDSU) Animal Nutrition and Physiology Center for animal care, and Austen Germolus from the NDSU abattoir. The use of trade, firm, or corporation names in this publication is for the information and convenience of the reader. Such use does not constitute an official endorsement or approval by the United States Department of Agriculture, the Agricultural 10993
DOI: 10.1021/acs.jafc.5b04565 J. Agric. Food Chem. 2015, 63, 10988−10994
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DOI: 10.1021/acs.jafc.5b04565 J. Agric. Food Chem. 2015, 63, 10988−10994
