Distribution and Excretion of Perfluorooctane Sulfonate (PFOS) in Beef

Jan 20, 2014 - Four Lowline steers (#179–182, Bos taurus) were purchased from Effertz EZ Ranch (Bismarck, ND). The steers were raised in 3.1 × 3.4 ...
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Distribution and Excretion of Perfluorooctane Sulfonate (PFOS) in Beef Cattle (Bos taurus) Sara J. Lupton,*,† Janice K. Huwe,† David J. Smith,† Kerry L. Dearfield,‡ and John J. Johnston§ †

Biosciences Research Laboratory, ARS, USDA, 1605 Albrecht Boulevard, Fargo, North Dakota 58102, United States Office of Public Health Science, FSIS, USDA, 1400 Independence Avenue SW, Washington, DC 20250, United States § Office of Public Health Science, FSIS, USDA, 2150 Centre Avenue, Building D Suite 320, Fort Collins, Colorado 80526, United States ‡

S Supporting Information *

ABSTRACT: Perfluorooctane sulfonate (PFOS), a perfluoroalkyl surfactant used in many industrial products, is present in industrial wastes and in wastewater treatment plant biosolids. Biosolids are commonly applied to pastures and crops used for animal feed; consequently, PFOS may accumulate in the edible tissues of grazing animals or in animals exposed to contaminated feeds. There are no data on the absorption, distribution, and excretion of PFOS in beef cattle, so a 28-day study was conducted to determine these parameters for PFOS in three Lowline Angus steers given a single oral dose of PFOS at approximately 8 mg/kg body weight. PFOS concentrations were determined by liquid chromatography−tandem mass spectrometry in multiple tissue compartments. The major route of excretion was in the feces (11 ± 1.3% of the dose, mean ± standard deviation) with minimal PFOS elimination in urine (0.5 ± 0.07% of the dose). At day 28 the mean plasma concentration remained elevated at 52.6 ± 3.4 μg/mL, and it was estimated that 35.8 ± 4.3% of the dose was present in the plasma. Plasma half-lives could not be calculated due to multiple peaks caused by apparent redistributions from other tissues. These data indicate that after an acute exposure PFOS persists and accumulates in edible tissues. The largest PFOS body burdens were in the blood (∼36%), carcass remainder (5.7 ± 1.6%), and the muscle (4.3 ± 0.6%). It was concluded that PFOS would accumulate in edible tissues of beef, which could be a source of exposure for humans. KEYWORDS: perfluorooctane sulfonate, beef cattle, tissue distribution, elimination, residues



INTRODUCTION Perfluorooctane sulfonate (PFOS), because of its chemical and thermal stability properties, is used as a surfactant in a wide variety of industrial and consumer products such as textiles, electronics, and plastics, 1−3 and it is in a variety of perfluoroalkyl-related substances which are also used in manufactured products.2,3 Because of its wide use, PFOS is often a waste product from manufactured goods and a breakdown product of perfluoroalkyl and polyfluoroalkyl substances.4 Consequently, PFOS is widely distributed throughout the environment and is considered a contaminant of toxicological concern for reasons detailed below.3,5,6 PFOS has been detected in biosolids from wastewater treatment plants (WWTPs) with concentrations ranging from 5 to 3120 ng/g dry weight (dw).7−9 Application of biosolids to land used for crop and forage production is thought to be a contributor to PFOS in the environment, and the transfer of PFOS from biosolids to soil has been demonstrated.9,10 For example, concentrations of PFOS ranged from 0 to 408 ng/g dw in soils of biosolid-amended fields.10 Further, Stahl et al. observed the concentration-dependent transfer of PFOS from soil to wheat, maize, and rye grasses by measuring PFOS present in stalks, stems, and grain products.11 Kowalczyk et al. also measured the transfer of PFOS into corn grown on PFOS contaminated fields where the corn was later used in PFOS studies in dairy cattle to show uptake .12 Of importance to exposures in grazing animals, 1−20 ng/g dw of PFOS was This article not subject to U.S. Copyright. Published 2014 by the American Chemical Society

detected in forages including tall fescue, Bermuda grass, and Kentucky bluegrass grown on biosolid-amended fields.13 Given the potential for PFOS transfer from soils to grains and forages, it is not unreasonable to expect the transfer of PFOS residues to food animals consuming contaminated grains or forages. Indeed, several studies have documented the presence of PFOS in retail beef (ranging from back fat > kidney > intraperitoneal fat > lung > spleen > muscle. Fat samples were analyzed in this study to determine if any PFOS is distributed to those tissues. The fat samples (back fat and IP fat) have consistently higher concentrations than muscle samples, averaging 5.7 and 3.5 μg/g, respectively, vs 1.1 μg/g in muscle. These results are not typical where some studies observe low accumulation of PFOS in fat tissues,31,34 however PFOS concentrations in fat samples from this study are lower than those concentrations observed in the liver and plasma, indicating that these tissues are still the primary accumulators of PFOS. Even though the muscle concentrations and carcass remainder (which consists of the remaining fat and tissues not collected separately) concentrations are lower than liver concentrations, muscle and carcass remainder still have the largest body burdens due to size of the tissue compartments compared to liver. For muscle (average mass 101 kg) and carcass remainder (average mass 46.4 kg), 4.3 ± 0.6% and 5.7 ± 1.6%, respectively, of the PFOS dose remained in these

Figure 5. Mean PFOS remaining in the steer body (mg) with time through the 28 days after a single oral dose. Points represent mean amounts (mg) of PFOS remaining of three animals ± one standard deviation. Linear regression analysis provided a line equation of y = −11.532x + 2639.5 and an r2 coefficient of 0.9759.

amounts of PFOS elimination in feces and urine, indicating PFOS was distributed to other parts of the steer. After day 17, plasma concentrations gradually increased to 52.6 ± 3.4 μg/mL at day 28, the last day of the study. A similar increase in PFOS concentration subsequent to an initial absorption and distribution phase has also been observed in an additional, longer duration study (Lupton et al., unpublished) in cattle. The secondary increase of PFOS plasma concentrations was possibly due to redistribution of PFOS from tissue. The continual high concentrations of PFOS in plasma could be the result of protein binding for transportation purposes throughout the body for distribution. At day 28 a large percentage of the dosed PFOS (∼35%) was still circulating in the blood. A terminal plasma elimination half-life was not calculated due to the lack of an observable PFOS depletion phase. Extremely slow PFOS elimination contrasts with that of PFOA, which has a plasma elimination half-life of 19 h and is nearly quantitatively eliminated via the urine within two weeks of dosing.25 PFOS serum depletion half-life estimates for monkeys and humans are on the order of hundreds of days to years.43 Due to the approved study design, it was not feasible to continue this study for the period of time needed to determine the PFOS plasma half-life in steers. Even though we were not able to calculate a plasma elimination half-life, it was possible to calculate a body burden half-life of 114.2 days from the PFOS amounts remaining in the steers over time using the linear regression equation. No metabolites of PFOS were observed in any of the compartments analyzed. The stability and chemical properties of PFOS would not likely allow for metabolite formation through defluorination or conjugation, and neither of these metabolic events were observed in other studies.6,33,44 Since PFOS was not metabolized in steers, it must be excreted intact to reduce the body burden. In this study, the major route of excretion was through feces (11% of the PFOS dose); and elevated levels of PFOS were still being excreted in the feces at 28 days. The small amount of PFOS found in feces during the first few days of the study suggests that a majority of the PFOS was absorbed into the body and not excreted directly into feces. Higher amounts of PFOS excreted in the feces during later days of the study are most likely through contributions from the biliary elimination in feces.6,12,44 At slaughter, biliary PFOS concentrations were second only to plasma at 36.9 μg/mL, which equates to approximately 0.9% of the dose in the bile 1171

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compartments, compared to 2.2 ± 0.2% in the liver (average mass 3.8 kg). Higher liver and kidney concentrations of PFOS compared to muscle were also observed in sheep and dairy cows.12,20 Unlike the observation of the high elimination of PFOA in steer urine,25 PFOS circulated and was redistributed in the steer for a long period of time; this was confirmed by the large portion of the dose circulating in the bloodstream (∼35%) at slaughter and the gradual decline then incline of PFOS concentrations in the plasma over the 28-day study. Approximately 39% of the dose was not accounted for in the mass balance, therefore, large compartments such as skin and bone, which were not in the carcass remainder, could be pools where PFOS is distributed in the steer. One other study that analyzed skin and bone observed concentrations similar to those observed in blood, indicating that distribution to these tissues is a likely source of the unaccounted PFOS.34 In this study an acute dose of PFOS was administered to steers. The elimination of PFOS was slow, and the study time of 28 days was not sufficient to allow us to calculate a plasma elimination half-life; however, a body burden half-life was calculated to be 114.2 days. An additional longer study is being conducted to determine the plasma elimination half-life in steers. To fully assess accumulation of PFOS in cattle and the possible human exposure to PFOS through beef consumption, studying the effects of chronic exposure would be necessary. Chronic exposure is an important aspect to consider because it will occur with beef cattle due to the continual application of biosolids to pastures.8−10,24



of others that may be suitable. USDA is an equal opportunity provider and employer.



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ASSOCIATED CONTENT

S Supporting Information *

The mean ± SD PFOS plasma concentrations (μg/mL, n = 3) for each time point (Table S1). The mean ± SD urine and fecal concentrations (μg/mL or μg/g dw, n = 3) for each day (Table S2). This material is available free of charge via the Internet at http://pubs.acs.org.



REFERENCES

AUTHOR INFORMATION

Corresponding Author

*Tel: (701)239-1236. Fax: (701)239-1430. E-mail: Sara. [email protected]. Funding

Partial funding for this study was provided via an FSIS-ARS Interagency Agreement FSIS-IA-9-102. Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS The authors would like to acknowledge Dee Ellig, Theresa Wilson, Grant Herges, Santana Nez, Colleen Pfaff, Jason Holthusen, Grant Harrington, Margaret Lorentzsen, Michael Giddings, Kristin McDonald, Theresa Goering, Jean Picard, and Erin Loeb for their help with animal care and sample collection. We would also like to acknowledge Dr. Sarah Wagner, North Dakota State University, for her help with inserting jugular catheters. 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 Research Service, or the Food Safety and Inspection Service of any product or service to the exclusion 1172

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