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Blood-Based Ante-Mortem Method for Estimating PFOS in Beef from Contaminated Dairy Cattle
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  • John J. Johnston
    John J. Johnston
    Department of Food Science and Human Nutrition, Colorado State University, 1571 Campus Delivery, Fort Collins, Colorado 80523, United States
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  • Eric D. Ebel
    Eric D. Ebel
    USDA Food Safety and Inspection Service, 1400 Independence Avenue SW, Washington, District of Columbia 20250, United States
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    Orcidhttps://orcid.org/0009-0007-7663-2732
  • Michael S. Williams*
    Michael S. Williams
    USDA Food Safety and Inspection Service, 1400 Independence Avenue SW, Washington, District of Columbia 20250, United States
    *Email: [email protected]
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    Orcidhttps://orcid.org/0000-0002-9094-9695
  • Emilio Esteban
    Emilio Esteban
    USDA Food Safety and Inspection Service, 1400 Independence Avenue SW, Washington, District of Columbia 20250, United States
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  • Sara J. Lupton
    Sara J. Lupton
    USDA Agricultural Research Service, Edward T. Schafer Agricultural Research Center, 1616 Albrecht Blvd. North Fargo, North Dakota 58102, United States
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  • Eric J. Scholljegerdes
    Eric J. Scholljegerdes
    Dept. Animal and Range Sciences, New Mexico State University, Box 30003, MSC 3-I, Las Cruces, New Mexico 88003, United States
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  • Shanna L. Ivey
    Shanna L. Ivey
    Dept. Animal and Range Sciences, New Mexico State University, Box 30003, MSC 3-I, Las Cruces, New Mexico 88003, United States
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  • Mark R. Powell
    Mark R. Powell
    USDA Office of Risk Assessment and Cost Benefit Analysis, 1400 Independence Avenue SW, Washington, District of Columbia 20250, United States
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  • David J. Smith
    David J. Smith
    USDA Agricultural Research Service, Edward T. Schafer Agricultural Research Center, 1616 Albrecht Blvd. North Fargo, North Dakota 58102, United States
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    Orcidhttps://orcid.org/0000-0001-8883-4744
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ACS Agricultural Science & Technology

Cite this: ACS Agric. Sci. Technol. 2023, 3, 10, 835–844
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https://doi.org/10.1021/acsagscitech.3c00102
Published September 20, 2023

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Abstract

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A blood-based screening method was developed to facilitate ante-mortem screening of dairy cattle suspected of containing elevated concentrations of perfluorooctanesulfonic acid (PFOS) in their muscle tissue. The collection and subsequent laboratory analyses of 28 paired blood plasma and muscle samples from PFOS-exposed dairy cattle provided the PFOS plasma and muscle data to develop a model to estimate muscle PFOS concentrations based on plasma PFOS concentrations. The blood-based ante-mortem screening approach could be applied to predict whether beef (skeletal bovine muscle) from suspect cattle populations (or subpopulations) exceeds a particular level of concern. The data analyses indicated that the relationship between muscle and plasma PFOS concentrations differed by the class of dairy cattle (heifer, lactating, and dry) and the duration of removal (withdrawal time) from exposure to PFOS. A plasma depletion model was also developed to evaluate the estimated withdrawal time required to reduce PFOS in dairy cattle muscle to below an identified level of concern. The model indicated complex PFOS plasma depletion dynamics with a nonconstant rate of depletion. The required withdrawal time also depends on the initial concentration distribution (which differed between heifers and lactating/dry cows) and the identified level of concern.

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1. Introduction

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A New Mexico dairy herd of approximately 5000 cows consumed drinking water and forage contaminated with poly- and perfluoroalkyl substances (PFASs), including perfluorooctanoic acid (PFOA) and perfluorooctanesulfonic acid (PFOS). In October 2018, the U.S. Food and Drug Administration (USFDA) tested and determined that the milk from this herd was adulterated due to the presence of PFOS (1) and notified the U.S. Department of Agriculture Food Safety and Inspection Service (USDA-FSIS), the public health regulatory agency responsible for ensuring the safety of the commercial supply of meat. (2,3)
PFOS bioaccumulates in humans and animals, resulting in potential reproductive, developmental, and immune response effects. PFOA is likely to be a human carcinogen. Previously, the U.S. Environmental Protection Agency (USEPA) derived oral noncancer reference doses (RfDs) of 0.00002 mg/kilogram bodyweight (kg-bw) per day for each of PFOS and PFOA. The USEPA 2016 RfDs apply to the total linear and branched isomers. (4,5)
To address concerns regarding the safety of beef (skeletal bovine muscle) derived from these PFAS-exposed cattle in New Mexico, USDA-FSIS convened experts from USFDA, USEPA, USDA, and the Agency for Toxic Substances and Disease Registry (ATSDR) to consider the available science and methodologies for evaluating what concentration of PFOS in beef would constitute a public health concern. Considering the input from this interagency group, an interim screening level of 4.1 ppb (ng/g) of PFOS in raw beef was derived that could be used to evaluate the safety of beef derived from cattle at the New Mexico dairy.
USDA-FSIS collaborated with USDA Agricultural Research Service (USDA-ARS) and New Mexico State University (NMSU) research partners to (1) develop an approach for estimating PFOS concentrations in beef based on blood samples collected from PFOS-exposed dairy cattle ante-mortem and (2) improve understanding of PFOS depletion in dairy cattle after removal from exposure. The results from both parts of this study were used to inform decisions related to the marketability of the cattle on New Mexico dairy and potential risk mitigation options.
Blood was sampled from a group of PFAS-exposed dairy cattle. Additionally, a subset of these animals was subsequently moved to an area without known PFAS contamination. PFOS in blood and muscle tissue samples was quantified periodically across 6 months. Decreases in PFOS concentrations in blood and muscle were modeled to (1) estimate muscle PFOS concentrations based on blood plasma PFOS concentrations and (2) estimate the duration of removal (withdrawal time) from exposure to PFOS needed to achieve PFOS concentrations in dairy cattle below the interim screening level of 4.1 ng/g PFOS in raw beef that was being used to evaluate these cattle.
There are no other reported models for ante-mortem estimation of PFAS concentrations in beef. Furthermore, there are relatively few studies that investigated the accumulation of PFAS in food animals. These include short-term feeding studies in dairy cattle and sheep fed forage grown on contaminated soil, (6−8) single bolus dosing (via capsule) of beef cattle, (9−11) a longer term (365 day) investigation in which dairy cattle were fed silage containing very low “background” PFAS, (12) and chickens exposed to multiple PFAS concentrations in water. (13) These studies demonstrated accumulation of PFAS in sheep and cattle tissues and significant transfer to milk and eggs. However, these studies are of limited value for risk assessments because the PFAS exposures were not of sufficient duration to achieve steady-state body burdens.
Drew (14) described accumulation of several PFAS by beef cattle and sheep at a farm where stock water was PFAS-affected. Because animals had been exposed for more than 3–5 half-lives of the PFAS with the longest half-life and water concentrations were constant, the relationship between water exposure and steady-state PFAS serum concentrations could be determined. Drew (15) also investigated the excretion of PFAS in cattle sera and tissues. However, there was no attempt to model the correlation of sera residues with tissue residues. Hence, these studies do not provide an ante-mortem method for the estimation of PFAS in edible tissues and a means to determine when PFAS-exposed cattle are safe for slaughter and subsequent human consumption.

2. Data and Methods

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2.1. Sample Collection and Data

Samples were collected as previously described. (2) Briefly, on-farm, blood plasma and ear notch (skin) samples were collected from 175 cattle. Subsequently, a cohort of 30 of these cattle were purchased and moved to an uncontaminated site (NMSU). Widespread PFAS contamination of the site was confirmed by PFAS analysis of water and silage collected on the farm. (16) Among the nine PFAS detected in water, the mean PFOS levels were 818 ng/kg. Among the eight PFAS detected in silage, mean PFOS levels were 3482 ng/kg. To assess the within-herd distribution of PFOS plasma concentrations, blood samples were collected on the farm from 175 dairy cattle: 100 dry cows, 39 heifers, 30 lactating cows, and 6 of unknown class (Supporting Information, Table A*). A cow that had not previously been lactated was classified as a heifer. Due to differences in plasma concentrations among classes, the results from the 6 cows of an unknown class were omitted from the data analysis.
To analyze the relationship between plasma and muscle PFOS concentrations, 30 of these cows (10 heifers, 15 lactating, and 5 dry) were transported to NMSU. Approximately 14 days later, 20 of these cows (cohort 1) were euthanized and necropsied; blood plasma and tissues (including muscle) were collected and shipped to the USDA-ARS Edward T. Schafer Agricultural Research Center in Fargo, ND, for determination of PFOS concentrations. Blood samples were collected every 2 weeks from the remaining 10 cows. Subsequently, 8 of these 10 cows (cohort 2) were necropsied at 137 or 153 days after arriving at NMSU and provided blood plasma and muscle tissues for laboratory analyses. The two oldest cows (both lactating) died prior to day 137. Due to the potential for nonrepresentative toxicokinetics, the results of the plasma and muscle analysis from these two cows were omitted from the data analysis (Supporting Information, Table B*).
To evaluate its depletion from plasma, PFOS was quantified in plasma from blood samples collected from cohort 2 cows at approx. 2-week intervals from 0 to 153 days after removal from the contaminated dairy. These analyses were based on 92 plasma PFOS concentrations of the 8 cows (5 heifers and 3 lactating) that survived the full duration of the study (Supporting Information, Table C*). Given the temporal nature of these data, they are termed time-course data.
To confirm that PFAS exposure was negligible while the cows were located at NMSU, water and feed samples were shipped to USDA-ARS for PFAS analyses. Analyses were performed for 4 water samples and 5 feed samples including the total mixed ration and each feed component. Samples were analyzed in duplicate.

2.2. Laboratory Methods

2.2.1. PFOS Extraction from Plasma and Muscle

Plasma and muscle samples were extracted and analyzed similarly as previously described. (2,9) Briefly, both plasma (0.5 mL) and muscle (2 g) samples were extracted with an ion pairing utilizing tetrabutylammonium hydrogen sulfate (TBAHS; 1 mL of 0.5 M) and sodium carbonate (2 mL of 0.25 M) and then extracted with methyl tert-butyl ether (MTBE; 5 mL 3 times). Before extraction, samples were fortified with a 13C8–PFOS recovery surrogate for linear PFOS at 100 ng/mL for plasma (recovery = 85 ± 12%) and 10 ng/g for muscle (recovery = 58 ± 19%). Observed PFAS recoveries for positive control samples were subsequently corrected for surrogate recoveries to yield corrected recoveries of essentially 100%. Muscles samples underwent an extra protein precipitation step using 1,1,1,3,3,3-hexafluoro-2-propanol (0.5 mL).
Sample extracts were evaporated under nitrogen at 30 °C until dryness and then reconstituted in 0.5 mL of methanol. A 13C4–PFOS internal standard was added at a concentration of 100 ng/mL to each extract. Matrix-matched standard curves were made for plasma and muscle with a dynamic range of 0.4 to 400 ng/mL. A sample set typically consisted of 2 negative controls, 2 positive controls, and 10 (muscle) or 15 (plasma) samples extracted in duplicate.

2.2.2. Ultraperformance Liquid Chromatography–Tandem Mass Spectrometry (UPLC-MS/MS) Analysis

Sample analysis was performed on a Waters Acquity UPLC-MS/MS system (Waltham, MA). The initial separation method was run at 0.6 mL/min with starting conditions of 70% A (10 mM ammonium acetate in water)/30% B (1:1 MeOH/acetonitrile v/v). The solvent composition was held isocratic for 0.10 min and then ramped to 35% A/65% B over 7 min to a final ramp over 0.10 min to 15% A/85% B and held for 2.5 min. The system was taken to starting conditions over 0.5 min and held for 6 min for equilibration. The mass spectrometric data were collected using ESI negative mode with a source temperature of 150 °C and desolvation temperature of 500 °C. See Supporting Information, Table D* for precursor ions, product ions, cone voltages, and collision energies. Analytes were quantified using isotope dilution with limits of detection (LOD) and quantification (LOQ) for linear PFOS in plasma at 1.1 and 3.7 ng/mL, respectively. The LOD and LOQ for linear PFOS in muscle were 0.17 and 0.24 ng/g, respectively.
For determination of LODs and LOQs, the following method was used. (17) Briefly, 7 blank matrix extracts were spiked with each compound at a low concentration reflective of the lower end of the standard curve (typically 0.4–1.6 ng/mL). Each spiked matrix extract was analyzed by LC-MS/MS and the compounds quantified. The standard deviations between replicates were determined for each compound from the 7 spiked extracts. The LOD is equal to 3 times (based on Student’s t-test of n samples) the standard deviation and LOQ is equal to 10 times the standard deviation of the 7 replicates.
During the initial analysis, two unresolved coeluting peaks were observed in the linear PFOS ion windows. To investigate these peaks as possible branched chain PFOS isomers, isomer standards were purchased from Wellington Laboratories (Guelph, Ontario, Canada). The two peaks were attributed to perfluoro-3-methyl heptanesulfonate (3Me-PFOS) and perfluoro-6-methyl heptanesulfonate (6Me-PFOS). Modifications were made to the UPLC-MS/MS method to achieve resolution among the three peaks. The mobile phase flow rate was changed to 0.4 mL/min with starting conditions of 90% A/10% B and held for 0.5 min. The mobile phase was ramped to 50% A/50% B over 16 min and held for 3.5 min. A second ramp was performed to 10% A/90% B over 0.5 min and held for 2.5 min and then back to 90% A/10% B for a 7 min equilibration. These new separation conditions allowed for the 3 PFOS isomers to be completely resolved and quantified. The LOD and LOQ for 3Me-PFOS and 6Me-PFOS in plasma were 0.48 and 1.60 ng/mL, respectively. The LOD and LOQ for 3Me-PFOS were 0.07 and 0.10 ng/g, respectively, and for 6Me-PFOS in muscle, they were 0.18 and 0.26 ng/g, respectively.
All time-course plasma and muscle samples were reanalyzed with the new UPLC-MS/MS method to quantify the PFOS isomers. To determine if all plasma samples collected from cattle on the farm needed to be reanalyzed, a comparison was done with the initial analysis of the plasma samples (all unresolved peaks integrated in the PFOS window) against the sum of PFOS isomers quantified individually for each matrix (see Supporting Information, Table E*). The comparison demonstrated that total PFOS was accurately estimated in the on-farm plasma samples by integrating all unresolved peaks in the PFOS window as one peak.
On-farm measurements of linear and unresolved PFOS isomers in plasma were available for all 169 cows. Resolved on-farm linear and branched PFOS isomer plasma measurements were performed for 16 cows (8 heifers, 5 lactating cows, and 3 dry cows) sampled on the farm. The linear and branched PFOS isomer plasma on-farm concentrations for the remaining 153 cows were estimated by a simple log–log-transformed regression of 42 paired observations.a The 42 paired observations (16 on-farm (week 0), 18 at week 2 after removal from exposure, and 8 at week 10 after removal from exposure) represent analyses of results from 18 cows (8 heifers, 7 lactating, and 3 dry). SAS PROC MIXED failed to reject the assumption of homogeneous intercepts and slopes among the observations from weeks 0, 2, and 10 at a significance level of 0.05. Tests of the normality of the residuals from the simple log–log-transformed regression using SAS PROC UNIVARIATE failed to reject the assumption that the residuals are normally distributed at a significance level of 0.05. (Regression of the untransformed data resulted in rejecting the assumption that the residuals are normally distributed at a significance level of ≤0.05.) Regression of the residuals on the independent variable confirmed no significant linear or quadratic trends in the residuals. This provided no evidence to reject the assumed model form. White’s test (18) provided no evidence to reject the assumption of homogeneous variance about the regression line.

2.3. Interim Screening Level for PFOS in Beef

The interim screening level for PFOS in beef was derived by USDA-FSIS, in consultation with an interagency group, as a tool for evaluating the situation at the New Mexico dairy. It was based on the USEPA 2016 PFOS RfD of 0.00002 mg/kg-bw per day (20 ng/kg-bw per day) and a high-end beef consumption estimate for the U.S. population. (4) Specifically, the PFOS RfD was divided by the 90th percentile beef consumption (3.7 g cooked beef/kg-bw per day) for 0–6-year-old children, the subpopulation with the highest beef consumption per bodyweight, after adjustment to a raw beef basis (4.9 g raw beef/kg-bw per day) to account for weight loss during cooking. (19) b Therefore, the interim screening level in raw beef was calculated as 4.1 ng PFOS/g raw beef (ppb). This interim screening level was based on the toxicological reference values available in 2019 and was intended for use with New Mexico dairy cattle. It should not be taken as a generally applicable screening level in the present.

2.4. Relationship between Cattle Plasma and Muscle PFOS Concentrations

To facilitate the estimation of muscle PFOS concentrations in the exposed herd, we analyzed the relationship between PFOS concentrations in muscle and plasma. The analysis incorporated paired muscle tissue and plasma total PFOS concentrations collected from 28 necropsied cattle. Total PFOS is the sum of linear and branched (3Me-PFOS and 6Me-PFOS) isomer concentrations. For the samples collected from the 20 cattle necropsied at day 14 following removal from exposure (cohort 1), muscle PFOS concentrations ranged from 1.52 to 10.17 ng/g, and plasma PFOS concentrations ranged from 28.97 to 156.29 ng/mL. For the samples collected from the 8 cows necropsied at day 137 or 153 following removal from exposure (cohort 2), muscle PFOS concentrations ranged from 0.68 to 2.78 ng/g, and plasma PFOS concentrations ranged from 15.21 to 61.09 ng/mL (Supporting Information, Table B*).
Three of the 28 muscle 6Me-PFOS concentration measurements were interval-censored, above the limit of detection (LOD, 0.18 ng/g) but below the limit of quantitation (LOQ, 0.26 ng/g). One muscle 6Me-PFOS concentration measurement was left censored, below the LOD. Given that the censored observations represented less than 15% of the paired muscle-plasma data, the censored data values were replaced by 1/2 LOQ and 1/2 LOD. (20) To investigate the sensitivity of the estimated plasma-muscle PFOS relationship to this default treatment of censored data values, bounding estimates were considered. A lower bound was obtained by replacing the censored data values by LOD and 0. An upper bound was obtained by replacing the censored data values by LOQ and LOD.

2.4.1. Linear Regression of Log-Transformed Data

As chemical concentrations have a lower bound of zero, linear regression was applied to natural log-transformed muscle and plasma concentration data (ln([ppb])) to analyze the relationship between PFOS concentrations in muscle tissue and plasma. The exponentiated results produced a curvilinear model form that effectively passed through the origin without imposing a constraint on the intercept term, and the resultant model predictions did not contain infeasible negative concentration values.

2.4.2. Model Selection

The selection of independent variables to include in the muscle-plasma regression model began by considering a complete linear regression model containing three animal classes (heifer, lactating, and dry), two necropsy date cohort classes (cohort 1 (old) = 14 days and cohort 2 (new) = 137 or 153 days), and three plasma concentration–class interaction terms
Yi=b0+b1Xi+b2lactatingi+b3dryi+b4newi+b5(Xi×lactatingi)+b6(Xi×dryi)+b7(Xi×newi)+ei
(1)
where Yi = ln([PFOS musclei]); Xi = ln([PFOS plasmai]); lactating and dry class variables and the cohort class variables were coded as 0 or 1 for i = 1, 2, ···, 28 cows; and e is the residual error. Equation 1 allows both the intercept and slope terms to vary by the animal class and necropsy date cohort.
Among all possible regressions under the complete model (eq 1), the model containing ln([PFOS plasma]), the dry class variable, the lactating class interaction term (ln([PFOS plasma])*lactating), and the cohort interaction term (ln([PFOS plasma])*new) was preferred based on the Akaike information criterion (AIC) (21) and Bayesian information criterion (BIC). (22) Therefore, the following linear regression model (eq 2) was selected for analysis
Yi=b0+b1Xi+b2dryi+b3(Xi×lactatingi)+b4(Xi×newi)+ei
(2)
The dry cattle class variable indicates that the intercept term for the dry class differs from those of the heifers or lactating cows. The lactating interaction term indicates that the slope term for the lactating class differs from that of heifers or dry cows. The cohort interaction term indicates that the slope term differs between the two cohorts with widely separated necropsy dates.

2.4.3. Ordinary Least-Squares Diagnostics

The muscle-plasma regression model (eq 2) was fit using ordinary least-squares (OLS) methods. Diagnostics were performed to evaluate the regression model assumptions. Regression on the residuals for the independent variables confirmed no significant linear or quadratic trends in the residuals. This provided no evidence to reject the assumed model form. Tests of the normality of the residuals using SAS PROC UNIVARIATE failed to reject the assumption that the residuals are normally distributed.c White’s (18) test provided no evidence to reject the assumption of homogeneous variance about the regression line.

2.4.4. Prediction Interval Calculation

A prediction interval accounts for uncertainty about the regression parameters and random variability around the predicted values. Predicted values of the log-transformed data were calculated as
Y0=b0+b1X0+b2dry0+b3(X0×lactating0)+b4(X0×new0)
(3)
For OLS, the standard error of prediction (SEP) is defined as
SEP0=(s2(1+h0))
(4)
where h0 = x0 [X′X]–1 x0′, s2 = mean square residual (MSR), and X is the observed (28 × 5) X matrix with
xi=[1Xidryi(Xi×lactatingi)(Xi×newi)]
A (1 – α)% prediction interval for the log-transformed data were calculated as
Y0^±t1−(α/2),23SEP0
(5)
The upper bound of a 90% prediction interval (with α = 0.1) is the 95th percentile. The predicted values and the prediction interval for the untransformed PFOS concentration values (ppb) were obtained by exponentiation of eqs 3 and 5.

2.4.5. Calculation of a Plasma PFOS Concentration of Concern Equivalent to the Interim Screening Level in Beef

In 2019, an interim PFOS screening level in the muscle tissue of 4.1 ng/g was derived. USDA-FSIS determined the plasma PFOS concentration of concern (COC) associated with this interim screening level in muscle as the 95th percentile of the prediction interval for the estimated regression curve.
The muscle concentration values of the 95th percentile of the prediction intervals were calculated by class x cohort combination for a series of plasma PFOS concentration values between 0 and 150 ng/mL in increments of 1 ng/mL. The plasma PFOS concentration value associated with a 95th percentile muscle tissue concentration value of 4.1 ng/g was obtained from the lower bound of the 1 ng/mL increment containing the screening level.

2.5. PFOS Plasma Depletion Analysis

The objective of the PFOS plasma depletion analysis was to estimate the duration of removal (withdrawal time) from exposure to PFOS required for beef from PFOS contaminated dairy cattle to decrease to the interim screening level. The analysis was based on plasma PFOS concentrations of the 8 cows necropsied 137 and 153 days after removal from PFOS exposure (Supporting Information, Table C*).

2.5.1. Analysis of Repeated Measures

To account for the lack of independence of repeated measures within cows across time, longitudinal data analysis was performed by using generalized estimating equations (GEE) in SAS PROC GENMOD under default settings. This results in GEE parameter point estimates equivalent to OLS regression but with standard errors that reflect repeated measures.

2.5.2. Model Selection

Four depletion model forms were considered
log‐linear:ln(Cit)=ln(C0)+bicowi+b1days+b2heiferi×days
(6)
log‐quadratic:ln(Cit)=ln(C0)+bicowi+b1days+b2days2+b3heiferi×days
(7)
log‐cubic:ln(Cit)=ln(C0)+bicowi+b1days+b2days2+b3days3+b4heiferi×days
(8)
second‐order:1Cit=1C0+bicowi+b1days+b2heiferi×days
(9)
where Cit = plasma PFOS concentration in cow i at time t, cowi = an animal identification class variable (such that each cow has an estimated intercept value at time zero (Ci0)), and heiferix days is an interaction term.
The animal class was identified by a binary indicator variable (heifer = 0,1). (There were 5 heifers, 3 lactating cows, and no dry cows.) A difference in plasma depletion rates between heifers and lactating cow classes was evaluated by including the heiferix days interaction term in the models. The four model forms (eqs 6–9) were evaluated (with and without an interaction term) based on the GEE fit criterion: Quasi-likelihood under the Independence model Criterion (QIC).
The log-linear model assumes a constant proportional depletion rate across time. The log-quadratic, log-cubic, and second-order models allow the depletion rate to vary with time. The second-order model also implies that subsequent PFOS concentrations must be lower than the initial concentration:
1Ct=1C0+b1days:=ln(C0−CtC0Ct)=ln(b1)+ln(days)
(10)
If Ct ≥ C0, ln(C0 – Ct) and eq 10 are undefined.
The interaction term (heifer x days) was not significant in any of the models (p ≥ 0.12), providing no evidence that the depletion rate differs between animal classes.
The log-linear model without an interaction term provided the best fit among the candidate models based on the QIC criterion value (88.5, where smaller is better). However, the log-linear model (with or without an interaction term) was rejected due to a significant, U-shaped quadratic pattern in the residuals (p < 0.01), indicating a nonconstant depletion rate across time.d
The log-quadratic model (with or without an interaction term) indicated significant nonlinearity (p < 0.05), with QIC values of 95.23 and 91.27, respectively. The log-cubic model quadratic and cubic terms were not individually significant (p ≥ 0.05), but their inclusion resulted in a better fit (QIC = 94.67 and 90.79, respectively) relative to the log-quadratic model. Nevertheless, both the estimated log-quadratic and log-cubic models resulted in convex (U-shaped) curves that would predict that after an animal is removed from exposure, its plasma PFOS concentration would decrease to a minimum value and then subsequently increase without bound across time. Therefore, neither model is appropriate for extrapolation beyond the observed study duration (153 days).
The second-order model implies that subsequent concentrations must be lower than the initial plasma concentration (eq 10). However, the plasma PFOS concentrations observed 14 days after removal from exposure were not lower than the initial concentrations for all cows. For all cows in the depletion study, the plasma PFOS concentration temporal pattern did not strictly decrease (higher concentrations frequently followed lower concentrations). Under these conditions, the second-order model resulted in a curvilinear pattern in the residuals and provided the poorest fit among the candidate models (QIC = 105.41 and 96.89, respectively).
None of the candidate models provide an ideal characterization of PFOS plasma depletion dynamics across time. This reflects apparently complex PFOS plasma depletion dynamics measured in previous studies with cattle. (9,11) On the basis of the model fit (QIC) and regression diagnostics, the log-cubic model form was selected to characterize depletion within the observed study duration. Omitting the insignificant interaction term improved the model fit, resulting in the final plasma depletion model
ln(Cit)=b0+bicowi+b1days+b2days2+b3days3
(11)
Note that the intercept terms (b0 + bi cowi) represent the initial PFOS concentration prior to removal from exposure and are animal-specific. The nonintercept parameters (b1, b2, and b3) determine the predicted depletion slope behavior across time. (Positive higher-order terms (b2 and/or b3) result in convex (U-shaped) curves.)
Diagnostics were performed to evaluate the log-cubic depletion regression model assumptions. Regression of the residuals on days confirmed no significant linear or quadratic trends in the residuals. This provides no evidence to reject the assumed model form within the observed study duration but does not provide evidence to support extrapolation beyond the observed data. Regression of the squared residuals on days indicated no significant linear or quadratic trends, providing no evidence to reject the assumption of homogeneous variance about the regression. Tests of the normality of the residuals using SAS PROC UNIVARIATE failed to reject the assumption that the residuals are normally distributed.

2.6. Estimation of Within-Herd Variability in PFOS Plasma Concentrations

Prewithdrawal PFOS plasma concentrations are required for estimating withdrawal times. Therefore, the objective of this section is to provide an illustrative scenario for a prewithdrawal baseline of within-herd variability in PFOS plasma concentrations resulting from exposure to the same sources (drinking water and feed) This section also describes a process for estimating the within-herd variability distribution of PFOS plasma concentrations from a sample of the potentially exposed herd. To estimate potential differences in the plasma PFOS concentration distributions among animal classes and characterize the uncertainty associated with these distributions, on-farm plasma PFOS concentrations from 169 cows (39 heifers, 30 lactating, and 100 dry) were analyzed (Supporting Information, Table A*)
Chemical concentrations have a lower bound of zero. Therefore, the log-normal distribution was selected for characterizing variability in PFOS plasma concentrations. To test the hypothesis that the sample data are log-normally distributed, the data were log-transformed, and a test of the hypothesis that the log-transformed data were normally distributed within animal classes was performed using SAS PROC UNIVARIATE. Three animal classes were considered: heifer, lactating, and dry. For each of the three animal classes considered, SAS PROC UNIVARIATE failed to reject the hypothesis of a normal distribution at a significance level of 0.05. Therefore, the within-class plasma PFOS concentration variability was considered to be log-normally distributed.
Tests for the same plasma PFOS concentration variability distribution among classes were performed by using SAS PROC NPAR1WAY. The procedure was applied to the log-transformed concentration data. Analysis of variance (ANOVA) results rejected the hypothesis that the heifer, lactating, and dry animal classes all share the same variability distribution at a significance level of <0.001. Inspection of the empirical distributions clearly distinguished the heifer class from the lactating and dry classes. None of the tests rejected the hypothesis that the lactating and dry cows have the same variability distribution at a significance level of <0.10. Therefore, the baseline plasma PFOS concentration variability distributions were considered to differ between heifer and lactating/dry cows.
Ninety percent confidence intervals for the class-specific plasma PFOS concentration log-normal variability distributions were calculated using SAS PROC LIFEREG. Thus, the upper bound is the 95th percentile of the confidence interval, which can be calculated for any percentile of the variability distribution (e.g., the 95% confidence level for the 95th percentile of the distribution).

2.7. Estimation of Withdrawal Times

Under the baseline scenario described in Section 2.6, withdrawal times were estimated to determine the duration of removal (withdrawal time) from exposure to PFOS required for a cow containing a particular percentile PFOS contamination to decrease to the target plasma PFOS concentration of concern identified for cohort 1 cows. (There were no dry cows in cohort 2.)
To estimate the withdrawal time for the plasma PFOS concentration to decrease to the desired concentration, we treated the 169 on-farm plasma PFOS concentration values as initial values (Supporting Information, Table A*), applied the nonintercept parameter estimates of the depletion model (eq 11), and solved numerically for the time required for the estimated within-class mean plasma PFOS concentration to decrease to a specified level. The arithmetic mean (μ) of a log-normal distribution was obtained from the mean and standard deviation of the log-transformed data (μln and σln, respectively) (23)
μ=exp(μln+12σln2)
(12)
Numerical solutions were obtained using Excel Solver.

3. Results

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Analysis of water and feed from NMSU indicated that PFOS was below the method LOD for all samples. Thus, external PFOS exposures were considered to be terminated when the cows were transferred to NMSU.

3.1. Relationship between Cattle Plasma and Muscle PFOS Concentrations

Table 1 summarizes the regression analysis results for the relationship between log-transformed dairy cattle PFOS plasma and muscle concentrations (eq 2). The significant positive value for the dry class term (b2) indicates a larger intercept term for dry cows relative to those of heifers or lactating cows. The significant positive value for the lactating interaction term (b3) indicates a larger slope term for lactating cows relative to heifers or dry cows. The significant negative value for the cohort interaction term (b4) indicates a smaller slope term for cohort 2 relative to cohort 1. Figure 1 compares the log-transformed observed muscle and plasma data with the regression model predictions and the interim screening level of 4.1 ng/g PFOS in beef (65% of the observed muscle PFOS concentrations in cohort 1 exceeded the interim screening level at the 2 week necropsy).

Figure 1

Figure 1. Observed versus predicted muscle and plasma PFOS concentrations (log-transformed).

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Table 1. Summary of Regression Analysis for Plasma and Muscle PFOS Concentration Relationship
 regression statistics
adjusted R square0.88
root mean square error0.27
observations28
ANOVA
sourcedfSSMSFp ≥ F
regression414.89433.723650.88<.0001
residual231.68310.0732  
total2716.5774   
parameterestimatestandard errort valuep ≥ |t|
b0 (intercept)–1.77830.5370–3.31000.0030
b1 (ln(PFOS plamsa))0.67300.13654.9300<.0001
b2 (dry)0.55800.19872.81000.0100
b3 (ln(PFOS plamsa)*lactating)0.10630.03383.15000.0045
b4 (ln(PFOS plamsa)*new)–0.09980.0439–2.28000.0325
Figure 2, 3 and 4 present the predicted values and upper bounds (95 percentiles) of the prediction intervals of the muscle PFOS concentration for each animal class (heifer, lactating, and dry) by cohorts (1 and 2). Because all cohort 2 cows had plasma PFOS concentrations <62 ng/mL and there were no dry cows in cohort 2, Figures 2–4 do not extrapolate beyond the observed data. Based on the prediction interval, we can estimate the plasma PFOS concentration such that 95% of cattle in a class–cohort combination with that plasma concentration would have muscle PFOS concentrations not exceeding 4.1 ng/g. This is illustrated in Figures 2–4 and summarized in Table 2.

Figure 2

Figure 2. Predicted values and prediction interval upper bounds for the relationship between PFOS concentrations in muscle and plasma for the heifer animal class by the cohort.

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Figure 3

Figure 3. Predicted values and prediction interval upper bounds for the relationship between PFOS concentrations in muscle and plasma for the lactating animal class by the cohort.

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Figure 4

Figure 4. Predicted values and prediction interval upper bounds for the relationship between PFOS concentrations in muscle and plasma for the dry animal class by the cohort.

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Table 2. Plasma PFOS Concentrations for 95% of Cattle to Have Muscle PFOS Concentrations Not Exceeding 4.1 ng/g (Default Censored Data Treatment)
plasma PFOS (ng/mL)
classcohort 1cohort 2
heifer5489a
lactating3051
dry1836b
a

Cohort 2 cows <62 ng/mL plasma PFOS.

b

No dry cows in cohort 2.

Sensitivity analysis of the four censored muscle concentration values demonstrates that the default handling of the censored observations provides robust estimates for the plasma concentration of concern (Tables 3 and 4). Despite extreme lower and upper bounds for the censored values, plasma PFOS concentrations of concern change by 3 ng/mL or less relative to the default assumptions.
Table 3. Plasma PFOS Concentrations for 95% of Cattle to Have Muscle PFOS Concentrations Not Exceeding 4.1 ng/g (Lower Bound Censored Data Treatment)
plasma PFOS (ng/mL)
classcohort 1cohort 2
heifer5486a
lactating3150
dry1937b
a

Cohort 2 cows <62 ng/mL plasma PFOS.

b

No dry cows in cohort 2.

Table 4. Plasma PFOS Concentrations for 95% of Cattle to Have Muscle PFOS Concentrations Not Exceeding 4.1 ng/g (Upper Bound Censored Data Treatment)
plasma PFOS (ng/mL)
classcohort 1cohort 2
heifer5591a
lactating2950
dry1735b
a

Cohort 2 cows <62 ng/mL plasma PFOS.

b

No dry cows in cohort 2.

3.2. PFOS Plasma Depletion

Table 5 summarizes the regression analysis results for the log-cubic plasma depletion model (eq 11). Because initial concentrations are animal-specific, only the parameters that determine the predicted depletion slope behavior across time are of interest to estimate the required withdrawal time. To avoid estimated parameter values <0.0001 (that SAS would report as zero), the time was rescaled as months (days/30).
Table 5. Analysis of GEE Parameter Estimates for the Log-Cubic Plasma Depletion Model
parameterestimateempirical standard errorZPr ≥ |Z|
b1 (months)–0.29500.0578–5.1<.0001
b2 (months2)0.00440.02170.20.841
b3 (months3)0.00170.00260.640.521
Figure 5 compares the observed data to the log-cubic model predictions for the 8 cows that were necropsied after extended withdrawal periods. The comparison indicates a good fit (for the analogous ordinary least-squares model, the adjusted R2 = 0.94).

Figure 5

Figure 5. Comparison of plasma PFOS concentrations observed and predicted by the log-cubic depletion model.

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Independent of the data used to estimate the depletion model, paired plasma PFOS concentration data for 19 cohort 1 cattle were collected on-farm and at necropsy 14 days after removal from PFOS exposure (Supporting Information, Tables A* and B*).e The observed mean reduction in plasma PFOS concentration for the cattle after 14 days was 15.2% (standard deviation = 14.8%). The predicted mean reduction based on the log-cubic depletion model was 15.5%. A paired two sample t-test performed using the Excel AnalysisToolPak found no significant difference between the observed and predicted mean concentrations for cohort 1 cattle at 14 days of withdrawal. Therefore, the depletion model made an accurate out-of-sample prediction for a 14 day withdrawal period. This provides a degree of confidence in the utility of the plasma depletion model for making predictions during the early withdrawal period.

3.3. Within-Herd Variability in Plasma PFOS Concentrations

The within-herd plasma PFOS concentration variability analysis results are summarized in Figure 6. This provides an empirically based, illustrative scenario for a prewithdrawal baseline in a PFOS-exposed dairy herd.

Figure 6

Figure 6. Plasma PFOS concentration variability distribution for heifer and lactating/dry cows. (MLE─maximum likelihood estimate; 0.95 = 95% confidence limit; 0.05 = 5% confidence limit).

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3.4. Withdrawal Time

Under the baseline scenario described in Section 2.6, the estimated withdrawal time under the log-cubic depletion model for approximately 99% of cows to reach the target plasma PFOS concentration ranged from 119 days (heifers) to an undetermined period exceeding the study duration of 153 days (lactating/dry cows) (Table 6). The estimated withdrawal time for the mean plasma PFOS concentration to reach the target plasma PFOS concentration ranged from 25 days (heifers) to an undetermined period exceeding the study duration of 153 days (lactating/dry cows). After 153 days of withdrawal, the 99th percentile on-farm PFOS plasma concentration for lactating/dry cows was estimated to decrease to 61.03 ng/mL. Similarly, the mean on-farm PFOS plasma concentration for lactating/dry cows was estimated to decrease to 36.49 ng/mL.
Table 6. Estimated Withdrawal Times to Reach PFOS Plasma Concentration of Concern
animal class (COCb ng/mL)MLEa of 99th %ile on-farm PFOS plasma concentration (ng/mL)estimated withdrawal time for 99th %ile to reach COC (days)MLEa of mean on-farm PFOS plasma concentration (ng/mL)estimated withdrawal time for class to reach mean COC (days)
heifer (54)145.611968.625
lactating (30)195.6≥153116.9≥153
dry (18)195.6≥153116.9≥153
a

Maximum likelihood estimate (MLE)

b

PFOS plasma concentration of concern (cohort 1).

As an alternative to the baseline scenario, under the log-cubic depletion model, we can solve for the initial plasma concentration within a class that would result in a maximum likelihood estimate at 153 days (study duration) equal to the concentration of concern (54, 30, and 18 ng/mL for heifers, lactating cows, and dry cows, respectively). In heifers, this initial plasma concentration is 173 ng/mL. In comparison, the 95% confidence limit for the 99th percentile of the plasma concentration variability distribution for heifers is 174 ng/mL (Figure 6). In lactating cows, this initial plasma concentration is 96 ng/mL. This corresponds to the 95% confidence limit for the 18th percentile of the plasma concentration variability distribution for lactating and dry cows (Figure 6). In dry cows, this initial plasma concentration is 58 ng/mL. In comparison, the 5% confidence limit for the first percentile of the plasma concentration variability distribution for lactating and dry cows is 62 ng/mL (Figure 6).
The log-linear depletion model’s slope coefficient is −0.2365 per month. Using this estimate to approximate withdrawal times beyond the study period suggests that lactating and dry cows might require more than 238 and 303 days of withdrawal, respectively, to reach their target PFOS concentrations when starting at the 99th percentile of their on-farm plasma concentration. Similarly, a starting on-farm mean concentration for lactating and dry cows might require more than 173 and 238 days of withdrawal, respectively.f

4. Discussion

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Using the paired muscle and plasma PFOS concentrations for 28 cows necropsied at NMSU afforded the opportunity to correlate PFOS residue data in plasma and muscle that were collected nearly simultaneously (within 1 h) from the same animal. This permitted the analysis of plasma versus muscle PFOS concentrations and the subsequent development of a model to estimate plasma PFOS concentrations for ante-mortem screening of cattle suspected of having muscle PFOS concentrations greater than the interim screening level of 4.1 ng/g. This cross-sectional model estimated that among cows included in this study, at least 95% of heifers with a plasma PFOS concentration of 54 ng/mL, lactating cows with a plasma PFOS concentration of 30 ng/mL, and dry cows with a plasma PFOS concentration of 18 ng/mL would have a muscle PFOS concentration of less than 4.1 ng/g (Table 2). Application of these ante-mortem plasma screening levels to suspect cattle could be used to predict whether beef derived from suspect dairy cattle populations (or subpopulations) exceeds a particular screening level. An ante-mortem screening approach such as this would likely limit both the unwarranted condemnation of carcasses from PFOS-exposed cattle and the probability of human consumption of PFOS contaminated beef.
Nevertheless, the conclusions of this analysis depend on the interim screening level which was based on the USEPA 2016 PFOS RfD. (4) This level may change as the science of PFOS evolves. In May 2021, ATSDR published an oral minimal risk level (MRL) for PFOS. (24) In June 2022, USEPA issued an updated Interim Drinking Water Health Advisory for PFOS. (25) In August 2022, the USEPA Science Advisory Board issued its “Review of EPA’s Analyses to Support EPA’s National Primary Drinking Water Rulemaking for PFAS,” which among other topics addressed USEPA’s development of the PFOA and PFOS RfDs. (26) In light of ongoing changes to health-based guidance values for PFAS, USDA-FSIS routinely reviews and updates its approach in close collaboration with the USFDA and other relevant agencies.
The estimated withdrawal times generated with the plasma depletion model may provide guidance for the implementation of a risk management strategy for the potential harvesting of beef from PFOS-exposed cattle. Among animal classes (heifer, dry, or lactating), the plasma PFOS concentration of concern differs. Within a class, the estimated time for cattle to decrease to the concentration of concern is dependent on the initial plasma PFOS concentrations. Due to the limited duration of the plasma depletion study, the withdrawal times for the 99th percentile and mean plasma PFOS concentrations in dry and lactating cows under the baseline scenario (described in Section 2.6) are estimated to exceed 153 days. Extrapolation of the log-linear depletion model past 153 days suggests that the lactating cattle population in this study would require a withdrawal period of at least 238 days. Similarly, the dry cattle population would require at least 303 days of withdrawal to reach its respective target PFOS concentrations. Similarly, a starting on-farm mean concentration for lactating and dry cattle would likely require at least 173 and 238 days of withdrawal, respectively. Under different baseline conditions with lower initial plasma PFOS concentrations, it may be possible to estimate withdrawal times for all animal classes based on the results of this study.
As it is likely that the beef from slaughtered dairy cattle will be fabricated into ground beef, applying a risk management strategy based on the mean concentration would provide a cost-effective strategy to produce beef that does not exceed the interim screening level. Under normal conditions, lactating cows are rarely slaughtered for beef. However, if a dairy operation with PFAS-exposed cows cannot market its milk, lactating cows may be included in the set of animals intended for slaughter. Another strategy could be to remove the herd from PFOS exposure (e.g., transfer to a different location or provision of alternate feed or water sources). The plasma from heifers could be monitored until it decreases below a concentration of concern, and then the heifers could be slaughtered to generate working capital for the operation while the remaining cattle are monitored.
In summary, the method presented here provides a valuable ante-mortem approach to determine the fate of PFAS-exposed cattle. Monitoring blood PFOS levels would permit farmers to determine whether the cattle are suitable for slaughter. If blood and estimated muscle PFOS levels exceed regulatory limits, this method can be applied to estimate the required time for cattle PFOS residues to decrease to an acceptable level after the removal of cattle from the contaminated site. If the estimated time for the cattle to reach acceptable PFOS concentrations is economically unfeasible, then the cattle must be disposed of. In this situation, application of this approach to estimate tissue PFOS concentrations for highly PFAS-contaminated cattle could provide guidance regarding the proper disposal of carcasses (hazardous waste disposal vs municipal waste disposal site).

Supporting Information

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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsagscitech.3c00102.

  • Time-course data used in the study; on-farm PFOS plasma concentrations; paired PFOS muscle-plasma concentrations; PFOS plasma depletion data; precursor and product ions, cone voltages, and collision energies used for the mass spectrometric quantification of PFOS isomers and internal standards; paired observations used to estimate on-farm PFOS plasma concentrations (PDF)

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Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Author Information

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  • Corresponding Author
  • Authors
    • John J. Johnston - Department of Food Science and Human Nutrition, Colorado State University, 1571 Campus Delivery, Fort Collins, Colorado 80523, United States
    • Eric D. Ebel - USDA Food Safety and Inspection Service, 1400 Independence Avenue SW, Washington, District of Columbia 20250, United States;  Orcidhttps://orcid.org/0009-0007-7663-2732
    • Emilio Esteban - USDA Food Safety and Inspection Service, 1400 Independence Avenue SW, Washington, District of Columbia 20250, United States
    • Sara J. Lupton - USDA Agricultural Research Service, Edward T. Schafer Agricultural Research Center, 1616 Albrecht Blvd. North Fargo, North Dakota 58102, United States
    • Eric J. Scholljegerdes - Dept. Animal and Range Sciences, New Mexico State University, Box 30003, MSC 3-I, Las Cruces, New Mexico 88003, United States
    • Shanna L. Ivey - Dept. Animal and Range Sciences, New Mexico State University, Box 30003, MSC 3-I, Las Cruces, New Mexico 88003, United States
    • Mark R. Powell - USDA Office of Risk Assessment and Cost Benefit Analysis, 1400 Independence Avenue SW, Washington, District of Columbia 20250, United States
    • David J. Smith - USDA Agricultural Research Service, Edward T. Schafer Agricultural Research Center, 1616 Albrecht Blvd. North Fargo, North Dakota 58102, United States;  Orcidhttps://orcid.org/0000-0001-8883-4744
  • Notes
    The authors declare no competing financial interest.

Additional Notes

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a The PFOS concentrations for animal 7840 were identified as an outlier by Cook’s D value and were not included in this stage of the analysis.

b The adjustment is based on cooked mass = 0.748 x raw mass, where a 74.8% cooking yield is the average yield found in Showell et al.

c SAS© PROC UNIVARIATE provides four test statistics for testing the normality of data: Shapiro–Wilk, Kolmogorov–Smirnov, Cramer–von Mises, and Anderson–Darling.

d The U-shaped pattern in the residuals indicates that early and late in the observed withdrawal period, the log-linear model underestimates concentration. In the middle period, it overestimates concentration. To provide crude withdrawal time estimates that extend beyond the observed data, we used the log-linear model despite its bias to underestimate plasma concentrations for longer withdrawal times.

e On-farm measurement not available for one of the cohort 1 cattle (id 21634).

f Because the log-linear depletion model underestimates plasma concentrations late in the withdrawal period, the extrapolated withdrawal times for the lactating and dry classes are lower bounds.

References

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This article references 26 other publications.

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    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 det. plasma and tissue depletion kinetics in cattle, 2 steers and 4 heifers were dosed with PFOS at 0.098 mg/kg body wt. and 9.1 mg/kg, resp. Plasma depletion half-lives for steers and heifers were 120 ± 4.1 and 106 ± 23.1 days, resp. Specific tissue depletion half-lives ranged from 36 to 385 days for i.p. 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.
  10. 10
    Lupton, S. J.; Huwe, J. K.; Smith, D. J.; Dearfield, K. L.; Johnston, J. J. Absorption and excretion of 14C-perfluorooctanoic acid (PFOA) in Angus cattle (Bos taurus). J. Agric. Food Chem. 2012, 60 (4), 1128– 1134,  DOI: 10.1021/jf2042505
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    10
    Absorption and Excretion of 14C-Perfluorooctanoic Acid (PFOA) in Angus Cattle (Bos taurus)
    Lupton, Sara J.; Huwe, Janice K.; Smith, David J.; Dearfield, Kerry L.; Johnston, John J.
    Journal of Agricultural and Food Chemistry (2012), 60 (4), 1128-1134CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
    Perfluoroalkyl substances (PFASs), such as perfluorooctanoic acid (PFOA), are environmentally persistent industrial chems. often found in biosolids. Application of these biosolids to pastures raises concern about the accumulation of PFOA in the edible tissues of food animals. Because data on the absorption, distribution, metab., and excretion (ADME) of PFOA in cattle were unavailable, a study was conducted to det. pharmacokinetic parameters following a single oral exposure (1 mg/kg body wt. of 14C-PFOA) in four Lowline Angus steers. Radiocarbon was quantified in blood, urine, and feces for 28 days and in tissues at the time of slaughter (28 days) by liq. scintillation counting (LSC) or by combustion anal. with LSC with confirmation by liq. chromatog.-tandem mass spectrometry (LC-MS/MS). 14C-PFOA was completely absorbed and excreted (100.7 ± 3.3% recovery) in the urine within 9 days of dosing. The plasma elimination half-life was 19.2 ± 3.3 h. No 14C-PFOA-derived radioactivity was detected in edible tissues. Although PFOA was rapidly absorbed, it was also rapidly excreted by steers and did not persist in edible tissues, suggesting meat from cattle exposed to an acute dose of PFOA is unlikely to be a major source of exposure to humans.
  11. 11
    Lupton, S. J.; Huwe, J. K.; Smith, D. J.; Dearfield, K. L.; Johnston, J. J. Distribution and excretion of perfluorooctane sulfonate (PFOS) in beef cattle (Bos taurus). J. Agric. Food Chem. 2014, 62 (5), 1167– 1173,  DOI: 10.1021/jf404355b
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    11
    Distribution and excretion of perfluorooctane sulfonate (PFOS) in beef cattle (Bos taurus)
    Lupton, Sara J.; Huwe, Janice K.; Smith, David J.; Dearfield, Kerry L.; Johnston, John J.
    Journal of Agricultural and Food Chemistry (2014), 62 (5), 1167-1173CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
    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 det. these parameters for PFOS in three Lowline Angus steers given a single oral dose of PFOS at approx. 8 mg/kg body wt. PFOS concns. were detd. by liq. chromatog.-tandem mass spectrometry in multiple tissue compartments. The major route of excretion was in the feces (11 ± 1.3% of the dose, mean ± std. deviation) with minimal PFOS elimination in urine (0.5 ± 0.07% of the dose). At day 28 the mean plasma concn. remained elevated at 52.6 ± 3.4 μg/mL, and it was estd. that 35.8 ± 4.3% of the dose was present in the plasma. Plasma half-lives could not be calcd. 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.
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    Vestergren, R.; Orata, F.; Berger, U.; Cousins, I. T. Bioaccumulation of perfluoroalkyl acids in dairy cows in a naturally contaminated environment. Environ. Sci. Pollut. Res. 2013, 20, 7959– 7969,  DOI: 10.1007/s11356-013-1722-x
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    Bioaccumulation of perfluoroalkyl acids in dairy cows in a naturally contaminated environment
    Vestergren, Robin; Orata, Francis; Berger, Urs; Cousins, Ian T.
    Environmental Science and Pollution Research (2013), 20 (11), 7959-7969CODEN: ESPLEC; ISSN:0944-1344. (Springer)
    Beef and dairy products may be important vectors of human exposure to perfluoroalkyl acids (PFAAs), but the understanding of how PFAAs are accumulated and transferred through agricultural food chains is very limited. Here, the bioaccumulation of PFAAs in dairy cows receiving naturally contaminated feed and drinking water was investigated by conducting a mass balance of PFAAs for a herd of dairy cows in a barn on a typical Swedish dairy farm. It was assumed that the cows were able to reach steady state with their dietary intake of PFAAs. Perfluorooctane sulfonic acid (PFOS) and perfluoroalkyl carboxylic acids (PFCAs) with 8 to 12 carbons were detected in cow tissue samples (liver, muscle, and blood) at concns. up to 130 ng kg-1. Mass balance calcns. demonstrated an agreement between total intake and excretion within a factor of 1.5 and consumption of silage was identified as the dominant intake pathway for all PFAAs. Biomagnification factors (BMFs) were highly tissue and homolog specific. While BMFs of PFOS and PFCAs with 9 and 10 fluorinated carbons in liver ranged from 10 to 20, perfluorooctanoic acid (PFOA) was not biomagnified (BMF<1) in any of the investigated tissues. Biotransfer factors (BTFs; defined as the concn. in tissue divided by the total daily intake) were calcd. for muscle and milk. Log BTFs ranged from -1.95 to -1.15 day kg-1 with the highest BTF obsd. for PFOS in muscle. Overall, the results of this study suggest that long-chain PFAAs have a relatively high potential for transfer to milk and beef from the diet of dairy cows. However, a low input of PFAAs to terrestrial systems via atm. deposition and low bioavailability of PFAAs in soil limits the amt. of PFAAs that enter terrestrial agricultural food chains in background contaminated environments and makes this pathway less important than aquatic exposure pathways. The BTFs estd. here provide a useful tool for predicting human exposure to PFAAs via milk and beef under different contamination scenarios.
  13. 13
    Wilson, T. B.; Stevenson, G.; Crough, R.; de Araujo, J.; Fernando, N.; Anwar, A.; Scott, T.; Quinteros, J. A.; Scott, P. C.; Archer, M. J. G. Evaluation of Residues in Hen Eggs After Exposure of Laying Hens to Water Containing Per-and Polyfluoroalkyl Substances. Environ. Toxicol. Chem. 2021, 40 (3), 735– 743,  DOI: 10.1002/etc.4723
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    Evaluation of Residues in Hen Eggs After Exposure of Laying Hens to Water Containing Per- and Polyfluoroalkyl Substances
    Wilson, Timothy B.; Stevenson, Gavin; Crough, Robert; de Araujo, Jesuina; Fernando, Nilhan; Anwar, Arif; Scott, Tyrone; Quinteros, Jose A.; Scott, Peter C.; Archer, Michael J. G.
    Environmental Toxicology and Chemistry (2021), 40 (3), 735-743CODEN: ETOCDK; ISSN:0730-7268. (Wiley-Blackwell)
    Per- and polyfluoroalkyl substances (PFAS) have been used in aq. film-forming foams used in firefighting, resulting in soil and groundwater contamination and leading to human exposure via animal products grown in contaminated areas. The present study reports the relationship between PFAS intake by hens and the PFAS concns. in the edible parts of eggs. Laying hens were exposed via drinking water to different concns. of 4 PFAS compds. (perfluorooctane sulfonate [PFOS], perfluorohexane sulfonate [PFHxS], perfluorooctanoic acid [PFOA], and perfluorohexanoic acid) over 61 d. Egg PFAS residues were assessed for a further 30 d after exposure ceased. The target concns. of PFAS were 0, 0.3, 3, 30, and 300μg/L for the treatment groups T1-T5, resp.; and PFAS residues were detd. from the eggs collected every second day. There was a linear correlation between the PFAS concns. in the drinking water of hens and those detected in the egg, which could be useful in estg. PFAS concns. in the egg by measuring water concns. Exposure of hens to drinking water with PFAS concns. below the Australian Government Department of Health limits (PFOS and PFHxS, 0.07μg/L; PFOA, 0.56μg/L), and with no other sources of PFAS exposure, is unlikely to result in egg PFAS concns. that would exceed the 10% limit set by Food Stds. Australia New Zealand for human consumption.
  14. 14
    Drew, R.; Hagen, T. G.; Champness, D. Accumulation of PFAS by livestock–determination of transfer factors from water to serum for cattle and sheep in Australia. Food Addit. Contam.: Part A 2021, 38 (11), 1897– 1913,  DOI: 10.1080/19440049.2021.1942562
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    Accumulation of PFAS by livestock - determination of transfer factors from water to serum for cattle and sheep in Australia
    Drew, Roger; Hagen, Tarah G.; Champness, David
    Food Additives & Contaminants, Part A (2021), 38 (11), 1897-1913CODEN: FACPAA; ISSN:1944-0057. (Taylor & Francis Ltd.)
    In this study accumulation has been detd. of several per- and polyfluoroalkyl substances (PFAS) from ingested water to steady state serum concn. for adult beef cattle and sheep raised on a hobby farm impacted by PFAS contamination. PFAS concns. in stock water were stable for more than a year, they were non-measurable in grass but present at very low levels in soil which equated to just 1% of the intake from water. Prior to quantifying PFAS in cattle serum there had been no breeding for 18 mo. Although there were high concns. of several PFAS in the water, only perfluorooctane sulfonate (PFOS) and perfluorohexane sulfonate (PFHxS) were in cattle serum in appreciable amts.; perfluoroheptane sulfonate (PFHpS), perfluorononanoic acid (PFNA) and perfluorodecanoic acid (PFDA) were much lower. Transfer factors (TFs) for cattle were calcd. by dividing steady state serum concn. (ng PFAS/mL) by water concn. (μg PFAS/L). Av. and upper est. TF values for cattle were calcd.; the former were 140 (total PFOS, i.e. tPFOS), 130 (PFHpS), 65 (PFHxS), 170 (PFNA), and 120 (PFDA). Previous investigation campaigns at the farm provided relative steady state serum PFAS concns. for sheep and cattle that allowed adjustment of the cattle TFs. The resulting av. est. TFs for ewes (non-pregnant and not lactating) were 20 (tPFOS) and 30 (PFHxS), other PFAS were not measurable in sheep serum. Discussion on using these TFs in human health risk assessments is provided. With certain assumptions/caveats the TFs allow estns. of PFAS steady state serum concns. for use in preliminary human health risk assessments (HHRAs) when only PFAS in stock water is known.
  15. 15
    Drew, R.; Hagen, T. G.; Champness, D.; Sellier, A. Half-lives of several polyfluoroalkyl substances (PFAS) in cattle serum and tissues. Food Addit. Contam.: Part A 2022, 39 (2), 320– 340,  DOI: 10.1080/19440049.2021.1991004
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    Half-lives of several polyfluoroalkyl substances (PFAS) in cattle serum and tissues
    Drew, Roger; Hagen, Tarah G.; Champness, David; Sellier, Amelie
    Food Additives & Contaminants, Part A (2022), 39 (2), 320-340CODEN: FACPAA; ISSN:1944-0057. (Taylor & Francis Ltd.)
    Cattle that were at steady-state serum polyfluoroalkyl substances (PFAS) concns. due to several years of exposure to water contaminated by residues of Aq. Film-Forming (AFFF) firefighting foam had perfluorooctane sulfonate (PFOS) isomers, perfluoroheptane sulfonate (PFHpS), perfluorohexane sulfonate (PFHxS), perfluorononanoic acid (PFNA) and perfluorodecanoic acid (PFDA) in serum. Elimination serum half-lives were detd. in five heifers from serial blood sampling over 215 days. Eleven addnl. animals that had blood sampled on day 19 (d19) were euthanised on d63. PFAS half-life ests. from the serial blood sampling and from d19/d63 data were not significantly different. The combined (n = 16) serum half-lives (in days) were: total PFOS (tPFOS, 74.1 ± 13.4), PFHpS (45.7 ± 9.4), PFHxS (9.3 ± 1.3), PFNA (12.3 ± 3.2) and PFDA (60.4 ± 10.4). The half-lives of linear PFOS (L-PFOS, 69.4 ± 11.6) and mono branched PFOS isomers (m-PFOS, 83.6 ± 19) were not significantly different than tPFOS, but for the di-branched isomers (di-PFOS), the serum half-life was significantly lower (29.9 ± 5.8). Animal age (1.4-12.3 years old) and serum concn. at the start of depuration did not influence half-lives, and there was no difference between steers and heifers. Consideration of serum and tissue PFAS concns. at d63 and d215 indicated there was no difference in tPFOS depuration from serum or muscle, but elimination from liver and kidney may be slightly longer. Depuration of PFHpS is essentially the same in serum, kidney and liver, and it is expected depletion from muscle would be comparable. The short half-life of di-PFOS, PFHxS and PFNA did not allow an assessment of clearance from tissues because they were not measurable at d215 but based on the results for PFOS and PFHpS, elimination of PFHxS from tissues is expected to mirror that from serum. Human health risk assessment implications are discussed.
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    Lupton, S. J.; Casey, F.; Smith, D. J.; Hakk, H. Perfluorooctanoic Acid Transport in Soil and Absorption and Distribution in Alfalfa (Medicago sativa). J. Food Prot. 2022, 85 (1), 164– 172,  DOI: 10.4315/JFP-21-276
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    Perfluorooctanoic acid transport in soil and absorption and distribution in Alfalfa (Medicago sativa)
    Lupton, Sara J.; Casey, Francis; Smith, David J.; Hakk, Heldur
    Journal of Food Protection (2022), 85 (1), 164-172CODEN: JFPRDR; ISSN:0362-028X. (International Association for Food Protection)
    Perfluorooctanoic acid (PFOA) is used as a surfactant in consumer and industrial products and is frequently found in biosolids from wastewater treatment plants. When present in biosolids applied to croplands, PFOA can contaminate feed and fodder used by livestock, but the extent of PFOA transfer from soil to plants is not well characterized. A single dose of radiocarbon (14C)-tagged PFOA was applied to unplanted soil or soil contg. growing alfalfa. PFOA transport through unplanted soil and uptake by alfalfa was monitored over a 10-wk study period. Radiocarbon was initially measured in roots, stems, and leaves 7 days after [14C]-PFOA application to soil. PFOA accumulation was greatest in leaves during the 10-wk sampling. By week 10, PFOA migration through unplanted soil had reached a depth of 22.8 ± 2.5 cm. In contrast, PFOA migrated to 7.5 ± 2.5 cm in soil contg. alfalfa plants. The greatest predictor of PFOA concn. in alfalfa leaves was PFOA concn. in the top 5 cm of soil; PFOA concns. at lower depths were not correlated with alfalfa PFOA concns. PFOA transport through soil may be slowed by the presence of forage; however, PFOA accumulation in edible portions of forage plants may increase food animal exposure to PFOA residues.
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  1. Sara J. Lupton, David J. Smith, Erin B. Howey, Ann S. Predgen, Carrie E. Schmidt, Eric Scholljegerdes, Shanna Ivey, Emilio Esteban, John J. Johnston. Tissue histology and depuration of per- and polyfluoroalkyl substances (PFAS) from dairy cattle with lifetime exposures to PFAS-contaminated drinking water and feed. Food Additives & Contaminants: Part A 2025, 42 (2) , 223-239. https://doi.org/10.1080/19440049.2024.2444560
  2. Xin Xu, Lisa A. Murphy. Targeted quantification of per- and polyfluoroalkyl substances (PFASs) in livestock serum by liquid chromatography–high-resolution mass spectrometry. Journal of Veterinary Diagnostic Investigation 2024, 36 (6) , 902-906. https://doi.org/10.1177/10406387241268224
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  • Abstract

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    Figure 1

    Figure 1. Observed versus predicted muscle and plasma PFOS concentrations (log-transformed).

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    Figure 2

    Figure 2. Predicted values and prediction interval upper bounds for the relationship between PFOS concentrations in muscle and plasma for the heifer animal class by the cohort.

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    Figure 3

    Figure 3. Predicted values and prediction interval upper bounds for the relationship between PFOS concentrations in muscle and plasma for the lactating animal class by the cohort.

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    Figure 4

    Figure 4. Predicted values and prediction interval upper bounds for the relationship between PFOS concentrations in muscle and plasma for the dry animal class by the cohort.

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    Figure 5

    Figure 5. Comparison of plasma PFOS concentrations observed and predicted by the log-cubic depletion model.

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    Figure 6

    Figure 6. Plasma PFOS concentration variability distribution for heifer and lactating/dry cows. (MLE─maximum likelihood estimate; 0.95 = 95% confidence limit; 0.05 = 5% confidence limit).

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  • References

    This article references 26 other publications.

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      Lupton, Sara J.; Smith, David J.; Scholljegerdes, Eric; Ivey, Shanna; Young, Wendy; Genualdi, Susan; DeJager, Lowri; Snyder, Abigail; Esteban, Emilio; Johnston, John J.
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      Kowalczyk, J.; Ehlers, S.; Fürst, P.; Schafft, H.; Lahrssen-Wiederholt, M. Transfer of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) from contaminated feed into milk and meat of sheep: pilot study. Arch. Environ. Contam. Toxicol. 2012, 63, 288– 298,  DOI: 10.1007/s00244-012-9759-2
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      Transfer of Perfluorooctanoic Acid (PFOA) and Perfluorooctane Sulfonate (PFOS) From Contaminated Feed Into Milk and Meat of Sheep: Pilot Study
      Kowalczyk, Janine; Ehlers, Susan; Fuerst, Peter; Schafft, Helmut; Lahrssen-Wiederholt, Monika
      Archives of Environmental Contamination and Toxicology (2012), 63 (2), 288-298CODEN: AECTCV; ISSN:0090-4341. (Springer)
      A pilot study was performed with dairy sheep to generate the first data on the transfer of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) from feed into food of animal origin. Corn silage was cultivated on cropland in Lower Saxony in Germany where, as a result of illegal waste disposal in 2006, farmland was contaminated with perfluorinated alkylacids (PFAAs). Two sheep were exposed by way of PFAA-contaminated corn silage to PFOS (1.16 and 1.45 μg/kg body wt. [bw]/d, resp.) and PFOA (0.43 and 0.53 μg/kg bw/d) during a period of 21 days. During the PFAA-feeding period, PFOS levels in plasma increased continuously to max. concn. of 103 and 240 μg/L for sheep 1 and sheep 2, resp. The PFOA plasma concn. remained low (sheep 1 = 3.3 ± 2.2 μg/L; sheep 2 = 15.6 ± 8.3 μg/L). Data indicate that urinary excretion is the primary clearance route for PFOA (sheep 1 = 51 %; sheep 2 = 55 %), whereas PFOS excretion by way of urine could not be quantified. The highest PFOS excretion (4 to 5 %) was detected in faeces. PFOS was also excreted at higher levels than PFOA by way of milk. During a period of 21 days, a total PFOS transfer into milk ≤2 % was calcd. Overall, total excretion of PFOS was significantly lower compared with that of PFOA (PFOS 6 %; PFOA 53 to 56 %). PFOS levels in sheep 1 and sheep 2 were highest in liver (885 and 1,172 μg/kg wt. wet [ww], resp.) and lowest in muscle tissue (24.4 and 35.1 μg/kg ww, resp.). PFOA levels in muscle tissue were low for sheep 2 (0.23 μg/kg ww) and not detectable after the PFAA-free feeding period in sheep 1. A slight background load of PFOS in liver (1.5 μg/kg ww) and kidney (0.3 μg/kg ww) was detected in sheep 3 (control).
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      Kowalczyk, Janine; Ehlers, Susan; Oberhausen, Anja; Tischer, Marion; Fuerst, Peter; Schafft, Helmut; Lahrssen-Wiederholt, Monika
      Journal of Agricultural and Food Chemistry (2013), 61 (12), 2903-2912CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      The transfer of the perfluoroalkyl acids (PFAAs) perfluorobutanesulfonate (PFBS), perfluorohexanesulfonate (PFHxS), perfluorooctanesulfonate (PFOS), and perfluorooctanoate (PFOA) from feed into tissue and milk of dairy cows was investigated. Holstein cows (n = 6) were fed a PFAA-contaminated feed for 28 days. After the PFAA-feeding period, three cows were slaughtered while the others were fed PFAA-free feed for another 21 days (depuration period). For PFAA anal. plasma, liver, kidney, and muscle tissue, urine, and milk were sampled and analyzed using high-performance liq. chromatog. (HPLC) with tandem mass spectrometry (MS/MS). The av. daily intake of dairy cows was 3.4±0.7, 4.6±1.0, 7.6±3.7 and 2.0±1.2 μg/kg body wt. (bw) for PFBS, PFHxS, PFOS, and PFOA, resp. Overall, PFBS, PFHxS, PFOS, and PFOA showed different kinetics in dairy cows. In plasma, concns. of PFBS (mean = 1.2±0.8 μg/L) and PFOA (mean = 8.5±5.7 μg/L) were low, whereas PFHxS and PFOS continuously increased during the PFAA-feeding period up to maximal concns. of 419±172 and 1903±525 μg/L, resp. PFOS in plasma remained constantly high during the depuration period. PFOS levels were highest in liver, followed by kidney, without significant differences between feeding periods. The highest PFHxS levels were detected in liver and kidney of cows slaughtered on day 29 (61±24 and 98±31 μg/kg wet wt. (ww)). The lowest PFAA levels were detected in muscle tissue. At the end of the feeding study, cumulative secretion in milk was detd. for PFOS (14±3.6%) and PFHxS (2.5±0.2%). The other two chems. were barely secreted into milk: PFBS (0.01±0.02%) and PFOA (0.1±0.06%). Overall, the kinetics of PFOA were similar to those of PFBS and substantially differed from those of PFHxS and PFOS. The very low concn. of PFBS in plasma and milk, the relatively high urinary excretion, and only traces of PFBS in liver (0.3±0.3 μg/kg ww) and kidney (1.0±0.3 μg/kg ww) support the conclusion that PFBS does not accumulate in the body of dairy cows.
    8. 8
      Zafeiraki, E.; Vassiliadou, I.; Costopoulou, D.; Leondiadis, L.; Schafft, H. A.; Hoogenboom, R. L. A. P.; van Leeuwen, S. P. J. Perfluoroalkylated substances in edible livers of farm animals, including depuration behaviour in young sheep fed with contaminated grass. Chemosphere 2016, 156, 280– 285,  DOI: 10.1016/j.chemosphere.2016.05.003
      8
      Perfluoroalkylated substances in edible livers of farm animals, including depuration behaviour in young sheep fed with contaminated grass
      Zafeiraki, Effrosyni; Vassiliadou, Irene; Costopoulou, Danae; Leondiadis, Leondios; Schafft, Helmut A.; Hoogenboom, Ron L. A. P.; van Leeuwen, Stefan P. J.
      Chemosphere (2016), 156 (), 280-285CODEN: CMSHAF; ISSN:0045-6535. (Elsevier Ltd.)
      Perfluoroalkylated substances (PFASs) present a potential health risk for consumers. In animals these compds. are known to accumulate in livers. In order to det. potential PFASs contamination in com. available livers, samples from farmed sheep, horses, cows, pigs and chicken were collected from the Dutch market. PFOS was the only detectable PFAS and its concn. was higher in free ranging animals like cows and sheep. The detected levels of PFOS in the liver samples were very low (up to 4.5 ng g-1 ww). To further study the kinetic behavior in foraging animals, samples from a study in which sheep were fed with grass obtained from a river floodplain, were examd. PFOS was the only detectable PFAS in the contaminated grass pellets, showing a level of about 0.5 μg kg-1. Young blackhead sheep were fed with either clean or contaminated grass for a period up to 112 days. A time-dependent increase in liver PFOS concns. was obsd. from 2.4 to 10.9 ng g-1 ww after 8 and 112 days resp. A time-dependent depuration was obsd. in livers of animals switched to clean grass after 56 days of exposure, from 9.2 to 4.7 ng g-1 ww after 64 and 112 days resp. The percentage of PFOS ingested from the grass and retained in the liver was estd. to be 12% at day 56, and decreased gradually to 6% after 56 days on clean grass, showing that the decrease in levels is not only caused by an increase in liver wt. Levels detected in com. livers but also those in the sheep study would not lead to exceedance of the current TDI for PFOS set by EFSA. Therefore, it can be assumed that they do not present a risk for human health.
    9. 9
      Lupton, S. J.; Dearfield, K. L.; Johnston, J. J.; Wagner, S.; Huwe, J. K. Perfluorooctane sulfonate plasma half-life determination and long-term tissue distribution in beef cattle (Bos taurus). J. Agric. Food Chem. 2015, 63 (51), 10988– 10994,  DOI: 10.1021/acs.jafc.5b04565
      9
      Perfluorooctane Sulfonate Plasma Half-Life Determination and Long-Term Tissue Distribution in Beef Cattle (Bos taurus)
      Lupton, Sara J.; Dearfield, Kerry L.; Johnston, John J.; Wagner, Sarah; Huwe, Janice K.
      Journal of Agricultural and Food Chemistry (2015), 63 (51), 10988-10994CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      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 det. plasma and tissue depletion kinetics in cattle, 2 steers and 4 heifers were dosed with PFOS at 0.098 mg/kg body wt. and 9.1 mg/kg, resp. Plasma depletion half-lives for steers and heifers were 120 ± 4.1 and 106 ± 23.1 days, resp. Specific tissue depletion half-lives ranged from 36 to 385 days for i.p. 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.
    10. 10
      Lupton, S. J.; Huwe, J. K.; Smith, D. J.; Dearfield, K. L.; Johnston, J. J. Absorption and excretion of 14C-perfluorooctanoic acid (PFOA) in Angus cattle (Bos taurus). J. Agric. Food Chem. 2012, 60 (4), 1128– 1134,  DOI: 10.1021/jf2042505
      10
      Absorption and Excretion of 14C-Perfluorooctanoic Acid (PFOA) in Angus Cattle (Bos taurus)
      Lupton, Sara J.; Huwe, Janice K.; Smith, David J.; Dearfield, Kerry L.; Johnston, John J.
      Journal of Agricultural and Food Chemistry (2012), 60 (4), 1128-1134CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      Perfluoroalkyl substances (PFASs), such as perfluorooctanoic acid (PFOA), are environmentally persistent industrial chems. often found in biosolids. Application of these biosolids to pastures raises concern about the accumulation of PFOA in the edible tissues of food animals. Because data on the absorption, distribution, metab., and excretion (ADME) of PFOA in cattle were unavailable, a study was conducted to det. pharmacokinetic parameters following a single oral exposure (1 mg/kg body wt. of 14C-PFOA) in four Lowline Angus steers. Radiocarbon was quantified in blood, urine, and feces for 28 days and in tissues at the time of slaughter (28 days) by liq. scintillation counting (LSC) or by combustion anal. with LSC with confirmation by liq. chromatog.-tandem mass spectrometry (LC-MS/MS). 14C-PFOA was completely absorbed and excreted (100.7 ± 3.3% recovery) in the urine within 9 days of dosing. The plasma elimination half-life was 19.2 ± 3.3 h. No 14C-PFOA-derived radioactivity was detected in edible tissues. Although PFOA was rapidly absorbed, it was also rapidly excreted by steers and did not persist in edible tissues, suggesting meat from cattle exposed to an acute dose of PFOA is unlikely to be a major source of exposure to humans.
    11. 11
      Lupton, S. J.; Huwe, J. K.; Smith, D. J.; Dearfield, K. L.; Johnston, J. J. Distribution and excretion of perfluorooctane sulfonate (PFOS) in beef cattle (Bos taurus). J. Agric. Food Chem. 2014, 62 (5), 1167– 1173,  DOI: 10.1021/jf404355b
      11
      Distribution and excretion of perfluorooctane sulfonate (PFOS) in beef cattle (Bos taurus)
      Lupton, Sara J.; Huwe, Janice K.; Smith, David J.; Dearfield, Kerry L.; Johnston, John J.
      Journal of Agricultural and Food Chemistry (2014), 62 (5), 1167-1173CODEN: JAFCAU; ISSN:0021-8561. (American Chemical Society)
      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 det. these parameters for PFOS in three Lowline Angus steers given a single oral dose of PFOS at approx. 8 mg/kg body wt. PFOS concns. were detd. by liq. chromatog.-tandem mass spectrometry in multiple tissue compartments. The major route of excretion was in the feces (11 ± 1.3% of the dose, mean ± std. deviation) with minimal PFOS elimination in urine (0.5 ± 0.07% of the dose). At day 28 the mean plasma concn. remained elevated at 52.6 ± 3.4 μg/mL, and it was estd. that 35.8 ± 4.3% of the dose was present in the plasma. Plasma half-lives could not be calcd. 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.
    12. 12
      Vestergren, R.; Orata, F.; Berger, U.; Cousins, I. T. Bioaccumulation of perfluoroalkyl acids in dairy cows in a naturally contaminated environment. Environ. Sci. Pollut. Res. 2013, 20, 7959– 7969,  DOI: 10.1007/s11356-013-1722-x
      12
      Bioaccumulation of perfluoroalkyl acids in dairy cows in a naturally contaminated environment
      Vestergren, Robin; Orata, Francis; Berger, Urs; Cousins, Ian T.
      Environmental Science and Pollution Research (2013), 20 (11), 7959-7969CODEN: ESPLEC; ISSN:0944-1344. (Springer)
      Beef and dairy products may be important vectors of human exposure to perfluoroalkyl acids (PFAAs), but the understanding of how PFAAs are accumulated and transferred through agricultural food chains is very limited. Here, the bioaccumulation of PFAAs in dairy cows receiving naturally contaminated feed and drinking water was investigated by conducting a mass balance of PFAAs for a herd of dairy cows in a barn on a typical Swedish dairy farm. It was assumed that the cows were able to reach steady state with their dietary intake of PFAAs. Perfluorooctane sulfonic acid (PFOS) and perfluoroalkyl carboxylic acids (PFCAs) with 8 to 12 carbons were detected in cow tissue samples (liver, muscle, and blood) at concns. up to 130 ng kg-1. Mass balance calcns. demonstrated an agreement between total intake and excretion within a factor of 1.5 and consumption of silage was identified as the dominant intake pathway for all PFAAs. Biomagnification factors (BMFs) were highly tissue and homolog specific. While BMFs of PFOS and PFCAs with 9 and 10 fluorinated carbons in liver ranged from 10 to 20, perfluorooctanoic acid (PFOA) was not biomagnified (BMF<1) in any of the investigated tissues. Biotransfer factors (BTFs; defined as the concn. in tissue divided by the total daily intake) were calcd. for muscle and milk. Log BTFs ranged from -1.95 to -1.15 day kg-1 with the highest BTF obsd. for PFOS in muscle. Overall, the results of this study suggest that long-chain PFAAs have a relatively high potential for transfer to milk and beef from the diet of dairy cows. However, a low input of PFAAs to terrestrial systems via atm. deposition and low bioavailability of PFAAs in soil limits the amt. of PFAAs that enter terrestrial agricultural food chains in background contaminated environments and makes this pathway less important than aquatic exposure pathways. The BTFs estd. here provide a useful tool for predicting human exposure to PFAAs via milk and beef under different contamination scenarios.
    13. 13
      Wilson, T. B.; Stevenson, G.; Crough, R.; de Araujo, J.; Fernando, N.; Anwar, A.; Scott, T.; Quinteros, J. A.; Scott, P. C.; Archer, M. J. G. Evaluation of Residues in Hen Eggs After Exposure of Laying Hens to Water Containing Per-and Polyfluoroalkyl Substances. Environ. Toxicol. Chem. 2021, 40 (3), 735– 743,  DOI: 10.1002/etc.4723
      13
      Evaluation of Residues in Hen Eggs After Exposure of Laying Hens to Water Containing Per- and Polyfluoroalkyl Substances
      Wilson, Timothy B.; Stevenson, Gavin; Crough, Robert; de Araujo, Jesuina; Fernando, Nilhan; Anwar, Arif; Scott, Tyrone; Quinteros, Jose A.; Scott, Peter C.; Archer, Michael J. G.
      Environmental Toxicology and Chemistry (2021), 40 (3), 735-743CODEN: ETOCDK; ISSN:0730-7268. (Wiley-Blackwell)
      Per- and polyfluoroalkyl substances (PFAS) have been used in aq. film-forming foams used in firefighting, resulting in soil and groundwater contamination and leading to human exposure via animal products grown in contaminated areas. The present study reports the relationship between PFAS intake by hens and the PFAS concns. in the edible parts of eggs. Laying hens were exposed via drinking water to different concns. of 4 PFAS compds. (perfluorooctane sulfonate [PFOS], perfluorohexane sulfonate [PFHxS], perfluorooctanoic acid [PFOA], and perfluorohexanoic acid) over 61 d. Egg PFAS residues were assessed for a further 30 d after exposure ceased. The target concns. of PFAS were 0, 0.3, 3, 30, and 300μg/L for the treatment groups T1-T5, resp.; and PFAS residues were detd. from the eggs collected every second day. There was a linear correlation between the PFAS concns. in the drinking water of hens and those detected in the egg, which could be useful in estg. PFAS concns. in the egg by measuring water concns. Exposure of hens to drinking water with PFAS concns. below the Australian Government Department of Health limits (PFOS and PFHxS, 0.07μg/L; PFOA, 0.56μg/L), and with no other sources of PFAS exposure, is unlikely to result in egg PFAS concns. that would exceed the 10% limit set by Food Stds. Australia New Zealand for human consumption.
    14. 14
      Drew, R.; Hagen, T. G.; Champness, D. Accumulation of PFAS by livestock–determination of transfer factors from water to serum for cattle and sheep in Australia. Food Addit. Contam.: Part A 2021, 38 (11), 1897– 1913,  DOI: 10.1080/19440049.2021.1942562
      14
      Accumulation of PFAS by livestock - determination of transfer factors from water to serum for cattle and sheep in Australia
      Drew, Roger; Hagen, Tarah G.; Champness, David
      Food Additives & Contaminants, Part A (2021), 38 (11), 1897-1913CODEN: FACPAA; ISSN:1944-0057. (Taylor & Francis Ltd.)
      In this study accumulation has been detd. of several per- and polyfluoroalkyl substances (PFAS) from ingested water to steady state serum concn. for adult beef cattle and sheep raised on a hobby farm impacted by PFAS contamination. PFAS concns. in stock water were stable for more than a year, they were non-measurable in grass but present at very low levels in soil which equated to just 1% of the intake from water. Prior to quantifying PFAS in cattle serum there had been no breeding for 18 mo. Although there were high concns. of several PFAS in the water, only perfluorooctane sulfonate (PFOS) and perfluorohexane sulfonate (PFHxS) were in cattle serum in appreciable amts.; perfluoroheptane sulfonate (PFHpS), perfluorononanoic acid (PFNA) and perfluorodecanoic acid (PFDA) were much lower. Transfer factors (TFs) for cattle were calcd. by dividing steady state serum concn. (ng PFAS/mL) by water concn. (μg PFAS/L). Av. and upper est. TF values for cattle were calcd.; the former were 140 (total PFOS, i.e. tPFOS), 130 (PFHpS), 65 (PFHxS), 170 (PFNA), and 120 (PFDA). Previous investigation campaigns at the farm provided relative steady state serum PFAS concns. for sheep and cattle that allowed adjustment of the cattle TFs. The resulting av. est. TFs for ewes (non-pregnant and not lactating) were 20 (tPFOS) and 30 (PFHxS), other PFAS were not measurable in sheep serum. Discussion on using these TFs in human health risk assessments is provided. With certain assumptions/caveats the TFs allow estns. of PFAS steady state serum concns. for use in preliminary human health risk assessments (HHRAs) when only PFAS in stock water is known.
    15. 15
      Drew, R.; Hagen, T. G.; Champness, D.; Sellier, A. Half-lives of several polyfluoroalkyl substances (PFAS) in cattle serum and tissues. Food Addit. Contam.: Part A 2022, 39 (2), 320– 340,  DOI: 10.1080/19440049.2021.1991004
      15
      Half-lives of several polyfluoroalkyl substances (PFAS) in cattle serum and tissues
      Drew, Roger; Hagen, Tarah G.; Champness, David; Sellier, Amelie
      Food Additives & Contaminants, Part A (2022), 39 (2), 320-340CODEN: FACPAA; ISSN:1944-0057. (Taylor & Francis Ltd.)
      Cattle that were at steady-state serum polyfluoroalkyl substances (PFAS) concns. due to several years of exposure to water contaminated by residues of Aq. Film-Forming (AFFF) firefighting foam had perfluorooctane sulfonate (PFOS) isomers, perfluoroheptane sulfonate (PFHpS), perfluorohexane sulfonate (PFHxS), perfluorononanoic acid (PFNA) and perfluorodecanoic acid (PFDA) in serum. Elimination serum half-lives were detd. in five heifers from serial blood sampling over 215 days. Eleven addnl. animals that had blood sampled on day 19 (d19) were euthanised on d63. PFAS half-life ests. from the serial blood sampling and from d19/d63 data were not significantly different. The combined (n = 16) serum half-lives (in days) were: total PFOS (tPFOS, 74.1 ± 13.4), PFHpS (45.7 ± 9.4), PFHxS (9.3 ± 1.3), PFNA (12.3 ± 3.2) and PFDA (60.4 ± 10.4). The half-lives of linear PFOS (L-PFOS, 69.4 ± 11.6) and mono branched PFOS isomers (m-PFOS, 83.6 ± 19) were not significantly different than tPFOS, but for the di-branched isomers (di-PFOS), the serum half-life was significantly lower (29.9 ± 5.8). Animal age (1.4-12.3 years old) and serum concn. at the start of depuration did not influence half-lives, and there was no difference between steers and heifers. Consideration of serum and tissue PFAS concns. at d63 and d215 indicated there was no difference in tPFOS depuration from serum or muscle, but elimination from liver and kidney may be slightly longer. Depuration of PFHpS is essentially the same in serum, kidney and liver, and it is expected depletion from muscle would be comparable. The short half-life of di-PFOS, PFHxS and PFNA did not allow an assessment of clearance from tissues because they were not measurable at d215 but based on the results for PFOS and PFHpS, elimination of PFHxS from tissues is expected to mirror that from serum. Human health risk assessment implications are discussed.
    16. 16
      Lupton, S. J.; Casey, F.; Smith, D. J.; Hakk, H. Perfluorooctanoic Acid Transport in Soil and Absorption and Distribution in Alfalfa (Medicago sativa). J. Food Prot. 2022, 85 (1), 164– 172,  DOI: 10.4315/JFP-21-276
      16
      Perfluorooctanoic acid transport in soil and absorption and distribution in Alfalfa (Medicago sativa)
      Lupton, Sara J.; Casey, Francis; Smith, David J.; Hakk, Heldur
      Journal of Food Protection (2022), 85 (1), 164-172CODEN: JFPRDR; ISSN:0362-028X. (International Association for Food Protection)
      Perfluorooctanoic acid (PFOA) is used as a surfactant in consumer and industrial products and is frequently found in biosolids from wastewater treatment plants. When present in biosolids applied to croplands, PFOA can contaminate feed and fodder used by livestock, but the extent of PFOA transfer from soil to plants is not well characterized. A single dose of radiocarbon (14C)-tagged PFOA was applied to unplanted soil or soil contg. growing alfalfa. PFOA transport through unplanted soil and uptake by alfalfa was monitored over a 10-wk study period. Radiocarbon was initially measured in roots, stems, and leaves 7 days after [14C]-PFOA application to soil. PFOA accumulation was greatest in leaves during the 10-wk sampling. By week 10, PFOA migration through unplanted soil had reached a depth of 22.8 ± 2.5 cm. In contrast, PFOA migrated to 7.5 ± 2.5 cm in soil contg. alfalfa plants. The greatest predictor of PFOA concn. in alfalfa leaves was PFOA concn. in the top 5 cm of soil; PFOA concns. at lower depths were not correlated with alfalfa PFOA concns. PFOA transport through soil may be slowed by the presence of forage; however, PFOA accumulation in edible portions of forage plants may increase food animal exposure to PFOA residues.
    17. 17
      Harris, D. C. Quantitative Chemical Analysis, 8th ed.; W. H. Freeman and Co: New York, NY, 2010.
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      Greene, W. H. Econometric Analysis, 4th ed.; Prentice Hall: NJ, 2000; pp 201– 215.
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      Showell, B. A.; Williams, J. R.; Duvall, M.; Howe, J. C.; Patterson, K. Y.; Roseland, J. M.; Holden, J. M. USDA Table of Cooking Yields for Meat and Poultry United States Department of Agriculture: Baltimore, MD, USA, 2012.
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      USEPA. Assigning Values to Nondetected/Nonquantified Pesticide Residues in Human Health Food Exposure Assessments, United States Department of the Interior, Environmental Protection Agency; Office of Pesticide Programs: Washington, DC, 2000.
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      Akaike, H. Fitting Autoregreesive Models for Prediction. In Selected Papers of Hirotugu Akaike; Springer, 1969; pp 131– 135.
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      Schwarz, G. Estimating the dimension of a model. Ann. Stat. 1978, 6 (2), 461– 464,  DOI: 10.1214/aos/1176344136
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      Evans, N.; Hastings, M.; Peacock, P. Statistical Distributions, 2nd ed.; John Wiley & Sons: New York, NY.
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      ATSDR. Toxicological Profile for Perfluoroalkyls; Centers for Disease Control and Prevention, Agency for Toxic Substances and Disease Registry: Atlanta, GA, 2021.
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      USEPA. Interim Drinking Water Health Advisory: Perfluorooctane Sulfonic Acid (PFOS) Environmental Protection Agency; Office of Water Health and Ecological Criteria Division: Washington, D.C., 2022.
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      USEPA. Transmittal of the Science Advisory Board Report titled, “Review of EPA’s Analyses to Support EPA’s National Primary Drinking Water Rulemaking for PFAS; Environmental Protection Agency: Washington, D.C., 2022.
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  • Supporting Information

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    • Time-course data used in the study; on-farm PFOS plasma concentrations; paired PFOS muscle-plasma concentrations; PFOS plasma depletion data; precursor and product ions, cone voltages, and collision energies used for the mass spectrometric quantification of PFOS isomers and internal standards; paired observations used to estimate on-farm PFOS plasma concentrations (PDF)


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