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Dynamic Transgenerational Fate of Polychlorinated Biphenyls and Dioxins/Furans in Lactating Cows and Their Offspring Christian Bogdal,*,† Selina Züst,† Peter Schmid,‡ Tenzing Gyalpo,†,§ Anicia Zeberli,† Konrad Hungerbühler,† and Markus Zennegg‡ †

Institute for Chemical and Bioengineering, ETH Zurich, Vladimir-Prelog-Weg 1, CH-8093 Zürich, Switzerland Empa, Swiss Federal Laboratories for Materials Science and Technology, Ü berlandstrasse 129, CH-8600 Dübendorf, Switzerland

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S Supporting Information *

ABSTRACT: We report on two farms in Switzerland heavily contaminated by polychlorinated biphenyls (PCBs) and dioxins (PCDD/Fs), occurring in the first case from diffuse sources and in the second case from PCB-containing wall paint. Extensive measurements of PCBs and PCDD/Fs on site (soil, forage, and paint) and in cattle (blood, fat, and milk) allowed validation of our novel dynamic toxicokinetic model, which includes the transfer of contaminants from the mother cows to their suckling calf and the uptake of soil by grazing cattle. We show that for calves, the mother milk is the main uptake route of contaminants. For both cows and calves, ingestion of contaminated soil, although often overlooked, is an appreciable uptake path. The remediation of the contaminated stable lead to a 2−3 fold reduction of the PCB levels in animals within one year. The transfer of animals to an uncontaminated mountain site during summer proved to be an effective decontamination procedure with up to 50% reduction of the levels within three months. Our study calls for a rapid removal of PCB-containing materials in animal husbandry farms and shows that the diffuse contamination of soils will remain a source for PCBs and PCDD/Fs in our food chain for decades to come.

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INTRODUCTION Polychlorinated biphenyls (PCBs) and polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) belong to a group of substances classified as persistent organic pollutants (POPs). POPs are anthropogenic compounds that are highly resistant to environmental degradation and accumulate in biota and humans.1 PCBs have been widely used in the 1950−1980s as dielectrics in capacitors and transformers and as plasticizers in paints and joint sealants.2,3 Some PCBs have long-term toxic effects equivalent to those of PCDD/Fs and are, therefore, called “dioxin-like PCBs” (dl-PCBs).1 PCBs have mainly been used in industrialized countries,3 which have still high levels of PCBs in biota and humans. In a worldwide comparison, the contamination by PCBs of human breast milk in European countries is at the upper end.4 Depending on the population group, between 7% and 53% of the population in the European Union has chronic exposure higher than the tolerable daily intake recommended by the World Health Organization (2 pg TEQWHO05/kg body weight per week) due to the consumption of lipid-rich food contaminated by dl-PCBs and PCDD/Fs, mainly fish, meet, and dairy products.5 Also in Switzerland, levels of dl-PCBs above the regulatory thresholds for food consumption are frequently found in meat and dairy products, especially from animals from extensive farming.6 This is not only a public © XXXX American Chemical Society

health problem but predominantly leads to a noticeable depreciation of the products and an important stress factor for concerned farmers. In cases of excessive dl-PCB or PCDD/F contamination of agricultural products, the responsible authorities issue the complete discontinuation of production, together with the slaughtering of all of the livestock and the destruction of the products, at the cost of the farmers. In Switzerland, the Federal Food Safety and Veterinary Office (FSVO) regularly examines levels of dl-PCBs and PCDD/Fs in different foodstuffs. In 2003, 2006, and 2008, three monitoring programs revealed that cattle meat (especially veal) from extensive farming (i.e., suckler cow husbandry) occasionally exceeded the maximum levels allowed in the European Union and in Switzerland for food consumption (for meat and meat products 2.5 and 4.0 pg TEQWHO05/glipid for PCDD/Fs and dl-PCBs + PCDD/Fs, respectively; for raw milk and dairy products 2.5 and 5.5 pg TEQWHO05/glipid for PCDD/ Fs and dl-PCBs + PCDD/Fs, respectively).7,8 In these cases, dlPCBs dominated by far the total contamination (83−97% of total TEQWHO05), compared to PCDD/Fs.6 During the last of Received: June 9, 2017 Revised: August 14, 2017 Accepted: August 22, 2017

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DOI: 10.1021/acs.est.7b02968 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology

Figure 1. Model setup consisting of the combination of two physiologically based toxicokokinetic (PBTK) models for a mother cow and its suckling calf. Chemical intake into the animals occurs via forage, concentrate (only cow), soil, or milk (only calf), which results in a reduced chemical uptake based on the absorption efficiencies. Each PBTK model consists of the compartments liver, fat, richly perfused tissue, slowly perfused tissue, blood, and udder (only cow), which are connected by the blood flow. Chemicals are transported between compartments via the blood and partition between the blood and the other compartments depending on their equilibrium partitioning coefficients.

these monitoring studies, two farms stood out because of their particularly elevated levels of dl-PCBs in cattle. While for the first farm, in the following referenced as “case LU”, diffuse sources are assumed to be the cause for elevated contaminant levels, in the second “case GR”, investigations revealed the wall paint in the stable to be responsible for the high animal contamination and resulted in the emergency slaughter of the contaminated cows and calves. Thus, there is a need for a tool to identify and understand the elevated contaminant levels in cattle before slaughtering, in order to prevent unnecessary sacrifice of animals and avoid the presence of highly contaminated foodstuff on the market. The goals of this study were (i) the identification and confirmation of the contaminant sources in these two specific cases, LU and GR, and (ii) the contribution to a better understanding of the unintentional sources and the fate of PCBs and PCDD/F in cattle. Here, we report on our extensive field measurements performed during the last three years in these two farms. Furthermore, we developed a dynamic physiologically based toxicokinetic (PBTK) model for PCBs and PCDD/Fs in mother cows and their suckling calves. The combination of the experimental field study and the modeling provides a particularly powerful approach to address the important issue of the contamination of the food chain by PCBs and PCDD/Fs. Whereas the uptake, accumulation, and excretion of PCBs and PCDD/Fs has been studied experimentally by numerous authors, (e.g., refs 9−29), quantitative modeling studies are considerably less common. Additionally, the existing modeling studies (e.g., refs 30−39) targeted mainly PCDD/Fs, focusing on lactating cows, including mostly feed as the sole source of contaminants, and considering adult cows at steady-state. Here, we present two coupled PBTK models for a mother cow and its suckling calf. Our dynamic model setup includes the complex physiology changes of the growing calf and the mother cow

undergoing annual pregnancy−calving−lactation cycles. The model was parametrized for dl-PCBs and PCDD/Fs and includes the uptake of soil by grazing animals as a contamination source. Our model is validated with the two special contamination cases LU and GR and is applicable to a wide range of situations in the future.

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MATERIALS AND METHODS Field Sampling. Triggered by the detection of the elevated PCB levels in cattle from the two farms mentioned above, further investigations at these sites were carried out. The farm LU is located in the Canton of Lucerne, has a grassland area of approximately 20 ha and has about 20 mother cows and 20 calves, which are driven to higher altitudes during the summer months for alpine pasture estivation. The farm GR is located in the Canton of Grisons, has approximately 25 ha grassland with 30 mother cows and about 30 calves and practices alpine pasture estivation. At both sites, field sampling of feed, including concentrate and forage (dry herbage and silage), soil, and wall paint (only case GR) was performed. Animal sampling included cow blood and milk (only GR) and calf blood and meat fat. Further information about the study sites and the sampling are provided in the Supporting Information (SI, section 1.1) and Figures 2 and 4. Sample Preparation and Analysis. The analytical method followed the procedure previously reported40 and is described in detail in the SI (sections 1.2. and 1.3.). Sample extraction was based on Soxhlet for solid samples (feed, soil, meat, and paint) and liquid−liquid extraction for liquid samples (milk and blood). Sample extracts were spiked with 13C-labeled internal standards and purified based on silica, alumina, and carbon column chromatography cleanup. For the detection of the target compounds, gas chromatography/high resolution mass spectrometry was applied. The quantification was based on the isotope dilution method. B


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Figure 2. Measured concentrations of dl-PCBs (circles) and PCDD/Fs (triangles) in the different sample types of the case LU, including (a) feed concentrate, (b) forage (dry herbage and silage), (c) soil, (d) cow blood, (e) calf fat (in animals at age of 5 and 10 months), and (f) calf blood (in animals at age of 5 and 10 months). For each group of samples, the mean of the individual measurements is included in the plots (black stroke).

Quality Assurance and Control. Method blank levels were determined by subjecting all the chemicals, materials, and glassware used for the quantitative determination of the analytes to the entire analytical procedure. The glassware was cleaned with alkaline detergents, rinsed with deionized water, backed out overnight at 450 °C, and rinsed directly before use with solvent (SI, section 1.4). Physiologically Based Toxicokinetic Model. The model framework consists of two PBTK models for a mother cow and a calf, connected by the transfer of milk from the mother cow to its suckling calf (Figure 1). The model setup is based on the model for a lactating cow presented by Derks and coworkers30,31 with some important modifications and extensions. Here, first a mother cow is modeled by considering six compartments representing the main tissues and organs, including the liver, adipose tissue, richly perfused tissue (accounting mainly for the gastrointestinal tract and kidneys), slowly perfused tissue (comprising muscles, skin, and bones), the blood, and the udder, where the milk production takes place. Second, a calf is modeled including the same compartments, excluding the udder. The mother cow is modeled from birth to the adult stage (so-called heifer) achieved after 48 months. At the age of 24 months, the cow gives birth to a first calf, followed by annual lactation−pregnancy−calving cycles. For calves born annually, a growth period from the birth to the age of 15 months is modeled. Input of chemicals into the animals occurs via oral intake corrected by the absorption efficiency to calculate the uptake of chemicals into the body (absorbed fraction). The absorbed fraction is modeled as direct deposition of chemicals in the liver, assuming absorption to be

very fast compared to distribution and elimination of the chemicals in the body. Chemicals entering the liver are distributed through the animals’ body via the blood flow, accompanied by the equilibrium partitioning of chemicals between the blood and the different compartments. Elimination of chemicals from the animals’ body occurs through metabolism and milk transfer (only in the mother cow). Feces and urine excretion is represented by the nonabsorbed fraction of chemicals. In the model, the animal system is divided into the internally well-mixed compartments. A mass balance equation of the chemical is set up for each compartment and the fluxes of the chemical between the compartments are described by firstorder differential equations, as described in the SI (section 2.8). The system of differential equations is solved numerically for every compartment using MATLAB R2015. Dynamic Animal-Specific Model Parameters and Chemical Input. To account for the physiological and behavioral changes occurring in the growth periods and in the lactation−pregnancy−calving cycles, animal-specific model parameters are time-dependent, including the volumes of the cow’s and calf’s compartments, the lipid content of the compartments, the blood flow between compartments, and the milk production of the mother cow. Cows take up chemicals via the consumption of forage and feed concentrate, as well as the ingestion of soil while grazing on pastures. Calves take up chemicals via the consumption of mother milk and forage, and via soil ingestion. In the case GR, an additional ingestion of paint particles contaminated with PCBs is considered. The amount and proportion of the C


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Figure 3. Concentrations of dl-PCBs in the case LU in (a) mother cow blood, (b) mother cow milk, (c) suckling calf blood, and (d) calf fat. The curves and the shaded areas represent the model results (median) and the model uncertainty range (95% confidence interval), respectively. The circles represent the measurements.

The model was run for each of the i-PCB, dl-PCB, and PCDD/ F congeners individually and the sum of the dl-PCBs and the PCDD/F congeners was calculated as toxicity equivalency (TEQ) based on the WHO toxicity equivalency factors (TEF) of 2005.42 The main focus of this study lies in the dl-PCBs, as they represented the main contamination problem in both cases compared to the PCDD/Fs. The results of the measurements and the modeling of the indicator PCBs are provided in the SI (Tables S1−S13 and Figures S1−S2, section 1.5) but not further discussed here.

different food items consumed by the animals are modeled dynamically over the course of their stage of life (SI sections 2.2 and 2.3). The concentrations of dl-PCBs and PCDD/Fs in the forage, feed concentrate, soil, and in the wall paint (only in the case GR) considered in the model as a chemical input into the animals, is derived from the measurements, taking the average of the measurements as the contamination level of feed, soil, and paint. Chemical-Specific Properties. Chemical-specific properties include the partition coefficients between blood and the different compartments of the animals, the absorption efficiencies translating the intake of chemicals into the uptake fraction transferred to the liver, and the metabolic rate constants (i.e., degradation half-lives). An extensive literature review was performed to determine the chemical properties, which are provided in the SI (section 2.4). Sensitivity and Uncertainty Analysis. A sensitivity analysis was performed to identify the input parameters that most significantly affect the model outputs. Furthermore, the uncertainty of the model input parameters was considered to derive the uncertainty of the model output (uncertainty analysis). The sensitivity and uncertainty analysis was performed on the basis of the error propagation method presented by MacLeod et al.,41 where log-normal distributions of independent input variables are assumed. Further explanations about this method and the confidence factors of the input parameters are reported in the SI (section 2.9). Target Compound Classes. The target compounds in the measurements included the six marker PCB congeners 28, 52, 101, 138, 153, and 180 (so-called indicator PCBs), the 12 dlPCB congeners 77, 81, 105, 114, 118, 123, 126, 156, 157, 167, 169, and 189, and the 17 2,3,7,8-chlorosubstituted PCDD/Fs.

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RESULTS Case LU−Measurements. Measured concentrations of dlPCBs and PCDD/Fs in the cattle samples from the case LU and their environment are summarized in Figure 2. The concentrations of the individual congeners are provided in the SI (Tables S1−S13, section 1.5). Among the animal feed, the lowest concentrations of dlPCBs were measured in concentrate (mean 0.010, min−max 0.06−0.016 pg TEQWHO05/gdw (dry weight), n = 3; Figure 2a). In the forage samples, the concentrations were lower in dry herbage (mean 0.13 pg TEQWHO05/gdw n = 7) than in silage (mean 0.27 pg TEQWHO05/gdw n = 3; Figure 2b). In soil, the concentrations of dl-PCBs were in a narrow range (mean 1.0, min−max 0.7−1.5 pg TEQWHO05/gdw, n = 12), whereas the concentrations of PCDD/Fs were higher (mean 4.1, min−max 2.0−5.3 pg TEQWHO05/gdw, n = 3) and showed higher variability (Figure 2c). In a 5 month old calf, the measured concentrations of dl-PCBs in fat (3.0, 2.2−3.1 pg TEQWHO05/ glipid, n = 3) and in blood (mean: 3.6, min−max 2.0−5.7 pg TEQWHO05/glipid, n = 3) were higher than in animals with age of 10 months (blood 1.6, 0.79−3.9, n = 8; fat 2.1, 0.92−6.3 pg TEQWHO05/glipid, n = 7) (Figure 2e and f). In cow blood, the D


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Figure 4. Measured concentrations of dl-PCBs (circles) and PCDD/Fs (triangles) in the different sample types of the case GR, including (a) wall paint, (b) forage (dry herbage and silage), (c) soil, (d) cow blood (after remediation of the stable), (e) cow milk (before and after remediation), (f) calf blood (after remediation), and (g) calf fat (before and after remediation). For each group of samples, the mean of the individual measurements is included in the plots (black stroke).

The uncertainty analysis provides confidence factors for the modeled concentrations of dl-PCBs and PCDD/Fs in blood of the mother cow of 2.0, meaning that the 95% confidence interval of the modeled concentrations spreads by this factor around the median (i.e., total uncertainty range of the model in Figure 3a covers a factor of 4.0). For the modeled concentrations of milk in the mother cow, the confidence factor is 1.6 (uncertainty range of the model in Figure 3b covers a factor of 2.6). In the suckling calf, the confidence factor is 2.7 for the modeled blood concentration (uncertainty range of the model in Figure 3c covers a factor of 7.0) and 2.4 for the modeled fat concentration (uncertainty range of the model in Figure 3d covers a factor of 5.5). Case GR−Measurements. Figure 4 presents the measurements performed in the case GR (for congener details see Tables S14−S27 in the SI). The paint of unknown origin applied on the stable wall in the 1960/70s contained concentrations of dl-PCBs in the two analyzed samples at a level of 157 000 and 54 000 pg TEQWHO05/g, respectively (Figure 4a). In forage samples, the concentrations of dl-PCBs (mean 0.13, min−max 0.12−0.19 pg TEQWHO05/gdw, n = 4) and PCDD/Fs (mean 0.14, min−max 0.12−0.15 pg TEQWHO05/gdw, n = 4) were very similar and in a narrow range, regardless of the type being dry herbage of silage (Figure 4b). The soil showed somewhat higher variations of dl-PCBs between sampling sites (mean 0.32, min−max 0.17−0.52 pg TEQWHO05/glipid, n = 6; Figure 4c). Before remediation of the stable, three out of six cow milk samples exceeded the EU limit for food consumption. The

concentrations of dl-PCBs are lower than in calf blood (1.3, 0.96−1.6 pg TEQWHO05/glipid, n = 6) (Figure 2d). Case LU−Model. The model was run for a mother cow (over 10 y, i.e. eight lactations) and its suckling calf (over 15 months). In the mother cow, the modeled concentrations of dlPCBs increase from birth until the first lactation with 2 y of age (i.e., 24 months in Figure 3a and b), followed by a regular cycling of the blood and milk concentrations decreasing during lactation (lasting 300 days) and increasing during the dry period (65 days). In cow, median modeled concentrations of dl-PCBs oscillate in blood between 4.3 and 6.3 and in milk between 1.6 and 2.3 pg TEQWHO05/glipid. Modeled concentrations of PCDD/Fs in cow follow the same temporal pattern and oscillate between 1.5 and 2.1 in blood and between 0.7 and 1.0 pg TEQWHO05/glipid in milk (Figure S11). In the suckling calf, the modeled body concentrations of dl-PCBs are increasing during the first three months to reach 8.8 pg TEQWHO05/glipid in blood and 3.4 pg TEQWHO05/glipid in meat fat, followed by a slow decrease as a result of the so-called growth dilution, meaning that the absolute mass of chemicals in the body continues to increase but the body weight increases faster leading to a decrease of the concentration. Compared to dl-PCBs, the modeled concentrations of PCDD/Fs in the calf are three times lower. Contrary to dl-PCBs, concentrations of PCDD/F in calf increase steadily and reach 2.0 pg TEQWHO05/ glipid in blood and 0.9 pg TEQWHO05/glipid in fat at 15 months. Thus, throughout the 15 months, the increase in the mass of PCDD/Fs in the body still outbalances the increase of the body mass of the calf. E


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Figure 5. Concentrations of dl-PCBs in the case GR in (a) mother cow blood, (b) mother cow milk, (c) suckling calf blood before the remediation of the stable, (d) calf fat before the remediation, (e) calf blood after remediation, and (f) calf fat after remediation. The curves and the shaded areas represent the model results (median) and the model uncertainty range (95% confidence interval), respectively. The circles represent the measurements.

lactations), followed by an abrupt end of the paint exposure at the beginning of the third lactation (to represent the remediation). In this scenario, from the second year on the cow gives birth to a calf that is also exposed to 30 mg/d wall paint (Figure 5). The model calculations revealed a decrease of dl-PCBs in the cow compartments one year after the remediation by a factor of more than 3 (Figure 5a and b). The comparison of the modeled concentrations in the calf born in the fourth year (i.e., before remediation, Figure 5c and d) to the calf born in the sixth year (i.e., after the mother lived one entire year in the remediated stable, Figure 5e and f), shows also a decrease by the same factor of 3.

contribution of dl-PCBs (mean 6.0, min−max 3.3−9.7 pg TEQWHO05/glipid, n = 6) to the contamination was considerably larger than the part of the PCDD/Fs (0.38, 0.27−0.49 pg TEQWHO05/glipid; Figure 4e). Before remediation, the concentrations of dl-PCBs in the analyzed calf fat (17, 12−22 pg TEQWHO05/glipid, n = 5) were even higher than in cow milk by a factor of 2.8 on average, whereas the concentrations of PCDD/Fs in calf fat (0.69, 0.58−0.85 pg TEQWHO05/glipid) were close to the levels in cow milk (Figure 4g). After the extensive remediation of the stable, the field measurements revealed a decrease in the concentrations of dl-PCBs in cow milk (2.4, 1.6−3.6 pg TEQWHO05/glipid, n = 6) by a factor of 2.5 on average (Figure 4e). In calf fat, the levels (5.3, 3.9−6.9 pg TEQWHO05/glipid, n = 6) dropped even by a factor of 3.2 on average (Figure 4g). Further measurements in blood samples after the remediation showed higher concentrations of dl-PCBs in calf blood (5.0, 2.2−6.4 pg TEQWHO05/glipid, n = 6; Figure 4f) than in cow blood (2.2, 1.1−3.2 pg TEQWHO05/glipid, n = 6; Figure 4d). Case GR−Model. To estimate the exposure to PCBcontaminated paint of the animals living in the stable, the model was run with increasing ingestion amounts of paint particles (10−60 mg/d). These simulations revealed the best agreement between modeled concentrations of cow milk and calf fat to the measurements with a daily intake of 30 mg wall paint (Figures S10 and S11). Consequently, the model was run for ten consecutive years, by exposing the mother cow daily to 30 mg wall paint from birth for up to four years (incl two

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DISCUSSION The combination of measurements and modeling is a very powerful tool, particularly in this study where measurements of input into the animals (feed, soil, and paint) are available from the same farm as the sampled animals. As discussed in the following sections, the two cases investigated here provide many relevant insights into the issue of uptake, transfer, and accumulation of PCBs and PCDD/Fs in cattle. Furthermore, the model allows deriving recommendations for farming practices leading to a potential mitigation of PCB contamination in cattle. Performance of the PBTK Model. In general, a close agreement is observed between the model calculations and the field measurements. Note that the model results in cow and in calf are independent from the measurements, i.e. no tuning of F


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Environmental Science & Technology the model parameters was performed to fit to the measurements. In the model, only the uptake of dl-PCBs and PCDD/Fs in cow is based on the own measurements (feed, soil, and paint). Comparing concentrations of dl-PCBs in blood of cows and calves, we observe that the model is generally higher than the measurements by a factor of 2−4, although, the 95% confidence interval of the model covers several individual measurements. Furthermore, the decreasing levels observed in the measurements between 5 and 10 months old calves in the case LU are also confirmed by the model (Figure 3c). Additionally, it has to be noted that for blood only very small sample amounts were available. This resulted in levels of dlPCBs that were close to the analytical detection limits. Therefore, the measurements of dl-PCBs in blood are affected by a high uncertainty. The measurements of dl-PCBs in milk or fat are much more robust and here, the median of the model deviates by less than 30% from the average of the measurements. This close agreement is observed for calf fat at 5 and 10 months in the case LU (Figure 3d), and for cow milk before and after the remediation of the stable in the case GR (Figure 4b). This agreement is a strong validation of the model performance, showing that the model captures satisfactorily the main input processes into the cow and the calf, as well as the physiological processes in cow and the transfer from the cow into the calf. The sensitivity and uncertainty analysis revealed the most important parameters in the model, showing where future efforts to improve the model could be invested. The parameters with the largest contribution to the uncertainty of the model results for the cow include the concentrations of pollutants in the forage, the absorption efficiency of the forage, and the milkfat-to-blood partitioning coefficient. The uncertainty of the concentrations modeled in the suckling calf is mainly attributed to the concentrations of pollutants in the cow milk and the absorption coefficient for cow milk. These parameters have concurrently a large uncertainty and are influential on the model results. The model is sensitive to further parameters, which, however, are relatively well-known, including the fat content of the cow milk or the milk production rate. The sensitivity and uncertainty analysis of the model is further discussed in the SI (section 3.4). Important Uptake Routes and On-Site Decontamination Scenarios in Cattle (Case LU). For the mother cow in the case LU, the uptake of dl-PCBs by the consumed forage is the most important uptake route and drives almost linearly the body concentrations of the cow. Increasing the concentrations of dl-PCBs in forage in a hypothetical model run by a factor of 2 results in an increase of the modeled concentrations in the cow by a factor of 1.9. Conversely, the uptake of dl-PCBs by concentrate is negligible for the contamination of the cow, due to the very low contamination level of concentrate and the small contribution to the diet of the cow. Therefore, to reduce contamination by dl-PCBs of cattle products on a farm, animals should be fed by forage with the lowest possible concentrations. Ideally, farmers would grow grass on their fields that are least contaminated by dl-PCBs. Otherwise, the supplement of forage with low contaminated concentrate could help to reduce the exposure of cows to dl-PCBs. The second most important uptake route for dl-PCBs in cattle is the unintentional ingestion of soil particles by grazing animals. This pathway is considerably less intuitive than uptake via forage and is, therefore, a very relevant outcome of the model. Particularly in the case of extensive or so-called near-

natural meat production, the long periods of grazing and the large surface areas covered by the animals, can result in a significant uptake of soil and with these also contaminants. In the standard model run, an uptake of 3% soil relative to the entire animal feed is considered (i.e., a cow consuming 10 kg of feed daily takes up additionally 0.3 kg of soil). While leaving the concentrations of dl-PCBs in soil as measured in the case LU, but increasing the amount of soil taken up from 3% to 10%, which is still in a realistic range,9 the concentrations in cattle increase by 30%. Thus, attempts for decreasing the contamination by dl-PCBs of cattle products on a farm should include grazing regimes minimizing the soil uptake. For instance, higher grass or a lower density of animals on the pasture may avoid that cattle to eat off the grass near to the ground and, thus, may lead to a reduced ingestion of soil. The suckling calf takes up dl-PCBs mainly by cow milk, especially in the first 5 months of its life when milk is by far the main nutriment. Increasing the concentrations of dl-PCBs in the cow milk by a factor of 2 in the model leads to higher concentrations in calf fat by a factor of 1.9 for a 5 months old calf consuming mainly cow milk and a factor of 1.7 for a 10 months old calf consuming less milk. Thus, the reduction of the levels of dl-PCBs in cow milk is crucial for a decrease of the contamination of calves. Furthermore, the growth dilution for dl-PCBs in the calf shows that one option to reduce contamination could be to raise the calves longer. At an age of 10 months (i.e., slaughtering age of beef), the concentrations in muscle tissue are 15% lower than at an age of 5 months (i.e., slaughtering age of veal). Decontamination by Alpine Pasture Estivation (Case LU). The transfer of cattle to mountain pastures during summer for grazing (i.e., alpine pasture estivation) has a long tradition in Alpine countries and is not only of cultural importance but has also a relevant positive contribution to landscape maintenance and biodiversity.43 In Switzerland, about 400 000 out of the 1.6 million cattle (i.e., 25%) go to alpine pastures at an altitude between approximately 1000 and 2500 m above sea level and spend the summer there between June and approximately end of August (i.e., three months). The alpine pastures represent about 35% of the total agricultural land in Switzerland and the animal density on these pastures is considerably lower compared to low-altitude meadows. Next to the goal of producing high-quality dairy products, alpine pasture estivation may have a positive impact on the contamination of the products by PCBs, as the concentrations of pollutants is often expected to be smaller in remote alpine regions, compared to lowlands. Indeed, previous analyses of PCBs in soil samples from 105 sampling sites distributed all over Switzerland revealed a significant negative correlation between the altitude of the sampling sites and the concentrations of PCBs in soil samples.44 To investigate the relevance of alpine pasture estivation on the contamination of cattle by dl-PCBs, blood samples from cows and calves were analyzed before and after the summer 2014. These measurements revealed a decrease of the concentrations of dl-PCBs by 9% in cow blood (Figure S16a) and 50% in calf blood (Figure S16b). Although the calf blood samples taken before the estivation show unexpected high concentrations in one animal suffering from chronic diseases, the decrease is still 39% omitting this outlier. To test the hypothesis of a decrease of dl-PCB levels in blood over the course of a summer, the model was run by assuming a typical estivation scenario where cows go annually to an alpine G


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long-term best practices for mitigation of PCB contamination in animals (e.g., practices leading to reduced soil uptake) can be assessed.

pasture for three months (June to end of August). These cows give birth annually to a calf in April. The calf is accompanying the mother cow at the age of two months to the alpine pasture for three months in summer and stays for five additional months in fall in the stable before being slaughtered. For this model run, the concentrations of dl-PCBs in forage and in soil were assumed to be lower in the mountains by a factor of 4 compared to the case LU. Comparing the concentrations of PCBs measured in the case LU to typical levels found in remote background sites in Switzerland, this is a realistic assumption.44−46 This model run revealed a decrease of the concentrations of dl-PCBs in blood and milk of cows by 21% and in blood and fat of calves by 17%. In summary, the measurements as well as the model reveal that alpine pasture estivation can be an efficient decontamination procedure for cattle. In the case of mountain sites with lower PCB contamination than low-altitude sites, the concentrations of PCBs are noticeably lower in cattle after the summer. Although alpine pasture estivation is a procedure that is quite specific for alpine regions, it still shows that the transfer of animals to an uncontaminated site for a relatively short period, has already a noticeably positive effect on the contamination levels of these animals. Contribution of Point Sources to the Contamination of Cattle (Case GR). The case GR illustrates the relevance of local point sources for the contamination of the food chain by PCBs. Whereas the concentrations of dl-PCBs in forage and soil are in a typical range for Switzerland, the paint applied on the walls of the stable in GR in the 1960−1970s heavily contaminates the cattle. Comparison of the congener patterns of dl-PCBs in the different samples reveals that some of the forage samples and all animal samples exhibit a pattern very similar to the paint indicating the paint being the dominant contamination source. The measurements, as well as the model, confirm the effectiveness of the stable remediation on the 2−3fold decrease of the PCB contamination in cattle. Recently, a comprehensive inventory of use, stock, and emissions of PCBs in Switzerland between 1930 and 2100 has been established,2 which shows the relevance of PCBs in open applications such as the use in paints or building sealants for the mass budget of PCBs in Switzerland. Paints and sealants accounted each for only 250 t of the total of 5000 t of PCBs used in Switzerlandthe remaining 4500 t were used in closed applications such as capacitors and transformersbut have the largest share in the emissions of PCBs today. Currently, more than 86 t of PCBs remain in paints and this application will still represent a stock of more than 1 t in 2030, assuming a continuous renovation of former buildings and installations where such paints were applied. Thus, there is an urgent need for further efforts in the identification of PCB-containing materials in farms as well as professional removal and disposal of these applications. As long as paints and joint sealants are still present in stables, the animals and farming products will be seriously contaminated by PCBs. In industrialized countries, the environmental contamination by PCBs is still a relevant problem and will remain an issue for more decades. Many stables might be contaminated by PCBcontaining materials2 and also the background contamination of PCBs will decrease only very slowly.47 In the future it is possible to test different agricultural practices and derive recommendations. On the one hand, short-term actions for a physiological decontamination of animals (e.g., alpine pasture estivation) can be evaluated with the model. On the other hand,

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.7b02968. Additional text, tables, and figures as mentioned in the text (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: +41 44 632 5951. ORCID

Christian Bogdal: 0000-0001-9137-8663 Present Address §

Swiss Federal Office for the Environment, Worblentalstrasse 68, CH-3003 Bern, Switzerland.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The farmers of the cases LU and GR are deeply acknowledged for their support to the research. The authors thank Juliane Glüge (ETH Zurich) for her contributions to the modeling. The Swiss Federal Office for Agriculture (FOAG) and the Federal Food Safety and Veterinary Office (FSVO) are acknowledged for funding the measurement campaigns.

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REFERENCES

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