Skip to main content
EPA Author Manuscripts logoLink to EPA Author Manuscripts
. Author manuscript; available in PMC: 2023 Sep 14.
Published in final edited form as: Environ Sci Technol. 2023 Feb 7;57(9):3825–3832. doi: 10.1021/acs.est.2c06189

Underestimation of Per- and Polyfluoroalkyl Substances in Biosolids: Precursor Transformation During Conventional Treatment

Jake T Thompson 1, Nicole M Robey 2, Thabet M Tolaymat 3, John A Bowden 4, Helena M Solo-Gabriele 5, Timothy G Townsend 6
PMCID: PMC10500628  NIHMSID: NIHMS1919596  PMID: 36749308

Abstract

Wastewater treatment plants generate a solid waste known as biosolids. The most common management option for biosolids is to beneficially reuse them as an agricultural amendment, but because of the risk of pathogen exposure, many regulatory bodies require pathogen reduction before biosolids reuse. Per- and polyfluoroalkyl substances (PFAS) are well documented in biosolids, but limited information is available on how biosolids treatment processes impact PFAS. Furthermore, quantification of PFAS has focused on perfluoroalkyl acids (PFAAs) which are a small fraction of thousands of PFAS known to exist. The objective of this study was to quantify 92 PFAS in biosolids collected from eight biosolids treatment facilities before and after four pathogen treatment applications: composting, heat treatment, lime treatment, and anaerobic digestion. Overall, total PFAS concentrations before and after treatment were dominated by PFAA precursor species, in particular, diPAPs which accounted for a majority of the mass of the Σ92PFAS. This differs from historic data that found PFAAs, primarily PFOS, to dominate total PFAS concentrations. Treatment options such as heat treatment and composting changed the ratio of PFAA precursors to PFAAs indicating a transformation of PFAS during treatment. This study finds that PFAA precursors are likely underrepresented by other studies and make up a larger percentage of the total PFAS concentration in biosolids than previously estimated.

Keywords: Wastewater sludge, diPAP, PFAA, pathogen removal

Graphical Abstract

graphic file with name nihms-1919596-f0004.jpg

INTRODUCTION

Municipal wastewater treatment plants (WWTPs) accept domestic and industrial wastewater before it is discharged or reused. The process of treating wastewater produces a solid waste referred to as wastewater treatment sludge or biosolids. Due to their high organic matter and nutrient content, biosolids are commonly used as an agricultural amendment in regions with advanced wastewater treatment. For example, in the United States, France, and Australia, 60%, 76%, and 83%, respectively, of biosolids generated are reused in agricultural applications.13 The requirements placed upon biosolids for reuse are designed to prevent pathogen exposure and the environmental release of constituents of potential concern (COPC). Typically this includes a form of treatment, dewatering, demonstration of coliform reduction, and acceptable COPC concentrations.2,4 In the U.S., biosolids application regulations require measures to reduce pathogen content and vector attraction and provide ceiling concentrations for 10 heavy metals (As, Cd, Cr, Cu, Pb, Hg, Mo, Ni, Se, and Zn) based on the type of application.4 Constituents of emerging concern, including per- and polyfluoroalkyl substances (PFAS), are often not regulated in biosolids. The U.S. Environmental Protection Agency (EPA) has released regional screening levels (RSLs) for perfluorooctanoic acid (PFOA), perfluorooctanesulfonic acid (PFOS), perfluorobutanesulfonic acid (PFBS), perfluorohexanesulfonic acid (PFHxS), perfluorononanoic acid (PFNA), and hexafluoropropylene oxide dimer acid (HFPO-DA) in soil and groundwater matrices,5 and in 2021, the EPA committed to finalize a risk assessment for PFOA and PFOS in biosolids in 2024.6 Furthermore, 21 state-level regulatory agencies have promulgated PFAS regulations, and more have released provisional risk-based thresholds for soil, groundwater, and drinking water.714 In Florida, where this study took place, provisional direct exposure risk-based thresholds, called Soil Cleanup Target Levels (SCTL), have been developed for PFOA and PFOS in commercial and residential applications.15 Currently, regulations are emerging for PFAS in biosolids such as state-level government ordinances in Queensland, Australia, and Maine, U.S.,16,17 but globally, there is a lack of federal regulation for PFAS in biosolids.

Due to their extensive use in consumer products and ongoing human exposure, PFAS have been found consistently in domestic wastewater for decades,1825 and there has been concern regarding the fate of PFAS during traditional wastewater treatment. Based on previous studies, a fraction of the PFAS load will pass through the wastewater treatment plant and be released to the environment as effluent, while a significant portion (especially larger molecular weight PFAS) partition to the solid fraction (i.e., biosolids).2628 Data from multiple countries have identified significant concentrations of PFAS in biosolids, and as analytical capabilities have improved, the variety of PFAS identified by these analyses has increased as well.2931 While PFAS in biosolids have been well studied, we hypothesize that existing research may underestimate the magnitude of PFAS in this waste stream as a result of two factors: analytical limitations which do not capture a significant fraction of PFAA precursors and sample selection which may not capture transformations which result from standard biosolids treatment processes, predominantly comprised of perfluoroalkyl carboxylic acids (PFCAs) and perfluoroalkyl sulfonic acids (PFSAs), which are end products of the degradation of larger and less stable PFAA precursor species.32,33 PFAA precursor species are susceptible to thermal and chemical decomposition and have been found to undergo biodegradation in standard environmental conditions.32 Though certain PFAA precursors have been identified in biosolids,3440 there are a limited number of compounds that have been quantified, and even further, their explicit transformation during conventional treatment of biosolids is relatively unknown. Quantifying these precursors before and after treatment is important to understanding the true environmental risk posed by PFAS in biosolids.

In this study, 92 PFAS, including 72 PFAA precursors, were quantified in biosolids collected from eight treatment facilities which represent four conventional treatment types: composting, heat treatment, lime treatment, and anaerobic digestion. Samples were collected before and after treatment from each facility. Additionally, a laboratory-controlled heat treatment experiment was conducted on one sample of raw biosolids to corroborate transformations which were suspected to have resulted from heat treatment. This study is needed to address the remaining gaps in knowledge regarding PFAS in biosolids and to provide additional context for the interpretation of previous work. The quantitation of such a large suite of PFAS, including PFAA precursors of emerging concern, provides a more accurate estimate of the total abundance of PFAS in biosolids, and the collection of samples before and after conventional treatment processes highlights the transformations which are likely occurring and the potential underestimation of total PFAS when these transformations are not taken into consideration. When treated biosolids are recycled as an agricultural amendment, the presence of precursor PFAS and transformations should be taken into consideration as part of an assessment of potential environmental risk.

MATERIALS AND METHODS

Sample Collection.

Biosolids are commonly transported from the WWTP to a separate facility for treatment. Here, all operations that treat biosolids to meet pathogen requirements will be referred to as biosolids processing facilities or simply “facilities.” In 2019 (the most recent year for which these data were available), the Florida Department of Environmental Protection (FDEP) identified 39 biosolids processing facilities which cumulatively generated over 200,000metric tons (mt) of Class A/AA treated biosolids.41 Class A/AA biosolids are subject to the most stringent treatment standards and are approved for most distribution and marketing scenarios for land application.42 An estimate of the types of biosolids treatment processes implemented at Florida facilities based on FDEP data and interviews with WWTP operators is included in Figure 1. Each fraction represents the fraction of biosolids, by mass, generated from each type of facility for which process information was available (corresponding to 93% of total Class AA biosolids). Aerobic composting was the most common treatment types used to treat 41% of Class AA biosolids, followed by lime treatment (27%), heat treatment (16%), anaerobic digestion (5%), and chemical oxidation (4%). Sixteen biosolid samples across Florida were collected from eight facilities which reflected the four most common treatment types: one sample before treatment and one treated sample. Additionally, two samples of material added during the composting process (animal bedding and yard waste) were collected from two facilities. All sample collections took place between June 2021 and August 2021.

Figure 1.

Figure 1.

Class A biosolids treatment types implemented across 39 facilities in Florida. Data collected from Florida Department of Environmental Protection and phone interviews with wastewater treatment plant operators from 2019 through 2021. Percentages reflect mass generated with each treatment type as a fraction of total Class A biosolids generated in Florida.

Samples were collected in 23 L high-density polyethylene (HDPE) buckets using stainless steel shovels washed with methanol prior to and between collection. Samples were transported to the laboratory, aliquoted into 2 L HDPE bottles and stored at −20 °C until analysis (see Section 1 in the Supporting Information (SI) for detailed sample collection protocols). Facility information is presented below in Table 1, and a more detailed table including treatment details, samples collected, and facility information can be found in SI Table S1.

Table 1.

Information on Treatment Process Utilized by Facilities Sampled

Sample name Treatment description Treatment Type Dry tonnes produced each year
Facility 1 1:2 Ratio of biosolids to yard waste/animal bedding. Windrows are left outside to weather for 45 days where internal temperatures can reach 60 °C. Piles are inoculated with thermophilic actinomycetes during initial mixing. Piles are screened to 3/4 in. for final processing. Aerobic compost 2700
Facility 2 1:2 Ratio of biosolids to yard waste. Windrows are left outside to weather for 45 days where internal temperatures can reach 60 °C. Windrows are covered by an awning to shield the mixtures from rain. Piles are screened to 3/4 in. when aging is completed. Aerobic compost 4000
Facility 3 Biosolids are solar dried for 14 days going from ~12% solids to ~60%. Then, biosolids go into a natural gas thermal chamber for pasteurization at 90–120 °C for 2 h and exit at a ~ 90% solids content. Heat treatment 2700
Facility 4 Wet cake is centrifuged before entering a natural gas fueled dryer drum. Hot air is passed over the biosolids (90–120 °C) until they reach ~90% solids content and exit the drum via a cyclone separator. Heat treatment 20,000
Facility 5 Dewatered sludge is mechanically mixed with CaO (quicklime) until a pH of 12 is reached. Sulfamic acid is added to the mix to decrease pH and increase the temperature to 60 °C for a 40 min retention time. Lime treatment 8200
Facility 6 Lime is added as a stabilizing agent (pH < 12), while biosolids are dried by a combination of solar and a natural gas burner to reach a 90% solids content. Lime treatment 4500
Facility 7 Belt filter pressed biosolids are fed into a two stage digestor: mesophilic (35 °C /thermophilic (50 °C) for a retention time of ~20 days. Post digestion biosolids are then dried by a belt filter press to reach 40% solids content. Anaerobic digestion 6300
Facility 8 Belt filter pressed biosolids are fed into a two stage digestor: mesophilic (35 °C)/thermophilic (50 °C) for a retention time of ~20 days. Post digestion biosolids are then dried by natural gas burner (90–120 °C) until 90% solids content. Anaerobic digestion 11,000

Laboratory Treatment Simulations.

To investigate the effects of heat treatment on a single sample, raw biosolids were subjected to heating processes meant to replicate holding times and temperatures reached during heat treatment. Homogenized raw biosolids collected from Facility 3 were heated to 115 °C for 2 h mixing frequently (like heat treatment used at Facilities 3 and 4). Subsamples collected before heat treatment and after heat treatment underwent the same sample extraction and analysis (including moisture content) as other samples.

Standards and Reagents.

Reagents used in these analyses include methanol, ammonium hydroxide, and water (all Optima grade) purchased from Fisher Scientific. A total of 92 PFAS standards (a mixture of PFCA-24PAR and individual standards) were used to quantify PFAS in biosolid samples. These include 71 standards purchased from Wellington Laboratories, Inc. (Guelph, ON, Canada), 26 standards donated by Synquest Laboratories, Inc. (Alachua, FL, USA; standards are abbreviated as Syn # hereafter), and 12 standards donated by Oakwood Products Inc. (Estill, SC, USA; standards are abbreviated as Oak # hereafter). In addition, 27 isotopically labeled standards (a mixture of MPFAC-24ES and individual standards) which were used as internal standards (IS) were also purchased from Wellington Laboratories, Inc. Details about the targeted PFAS abbreviation, chemical formulas, and corresponding IS used for quantification are summarized in the SI Table S3.

Sample Extraction and LC-MS/MS Analysis.

The sample extraction method is a modified version of a previously reported solid matrix extraction method.43 Prior to extraction, biosolids samples were homogenized by rotating for 20 min at 70 rpm and air-dried in a fume hood for a period of 3 days. A subsample of air-dried biosolids was taken to complete dryness at 110 ± 5 °C according to ASTM D2216 to determine moisture content for calculating PFAS concentrations on a per dry mass basis (ASTM, 2019). Air-dried biosolids samples were divided into 10.0 ± 0.1 g subsamples, added to a 50 mL polypropylene tube, and spiked with 50 uL isotopically labeled PFAS IS mixture (see SI Table 3). Then, 8.5 mL of 0.3% ammonium hydroxide in methanol was added to the sample. The mixture was vortexed for 1 min, sonicated for 30 min, and rotated in an end-overend fashion for 30 min. The sample was centrifuged at 4000 rpm for 10 min, and the supernatant was removed using a pipet. An additional 8.5 mL of 0.3% ammonium hydroxide in methanol was added to the remaining sample, and the vortex, sonication, rotation, centrifugation, and supernatant removal steps were repeated. The combined extracts (17 mL) were concentrated to 10 mL under a gentle stream of high purity nitrogen gas (Biotage TurboVap II) at 35 °C. Evaporated extracts were aliquoted into 200 μL polypropylene autosampler vials for analysis by liquid chromatography and tandem mass spectrometry (LC-MS/MS).

PFAS analysis was performed using a Thermo Scientific Vanquish ultra high-pressure liquid chromatography (UHPLC) coupled to a TSQ Quantis triple quadrupole mass spectrometer (Thermo Scientific, San Jose, CA, USA). Chromatographic separation was achieved using a Phenomenex (Torrence, CA, USA) reverse phase column (Gemini C18 column, 100 mm × 2 mm; 3 μm). The LC was fitted with a Vanquish PFAS replacement kit, including an Acclaim 120 C18 delay column (2.1 mm × 50 mm, 5 μm, 120 Å), and PFAS-free plumbing and hardware to minimize background. Water (solvent B) and methanol (solvent A), both containing 5 mmol L−1 ammonium acetate, were used as the mobile phases at a flow rate of 0.5 mL min−1. The gradient elution was set as follows: 0–1 min 90% B, 1–2.5 min 90%–35% B, 2.5–17.5 min 35%–5% B, 17.5–17.51 min 5%–0% B, 17.51–22.5 min 0% B, 22.5–22.51 min 90% B, and then equilibrated back to initial conditions in 37 min. The autosampler and the column compartment temperature were set to 4 and 40 °C, respectively. Data were acquired in selected reaction monitoring (SRM) mode in negative polarity with the following parameters: ion source: HESI; ion spray voltage:, −3000 V; sheath gas flow, 60 arb; auxiliary gas flow, 5 arb; ion transfer tube temperature, 325 °C; and vaporizer temperature, 350 °C.

Calibration information for each PFAS in the sample extracts was derived and tailored using the prepared calibration levels. Each calibration level also contained a mixture of 27 mass-labeled PFAS internal standards (see SI Table S3) at a concentration of approximately 1000 ng L−1. The mass of all reagents and standards was recorded to report the most precise concentration. The LC/MS/MS operation conditions are shown in SI Table S4. For quantification, a calibration curve (14 levels, spanning from 10 to 100,000 ng L−1) was developed for all 92 PFAS (listed in SI Table S3) through serial dilutions of primary standard solutions.

Quality Control (QC) and Extraction Efficiency.

Fields blanks of deionized water (>18.2 MΩ cm) were prepared at each facility during sample collection. Three 10 mL deionized water extraction blanks underwent the sample extraction process and analysis to identify potential PFAS contamination or interference during the extraction. A solvent blank was included in the UHPLC-MS/MS sequence for every four samples to check for carryover. To monitor retention time (RT) shifting throughout the run, calibration levels (1–14) were included in the sequence randomly, and a midrange calibration level was analyzed frequently throughout the sample batch. Details on the method validation process are provided in SI Section 3.

Accuracy, extraction recovery, and matrix effects were evaluated using PFAS standards spiked into deionized water as well as pooled biosolids samples. Two pooled biosolids samples were created, one for untreated biosolids (a composite made with equal masses of eight raw biosolids samples) and one for treated biosolids (another composite, equal masses of eight treated biosolids samples). Each sample type was aliquoted into nine replicate 10.0 ± 0.1 g samples. To separate natively occurring PFAS in the pooled samples, three replicates (1–3) underwent extraction as described in the Sample Extraction and LC-MS/MS Analysis section, including the addition of 50 uL IS prior to extraction. To another three replicates (4–6), a 50 μL IS and a 20 μL mixture of nonmass-labeled PFAS standards were added before extraction; IS and nonmass-labeled PFAS standards were added to the remaining three replicates (7–9) after the evaporation step of extraction. For extraction efficiency calculations, the average mass-adjusted peak areas (peak area per gram of biosolids) of the PFAS in samples 1–3 were subtracted from the peak areas of the nonmass-labeled PFAS standards compounds and were compared between the samples where IS was added before any extraction (samples 1–3), after solid-phase extraction (samples 4–6), and after evaporation (samples 7–9). Results are included in SI Table S14.

RESULTS AND DISCUSSION

PFAS in Untreated Biosolids.

Of the 92 PFAS included in the analytical method, 25 were detected and quantified in samples collected from treatment facilities. Concentrations for PFAS on a per-dry-mass basis in every sample are included in SI Tables S6S13. The total concentration of PFAS (Σ92PFAS) in biosolids before treatment ranged from 182 to 1650 ng g−1 (median, 385 ng g−1; mean, 495 ng g−1), within the range of other studies, with average concentrations of 138 ± 50 ng g−1 Σ9PFAS44 and 539 ± 224 ng g−1 Σ13PFAS.45 Concentrations of PFOS, a legacy PFAS which has been phased out of most applications over the past decades46 ranged from 4.0 to 40 ng g−1, which is lower than the ranges of 10 to 370 and 308 to 618 ng g−1 reported by the Gallen et al.44 and Venkatesan and Halden45 studies. These studies and many others did not analyze for PFAA precursors which accounted for an average of 82 ± 11% of the Σ92PFAS for each sample in this study suggesting that historical characterization of biosolids may have underestimated the true mass of PFAS present (further comparison between the measurements reported in this study and previous studies are included in SI Section 2).

Fluorotelomer phosphate diesthers (diPAPs) represent the most significant class of PFAS among these biosolids samples and were quantified in 100% of raw biosolids samples. The sum of three diPAPs included in the analytical method, 6:2, 6:2/8:2, and 8:2 diPAP (Σ3diPAP), ranged from 73 to 1400 ng g−1 making up 54% ± 15% of the Σ92PFAS, on average, in raw biosolids. At all but one facility (Facility 8), Σ3diPAP was greater than the sum of all PFAAs (Σ20PFAA). Similar results were reported recently in Australian and U.S. studies where Σ3diPAP contributed a majority of the total mass of PFAS in biosolids sampled.40,47 Historically, however, most studies that have characterized PFAS in biosolids have focused on quantifying PFAAs and do not include PFAA precursors, such as diPAPs, suggesting they likely underestimate the total mass of PFAS present in biosolids.

PFAS in Treated Biosolids.

The treatment employed at each biosolids processing facility can be summarized into four groups: composting, heat treatment, lime treatment, and anaerobic digestion. In short, Facilities 1 and 2 employed composting, Facilities 3 and 4 heat treatment, Facility 5 lime treatment, Facility 6 a combination of lime and heat treatment, Facility 7 anaerobic digestion followed by belt press drying, and Facility 8 anaerobic digestion followed by heat drying. A more detailed description of each facility is found in SI Table S1.

Individual PFAS concentrations for Facilities 7 and 8 are included in the SI Tables S12 and S13, respectively. The Σ92 PFAS measured in the raw biosolids and biosolids treated with lime (Facility 5) were 182 and 112 ng g−1, respectively. This represents a 38.5% decrease; however, the proportional fraction of PFAS classes remained consistent between biosolids before and after lime treatment. Concentrations of each PFAS for Facility 5 is detailed in SI Tables S10.

Two facilities (Facility 7 and Facility 8) used anaerobic digestion in their treatment process; however, the integrated treatment and dewatering processes differed between facilities in ways which appear to impact PFAS profiles in the treated biosolids. Facility 7 used anaerobic treatment to remove pathogens followed by belt-press dewatering, and Σ92PFAS was 1650 ng g−1 in the raw biosolids and 584 ng g−1 (65% decrease) after treatment. At Facility 8, which followed anaerobic treatment with heat drying, the Σ92PFAS values were 192 ng g−1 in the raw biosolids and 388 ng g−1 (102% increase) after treatment. A possible explanation for this observation is that belt-press dewatering physically removes mobile PFAS with the water fraction, while heat drying removes water via evaporation, concentrating PFAS with the solid fraction and also potentially increasing the apparent concentration of PFAS as a result of PFAA precursor transformation. This suspected mode of PFAS transformation was explored further in a laboratory heat treatment simulation, described later in this section.

Biosolids underwent aerobic composting at Facilities 1 and 2. During the composting process, biosolids are mixed with other sources of organic matter such as animal bedding and yard waste. Individual PFAS concentrations for Facilities 1 and 2 are included in the SI Tables S6 and S7, respectively. In both cases, Σ92PFAS concentrations were lower in composted biosolids compared to the corresponding raw biosolids. PFAS analysis of the composting material found all compounds below detection limits. Both facilities added composting material at approximately 2:1 ratio (composting material:biosolids, v:v), indicating a theoretical dilution of 67% (assuming similar moisture contents). Σ92PFAS in composted biosolids decreased by 81% after treatment at Facility 1 and by 22% after treatment at Facility 2. While the overall reduction in Σ92PFAS can be attributed to the dilution of biosolids with low-PFAS composting material, a dramatic shift in the ratio of PFAA precursors to terminal species was observed compared to the other treatment options explored in this study. This change is illustrated in Figure 2, which shows relative percent contributions from short and long chain PFCAs, short and long chain PFSAs, and PFAA precursors. Short chain PFCAs perfluoropentanoic acid (PFPeA) and perfluorohexanoic acid (PFHxA) both increased after composting despite being diluted with low-PFAS composting material (Figure 2). PFPeA increased from 3.7 to 17 ng g−1 at Facility 1 and from 2.7 to 26 ng g−1 at Facility 2. PFHxA concentrations increased from 6.9 to 15 ng g−1 at Facility 1 and from 3.9 to 13 ng g−1 at Facility 2. These increases are believed to be attributed to the breakdown of PFAA precursors through microbial biodegradation. The PFAA precursor class diPAPs, which are a significant fraction of the PFAS measured in these samples, have been found to degrade into PFCA species through microbial breakdown of the phosphate ester to produce fluorotelomer alcohol (FTOH) species48,49 and PFCAs.49,50

Figure 2.

Figure 2.

Relative% contributions of each PFAS class to the average total PFAS concentration in biosolids undergoing aerobic composting normalized to the concentration of fluorine. The numbers in the bars represent the total mass of fluorine ng g−1 that each PFAS class contributed. PFAS classes are composed of short chain PFCAs (C4–C7), long chain PFCAs (C8–C12, C14), short chain PFSAs (C4), long chain PFSAs (C6, C8), and PFAA precursors. The total concentration of each class was divided by the Σ92PFAS. Total class concentrations (e.g., Σ4short chain PFCA, Σ20PFAA precursor) are also included in the figure.

Heat treatment for pathogen removal was utilized at two of the facilities (Facilities 3 and 4), and heat drying was used in the dewatering process at two additional facilities (Facilities 6 and 8). Individual PFAS concentrations for Facilities 3, 4, 6, and 8 are included in SI Tables S8, S9, S11, and S13, respectively. For the facilities that utilized heat treatment or drying, Σ92PFAS were sometimes slightly different, both higher and lower, after treatment or significantly higher. Facilities 3, 4, and 6 had slight increases or decreases from 519 to 501 ng g−1, 422 to 451 ng g−1, and 362 to 385 ng g−1, respectively, while Facility 8 increased from 192 to 388 ng g−1. There was no definitive trend in changes in PFAA concentrations among biosolids that underwent heat treatment. Facility 6 had a slight increase in average concentration for PFOS, from 15 to 19 ng g−1, and a slight decrease in average concentration for PFOA, from 3.8 to 3.2 ng g−1, while biosolids at Facilities 3, 4, and 8 decreased in average concentration for both PFOS and PFOA from 4.0 to 1.4 ng g−1 and 21 to 7.7 ng g−1 at Facility 3, 33 to 3.3 ng g−1 and 4.3 to 2.3 ng g−1 at Facility 4, and 30 to 14 ng g−1 and 6.3 to 4.9 ng g−1 at Facility 8. Most notably, concentrations of 6:2 diPAP increased in all heat treatment/drying samples after treatment, suggesting that heat treatment might increase the concentration of diPAP species due to the breakdown of larger precursors not included in this analytical method. This finding is illustrated in Figure 3, where 6:2 diPAP concentrations in biosolids before and after treatment are compared for facilities which utilize heat treatment in any stage of their process, and those which do not utilize any form of heat treatment. The observed increase in 6:2 diPAP was unanticipated and is difficult to explain given the lack of available literature on polyfluoroalkyl phosphate esters (PAP) transformation and formation pathways. A possible explanation is the breakdown of triPAPs or larger homologues not included in the set of quantified PFAS. To further investigate this topic and to confirm that the observed increase in diPAPs was not due to artifacts during treatment, extraction, and analysis, a laboratory heat treatment experiment was conducted.

Figure 3.

Figure 3.

6:2 diPAP concentrations measured in biosolids before and after treatment. Facilities 3, 3 (Laboratory experiment), 4, 6, and 8 employed heat treatment for pathogen reduction and/or drying, while Facilities 1, 2, 5, and 7 did not. Error bars represent one standard deviation in 6:2 concentrations between samples.

Raw biosolids collected from Facility 3 underwent controlled heat treatment to determine if the changes observed in the PFAS profile before and after treatment could be recreated in the laboratory as a result of the application of heat only. Concentrations of PFAAs, such as PFOA and PFOS, remained similar before and after treatment, changing from 9.4 to 10.6 ng g−1 and 4.9 to 4.3 ng g−1, respectively. However, certain PFAA precursors increased or decreased, such as 6:2 diPAP, increasing from 123 to 224 ng g−1 or FPePA decreasing from 92 to 45 ng g−1. Interestingly, when normalizing for the mass of florurine present, the combined concentration of measurable flourine increased by 30 ng g1 after treatment. The results of the experiment for 6:2 diPAP are included in Figure 3 alongside the samples collected before and after fullscale facility treatment. Concentrations of 6:2 diPAP increased significantly after the 2 h heat treatment at 115 °C, from 123 ± 7 to 224 ± 25 ng g−1, remarkably similar to before and after facility treatment.

Reuse Implications.

Shorter chain species are less commonly found in raw biosolids due to their solubility in water; therefore, biosolids are typically dominated by long chain species that favor partitioning to the solid phase.51 The presence of short chain PFCAs after treatment is likely due to the breakdown of 6:2 diPAP. The degradation of longer chain PFAS into shorter chain PFAAs has a significant impact on partitioning from solids into the aqueous phase. Higgins and Luthy52 found that longer chain length PFAS are more likely to partition to soil, and each chain length of a CF2 group has a 0.5 to 0.6 log increase of the partitioning coefficient. This provides a pathway for PFAS to leach out of land-applied biosolids and into the groundwater overtime as more PFAA precursors biodegrade. For example, transformation of 6:2 diPAP to PFHxA might increase the tendency for PFAS to partition from soil to water (i.e., the tendency to leach from biosolids into the surrounding environment) by a factor of 1000. The breakdown of PFAA precursors into terminal species has been demonstrated to take place during conventional treatment of biosolids and in soils that have had biosolids land applied to them.32,40 If PFAS, and particularly short chain PFAAs, are to be regulated in biosolids, analytical protocols as well as when and where samples are taken will have an impact on the outcome of any monitoring program. For example, in this study, it was reported that aerobically composted biosolids increased in short chain PFCAs (i.e., PFHxA and PFPeA); if guidelines were in place to monitor the concentrations of these compounds, it would be theoretically possible to be below risk-based thresholds before treatment but exceed the same thresholds after treatment. Furthermore, compounds such as large molecular weight PAP species which are not captured in even the most thorough targeted PFAS analysis may degrade into measurable precursor PFAS, and eventually PFAAs, as was observed by this study in heat treated biosolids. This implies that the mass release of short chain PFAAs in land-applied biosolids will be larger than what is initially measured through standard analytical characterization.

Supplementary Material

Supplementary Material

ACKNOWLEDGMENTS

The researchers have received support from the Hinkley Center for Solid and Hazardous Waste Management and from the U.S. Environmental Protection Agency under the Science To Achieve Results (STAR) grant program (EPA-G2018-STAR-B1; Grant 83962001-0) to investigate the occurrence, source, and fate of PFAS in landfills. Data presented herein did not undergo a formal quality assurance review as outlined in “US EPA Office of Research and Development’s Quality Management Plan for Scientific Research”. This manuscript was subjected to the US EPA internal review process. The research results presented do not necessarily reflect the views of the Agency or its policy. Mention of trade names or products does not constitute endorsement or recommendation for use.

Footnotes

Supporting Information

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.2c06189.

List of materials, sample collection information, previous studies, instrument parameters, extraction efficiencies, and complete data sets (PDF)

Complete contact information is available at: https://pubs.acs.org/10.1021/acs.est.2c06189

The authors declare no competing financial interest.

Contributor Information

Jake T. Thompson, Department of Environmental Engineering Sciences, University of Florida, Gainesville, Florida 32611-6450, United States

Nicole M. Robey, Department of Environmental Engineering Sciences, University of Florida, Gainesville, Florida 32611-6450, United States

Thabet M. Tolaymat, Office of Research and Development, United States Environmental Protection Agency, Cincinnati, Ohio 45268, United States

John A. Bowden, College of Veterinary Medicine, University of Florida, Gainesville, Florida 32610, United States

Helena M. Solo-Gabriele, Chemical, Environmental, and Materials Engineering, University of Miami, Coral Gables, Florida 33124, United States

Timothy G. Townsend, Department of Environmental, Engineering Sciences, University of Florida, Gainesville, Florida 32611-6450, United States

REFERENCES

  • (1).Collivignarelli MC; Abbà A; Frattarola A; Carnevale Miino M; Padovani S; Katsoyiannis I; Torretta V. Legislation for the Reuse of Biosolids on Agricultural Land in Europe: Overview. Sustainability 2019, 11 (21), 6015. [Google Scholar]
  • (2).Western Australian Guidelines for Biosolids Management. Department of Environment and Conservation. https://www.der.wa.gov.au/images/documents/our-services/approvals-and-licences/western-australian-guidelines-for-biosolids-management-dec-2012.pdf (accessed 2021–11–11).
  • (3).Lu Q; He ZL; Stoffella PJ Land Application of Biosolids in the USA: A Review. Appl. Environ. Soil Sci 2012, 2012, No. e201462. [Google Scholar]
  • (4).40 CFR Part 503 - Standards for the Use or Disposal of Sewage Sludge. U.S. EPA https://www.ecfr.gov/current/title-40/chapter-I/subchapter-O/part-503 (accessed 2022–01–24).
  • (5).Regional Screening Levels (RSLs) - Generic Tables, 2022. U.S. EPA https://www.epa.gov/risk/regional-screening-levels-rsls-generictables.
  • (6).PFAS Strategic Roadmap: EPA’s Commitments to Action 20212024, 2021. U.S. EPA https://www.epa.gov/system/files/documents/2021-10/pfas-roadmap_final-508.pdf.
  • (7).Colorado laws and policies related to chemicals from firefighting foam and other sources. Colorado Department of Public Health & Environment. https://cdphe.colorado.gov/pfas-laws (accessed 2022–01–24).
  • (8).Perfluoroalkyl Substances PFASs in DWHealth Concerns. Connecticut Department of Health. https://portal.ct.gov/-/media/Departments-and-Agencies/DPH/dph/environmental_health/PFAS/Perfluoroalkyl-Substances-PFASs-in-DWHealth-Concerns-2021-03-25-update.pdf (accessed 2022–01–24).
  • (9).New state drinking water standards pave way for expansion of Michigan’s PFAS clean-up efforts. Michigan Department of Environment, Great Lakes, and Energy. https://content.govdelivery.com/accounts/MIDEQ/bulletins/2988e74 (accessed 2022–01–24).
  • (10).Maine CDC Maximum Exposure Guidelines (MEGs) for Drinking Water. Maine Environmental and Occupational Health Program. https://www.maine.gov/dhhs/mecdc/environmentalhealth/eohp/wells/documents/megtable2016.pdf (accessed 2022–01–24).
  • (11).PFAS and Idaho Drinking Water. Idaho Department of Environmental Quality. https://www.deq.idaho.gov/water-quality/drinking-water/pfas-and-idaho-drinking-water/ (accessed 2022–01–24).
  • (12).Per- and Polyfluoroalkyl Substances (PFAS). Massachusetts Department of Environmental Protection. https://www.mass.gov/info-details/per-and-polyfluoroalkyl-substances-pfas (accessed 2022–01–24).
  • (13).Sun M. Notice of Intent to List Perfluorooctanoic Acid (PFOA) and Perfluorooctane Sulfonate (PFOS). California Environmental Protection Agency, Office of Environmental Health Hazard Assessment. https://oehha.ca.gov/proposition-65/crnr/notice-intent-list-perfluorooctanoic-acid-pfoa-and-perfluorooctane-sulfonate (accessed 2022–01–24).
  • (14).U.S. State Resources about PFAS. U.S. EPA https://www.epa.gov/pfas/us-state-resources-about-pfas (accessed 2022–01–24).
  • (15).Stuchal L; Roberts S. PFAS - Provisional Cleanup Target Levels and Screening Levels, 2019. Center for Environmental and Human Toxicology University of Florida. https://floridadep.gov/sites/default/files/PFAS-Presentation-CTLs_12Sep19_0.pdf (accessed 2020–06–25).
  • (16).End of Waste Code Biosolids; ABN 46 640 294 485; 2020. Queensland Government. https://environment.des.qld.gov.au/__data/assets/pdf_file/0029/88724/wr-eowc-approved-biosolids.pdf.
  • (17).PFOA and PFOS. Maine Department of Environmental Protection. https://www1.maine.gov/dep/spills/topics/pfas/index.html (accessed 2022–01–24).
  • (18).Eriksson U; Haglund P; Kärrman A. Screening of PFASs in Sludge and Water from Waste Water Treatment Plants; Swedish Environmental Protection Agency, 2015. [Google Scholar]
  • (19).Loganathan BG; Sajwan KS; Sinclair E; Senthil Kumar K; Kannan K. Perfluoroalkyl Sulfonates and Perfluorocarboxylates in Two Wastewater Treatment Facilities in Kentucky and Georgia. Water Res. 2007, 41 (20), 4611–4620. [DOI] [PubMed] [Google Scholar]
  • (20).Munoz G; Michaud AM; Liu M; Vo Duy S; Montenach D; Resseguier C; Watteau F; Sappin-Didier V; Feder F; Morvan T; Houot S; Desrosiers M; Liu J; Sauvé S. Target and Nontarget Screening of PFAS in Biosolids, Composts, and Other Organic Waste Products for Land Application in France. Environ. Sci. Technol 2022, 56, 6056. [DOI] [PubMed] [Google Scholar]
  • (21).Schultz MM; Higgins CP; Huset CA; Luthy RG; Barofsky DF; Field JA Fluorochemical Mass Flows in a Municipal Wastewater Treatment Facility. Environ. Sci. Technol 2006, 40 (23), 7350–7357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • (22).Sinclair E; Kannan K. Mass Loading and Fate of Perfluoroalkyl Surfactants in Wastewater Treatment Plants. Environ. Sci. Technol 2006, 40 (5), 1408–1414. [DOI] [PubMed] [Google Scholar]
  • (23).Venkatesan AK; Halden RU National Inventory of Perfluoroalkyl Substances in Archived U.S. Biosolids from the 2001 EPA National Sewage Sludge Survey. J. Hazard. Mater 2013, 252–253, 413–418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • (24).Xiao F; Halbach TR; Simcik MF; Gulliver JS Input Characterization of Perfluoroalkyl Substances in Wastewater Treatment Plants: Source Discrimination by Exploratory Data Analysis. Water Res. 2012, 46 (9), 3101–3109. [DOI] [PubMed] [Google Scholar]
  • (25).Yu J; Hu J; Tanaka S; Fujii S. Perfluorooctane Sulfonate (PFOS) and Perfluorooctanoic Acid (PFOA) in Sewage Treatment Plants. Water Res. 2009, 43 (9), 2399–2408. [DOI] [PubMed] [Google Scholar]
  • (26).Johnson GR PFAS in Soil and Groundwater Following Historical Land Application of Biosolids. Water Res. 2022, 211, 118035. [DOI] [PubMed] [Google Scholar]
  • (27).Navarro I; de la Torre A; Sanz P; Pro J; Carbonell G; Martinez M. d. l. A. Bioaccumulation of Emerging Organic Compounds (Perfluoroalkyl Substances and Halogenated Flame Retardants) by Earthworm in Biosolid Amended Soils. Environ. Res 2016, 149, 32–39. [DOI] [PubMed] [Google Scholar]
  • (28).Sepulvado JG; Blaine AC; Hundal LS; Higgins CP Occurrence and Fate of Perfluorochemicals in Soil Following the Land Application of Municipal Biosolids. Environ. Sci. Technol 2011, 45 (19), 8106–8112. [DOI] [PubMed] [Google Scholar]
  • (29).Gallen C; Eaglesham G; Drage D; Nguyen TH; Mueller JF A Mass Estimate of Perfluoroalkyl Substance (PFAS) Release from Australian Wastewater Treatment Plants. Chemosphere 2018, 208, 975–983. [DOI] [PubMed] [Google Scholar]
  • (30).Lenka SP; Kah M; Padhye LP Occurrence and Fate of Poly- and Perfluoroalkyl Substances (PFAS) in Urban Waters of New Zealand. J. Hazard. Mater 2022, 428, 128257. [DOI] [PubMed] [Google Scholar]
  • (31).Semerád J; Hatasová N; Grasserová A; Černá T; Filipová A; Hanč A; Innemanová P; Pivokonský M; Cajthaml T. Screening for 32 Per- and Polyfluoroalkyl Substances (PFAS) Including GenX in Sludges from 43 WWTPs Located in the Czech Republic - Evaluation of Potential Accumulation in Vegetables after Application of Biosolids. Chemosphere 2020, 261, 128018. [DOI] [PubMed] [Google Scholar]
  • (32).D’eon JC; Mabury SA Production of Perfluorinated Carboxylic Acids (PFCAs) from the Biotransformation of Polyfluoroalkyl Phosphate Surfactants (PAPS): Exploring Routes of Human Contamination. Environ. Sci. Technol 2007, 41 (13), 4799–4805. [DOI] [PubMed] [Google Scholar]
  • (33).Liu Y; Robey NM; Bowden JA; Tolaymat TM; da Silva BF; Solo-Gabriele HM; Townsend TG From Waste Collection Vehicles to Landfills: Indication of Per- and Polyfluoroalkyl Substance (PFAS) Transformation. Environ. Sci. Technol. Lett 2021, 8 (1), 66–72. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • (34).Allred BM; Lang JR; Barlaz MA; Field JA Physical and Biological Release of Poly- and Perfluoroalkyl Substances (PFASs) from Municipal Solid Waste in Anaerobic Model Landfill Reactors. Environ. Sci. Technol 2015, 49 (13), 7648–7656. [DOI] [PubMed] [Google Scholar]
  • (35).Dauchy X; Boiteux V; Bach C; Colin A; Hemard J; Rosin C; Munoz J-F Mass Flows and Fate of Per- and Polyfluoroalkyl Substances (PFASs) in the Wastewater Treatment Plant of a Fluorochemical Manufacturing Facility. Sci. Total Environ 2017, 576, 549–558. [DOI] [PubMed] [Google Scholar]
  • (36).D’eon JC; Crozier PW; Furdui VI; Reiner EJ; Libelo EL; Mabury SA Observation of a Commercial Fluorinated Material, the Polyfluoroalkyl Phosphoric Acid Diesters, in Human Sera, Wastewater Treatment Plant Sludge, and Paper Fibers. Environ. Sci. Technol 2009, 43 (12), 4589–4594. [DOI] [PubMed] [Google Scholar]
  • (37).Hamid H; Li L. Role of Wastewater Treatment Plant in Environmental Cycling of Poly- and Perfluoroalkyl Substances. Ecocycles 2016, 2 (2), 43–53. [Google Scholar]
  • (38).Houtz EF; Sutton R; Park J-S; Sedlak M. Poly- and Perfluoroalkyl Substances in Wastewater: Significance of Unknown Precursors, Manufacturing Shifts, and Likely AFFF Impacts. Water Res. 2016, 95, 142–149. [DOI] [PubMed] [Google Scholar]
  • (39).Lee H; Tevlin AG; Mabury SA; Mabury SA Fate of Polyfluoroalkyl Phosphate Diesters and Their Metabolites in Biosolids-Applied Soil: Biodegradation and Plant Uptake in Green-house and Field Experiments. Environ. Sci. Technol 2014, 48 (1), 340–349. [DOI] [PubMed] [Google Scholar]
  • (40).Schaefer CE; Hooper J; Modiri-Gharehveran M; Drennan DM; Beecher N; Lee L. Release of Poly- and Perfluoroalkyl Substances from Finished Biosolids in Soil Mesocosms. Water Res. 2022, 217, 118405. [DOI] [PubMed] [Google Scholar]
  • (41).List of Class AA Biosolids Facilities in Florida in 2019; Data set; Division of Water Resource Management, Wastewater Management Program, Florida Department of Environmental Protection: Tallahassee, FL, 2021. [Google Scholar]
  • (42).Chapter 62–640, Florida Administrative Code: Biosolids; Florida Department of Environmental Protection, 2021. [Google Scholar]
  • (43).Ahmadireskety A; Da Silva BF; Townsend TG; Yost RA; Solo-Gabriele HM; Bowden JA Evaluation of Extraction Workflows for Quantitative Analysis of Per- and Polyfluoroalkyl Substances: A Case Study Using Soil Adjacent to a Landfill. Sci. Total Environ 2021, 760, 143944. [DOI] [PubMed] [Google Scholar]
  • (44).Gallen C; Drage D; Kaserzon S; Baduel C; Gallen M; Banks A; Broomhall S; Mueller JF Occurrence and Distribution of Brominated Flame Retardants and Perfluoroalkyl Substances in Australian Landfill Leachate and Biosolids. J. Hazard. Mater 2016, 312, 55–64. [DOI] [PubMed] [Google Scholar]
  • (45).Venkatesan AK; Halden RU National Inventory of Perfluoroalkyl Substances in Archived U.S. Biosolids from the 2001 EPA National Sewage Sludge Survey. J. Hazard. Mater 2013, 252–253, 413–418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • (46).EPA and 3M Announce Phase out of PFOS. U.S. EPA https://archive.epa.gov/epapages/newsroom_archive/newsreleases/33aa946e6cb11f35852568e1005246b4.html (accessed 2022–08–21).
  • (47).Moodie D; Coggan T; Berry K; Kolobaric A; Fernandes M; Lee E; Reichman S; Nugegoda D; Clarke BO Legacy and Emerging Per- and Polyfluoroalkyl Substances (PFASs) in Australian Biosolids. Chemosphere 2021, 270, 129143. [DOI] [PubMed] [Google Scholar]
  • (48).Hamid H; Li LY; Grace JR Aerobic Biotransformation of Fluorotelomer Compounds in Landfill Leachate-Sediment. Sci. Total Environ 2020, 713, 136547. [DOI] [PubMed] [Google Scholar]
  • (49).Lee H; D’eon J; Mabury SA Biodegradation of Polyfluoroalkyl Phosphates as a Source of Perfluorinated Acids to the Environment. Environ. Sci. Technol 2010, 44 (9), 3305–3310. [DOI] [PubMed] [Google Scholar]
  • (50).Dinglasan MJA; Ye Y; Edwards EA; Mabury SA Fluorotelomer Alcohol Biodegradation Yields Poly- and Perfluorinated Acids. Environ. Sci. Technol 2004, 38 (10), 2857–2864. [DOI] [PubMed] [Google Scholar]
  • (51).Eriksson U; Haglund P; Kärrman A. Contribution of Precursor Compounds to the Release of Per- and Polyfluoroalkyl Substances (PFASs) from Waste Water Treatment Plants (WWTPs). J. Environ. Sci 2017, 61, 80–90. [DOI] [PubMed] [Google Scholar]
  • (52).Higgins CP; Luthy RG Sorption of Perfluorinated Surfactants on Sediments. Environ. Sci. Technol 2006, 40 (23), 7251–7256. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Material

RESOURCES