Abstract

An investigation of brominated flame retardants (BFRs), polybrominated diphenylethers (PBDEs), and chlorinated flame retardants was conducted in samples from Canadian wastewater treatment plants (WWTPs). The penta-BDE mixture and deca-BDE were most commonly detected. Median removal efficiencies of PBDEs by WWTPs were 71% to 99% and higher concentrations of PBDEs were found in influent samples in summer, compared to winter. Three novel brominated flame retardants (nBFRs) including 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), 2-ethylhexyl-2,3,4,5-tetrabromobenzoate (EHTeBB or TBB), and bis(2-ethyl-1-hexyl)tetrabromophthalate (BEHTBP or TBPH) were detected in greater than 80% of influents and biosolids. Median removal efficiencies were 45% to 99% for BTBPE, 63% to 99% for TBB, and 88% to 99% for TBPH. Detection of total dechlorane plus ((DP) syn and anti) was greater than 90% in both wastewater and biosolids samples. However, median removal efficiencies were between 51% and 66% for total DP. Overall, PBDEs were effectively removed via different treatment processes, while BTBPE, TBB, and DP exhibited lower removal rates, which could be due to their physical chemical properties.

INTRODUCTION

Halogenated flame retardants, including two main classes of commercial organobromine and organochlorine compounds, have been used in many industrial and domestic products for fire prevention (Alaee et al. 2003). However, concerns over the toxicity, persistence, and accumulation of some of the extensively used brominated flame retardants (BFRs), such as the polybrominated diphenyl ethers (PBDEs), have led to regulation and restriction of their production. Two of the three major PBDEs, penta-BDE and octa-BDE, have been banned under the Stockholm Convention on Persistent Organic Pollutants (POPs) in Europe and North America (Morf et al. 2005). Deca-BDE is no longer imported into Canada and is registered under the European Union's REACH program and has been designated as a persistent organic pollutant (POP) under the terms of the Stockholm Convention on POPs (http://chm.pops.int/TheConvention/ThePOPs/TheNewPOPs/tabid/2511/Default.aspx). As additive FRs, PBDEs are not covalently bound and can be released into the environment during production, application, and waste disposal processes. Due to restrictions in the utilization of PBDEs, the BFR industry has developed alternative and/or novel flame retardants (nFRs); replacements include bis(2-ethyl-1-hexyl)tetrabromophthalate (TBPH), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), decabromodiphenyl ethane (DBDPE), 2,3-dibromopropyl 2,4,6-tribromophenyl ether (DPTE), dechlorane plus (DP), 2-ethylhexyl-2,3,4,5-tetrabromobenzoate (TBB), hexabromobenzene (HBB), pentabromoethylbenzene (PBEB), pentabromotoluene (PBT), 1,2,3,4,5-pentabromobenzene (PBBZ), 2,3,5,6-tetrabromo-p-xylene (pTBX), and 3,4,5,6-tetrabromo-2-chlorotoluene (TBCT) (Papachlimitzou et al. 2012). Although hexabromocyclododecane was at one point the second-most heavily produced BFR globally and is included in monitoring programs for a wide range of environmental compartments, most laboratories globally have transitioned to methods based on liquid chromatography/mass spectrometry (LC/MS) that enables diastereomer-specific analysis (Marvin et al. 2011).

BTBPE, TBB, and TBPH are three novel BFRs used in commercial formulations (Covaci et al. 2011; Xiao et al. 2012; Houde et al. 2014). BTBPE is added in thermoplastics, thermoset resins, polycarbonate and coatings and has been used as a replacement for octa-BDE since 2005. Another commercial mixture contains the brominated components of TBB and TBPH and is used primarily in polyurethane foam, and found in furniture and baby products (Stapleton et al. 2008). All three nBFRs (BTBPE, TBB, and TBPH) have recently been identified in various biological and environmental matrices, including house dust, river sediment, sewage sludge, birds, mammals, and human serum (Covaci et al. 2011; Rocha-Gutierrez & Lee 2012; Lankova et al. 2013; Houde et al. 2014). Dechlorane plus (DP) is a chlorinated flame retardant introduced as a replacement for dechlorane (i.e., Mirex) (Sverko et al. 2008). In the DP technical mixture, two stereoisomers (syn and anti) are present at an approximate ratio of 1:2, respectively. DP is used mainly in cable coatings, plastic roofing materials, and hard connectors in computers and televisions (Qiu et al. 2007).

The growing human population and the expansion of industrial activities generate large volumes of wastewater which, in developed countries, is regularly treated by wastewater treatment plants (WWTPs) prior to discharge to the environment (Rocha-Gutierrez & Lee 2012, 2013). Although WWTPs are effective at removing many contaminants, such as nutrients and biodegradable organics, from residential, industrial, commercial, and institutional wastewater, WWTPs are not designed to remove POPs such as PBDEs (Kim et al. 2013a). Therefore, WWTP effluents and biosolids are considered to be pathways where organic pollutants, including PBDEs, are discharged to river ecosystems, to land and to lakes and oceans. Previous studies showed that lower concentrations of PBDEs were detected in treated effluent samples than in raw influents; this observation could be mainly due to the PBDEs' high partitioning affinity (octanol-water partition coefficient known as Log Kow, log Kow 5–10) to be adsorbed on suspended particles in wastewater (Song et al. 2006; Kim et al. 2013a). Despite the fact that PBDEs appear to be effectively removed in the liquid stream of WWTPs, the overall fate and occurrence of PBDEs during wastewater treatment requires further investigation. WWTP performance can be affected by environmental and operational parameters, including season, treatment time, and process complexity; however, only a handful of studies have investigated the relationship between the removal efficiency for PBDEs and varying environmental and/or operational conditions (Kim et al. 2013a, 2013b, 2014).

Eight Canadian WWTPs, encompassing lagoon, primary, secondary, and advanced liquid treatment processes, were selected for the analysis of flame retardants in this study. An analytical method based on gas chromatography (GC) with tandem mass spectrometry (GC-MS/MS) was used for identification and quantification of 15 PBDEs and 16 alternative flame retardants in a total of 186 liquid and 58 solid samples, which were collected over a three-year period. In addition, the removal efficiencies of the various types of liquid treatment processes were investigated. This study also examined trends related to seasonal, annual, and input (industrial versus domestic) variations. To the best of our knowledge, this is the first study to report the concentration ranges of the alternative flame retardants TBB and TBPH in influent, effluent, and biosolids samples from WWTPs.

MATERIALS AND METHODS

Chemicals and reagents

Polybrominated diphenyl ether predominant congener mixture (PBDE 17, 28, 47, 66, 71, 85, 99, 100, 138, 153, 154, 183, 190, and 209) was purchased from Cambridge Isotope Laboratories, Inc. (Andover, MA, USA). A custom mixture of brominated and chlorinated flame retardants, allyl 2,4,6-tribromophenyl ether (ATE), 2,3,5,6-tetrabromo-p-xylene (pTBX), 2-bromoallyl 2,4,6-tribromophenyl ether (BATE), 1,2,3,4,5-pentabromobenzene (PBBZ), 3,4,5,6-tetrabromo-2-chlorotoluene (TBCT), pentabromotoluene (PBT), pentabromoethylbenzene (PBEB), 2,3-dibromopropyl 2,4,6-tribromophenyl ether (DPTE), hexabromobenzene (HBB), 2,2′,4,5,5′-pentabromobiphenyl (BB-101), pentabromobenzyl acrylate (PBBA), 2-ethylhexyl-2,3,4,5-tetrabromobenzoate (TBB), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), bis(2-ethyl-1-hexyl)tetrabromophthalate (TBPH), anti-dechlorane plus (aDP), syn-dechlorane plus (sDP), and octabromotrimethylphenylindane (OBIND) were purchased from Wellington Laboratories Inc. (Guelph, ON, Canada). The analytical grade organic solvents used in this study were purchased from Fisher Scientific (Fair Lawn, NJ, USA).

Sample information

All detailed WWTP characteristics and sampling procedures have been described in previous studies (Kim et al. 2013a, 2014). Briefly, wastewater samples were collected from eight WWTPs and biosolids samples were collected from five WWTPs in three different provinces in Canada (Table 1). Influent and effluent samples were collected at a rate of 200 mL per 15 mins over a 24-hr period using a refrigerated auto sampler (HACH Company, Loveland, CO, USA). Residential inputs comprised more than 50% of the total influent flow whereas the sum of the industrial, commercial, and institutional inputs comprised less than 50%. Average water flow ranged from 700 to over 400,000 m3 day−1. With respect to treatment processes, the eight WWTPs consisted of three secondary treatment (ST) plants, one chemically assisted primary treatment (PT) plant, two aerated lagoons (AL), one facultative lagoon (FL), and one advanced treatment (AT) biological nutrient removal (AT) plant. PT is usually the first stage of wastewater treatment, which is designed to remove suspended solids from raw influent, and removes approximately 40% to 50% of the suspended solids and 30% to 40% of the BOD (biochemical oxygen demand) in the wastewater. ST removes the dissolved organic matter via biological treatment processes followed by settling tanks to remove suspended solids, resulting in a BOD removal of at least 90%. Tertiary treatment includes removal of nutrient (nitrogen and phosphorus), and additional suspended solids. Disinfection with chlorine or by ultraviolet radiation can be the final step prior to discharge of the effluent. Lagoons are an efficient and cost-effective system for wastewater treatment extensively utilized in small communities with a population of <2,000 (Lishman et al. 2006; Holeton et al. 2011; Woudneh et al. 2015). Treatment in lagoons is through a combination of physical, biological, and chemical processes. Although most of the treatment occurs naturally, some systems are equipped with aeration devices to increase the amount of oxygen in the wastewater. Sludge treatment types include digestion (aerobic/mesophilic anaerobic), dewatering, and alkaline stabilization; the treated biosolids from WWTPs are sent for land application to fertilize crops and can improve the quality of soil (Andrade et al. 2010). Sampling at all plants was conducted on three consecutive days once per year for the last three years to study annual variation, while two plants were selected to be sampled twice per year (again on three consecutive days) to investigate seasonal difference.

Table 1

Liquid and solid treatment processes for eight Canadian WWTPs (samples collected between 2013 and 2016)

WWTPs Liquid treatment type Solids treatment type Percent industrial/commercial/institutional inputs 
Secondary activated sludge Alkaline 10 
HG Secondary activated sludge Aerobic digestion 10 
Secondary activated sludge Mesophilic anaerobic digestion 50 
Facultative lagoon None 
Advanced biological nutrient removal with filtration Dewatering 20 
Primary with chemical addition Dewatering 30 
Aerated lagoon None 10 
TB Aerated lagoon None 
WWTPs Liquid treatment type Solids treatment type Percent industrial/commercial/institutional inputs 
Secondary activated sludge Alkaline 10 
HG Secondary activated sludge Aerobic digestion 10 
Secondary activated sludge Mesophilic anaerobic digestion 50 
Facultative lagoon None 
Advanced biological nutrient removal with filtration Dewatering 20 
Primary with chemical addition Dewatering 30 
Aerated lagoon None 10 
TB Aerated lagoon None 

Sample pre-treatment, wastewater

Each wastewater sample (approximately 0.6 L and 1.6 L of sample for influent and effluent, respectively) was spiked with 100 ng of BDE-71 as a recovery standard or surrogate, and extracted sequentially with dichloromethane (DCM, 100 mL, 50 mL, and 50 mL) by liquid–liquid extraction. Following each extraction, the organic layers were dried over anhydrous Na2SO4 (granular certified ACS, fired in a 600 °C muffle furnace overnight) and combined. If emulsion was present, the emulsion layer was removed and centrifuged for 10 min at 2,500 rpm and 24 °C to isolate the organic layer, which was subsequently added to the existing extracts. The combined extract was solvent-exchanged to iso-octane and concentrated to approximately 1 mL using a rotary evaporator followed by evaporation with nitrogen. One laboratory blank (deionized water, no standards spiked) and spiked blank (target standards spiked in influent sample) was included for every six-sample batch. Individual samples, laboratory blanks and spiked blanks were spiked with BDE-71. Laboratory blanks reflected extraneous FRs present in the laboratory environment while spiked blanks accounted for matrix effects. It is acknowledged that labeled surrogate standards are now available for many of the analytes targeted in our schema, which is an approach we fully advocate; however, use of BDE-71 was standard practice during the period of time we began our method development.

Sample pre-treatment, biosolids

Approximately 1 g of biosolids sample was ground with 15 g of anhydrous Na2SO4 to a homogenous mixture. This solid mixture was transferred to a centrifuge tube, spiked with 100 ng of BDE-71 as a recovery standard, and then 25 mL of hexane:acetone (1:1) was added as the extraction solvent. The mixture was vortexed for 30 min at 2,500 rpm then centrifuged for 10 min at 2,000 rpm at 24 °C. The supernatant was collected and the remaining solid mixture was extracted twice more using the same vortex/centrifuge procedure. The combined extract was solvent-exchanged to iso-octane and reduced in volume to about 1 mL using a rotary evaporator followed by evaporation with nitrogen.

Column clean-up

Liquid and solid extracts were further pre-treated using an open column cleanup. A chromatography column was prepared containing 10 g of 5% deactivated silica gel (dried at 160 °C overnight prior to the deactivation), which was rinsed and saturated with hexane and topped with 2 g of anhydrous Na2SO4. The concentrated extract was loaded onto the column and eluted with an additional 45 mL of a 1:1 mixture of hexane:ethyl acetate. The extract was solvent exchanged into iso-octane and concentrated to 1 mL using a rotary evaporator followed by evaporation with nitrogen; the extracts were analyzed using GC with tandem mass spectrometry (MS/MS).

Instrumental parameters

All sample extracts were analyzed using an Agilent 7890A GC system equipped with an Agilent 7693 auto-sampler and interfaced with an Agilent 7000A Triple Quadrupole or tandem Mass Spectrometer (GC-EI-MS/MS, Agilent Technologies, Foster City, USA). Separation of flame retardants was achieved with a fused silica DB-5 HT capillary column (15 m, 0.25 mm i.d., 0.1 μm film thickness; J&W Scientific, CA, USA) with a constant flow rate of 1 mL/min. The injection was performed with 2 μL at pulsed splitless mode and the inlet temperature was set to 300 °C. The GC temperature program was as follows: hold at 80 °C for 1 min, then increase to 300 °C at 22 °C min−1 and hold for 7.5 min. Under multiple reaction monitoring scan type, primary and secondary ions (m/z) were used for quantification and confirmation of flame retardants in the samples, respectively. The MRM transitions and instrumental detection limits for the 31 flame retardants are shown in Table 2.

Table 2

Instrumental detection limit and optimized GC-EI-MS-MS multiple reaction monitoring transitions for flame retardants and the average percent recovery (n = 30) of spike blanks containing flame retardant standards

Flame retardants CAS number Detection limit (ng/L)  % Recovery ±15 Precursor ion Primary ion (Quantifier) Secondary ion (Qualifier) 
BDE17 147217-75-2 0.0058 110 406.0 248.0 246.0 
BDE 28 41318-75-6 0.0031 110 406.0 248.0 246.0 
BDE 33 NA 0.0031 110 406.0 248.0 246.0 
BDE47 5436-43-1 0.0067 122 486.0 328.0 326.0 
BDE66 189084-61-5 0.0041 114 486.0 328.0 326.0 
BDE85 182346-21-0 0.0026 113 564.0 406.0 404.0 
BDE99 60348-60-9 0.0049 101 564.0 406.0 404.0 
BDE100 189084-64-8 0.0034 99 564.0 406.0 404.0 
BB101 67888-96-4 0.0023 111 468.7 389.6 387.7 
BDE138 182677-30-1 0.0036 110 484.0 377.0 324.0 
BDE153 68631-49-2 0.0032 106 484.0 377.0 375.0 
BDE154 207122-15-4 0.0033 112 484.0 377.0 375.0 
BDE183 207122-16-5 0.0023 105 562.0 455.0 402.0 
BDE190 189084-68-2 0.0019 111 562.0 455.0 453.0 
BDE209 1163-19-5 0.0027 112 799.0 642.0 639.0 
ATE 3278-89-5 0.0062 73 329.6 300.8 221.9 
BATE NA 0.0040 96 326.5 248.1 220.2 
BTBPE 37853-59-1 0.0045 96 359.0 254.0 252.0 
DPTE 35109-60-5 0.0058 99 327.8 220.9 219.9 
HBB 87-82-1 0.0036 106 555.8 395.8 393.6 
OBIND 155613-93-7 0.0074 118 772.1 453.7 451.9 
PBBA 59447-55-1 0.0055 104 476.5 368.1 367.6 
PBBE 608-90-2 0.0018 106 471.9 313.4 232.9 
PBEB 85-22-3 0.0017 110 500.0 342.0 340.0 
PBTO 87-83-2 0.0027 116 483.8 324.7 244.9 
PTBX 23488-38-2 0.0053 83 419.8 341.0 259.8 
TBPH 26040-51-7 0.0060 107 462.8 378.5 310.8 
TBB 183658-27-7 0.0085 107 418.6 390.6 311.7 
aDP 135821-74-8 0.0080 97 345.1 236.0 231.0 
sDP 135821-74-8 0.0045 117 345.2 236.1 231.1 
TBCT 39569-21-6 0.0019 100 445.9 204.5 203.0 
Flame retardants CAS number Detection limit (ng/L)  % Recovery ±15 Precursor ion Primary ion (Quantifier) Secondary ion (Qualifier) 
BDE17 147217-75-2 0.0058 110 406.0 248.0 246.0 
BDE 28 41318-75-6 0.0031 110 406.0 248.0 246.0 
BDE 33 NA 0.0031 110 406.0 248.0 246.0 
BDE47 5436-43-1 0.0067 122 486.0 328.0 326.0 
BDE66 189084-61-5 0.0041 114 486.0 328.0 326.0 
BDE85 182346-21-0 0.0026 113 564.0 406.0 404.0 
BDE99 60348-60-9 0.0049 101 564.0 406.0 404.0 
BDE100 189084-64-8 0.0034 99 564.0 406.0 404.0 
BB101 67888-96-4 0.0023 111 468.7 389.6 387.7 
BDE138 182677-30-1 0.0036 110 484.0 377.0 324.0 
BDE153 68631-49-2 0.0032 106 484.0 377.0 375.0 
BDE154 207122-15-4 0.0033 112 484.0 377.0 375.0 
BDE183 207122-16-5 0.0023 105 562.0 455.0 402.0 
BDE190 189084-68-2 0.0019 111 562.0 455.0 453.0 
BDE209 1163-19-5 0.0027 112 799.0 642.0 639.0 
ATE 3278-89-5 0.0062 73 329.6 300.8 221.9 
BATE NA 0.0040 96 326.5 248.1 220.2 
BTBPE 37853-59-1 0.0045 96 359.0 254.0 252.0 
DPTE 35109-60-5 0.0058 99 327.8 220.9 219.9 
HBB 87-82-1 0.0036 106 555.8 395.8 393.6 
OBIND 155613-93-7 0.0074 118 772.1 453.7 451.9 
PBBA 59447-55-1 0.0055 104 476.5 368.1 367.6 
PBBE 608-90-2 0.0018 106 471.9 313.4 232.9 
PBEB 85-22-3 0.0017 110 500.0 342.0 340.0 
PBTO 87-83-2 0.0027 116 483.8 324.7 244.9 
PTBX 23488-38-2 0.0053 83 419.8 341.0 259.8 
TBPH 26040-51-7 0.0060 107 462.8 378.5 310.8 
TBB 183658-27-7 0.0085 107 418.6 390.6 311.7 
aDP 135821-74-8 0.0080 97 345.1 236.0 231.0 
sDP 135821-74-8 0.0045 117 345.2 236.1 231.1 
TBCT 39569-21-6 0.0019 100 445.9 204.5 203.0 

Quality assurance and quality control

Three main quality control criteria were used to confirm the correct identification of the target flame retardants: (i) the GC retention times of FRs must be matched within ±0.1 min of standards, (ii) the ratio between the quantifier (primary) and qualifier (secondary) ions must be within ±15% of the theoretical values, and (iii) the signal to noise ratio must be greater than 5 and the recovery of the surrogate (spiked in samples and blanks prior to extraction), BDE 71, must be greater than 75%. One spike blank (containing flame retardants standards) and one laboratory blank were included for every six samples. No target analytes were detected in the laboratory blanks and the recovery range of the spike blanks (n = 30) was between 73% and 117% (Table 2). The instrumental limits of detection (Table 2) and quantification were defined as the amount of analyte that resulted in signal to noise ratio of 3:1 and 10:1, respectively. Quantification was performed based on an external calibration method containing at least six standard levels, covering a dynamic range of five orders of magnitude with correlation coefficient greater than R2 > 0.991.

Statistical analyses

Statistical analyses were carried out using SPSS 23.0 (IBM Corporation, USA) and Minitab 17 (Minitab Inc., PA, USA). The Shapiro–Wilk normality test showed that the data sets were not normally distributed and thus statistical data analysis was conducted using nonparametric methods such as the Mann–Whitney U test and the Kruskal–Wallis tests. Statistical significance was set as p < 0.05 unless otherwise specified.

RESULTS

Overview of flame retardants analysis

In total, 31 flame retardants, including PBDEs and nFRs, were analyzed in 93 influent, 93 effluent, and 58 biosolids samples collected over three years (2013–2015) from eight WWTPs in Canada. Of all target flame retardants analyzed, PBDE congeners 47, 99, 100, 153, 154, and 209 and the nFRs, TBPH, BTBPE, TBB, and DP were detected frequently in the samples; their median, percentile, and maximum concentration values are shown in Table 3. In addition, the concentration ranges for all flame retardants from the eight WWTPs can be found in Tables 4 and 5. Moreover, removal efficiency of total PBDEs and nFRs in wastewater samples from different types of liquid treatment processes was investigated (Figure 1) and correlations between seasonal, annual, and input variations were also examined.

Table 3

Statistical results of the most frequently detected PBDEs and nFRs in influent, effluent, and biosolids samples from eight WWTPs in Canada; units of median, maximum, 25th and 75th percentiles values for liquid and solid samples are in ng L−1 and ng g−1 dw (dry weight), respectively. The total number of samples analyzed is shown in parentheses

 BDE47 BDE99 BDE100 BDE153 BDE154 BDE209 BTBPE TBB TBPH Total DP 
Influent (93) 
 Number of detects 93 93 93 79 93 93 93 93 76 93 
 25 percentile 25 22 20 67 40 39 
 Median 39 42 10 44 119 85 73 
 75 percentile 51 60 12 86 163 139 116 
 Maximum 79 126 38 14 18 443 25 477 326 247 
Effluent (93) 
 Number of detects 63 84 83 25 72 51 50 83 53 93 
 25 percentile 0.8 0.3 0.2 0.1 0.4 10 
 Median 0.8 0.2 0.4 0.7 10 27 
 75 percentile 0.4 0.7 12 19 42 
 Maximum 14 15 34 29 44 139 
Biosolids (58) 
 Number of detects 52 58 58 49 48 58 50 58 49 58 
 25 percentile 179 127 34 12 19 153 112 149 222 
 Median 276 319 56 29 28 395 181 279 340 
 75 percentile 365 458 73 43 41 641 14 402 710 443 
 Maximum 731 954 139 85 91 4,541 54 1,227 1,820 740 
 BDE47 BDE99 BDE100 BDE153 BDE154 BDE209 BTBPE TBB TBPH Total DP 
Influent (93) 
 Number of detects 93 93 93 79 93 93 93 93 76 93 
 25 percentile 25 22 20 67 40 39 
 Median 39 42 10 44 119 85 73 
 75 percentile 51 60 12 86 163 139 116 
 Maximum 79 126 38 14 18 443 25 477 326 247 
Effluent (93) 
 Number of detects 63 84 83 25 72 51 50 83 53 93 
 25 percentile 0.8 0.3 0.2 0.1 0.4 10 
 Median 0.8 0.2 0.4 0.7 10 27 
 75 percentile 0.4 0.7 12 19 42 
 Maximum 14 15 34 29 44 139 
Biosolids (58) 
 Number of detects 52 58 58 49 48 58 50 58 49 58 
 25 percentile 179 127 34 12 19 153 112 149 222 
 Median 276 319 56 29 28 395 181 279 340 
 75 percentile 365 458 73 43 41 641 14 402 710 443 
 Maximum 731 954 139 85 91 4,541 54 1,227 1,820 740 
Table 4

The detected concentration ranges for polybrominated diphenyl ethers (PBDEs) in influent (ng L−1), effluent (ng L−1), and biosolids (ng g−1) samples from eight Canadian wastewater treatment plants, not detected (n.d) is below the instrumental detection limit (Table 2)

WWTPs BDE17 BDE28 = 33 BDE47 BDE66 BDE85 BDE99 BDE100 BB101 BDE138 BDE153 BDE154 BDE183 BDE190 BDE209 
Plant F 
 Influent n.d n.d 38.6–55.3 n.d 1.85–3.9 50.0–100.0 8.4–18.4 n.d n.d–0.6 3.0–6.5 3.6–10.5 n.d n.d 11.0–327.1 
 Effluent n.d n.d n.d–11.8 n.d n.d–0.49 1.1–14.5 0.6–2.8 n.d n.d–0.1 0.4–0.7 n.d–1.5 n.d n.d n.d–7.0 
 Biosolids n.d n.d 46.0–550.2 n.d n.d 11.4–625.9 10.1–98.8 n.d 1.4–2.8 3.9–47.3 3.1–54.7 n.d n.d–0.2 12.3–786.0 
Plant HG 
 Influent n.d n.d 13.5–78.7 n.d 0.7–5.9 17.9–126.0 3.2–33.1 n.d n.d–3.2 1.3–14.0 0.7–18.0 n.d n.d 7.1–124.6 
 Effluent n.d nd n.d–0.9 n.d n.d n.d–0.89 n.d–1.0 n.d n.d n.d–0.7 n.d–0.66 n.d n.d n.d–2.0 
 Biosolids n.d–28.0 n.d–11.5 88.7–730.5 n.d n.d–16.2 75.1–954.1 18.3–139.0 n.d 3.2–8.4 5.5–34.4 6.4–91.2 n.d n.d 25.3–4541.3 
Plant Q 
 Influent n.d n.d 9.3–43.6 n.d n.d–2.7 0.4–59.4 2.9–11.5 n.d n.d–0.6 0.8–4.3 0.8–4.3 n.d n.d 9.6–123.8 
 Effluent n.d n.d n.d–4.0 n.d n.d–2.6 0.2–8.7 0.2–1.4 n.d n.d n.d–0.4 0.1–2.5 n.d n.d n.d–33.6 
 Biosolids n.d–8.8  n.d–9.0 67.6–538.6 n.d n.d–18.25 17.1–621.1 9.0–99.9 n.d n.d–4.5 n.d–49.6 16.3–55.4 n.d n.d 78.8–1404.0 
Plant J 
 Influent n.d n.d 19.5–56.5 n.d 0.6–2.8 0.9–70.9 3.9–13.1 n.d n.d–0.5 2.0–7.9 0.8–7.9 n.d n.d 22.6–139.6 
 Effluent n.d n.d n.d–1.9 n.d n.d n.d–0.4 n.d–1.2 n.d n.d n.d–0.7 n.d–0.7 n.d n.d n.d–2.2 
Plant E 
 Influent n.d n.d 20.8–70.8 n.d 2.5–8.3 n.d–83.9 1.3–17.1 n.d n.d 0.4–4.4 0.9–7.1 n.d n.d 21.1–307.7 
 Effluent n.d n.d n.d–1.3 n.d n.d–0.2 n.d–1.5 n.d–0.8 n.d n.d n.d–0.3 n.d–0.3 n.d n.d n.d–1.4 
 Biosolids n.d n.d 158.7–533.9 n.d n.d–16.1 212.3–629.1 41.1–95.9 n.d n.d–4.0 21.8– 41.4 14.5–50.4 n.d n.d 386.5–2620.3 
Plant U 
 Influent n.d n.d 12.8–39.2 n.d 0.4–16.2 0.6–42.4 2.6–9.8 n.d n.d 0.8–3.6 1.1–3.8 n.d n.d 5.9–129.7 
 Effluent n.d n.d 2.4–12.2 n.d n.d–11.8 0.6–14.8 0.7–3.4 n.d n.d 0.4–1.1 0.3–1.4 n.d n.d n.d–11.2 
 Biosolids n.d n.d n.d–166.0 n.d n.d 8.7–187.3 2.7–34.5 n.d n.d–1.3 1.2–13.5 3.4–18.5 n.d n.d 8.3–544.6 
Plant R 
 Influent n.d n.d 20.6–70.6 n.d 0.3–6.0 1.3–93.7 4.8–38.1 n.d n.d 0.3–7.4 2.1–11.8 n.d n.d 7.7–197.0 
 Effluent n.d n.d n.d–2.0 n.d n.d n.d–2.0 0.2–1.1 n.d n.d n.d–0.2 n.d–0.1 n.d n.d n.d–1.9 
Plant TB 
 Influent n.d n.d 23.4–224.9 n.d 0.9–2.6 0.9–94.5 6.3–24.7 n.d n.d–0.5 0.23–7.2 0.6–5.4 n.d n.d 27.1–443.7 
 Effluent n.d n.d n.d–9.2 n.d n.d–0.5 3.2–14.7 0.9–2.6 n.d n.d–0.1 n.d –.4 n.d–1.5 n.d n.d n.d–32.3 
WWTPs BDE17 BDE28 = 33 BDE47 BDE66 BDE85 BDE99 BDE100 BB101 BDE138 BDE153 BDE154 BDE183 BDE190 BDE209 
Plant F 
 Influent n.d n.d 38.6–55.3 n.d 1.85–3.9 50.0–100.0 8.4–18.4 n.d n.d–0.6 3.0–6.5 3.6–10.5 n.d n.d 11.0–327.1 
 Effluent n.d n.d n.d–11.8 n.d n.d–0.49 1.1–14.5 0.6–2.8 n.d n.d–0.1 0.4–0.7 n.d–1.5 n.d n.d n.d–7.0 
 Biosolids n.d n.d 46.0–550.2 n.d n.d 11.4–625.9 10.1–98.8 n.d 1.4–2.8 3.9–47.3 3.1–54.7 n.d n.d–0.2 12.3–786.0 
Plant HG 
 Influent n.d n.d 13.5–78.7 n.d 0.7–5.9 17.9–126.0 3.2–33.1 n.d n.d–3.2 1.3–14.0 0.7–18.0 n.d n.d 7.1–124.6 
 Effluent n.d nd n.d–0.9 n.d n.d n.d–0.89 n.d–1.0 n.d n.d n.d–0.7 n.d–0.66 n.d n.d n.d–2.0 
 Biosolids n.d–28.0 n.d–11.5 88.7–730.5 n.d n.d–16.2 75.1–954.1 18.3–139.0 n.d 3.2–8.4 5.5–34.4 6.4–91.2 n.d n.d 25.3–4541.3 
Plant Q 
 Influent n.d n.d 9.3–43.6 n.d n.d–2.7 0.4–59.4 2.9–11.5 n.d n.d–0.6 0.8–4.3 0.8–4.3 n.d n.d 9.6–123.8 
 Effluent n.d n.d n.d–4.0 n.d n.d–2.6 0.2–8.7 0.2–1.4 n.d n.d n.d–0.4 0.1–2.5 n.d n.d n.d–33.6 
 Biosolids n.d–8.8  n.d–9.0 67.6–538.6 n.d n.d–18.25 17.1–621.1 9.0–99.9 n.d n.d–4.5 n.d–49.6 16.3–55.4 n.d n.d 78.8–1404.0 
Plant J 
 Influent n.d n.d 19.5–56.5 n.d 0.6–2.8 0.9–70.9 3.9–13.1 n.d n.d–0.5 2.0–7.9 0.8–7.9 n.d n.d 22.6–139.6 
 Effluent n.d n.d n.d–1.9 n.d n.d n.d–0.4 n.d–1.2 n.d n.d n.d–0.7 n.d–0.7 n.d n.d n.d–2.2 
Plant E 
 Influent n.d n.d 20.8–70.8 n.d 2.5–8.3 n.d–83.9 1.3–17.1 n.d n.d 0.4–4.4 0.9–7.1 n.d n.d 21.1–307.7 
 Effluent n.d n.d n.d–1.3 n.d n.d–0.2 n.d–1.5 n.d–0.8 n.d n.d n.d–0.3 n.d–0.3 n.d n.d n.d–1.4 
 Biosolids n.d n.d 158.7–533.9 n.d n.d–16.1 212.3–629.1 41.1–95.9 n.d n.d–4.0 21.8– 41.4 14.5–50.4 n.d n.d 386.5–2620.3 
Plant U 
 Influent n.d n.d 12.8–39.2 n.d 0.4–16.2 0.6–42.4 2.6–9.8 n.d n.d 0.8–3.6 1.1–3.8 n.d n.d 5.9–129.7 
 Effluent n.d n.d 2.4–12.2 n.d n.d–11.8 0.6–14.8 0.7–3.4 n.d n.d 0.4–1.1 0.3–1.4 n.d n.d n.d–11.2 
 Biosolids n.d n.d n.d–166.0 n.d n.d 8.7–187.3 2.7–34.5 n.d n.d–1.3 1.2–13.5 3.4–18.5 n.d n.d 8.3–544.6 
Plant R 
 Influent n.d n.d 20.6–70.6 n.d 0.3–6.0 1.3–93.7 4.8–38.1 n.d n.d 0.3–7.4 2.1–11.8 n.d n.d 7.7–197.0 
 Effluent n.d n.d n.d–2.0 n.d n.d n.d–2.0 0.2–1.1 n.d n.d n.d–0.2 n.d–0.1 n.d n.d n.d–1.9 
Plant TB 
 Influent n.d n.d 23.4–224.9 n.d 0.9–2.6 0.9–94.5 6.3–24.7 n.d n.d–0.5 0.23–7.2 0.6–5.4 n.d n.d 27.1–443.7 
 Effluent n.d n.d n.d–9.2 n.d n.d–0.5 3.2–14.7 0.9–2.6 n.d n.d–0.1 n.d –.4 n.d–1.5 n.d n.d n.d–32.3 
Table 5

The detected concentration ranges for novel brominated and chlorinated flame retardants in influent (ng L−1), effluent (ng L−1), and biosolids (ng g−1) samples from eight Canadian wastewater treatment plants, not detected (n.d) is below the instrumental detection limit (Table 2)

WWTPs ATE BATE BTBPE DPTE HBB OBIND PBBA PBBE PBEB PBTO PTBX TBB TBPH Total DP TBCT 
Plant F 
 Influent n.d n.d 2.3–6.1 n.d n.d n.d n.d n.d n.d n.d n.d 155.4–289.7 77.0–174.0 29.0–173.5 n.d 
 Effluent n.d n.d n.d–1.0 n.d n.d n.d n.d n.d n.d n.d n.d 5.4–29.2 6.8–54.0 6.8–54.0 n.d 
 Biosolids n.d n.d n.d–11.0 n.d n.d n.d n.d n.d n.d n.d n.d 72.3–1,226.8 n.d–384.8 163.9–384.8 n.d 
Plant HG 
 Influent n.d n.d 1.2–13.1 n.d n.d n.d n.d n.d n.d n.d n.d 44.2–172.6 37.6–180.0 18.4–146.6 n.d 
 Effluent n.d n.d n.d–0.9 n.d n.d n.d n.d n.d n.d n.d n.d n.d–1.5 n.d–8.0 2.0–49.5 n.d 
 Biosolids n.d n.d n.d–23.4 n.d n.d n.d n.d n.d n.d n.d n.d 5.4–540.1 n.d–1,820.3 219.0–739.6 n.d 
Plant Q 
 Influent n.d n.d 0.6–8.5 n.d n.d n.d n.d n.d n.d n.d n.d 14.8–141.6 0.4–180.1 29.3–212.7 n.d 
 Effluent n.d n.d n.d–1.8 n.d n.d n.d n.d n.d n.d n.d n.d 1.0–11.3 n.d–19.3 10.4–95.6 n.d 
 Biosolids n.d n.d n.d–54.2 n.d n.d n.d n.d n.d n.d n.d n.d 92.3–910.2 n.d–1,315.9 171.4–623.4 n.d 
Plant J 
 Influent n.d n.d 0.5–4.2 n.d n.d n.d n.d n.d n.d n.d n.d 51.9–476.8 1.8–272.9 55.9–99.7 n.d 
 Effluent n.d n.d n.d–0.5 n.d n.d n.d n.d n.d n.d n.d n.d n.d–3.0 n.d 22.2–33.2 n.d 
Plant E 
 Influent n.d n.d 2.8–3.2 n.d n.d n.d n.d n.d n.d n.d n.d 113.2–222.2 2.3–325.9 35.9–78.4 n.d 
 Effluent n.d n.d n.d–0.6 n.d n.d n.d n.d n.d n.d n.d n.d n.d–4.7 n.d–8.8 7.8–49.9 n.d 
 Biosolids n.d n.d n.d–24.4 n.d n.d n.d n.d n.d n.d n.d n.d 123.2–1,019.8 n.d–993.6 153.5–515.6 n.d 
Plant U 
 Influent n.d n.d 0.6–9.0 n.d n.d n.d n.d n.d n.d n.d n.d 11.2–87.6 10.2–172.9 17.2–177.9 n.d 
 Effluent n.d n.d n.d–6.9 n.d n.d n.d n.d n.d n.d n.d n.d 4.6–23.9 n.d–21.5 8.4–103.8 n.d 
 Biosolids n.d n.d n.d–8.9 n.d n.d n.d n.d n.d n.d n.d n.d 23.3–333.0 n.d–254.2 96.4–458.2 n.d 
Plant R 
 Influent n.d n.d 5.3–20.2 n.d n.d n.d n.d n.d n.d n.d n.d 81.7–351.4 35.9–231.7 25.2–201.7 n.d 
 Effluent n.d n.d n.d–1.4 n.d n.d n.d n.d n.d n.d n.d n.d 0.5–5.5 n.d–16.1 3.9–31.4 n.d 
Plant TB 
 Influent n.d n.d 1.3–12.1 n.d n.d n.d n.d n.d n.d n.d n.d 13.2–163.4 7.7–166.0 26.8–246.6 n.d 
 Effluent n.d n.d n.d–3.2 n.d n.d n.d n.d n.d n.d n.d n.d 0.2–21.0 n.d–44.3 4.3–138.6 n.d 
WWTPs ATE BATE BTBPE DPTE HBB OBIND PBBA PBBE PBEB PBTO PTBX TBB TBPH Total DP TBCT 
Plant F 
 Influent n.d n.d 2.3–6.1 n.d n.d n.d n.d n.d n.d n.d n.d 155.4–289.7 77.0–174.0 29.0–173.5 n.d 
 Effluent n.d n.d n.d–1.0 n.d n.d n.d n.d n.d n.d n.d n.d 5.4–29.2 6.8–54.0 6.8–54.0 n.d 
 Biosolids n.d n.d n.d–11.0 n.d n.d n.d n.d n.d n.d n.d n.d 72.3–1,226.8 n.d–384.8 163.9–384.8 n.d 
Plant HG 
 Influent n.d n.d 1.2–13.1 n.d n.d n.d n.d n.d n.d n.d n.d 44.2–172.6 37.6–180.0 18.4–146.6 n.d 
 Effluent n.d n.d n.d–0.9 n.d n.d n.d n.d n.d n.d n.d n.d n.d–1.5 n.d–8.0 2.0–49.5 n.d 
 Biosolids n.d n.d n.d–23.4 n.d n.d n.d n.d n.d n.d n.d n.d 5.4–540.1 n.d–1,820.3 219.0–739.6 n.d 
Plant Q 
 Influent n.d n.d 0.6–8.5 n.d n.d n.d n.d n.d n.d n.d n.d 14.8–141.6 0.4–180.1 29.3–212.7 n.d 
 Effluent n.d n.d n.d–1.8 n.d n.d n.d n.d n.d n.d n.d n.d 1.0–11.3 n.d–19.3 10.4–95.6 n.d 
 Biosolids n.d n.d n.d–54.2 n.d n.d n.d n.d n.d n.d n.d n.d 92.3–910.2 n.d–1,315.9 171.4–623.4 n.d 
Plant J 
 Influent n.d n.d 0.5–4.2 n.d n.d n.d n.d n.d n.d n.d n.d 51.9–476.8 1.8–272.9 55.9–99.7 n.d 
 Effluent n.d n.d n.d–0.5 n.d n.d n.d n.d n.d n.d n.d n.d n.d–3.0 n.d 22.2–33.2 n.d 
Plant E 
 Influent n.d n.d 2.8–3.2 n.d n.d n.d n.d n.d n.d n.d n.d 113.2–222.2 2.3–325.9 35.9–78.4 n.d 
 Effluent n.d n.d n.d–0.6 n.d n.d n.d n.d n.d n.d n.d n.d n.d–4.7 n.d–8.8 7.8–49.9 n.d 
 Biosolids n.d n.d n.d–24.4 n.d n.d n.d n.d n.d n.d n.d n.d 123.2–1,019.8 n.d–993.6 153.5–515.6 n.d 
Plant U 
 Influent n.d n.d 0.6–9.0 n.d n.d n.d n.d n.d n.d n.d n.d 11.2–87.6 10.2–172.9 17.2–177.9 n.d 
 Effluent n.d n.d n.d–6.9 n.d n.d n.d n.d n.d n.d n.d n.d 4.6–23.9 n.d–21.5 8.4–103.8 n.d 
 Biosolids n.d n.d n.d–8.9 n.d n.d n.d n.d n.d n.d n.d n.d 23.3–333.0 n.d–254.2 96.4–458.2 n.d 
Plant R 
 Influent n.d n.d 5.3–20.2 n.d n.d n.d n.d n.d n.d n.d n.d 81.7–351.4 35.9–231.7 25.2–201.7 n.d 
 Effluent n.d n.d n.d–1.4 n.d n.d n.d n.d n.d n.d n.d n.d 0.5–5.5 n.d–16.1 3.9–31.4 n.d 
Plant TB 
 Influent n.d n.d 1.3–12.1 n.d n.d n.d n.d n.d n.d n.d n.d 13.2–163.4 7.7–166.0 26.8–246.6 n.d 
 Effluent n.d n.d n.d–3.2 n.d n.d n.d n.d n.d n.d n.d n.d 0.2–21.0 n.d–44.3 4.3–138.6 n.d 
Figure 1

Boxplots of removal efficiencies for ΣPBDEs (BDE 47, 99, 100, 153, and 154) and BDE209 via different types of liquid treatments, aerated lagoons (AL), facultative lagoons (FL), primary treatment (PT), secondary treatment (ST), and advanced treatment (AT). Percentiles are shown: minimum, 25th, 75th, and maximum. The horizontal line, dot, and numbers shown next to boxplots are median values.

Figure 1

Boxplots of removal efficiencies for ΣPBDEs (BDE 47, 99, 100, 153, and 154) and BDE209 via different types of liquid treatments, aerated lagoons (AL), facultative lagoons (FL), primary treatment (PT), secondary treatment (ST), and advanced treatment (AT). Percentiles are shown: minimum, 25th, 75th, and maximum. The horizontal line, dot, and numbers shown next to boxplots are median values.

PBDEs

Although octa-BDE and penta-BDE have been banned in use of all applications since 2004, PBDEs have not been fully removed from the environment due to continual release from in-use products. Herein, the percent detection of frequently found PBDE congeners, the penta-BDE mixture (47, 99, 100, 153, and 154) and the major deca-BDE (209), in the influent wastewater samples was 100%, 100%, 100%, 85%, 100%, and 100%, respectively. The total concentration of ΣPBDE (BDE 47, 99, 100, 153, and 154) ranged from 39 to 262 ng L−1 in influent and from not detected (nd) to 33 ng L−1 in effluent, while the concentrations of BDE 209 ranged from 6 to 443 ng L−1 in influent and from not detected to 34 ng L−1 in effluent samples. The total concentration of ΣPBDE from this study is comparable with a previous study (Kim et al. 2013a) in which ΣPBDE (BDE 47, 99, 100, 153, 154, and 209) in influent and effluent collected from 20 Canadian WWTPs ranged from 21 to 1,000 ng L−1 and from 3 to 270 ng L−1, respectively.

Removal efficiencies of total PBDEs and BDE 209 in wastewater by various treatment types, including AL, FL, PT, ST, and AT are presented in Figure 1. Greater than 94% median removal efficiencies of PBDEs were observed in AL, FL, ST, and AT, while the PT rendered a median of 70% removal. Similarly, greater than 96% median removal efficiencies of BDE 209 were observed in AL, FL, ST, and AT, while there was removal of a median of 86% in the PT. However, PBDE removal rates can be strongly influenced by environmental and operational factors, such as season (summer vs. winter water temperatures), treatment type (biological vs. physical/chemical), size (urban with residential and industrial contributions vs. semi-rural with only residential contributions), and configurations and process complexity (aerobic treatment only vs. aerobic/anoxic/anaerobic treatment); a recent study investigated the influence of these factors on PBDE removal (Kim et al. 2013a). In this study, a higher concentration of ΣPBDE was observed in the influent collected in summer than in winter, while no statistically significant annual variations or domestic vs. industrial input variations were observed over three years (2013–2015, p < 0.05, data not shown).

PBDEs are adsorbed onto suspended solids in wastewater due to their physico-chemical properties such as a high octanol-water partition coefficient (Kow) and a high organic carbon-water partition coefficient (Koc). In this study, 58 treated biosolids samples were collected over a three-year period (2013–2015) from five WWTPs. The percent detection of frequently found PBDE congeners, BDE – 47, 99, 100, 153, 154, and 209, in the biosolids were 90%, 100%, 100%, 84%, 83%, and 100%, respectively as shown in Table 3. The total concentrations of major PBDE congeners in biosolids samples were in the range of 70 to 6,390 ng g−1 dry weight (dw), falling in the range previously reported for North America as shown in Table 6 (Hale et al. 2001; North 2004; Rayne & Ikonomou 2005; Song et al. 2006). In addition, deca-BDE (BDE 209) was the predominant congener found in the wastewater and biosolids samples as shown in Table 6.

Table 6

Comparison of range PBDE concentrations (ng g−1, dry weight) in biosolids from this study (Canadian WWTPs) with those reported in other regions in Canada and United States

Locations BDE47 BDE99 BDE100 BDE153 BDE154 BDE209 ΣPBDE 
Present study (8 WWTPs), Canada 92–731 100–954 16–139 7.0–85 7.0–91 140–4,541 362–6,541 
Windsor STP ON, Canada 407–971 540–1,267 89–211 69–145 36–145 n.d 1,141–2,739a 
Kelowna STP BC, Canada 518 675 103 101 57 n.d 1,455b 
Palo Alto STP CA, USA 722–778 894–973 158–172 83–91 61–72 1,010–1,440 2,928–3,535c 
Samples from Virginia, Mayland, New York and California (11 samples) 359–754 931–1,157 89–255 56–199 58–173 85–4,890 1,578–7,428d 
Locations BDE47 BDE99 BDE100 BDE153 BDE154 BDE209 ΣPBDE 
Present study (8 WWTPs), Canada 92–731 100–954 16–139 7.0–85 7.0–91 140–4,541 362–6,541 
Windsor STP ON, Canada 407–971 540–1,267 89–211 69–145 36–145 n.d 1,141–2,739a 
Kelowna STP BC, Canada 518 675 103 101 57 n.d 1,455b 
Palo Alto STP CA, USA 722–778 894–973 158–172 83–91 61–72 1,010–1,440 2,928–3,535c 
Samples from Virginia, Mayland, New York and California (11 samples) 359–754 931–1,157 89–255 56–199 58–173 85–4,890 1,578–7,428d 

2-ethyl-1-hexyl 2,3,4,5-tetrabromobenzoate (TBB) and bis(2-ethyl-1 hexyl)tetrabromophthalate (TBPH)

TBB and TBPH are two major components in a commercial mixture which is a replacement for penta-BDE in polyurethane foam applications (Houde et al. 2014). Both of these chemicals have been previously detected in house dust, air, and biosolids or sludge samples at concentrations approaching the concentration of PBDEs (Table 7) (Klosterhaus et al. 2008; Stapleton et al. 2008; Covaci et al. 2011; Davis et al. 2012; Lankova et al. 2013; Houde et al. 2014). To the best of our knowledge, this study is the first to report concentrations of TBB and TBPH in influent, effluent, and biosolids samples, as well as their removal efficiency via various types of treatments in Canadian WWTPs. The concentrations of TBB ranged from 11 to 477 ng L−1, nd to 29 ng L−1, and 5 to 1,227 ng g−1 dw, while the concentrations of TBPH ranged from 0.4 to 326 ng L−1, nd to 44 ng L−1, and 56 to 1,820 ng g−1 dw in influent, effluent, and biosolids samples, respectively, as shown in Table 7. The concentrations of TBB and TBPH measured in influent, effluent, and biosolids in this study are comparable to the ranges reported in a previous study from North America, as shown in Table 7 (Schreder & La Guardia 2014).

Table 7

Comparison of concentration ranges of novel brominated flame retardants (BTPBPE, TBB, and TBPH) in wastewater (ng L−1) and biosolids (ng/g, dry weight) samples from Canadian WWTPs in this study with those reported in other regions in Canada, United States and China (house dust, ng g−1 or μg kg−1, dw)

Locations BTBPE TBB TBPH 
Present study (8 WWTPs): Influent 0.6–25 11–477 0.4–326 
Effluent n.d–7 n.d–29 n.d–44 
Biosolid 2.0–54 5.0–1,227 56–1,820 
USA (sewage sludge) no data 120–3,749 206–1,631a 
Lake Ontario surface sediment 2.7–3.8 no data no datab 
China (sewage sludge samples from 21 provinces) 0.1–2.26 no data no datac 
USA (house dust) 1.6–789 6.6–15,030 1.5–10,630d 
Canada (house dust) no data no data 15–22,251e 
Locations BTBPE TBB TBPH 
Present study (8 WWTPs): Influent 0.6–25 11–477 0.4–326 
Effluent n.d–7 n.d–29 n.d–44 
Biosolid 2.0–54 5.0–1,227 56–1,820 
USA (sewage sludge) no data 120–3,749 206–1,631a 
Lake Ontario surface sediment 2.7–3.8 no data no datab 
China (sewage sludge samples from 21 provinces) 0.1–2.26 no data no datac 
USA (house dust) 1.6–789 6.6–15,030 1.5–10,630d 
Canada (house dust) no data no data 15–22,251e 

The mass ratio of TBB/TBPH in a commercial mixture is approximately 4:1; however, among the biosolids samples analyzed the ratio was 1:7. The lower ratio of TBB/TBPH in the biosolids samples suggests contributions from sources other than the commercial mixture. For instance, TBPH is the sole component of a liquid flame retarded plasticizer (Xiao et al. 2012); the use of TBPH in other unknown commercial products could have contributed to the TBPH levels in the biosolids. In addition, the discrepancy ratio of TBB/TBPH in biosolids from this study may suggest different migration or degradation behaviors of TBB relative to TBPH, both in consumer products and during the wastewater treatment process.

Greater than 96% median removal efficiency of TBB was observed for AL, FL, ST, and AT, while the PT rendered a median of 63% removal, presented in Figure 2. In contrast, a median of over 88% removal efficiency of TBPH was observed for PT, AL, FL, ST, and AT. The lower removal efficiency of TBB relative to TBPH in PT may be governed by differences in their physico-chemical properties, including water solubility constant (Log S), octanol-water partition coefficient (Log Kow) and soil organic carbon-normalized adsorption constant (Log KOC). TBB has a higher water solubility constant (Log S: 8.21) but lower octanol-water partition and organic carbon adsorption constants (Log Kow: 8.8 and Log KOC: 5.7) than does TBPH (Log S: 11.6, Log Kow: 12, and Log KOC: 7.4) (Davis et al. 2012, 2015).

Figure 2

Boxplots of removal efficiencies for novel brominated flame retardants (BTBPE, TBB, and TBPH) and chlorinated flame retardant, dechlorane plus (syn- and anti-DP), via different types of liquid treatment processes, aerated lagoons (AL, n = 26), facultative lagoons (FL, n = 8), primary treatment (PT, n = 11), secondary treatment (ST, n = 39), and advanced treatment (AT, n = 9). Percentiles are shown: minimum, 25th, 75th, and maximum. The horizontal line, dot, and numbers shown next to boxplots are median values and asterisks inside the box represent outliers.

Figure 2

Boxplots of removal efficiencies for novel brominated flame retardants (BTBPE, TBB, and TBPH) and chlorinated flame retardant, dechlorane plus (syn- and anti-DP), via different types of liquid treatment processes, aerated lagoons (AL, n = 26), facultative lagoons (FL, n = 8), primary treatment (PT, n = 11), secondary treatment (ST, n = 39), and advanced treatment (AT, n = 9). Percentiles are shown: minimum, 25th, 75th, and maximum. The horizontal line, dot, and numbers shown next to boxplots are median values and asterisks inside the box represent outliers.

1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE)

BTBPE (log Kow ∼ 7.88 ± 0.86) is an additive FR used as a replacement for octa-BDE since 2005 (Covaci et al. 2011). The major applications of BTBPE as an additive are in high impact polystyrene (HIPS), thermoplastics, textiles, acrylonitrile butadiene styrene (ABS), polypropylene, and polycarbonate; estimated worldwide production and usage of BTBPE was approximately 16,710 tons in 2001 (Xiao et al. 2012; Zeng et al. 2014). It was previously reported that BTPBE was frequently detected in the environment, for example, in indoor dust, sludge, sediment, and biota; high concentrations of BTPBE were detected in indoor dust samples in Europe, the United States, and China (octanol-air partition constant, KOA ∼ 15) (Stapleton et al. 2008; Xiao et al. 2012; Yang et al. 2012; Zeng et al. 2014 ; Peng et al. 2015). In this study, the concentrations of BTBPE ranged from 0.6 to 25 ng L−1, nd to 7 ng L−1, and 2–54 ng g−1 dw in influent, effluent, and biosolids samples, respectively (Table 7). It was recently reported that the concentrations of BTBPE found in biosolids samples from 20 different Canadian WWTPs ranged from 0.005 to 140 ng g−1, which was approximately three times higher than the concentrations found in this study. In contrast, the concentrations of BTBPE found in surface sediment from Lake Ontario (2.7 to 3.8 ng g−1) were about an order of magnitude lower than BTBPE concentrations found in biosolids from this study. Furthermore, it was reported that median removal efficiencies of BTBPE across 20 Canadian WWTPs ranged from 61% to 97%, whereas in this study a greater than 85% median removal efficiency of BTPBE was observed in AL, FL, ST, and AT, but the PT removed a median of only 45% of BTPBE as shown in Figure 2.

Dechlorane plus (DP)

Two stereoisomers, syn and anti, are present at an approximate ratio of 1:2, respectively, in the dechlorane plus (DP) technical mixture (De la Torre et al. 2011). It was previously shown that the total DP concentration in suspended sediment samples collected from the Niagara River had been declining, from 89 ng g−1 to 7.0 ng g−1, for over two decades (1980 to 2002) (Qiu et al. 2007; Sverko et al. 2008; De la Torre et al. 2011). However, a recent study reported the presence of DP in the eggs of peregrine falcons nesting in the Canadian Great Lakes and the Maritimes; DP was detected in all eggs with concentration ranging from 6.3 to 209 ng/g lw (lipid weight) (Guerra et al. 2011). The present study investigated the presence of syn- and anti-DP in wastewater and biosolids samples collected over a three-year period. The pre-treated (extraction/column clean up) wastewater and biosolids samples were stored in iso-octane at −20 °C. The percent detection of total DP was greater than 90% in both wastewater and biosolids samples, ranged from 17 to 247 ng L−1, 2 to 139 ng L−1, and 96 to 740 ng g−1 dw in influent, effluent, and biosolids, respectively. Similar to PBDEs, DP also has a relatively high affinity for lipids and solid particles due to its high molecular weight and high log Kow (9.3). Unlike the PBDEs, DP median removal efficiencies were lower and ranged from 51% to 70% for AL, FL, ST, PT, and AT treatment processes as shown in Figure 2. In addition, higher concentrations of total DP were found in influent samples collected in winter relative to summer, whereas no statistically significant correlations were found between total DP concentrations and annual or input variations (p < 0.05, data not shown). Syn-DP not being detected in any of the wastewater or biosolids samples could be due to conversion of syn-DP to anti-DP under extended storage conditions. This hypothesis was tested by analyzing pre-treated influent samples that were only stored for a few days at −20 °C, and syn-DP was detected in those samples. However, the conversion of syn-DP to anti-DP under extended storage conditions and low removal efficiency of DP within different liquid treatment processes in WWTPs will be investigated further.

CONCLUSIONS

This study evaluated the concentrations of PBDEs and novel halogenated flame retardants in wastewater and biosolids samples collected over a three-year period from eight Canadian WWTPs, representing a diverse range of treatment processes including two AL, one facultative lagoon, one PT plant, three ST plants, and one AT plant. Among the 15 PBDEs analyzed, the highest concentrations detected were deca-BDE (BDE-209) in influent and biosolids samples. Furthermore, three novel BFRs, TBPH, BTBPE, and TBB, were frequently detected in influent and biosolids samples, although at lower concentrations than BDE-209. All WWTPs reduced levels of TBB and BTBPE in wastewater; however, the PT process had relatively low removal efficiency for these compounds. In addition, WWTPs did not effectively remove high levels of the DP found in influent and biosolids samples; only 66% median removal of DP was observed in AT. Despite the effective removal of PBDEs in WWTPs, some nFRs, including BTBPE, TBB, and DP, have lower removal rate in WWTPs, which could be due to their physical/chemical properties. Further study is required to investigate conditions that would improve the removal efficiency of these nFRs both in biosolids and in effluent samples prior to discharge to the environment.

ACKNOWLEDGEMENTS

This work was supported by Environment Canada's Chemicals Management Plan (CMP). The authors would like to thank Ed Kaminski and Jeff Small of Environment and Climate Change Canada, Burlington, Ontario for technical support and Amber Albert, Scott Alexander, Eraj Gillani and Steve Teslic for sample collection.

REFERENCES

REFERENCES
Andrade
N. A.
,
Mcconnell
L. L.
,
Torrents
A.
&
Ramirez
M.
2010
Persistence of polybrominated diphenyl ethers in agricultural soils after biosolids applications
.
Journal of Agricultural and Food Chemistry
58
(
5
),
3077
3084
.
Covaci
A.
,
Harrad
S.
,
Abdallah
M. A. E.
,
Ali
N.
,
Law
R. J.
,
Herzke
D.
&
de Wit
C. A.
2011
Novel brominated flame retardants: a review of their analysis, environmental fate and behaviour
.
Environment International
37
(
2
),
532
556
.
Davis
E. F.
,
Klosterhaus
S. L.
&
Stapleton
H. M.
2012
Measurement of flame retardants and triclosan in municipal sewage sludge and biosolids
.
Environment International
40
(
1
),
1
7
.
Davis
E. F.
,
Gunsch
C. K.
&
Stapleton
H. M.
2015
Fate of flame retardants and the antimicrobial agent triclosan in planted and unplanted biosolid-amended soils
.
Environmental Toxicology and Chemistry
34
(
5
),
968
976
.
De la Torre
A.
,
Sverko
E.
,
Alaee
M.
&
Martinez
M. A.
2011
Concentrations and sources of Dechlorane Plus in sewage sludge
.
Chemosphere
82
(
5
),
692
697
.
Guerra
P.
,
Fernie
K.
,
Jimenez
B.
,
Pacepavicius
G.
,
Shen
L.
,
Reiner
E.
&
Alaee
M.
2011
Dechlorane plus and related compounds in peregrine falcon (Falco peregrinus) eggs from Canada and Spain
.
Environmental Science and Technology
45
(
4
),
1284
1290
.
Hale
R. C.
,
La Guardia
M. J.
,
Harvey
E. P.
,
Gaylor
M. O.
,
Mainor
T. M.
&
Duff
W. H.
2001
Flame retardants: persistent pollutants in land-applied sludges
.
Nature
412
,
140
142
.
Holeton
C.
,
Chambers
P. A.
&
Grace
L.
2011
Wastewater release and its impacts on Canadian Waters
.
Canadian Journal of Fisheries and Aquatic Sciences
68
,
1836
1859
.
Houde
M.
,
Berryman
D.
,
De Lafontaine
Y.
&
Verreault
J.
2014
Novel brominated flame retardants and dechloranes in three fish species from the St. Lawrence River, Canada
.
Science of the Total Environment
479
(
480
),
48
56
.
Kim
M.
,
Guerra
P.
,
Theocharides
M.
,
Barclay
K.
,
Smyth
S. A.
&
Alaee
M.
2013a
Parameters affecting the occurrence and removal of polybrominated diphenyl ethers in twenty Canadian wastewater treatment plants
.
Water Research
47
(
7
),
2213
2221
.
Kim
M.
,
Guerra
P.
,
Theocharides
M.
,
Barclay
K.
,
Smyth
S. A.
&
Alaee
M.
2013b
Polybrominated diphenyl ethers in sewage sludge and treated biosolids: effect factors and mass balance
.
Water Research
47
(
17
),
6496
6505
.
Kim
M.
,
Guerra
P.
,
Alaee
M.
&
Smyth
S. A.
2014
Occurrence and fate of four novel brominated flame retardants in wastewater treatment plants
.
Environmental Science and Pollution Research
21
(
23
),
13394
13404
.
Klosterhaus
S.
,
Konstantinov
A.
&
Stapleton
H.
2008
Characterization of the Brominated Chemicals in A PentaBDE Replacement Mixture and Their Detection in Biosolids Collected From Two San Francisco Bay Area Wastewater Treatment Plants
.
Northern California Society of Environmental Toxicology and Chemistry
.
Lishman
L.
,
Smyth
S. A.
,
Sarafin
K.
,
Kleywegt
S.
,
Toito
J.
,
Peart
T.
&
Seto
P.
2006
Occurrence and reductions of pharmaceuticals and personal care products and estrogens by municipal wastewater treatment plants in Ontario, Canada
.
Science of the Total Environment
367
(
2–3
),
544
558
.
Marvin
C. H.
,
Tomy
G. T.
,
Armitage
J. M.
,
Arnot
J. A.
,
McCarty
L.
,
Covaci
A.
&
Palace
V.
2011
Hexabromocyclododecane: current understanding of chemistry, environmental fate and toxicology and implications for global management
.
Environmental Science and Technology
45
,
8613
8623
.
Morf
L. S.
,
Tremp
J.
,
Gloor
R.
,
Huber
Y.
,
Stengele
M.
&
Zennegg
M.
2005
Brominated flame retardants in waste electrical and electronic equipment: substance flows in a recycling plant
.
Environmental Science and Technology
39
(
22
),
8691
8699
.
Papachlimitzou
A.
,
Barber
J. L.
,
Losada
S.
,
Bersuder
P.
&
Law
R. J.
2012
A review of the analysis of novel brominated flame retardants
.
Journal of Chromatography A
1219
,
15
28
.
Peng
H.
,
Saunders
D. M. V.
,
Sun
J.
,
Codling
G.
,
Wiseman
S.
,
Jones
P. D.
&
Giesy
J. P.
2015
Detection, identification, and quantification of hydroxylated bis(2-ethylhexyl)-tetrabromophthalate isomers in house dust
.
Environmental Science and Technology
49
(
5
),
2999
3006
.
Qiu
X.
,
Marvin
C. H.
&
Hites
R. A.
2007
Dechlorane plus and other flame retardants in a sediment core from Lake Ontario
.
Environmental Science and Technology
41
(
17
),
6014
6019
.
Rocha-Gutierrez
B.
&
Lee
W.-Y.
2012
Determination and comparison of polybrominated diphenyl ethers in primary, secondary, and tertiary wastewater treatment plants
.
International Journal of Environmental Analytical Chemistry
92
(
13
),
1518
1531
.
Schreder
E. D.
&
La Guardia
M. J.
2014
Flame retardant transfers from U.S. households (dust and laundry wastewater) to the aquatic environment
.
Environmental Science and Technology
48
(
19
),
11575
11583
.
Stapleton
H. M.
,
Allen
J. G.
,
Kelly
S. M.
,
Konstantinov
A.
,
Klosterhaus
S.
,
Watkins
D.
&
Webster
T. F.
2008
Alternate and new brominated flame retardants detected in U.S. house dust
.
Environmental Science and Technology
42
(
18
),
6910
6916
.
Sverko
E.
,
Tomy
G. T.
,
Marvin
C. H.
,
Zaruk
D.
,
Reiner
E.
,
Helm
P. A.
&
Mccarry
B. E.
2008
Dechlorane plus levels in sediment of the lower Great Lakes
.
Environmental Science and Technology
42
(
2
),
361
366
.
Xiao
H.
,
Shen
L.
,
Su
Y.
,
Barresi
E.
,
Dejong
M.
,
Hung
H.
,
Lei
Y.-D.
,
Wania
F.
,
Reiner
E. J.
,
Sverko
E.
&
Kang
S. C.
2012
Atmospheric concentrations of halogenated flame retardants at two remote locations: the Canadian high Arctic and the Tibetan plateau
.
Environmental Pollution
161
,
154
161
.
Yang
R.
,
Wei
H.
,
Guo
J.
&
Li
A.
2012
Emerging brominated flame retardants in the sediment of the Great Lakes
.
Environmental Science and Technology
46
(
6
),
3119
3126
.