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An international survey of decabromodiphenyl ethane (deBDethane) and decabromodiphenyl ether (decaBDE) in sewage sludge samples
Chemosphere 73 (2008) 1799–1804
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Chemosphere journal homepage: www.elsevier.com/locate/chemosphere
An international survey of decabromodiphenyl ethane (deBDethane) and decabromodiphenyl ether (decaBDE) in sewage sludge samples Niklas Ricklund *, Amelie Kierkegaard, Michael S. McLachlan Department of Applied Environmental Science (ITM), Stockholm University, SE-10691 Stockholm, Sweden
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Article history: Received 24 June 2008 Received in revised form 25 August 2008 Accepted 26 August 2008 Available online 14 October 2008 Keywords: DBDPE BDE209 Brominated flame retardant PBDE Waste water treatment plant
a b s t r a c t Decabromodiphenyl ethane (deBDethane) is an additive flame retardant marketed as a replacement for decabromodiphenyl ether (decaBDE). The structures of the two chemicals are similar, and hence deBDethane may also become an environmental contaminant of concern. Environmental data on deBDethane are scarce. Since sewage sludge is an early indicator of leakage of these chemicals into the environment, an international survey of deBDethane and decaBDE levels in sludge was conducted. Samples were collected from 42 WWTPs in 12 different countries and analyzed with GC/LRMS. DeBDethane was present in sludge from all countries and may therefore be a worldwide concern. The levels of deBDethane in sludge samples from the Ruhr area of Germany were the highest so far reported in the literature (216 ng g1 d.wt.). The [deBDethane]/[decaBDE] quotient for the whole data set ranged from 0.0018 to 0.83. High ratios were found in and around Germany where deBDethane imports are known to have been high and substitution of decaBDE with deBDethane is likely to have occurred. Low ratios were found in the USA and the UK, countries that have traditionally been large users of decaBDE. An estimate of the flux of deBDEthane from the technosphere via WWTPs to the environment within the European Union gave 1.7 ± 0.34 mg annually per person. The corresponding value for decaBDE was 41 ± 22 mg annually per person. Ó 2008 Elsevier Ltd. All rights reserved.
1. Introduction In the early 1990s, decabromodiphenyl ethane (deBDethane) was introduced as an alternative to its polybrominated diphenyl ether (PBDE) analogue, decabromodiphenyl ether (decaBDE). Over the past 20 years, PBDEs have been shown to be ubiquitously present and persistent in the environment (Hale et al., 2003; de Wit et al., 2006; Law et al., 2006; Wang et al., 2007a). PBDE usage has been voluntarily phased out in several countries or is restricted by law due to concerns regarding human and wildlife health. This has created a demand for alternative flame retardants. In 2003, deBDethane was discovered in the environment for the first time (Kierkegaard and Bjoerklund, 2003). It was identified in sewage sludge, sediment and indoor air. This work demonstrated that deBDethane, like decaBDE, is leaking out of the technosphere into the environment and accumulating there. Since then, deBDethane has been found in sludge from Spain (Eljarrat et al., 2005) and Canada (McCrindle et al., 2004), and also in tree bark (Qiu and Hites, 2008), and in a benthic food chain (Law et al., 2006) from North America. For many industrial chemicals, wastewater treatment plants (WWTPs) are major filters between the technosphere and the environment. Chemicals entering WWTPs may volatilize, be discharged * Corresponding author. Tel.: +46 86747565; fax: +46 86747637. E-mail address: [email protected] (N. Ricklund). 0045-6535/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2008.08.047
with the effluent, sequestrated into sewage sludge, or degraded. Data on degradation of deBDethane and decaBDE in WWTPs is scarce. However, it has been demonstrated by Gerecke et al. (2005, 2006) that decaBDE can undergo anaerobic degradation in sewage sludge under laboratory conditions. The behaviour of deBDethane and decaBDE in a WWTP in Stockholm, Sweden, serving 7.05 105 persons was recently investigated (Ricklund et al., 2008). The influent delivered 8.5 lg d1 person1 of deBDethane and 78 lg d1 person1 of decaBDE to the plant. In accordance with their hydrophobic and involatile properties, the chemicals associated primarily with the solids. As a result of the high solids removal efficiency in this WWTP (99.5%), <1% of the inflowing chemicals left the plant in the effluent; both deBDethane and decaBDE were almost completely sequestered into the sludge. Anaerobic degradation of the BFRs did not have a major influence on the overall mass balance. North (2004) reported a similar behaviour for decaBDE in a WWTP in California. In Ricklund et al. (2008), deBDethane was present in the digested sludge at 81 ng g1 d.wt., which was just ten times less than the concentration of decaBDE (800 ng g1 d.wt.). This indicates that environmental contamination with deBDethane may achieve a similar magnitude to decaBDE. Apart from a handful of measurements, it is currently not known how widespread the use of deBDethane is and to what extent it is being released to the environment. Concentrations in sludge can be used to achieve an overview of how much deBDethane is leaking
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out of the technosphere via wastewater. For this purpose, an international survey of deBDethane levels in sludge samples was conducted. DecaBDE was also analyzed to allow comparison of the leakage of the two flame retardants.
top. The analytes were eluted with n-hexane in the second fraction (4–7 mL). 13C-labeled 2,20 ,3,4,40 5,50 -heptachlorobiphenyl (2.1 ng) was added as a volumetric standard. Finally, the extracts were evaporated under nitrogen to approximately 250 lL prior to analysis with GC/LRMS.
2. Materials and methods 2.4. GC–LRMS analysis 2.1. Chemicals All chemicals were of analytical grade. Acetone, n-hexane, sodium sulphate and silica gel (0.063–0.200 mm) were obtained from Merck (Darmstadt, Germany); aminopropyl silica gel (0.040–0.070 mm) from Sorbent AB (V. Frölunda, Sweden); ethanol (99.5%) from Kemetyl AB (Stockholm, Sweden); potassium hydroxide (87.9%) from Eka Chemicals AB (Bohus, Sweden), sulfuric acid (98%) from Thermo Fischer Scientific (Waltham, MA, USA); 2,2,4trimethylpentane from Labscan Limited (Dublin, Ireland). Native and 13C-labeled deBDethane was obtained from Wellington Laboratories Inc. (Guelph, Ontario, Canada); native and 13C-labeled decaBDE and the volumetric standard, 13C-labeled 2,20 ,3,4,40 5,50 heptachlorobiphenyl, were obtained from Cambridge Isotopic Laboratories (CIL, Andover, MA, USA). 2.2. Sampling Sludge was collected from WWTPs around the world during the period between 1998 and 2006, whereby most of them were sampled during 2004 (countries and levels are presented in table s1, supplementary material). The plants employed different treatment techniques, but in most cases (in 20 out of 42 plants) the final product was anaerobically digested sludge. Collection was performed by WWTP staff on site or by research personal. Guidelines for sampling and a questionnaire were sent in advance to the person handling the sampling at each site. In the questionnaire, information about site specific technical and operational conditions was requested, e.g. the number of persons and any major industries connected, the wastewater flow, and the treatment processes. In addition, the contact persons were requested to document the drying method. In most cases the sludge was air dried in the dark and shipped in glass jars as specified in the sampling guidelines, but there were exceptions, and documentation was not complete in all cases (see Supplementary material, Table S2 for a summary of the questionnaire responses). Upon arrival at Stockholm University, the samples were immediately frozen (20 °C). 2.3. Extraction and cleanup The dried sludge was ground and between 0.4 and 1.8 g was extracted using an accelerated solvent extractor (ASE 300, Dionex). With some modifications the ASE cells (33 mL) were filled according to the method of Sporring and Bjorklund (2004). From the bottom of the cell the layers were: glass fibre filter, sodium sulphate, sulfuric acid treated silica gel (40% w/w), dried sludge spiked with 13 C-labeled decaBDE (60 ng), and finally sodium sulphate. The ASE parameters were set to 100 °C, two 5 min static cycles, 60% flush volume, and 60 s purge time with nitrogen gas. For additional cleanup, the extracts were transferred to new test tubes and evaporated to 2 mL under a gentle stream of nitrogen. Sulfur was removed by adding 2 mL potassium hydroxide (0.5 M) in ethanol (99%) and placing the extracts in a 45 °C water bath for 20 min. The alkaline treatment was interrupted by the addition of 4 mL water and the hexane phase was decanted to new test tubes. The water–ethanol phase was re-extracted twice with a small amount of hexane. The extracts were then evaporated to approximately 500 lL and fractionated on a column of 1 g preconditioned aminopropyl gel with 0.3 g acid silica (40%) added to the
The samples were analyzed with a GC (HP 5890 II, Agilent Technol.) equipped with a split/splitless injector. A 15 m, 0.25 mm i.d., 0.1 lm film thickness DB5MS column (J&W Scientific, Agilent Technologies Inc.) was employed. The GC temperature program was: start at 80 °C and hold for 2 min; ramp 20 °C min1 to 200 °C; ramp 6 °C min1 to 315 °C and hold for 10 min. The helium carrier gas flow was 1.4 mL min1. The GC was coupled to a Finnigan MAT SSQ 7000 mass spectrometer, operated in electron capture negative ionization (ECNI) mode with NH3 as reaction gas. For deBDethane the ions m/z = 78.9 and m/z = 80.9 were monitored. For decaBDE and 13C-decaBDE the ions m/z = 484.6; 486.6 and m/z = 494.6; 496.6 were used, respectively. 2.5. Identification and quantification The identification of native and labeled deBDethane and decaBDE was based on the retention time and the relative intensity of the fragment ions monitored. The relative intensities of the isotopes differed from the theoretical values by <10% in all samples except for 3, for which the difference was <15%. Quantification was performed using 8 point calibration curves of each native chemical. 13C-labeled decaBDE was used as an internal standard for both decaBDE and deBDethane. The deBDethane levels were corrected for its relative recovery compared to the internal standard. 2.6. Quality assurance Exposure of samples to UV-light was minimized by covering all lamps in the laboratory with UV-protective film. Procedural blanks (n = 7) that included the extraction and cleanup were analyzed in parallel to the samples. The samples were extracted in batches of 5. In addition to a procedural blank, each extraction batch included a reference matrix control sample (R-sample) and a spiked matrix control sample (S-sample). The R-samples were employed primarily to give information about the precision of the method. The R-samples were sub-sampled from a single sample of sludge from a WWTP in Stockholm, Sweden. The S-samples were included for determination of the relative recovery of deBDethane compared to decaBDE. Each S-sample was a duplicate randomly selected from the samples to be analyzed in the extraction batch. In 2 of the batches, the R-sample sludge was selected. The S-samples were spiked with a known quantity of unlabeled deBDethane prior to extraction. Following analysis, the amount of deBDethane determined in each unspiked duplicate sample was subtracted from the amount determined in the corresponding spiked sample, and the difference was divided by the spiked amount of deBDethane to give the relative recovery. By making the S-samples out of different sludge samples, the procedure yielded information on the influence of matrix variability on relative recovery. 3. Results and discussion 3.1. Quality control The data were examined for systematic errors related to the sampling and analytical procedures. The chemical concentrations
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in sewage sludge were plotted against different method variables such as sampling year, drying technique, recovery and extraction batch. No relationships were observed. The mean recovery of the surrogate standard in the final dataset, including blank samples, was 72%, but it varied considerably (CV 40%). 15 samples were re-extracted because of low recoveries, whereby additional quality assurance samples were also analysed. The recovery threshold for data acceptance was set at 20%. Four field samples and three quality control samples (1 S-sample, 1 Rsample and 1 blank sample) did not meet this criterion and were excluded from the dataset. The countries (Canada and Germany) that the excluded field samples originated from were already well represented in the data set. The reasons for the variable and occasionally insufficient recoveries could not be identified. No relationship was observed between recovery and extraction batch or sample size. The fact that the recovery was also poor in one of the blanks indicates that the losses were not primarily due to matrix effects. Degradation of BDE209 is known to occur during cleanup or through exposure to UV-light. However, in the sludge samples the recovery was only weakly correlated (R2 = 0.34) to the relative signal (at m/z = 496.6) of BDE209 to BDE207, a presumed degradation product. It is possible that degradation occurred via pathways that did not lead primarily to formation of debromination products, as was recently postulated by Stapleton and Dodder (2008). The deBDethane recovery was calculated from the spiked Ssamples. It was on average a factor of 1.2 (CV 27%) higher than the decaBDE recovery. In all samples, the deBDethane levels were corrected for this deviation, i.e. divided by 1.2. In 5 out of 7 of the procedural blank samples deBDethane was not detectable. In the same blank samples the decaBDE levels ranged between 0.34 and 1.2 ng. One of the remaining blank samples, was discarded because the recovery of the internal standard was <20%. In the other, relatively high levels of both BFRs were found, i.e. 2.7 ng of deBDethane and 59 ng of decaBDE. This blank was treated as an outlier, but there is a chance that a few of the samples could have been contaminated at this level. Nevertheless, there were only 7 samples for which the quantity of deBDethane in this blank was >20% of the quantity in the sample, while for decaBDE the corresponding number was 12 samples. The method limit of detection (LOD) and method limit of quantification (LOQ) for deBDethane were based on 3 and 5 times the detector noise in field samples, respectively. For decaBDE, the LOD and LOQ were calculated from the levels found in the blank samples and defined as the mean plus 3 and 10 times its standard deviation, respectively. The LOD and LOQ for deBDethane were 0.58–1.6 and 0.83–2.7 ng g1 d.wt., respectively. This corresponded to 1.4 and 2.3 ng per sample. The LOD and LOQ for decaBDE were 1.9 and 4.6 ng per sample, respectively. Good agreement was found between the R-sample replicates (n = 4). The CVs of deBDethane and decaBDE were 18 and 14% with mean levels of 54 and 786 ng g1 d.wt., respectively. In addition, duplicate determinations of decaBDE were available from the matrix (deBDethane-) spiked control samples and duplicate unspiked samples. The ratio of the decaBDE concentrations between the duplicates was in 3 cases between 0.97–1.1 and in 1 case higher (2.9).
3.2. Levels in sludge The levels and the international distribution of deBDethane and decaBDE in the sludge samples are illustrated in Figs. 1 and 2, while the data are tabulated in Supplementary material, Table S1. DeDBethane was found in all but 2 samples. It can be concluded that deBDethane is being used and emitted worldwide.
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DecaBDE was found in all samples. No relationships were observed between the levels of either of the two BFRs and the number of persons connected to the WWTP, in agreement with previous observations (Nylund et al., 2002; Kierkegaard et al., 2004; Tasaki et al., 2004). The levels were also not related to any of the other parameters documented in the sampling protocols. The level of deBDethane found in one sample from Germany is, at 220 ng g1 d.wt., the highest so far reported in the literature. It is a factor of 2.7 and 7.0 higher than the mean levels for the European samples (81 ng g1 d.wt.) and the North American samples (31 ng g1 d.wt.), respectively. The WWTP is located in a highly industrial area (the Ruhr Region) of Germany. According to the sampling protocol it receives water from the automobile industry. The automobile industry is a known user of BFRs (Gearhart et al., 2006). There were 3 other samples from the Ruhr Area containing deBDethane levels of 121, 74 and 70 ng g1 d.wt.. Two of these were also among the 10 highest in this study. The other 7 came from Switzerland, the Czech Republic, China, Singapore, and the USA. There was no information in the sampling protocols suggesting particular industrial sources. However, Germany was reported to account for a majority of the total import of deBDethane into Europe in 2001 (Kierkegaard, 2007). The high levels in sludge from Germany as well as Switzerland and the Czech Republic, which both have close economic ties to Germany, are consistent with the high imports. Unfortunately, more information on the import of deBDethane to the countries studied was not found. Two other studies have reported the presence of deBDethane in sewage sludge. In sludge from 8 Spanish WWTPs, deBDethane levels ranged between 0.2 and 15 ng g1 d.wt. (Eljarrat et al., 2005), while in 10 Canadian sludges it was between 6 and 30 ng g1 d.wt. (McCrindle et al., 2004). The levels in the Spanish sludge were more than five times lower than the European mean in this study, while the levels from Canada presented by McCrindle et al. (2004) were in the same range as the Canadian mean for this study. The highest levels of decaBDE were found in the USA and the United Kingdom; i.e. up to 19 000 and 12 000 ng g1 d.wt., respectively. For the USA these findings agree well with the fact that they had the world’s highest market demand for decaBDE in 2001(Law et al., 2006). The per capita market demand for decaBDE in the United Kingdom was suggested to be in line with that of North America due to the UK’s history of stringent fire regulations (Harrad et al., 2008). It was in samples from the UK that Harrad et al. (2008) found the highest ever recorded decaBDE levels in domestic or office dust, namely 520 and 100 ppm on dry weight basis. Relatively high decaBDE levels were also found in one sample from New Zealand and in one sample from China (9500 and 3300 ng g1 d.wt., respectively). Almost no existing data were found for these countries. One exception is the study by Wang et al. (2007b) that reported decaBDE levels between
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Fig. 1. Levels of deBDethane in sludge from different countries. Levels
used independently (Kierkegaard et al., 2004). In this study there were some indications that the levels of the two substances were not independent of each other, particularly for the samples grouped at the ends of the ratio range. Among the samples containing the 10 highest and 10 lowest ratios, an increasing ratio was accompanied by a concurrent increase in the deBDethane level (R2 = 0.42) and a decrease in the decaBDE level (R2 = 0.64) (see Fig. 3). This was less significant when plotting the whole data set (corresponding R2-values of 0.25 and 0.50). A similar pattern was previously indicated in a survey of Swedish sludge, where the highest [deBDethane]/[decaBDE] ratios were found in samples with low to medium levels of decaBDE (Kierkegaard et al. (2004). We interpret this observation to be partly a result of chemical substitution. As deBDethane emissions rise, a decrease in decaBDE emissions can be expected, because deBDethane is marketed as a replacement for decaBDE. Nevertheless, the decrease in decaBDE levels in Fig. 3 is very large compared to the increase in deBDethane levels (note the logarithmic scales), indicating there are other causal factors as well. Geographical patterns in the [deBDethane]/[decaBDE] ratio were also observed. All 3 samples from Switzerland were found in the high ratio group together with 3 out of 4 samples from the Czech Republic, 3 out of 5 samples from Germany, and 1 out of 3 samples from Singapore. In this high ratio group, 9 out of 10 samples originated from Germany or countries adjacent to Germany. All of the 5 samples from the USA were in the low ratio group together with both of the samples from England, 1 out of 3 samples from New Zeeland, 1 out of 4 samples from Australia, and 1 out of 9
samples from Canada. Only English speaking countries were represented in this group. Hence the geographical groupings of this ratio supports the interpretation that chemical substitution has occurred; the high ratios were found in and around Germany where deBDethane imports are known to have been high and substitution of decaBDE with deBDethane is likely to have progressed far, while the low ratios were found in countries that have traditionally been large users of decaBDE. From the flame retardant levels in sludge and data on sludge production, a rough estimate of deBDethane release from the technosphere via wastewater was made. It has been shown for both BFRs that virtually all of the chemical present in the wastewater stream is sequestered into sewage sludge (Ricklund et al., 2008), and hence the mass flow into the WWTP can be approximated by the mass flow in sludge. For samples that originated from EU states (n = 15; Czech Republic, England, Germany, Switzerland, Sweden), the level of deBDethane in sludge was 81 ± 16 ng g1 d.wt. (mean ± standard error). Multiplying this by the estimated annual production of sludge within the EU during 2005 (European Commission: the Directorate-General for the Environment, 1999) (8.3 million tonnes d.wt.), gives a total sequestration of 0.68 ± 0.13 tonnes of deBDethane annually. This is equivalent to 1.7 ± 0.34 mg annually per person. The corresponding estimates for decaBDE are 16 ± 8.6 tonnes annually and 41 ± 22 mg annually per person. The decaBDE usage within the EU was estimated to 8200 tonnes annually by the European Commission in a 2002 risk assessment report of decaBDE (European Commission: Joint Research Centre,
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Fig. 2. Levels of decaBDE in sludge from different countries. Levels
two BFRs. In this manner, the chemicals are being distributed in the environment. As has been shown for decaBDE (Sellstroem et al., 2005), there is a potential for bioaccumulation of this class of chemicals from sludge treated soils into food webs, thereby contributing to wildlife and human exposure. Acknowledgements
Fig. 3. Samples with the 10 highest and 10 lowest ratios. One sample with a deBDethane level between LOD and LOQ is included. Two samples with deBDethane levels
2002). Comparing this estimate to the total annual sequestration in sewage sludge from the present study suggests that the leakage of decaBDE from the technosphere via municipal wastewater is of the order of 0.2%. This is a small number, but not unexpected, since most of the decaBDE is expected to leave the technosphere via solid waste. It is notable that 19 of the sludges were used for land application or were so-called biosolids. Several of these samples were among the samples containing the 10 highest levels of one of the
Financial support was provided by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS). We greatly acknowledge the following persons for providing sludge samples and information: Jonathan Barber (Lancaster University), Les Burridge (Fisheries and Oceans Canada), Kai Bester (University of Duisburg-Essen), Cathleen Guo (ITT, Shanghai), Luke Chimuka (University of the Witwatersrand), Lao Choon Leng (Public Utilities Board, Singapore), Mark la Guardia (Virginia Institute of Marine Science), Harry Collins (Miramichi Environmental Assessment Committee), Dominique Grandjean (CECOTOX, Lausanne), Ivan Holoubek, Masaryk University), Jochen Müller (University of Queensland), Kuria Ndungu (Stockholm University), Olaf Päpke (Eurofins/ERGO, Hamburg), Erik Reiner (Ontario Ministry of the Environment), Sean Steller (Fisheries and Oceans Canada), Bryan S.F. Wong (Hong Kong), Veronica Ulfves (MWH Global, Dunedin NZ). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.chemosphere.2008.08.047.
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References De Wit, C.A., Alaee, M., Muir, D.C.G., 2006. Levels and trends of brominated flame retardants in the Arctic. Chemosphere 64, 209–233. Eljarrat, E., Labandeira, A., Martinez, A., Fabrellas, B., Barcelo, B., 2005. Occurrence of the ‘‘new” brominated flame retardant, decabromodiphenyl ethane, in sewage sludge from Spain. Organohalogen Compd. 67, 459–461. European Commission: Joint Research Centre, 2002. European union risk assessment report: bis(pentabromophenyl) ether. EUR 20402 EN. European Commission: The Directorate-General for the Environment, 1999. Workshop on problems around sludge. EUR 19657 EN. Gearhart, J., Posselt, H., Dempsey, D., Costner, P., Griffith, C., Juska, C., 2006. Toxic at any speed. Chemicals in cars and the need for safe alternatives. Ecology center report. Web site accessed June 2008:. Gerecke, A.C., Giger, W., Hartmann, P.C., Heeb, N.V., Kohler, H.-P.E., Schmid, P., Zennegg, M., Kohler, M., 2006. Anareobic degradation of brominated flame retardants in sewage sludge. Chemosphere 64, 311–317. Gerecke, A.C., Hartmann, P.C., Heeb, N.V., Kohler, H.-P.E., Giger, W., Schmid, P., Zennegg, M., Kohler, M., 2005. Anaerobic degradation of decabromodiphenyl ether. Environ. Sci. Technol. 39, 1078–1083. Hale, R.C., Alaee, M., Manchester-Neesvig, J.B., Stapleton, H.M., Ikonomou, M.G., 2003. Polybrominated diphenyl ether flame retardants in the North American environment. Environ. Int. 29, 771–779. Harrad, S., Ibarra, C., Diamond, M., Melymuk, L., Robson, M., Douwes, J., Roosens, L., Dirtu, A.C., Covaci, A., 2008. Polybrominated diphenyl ethers in domestic indoor dust from Canada, New Zealand, United Kingdom and United States. Environ. Int. 34, 232–238. Kierkegaard, A., 2007. PBDEs in the Environment: time trends, bioaccumulation and the identification of their successor, decabromodiphenyl ethane. Ph.D. thesis, Department of Applied Environmental Science, Stockholm University, ISBN: 917155-410-6. Kierkegaard, A., Bjoerklund, J., 2003. The presence of a ‘new’ flame retardant, decabromodiphenyl ethane, in environmental samples. Organohalogen Compd. 61, 183–186. Kierkegaard, A., Bjoerklund, J., Friden, U., 2004. Identification of the flame retardant decabromodiphenyl ethane in the environment. Environ. Sci. Technol. 38, 3247–3253.
Law, R.J., Allchin, C.R., de Boer, J., Covaci, A., Herzke, D., Lepom, P., Morris, S., Tronczynski, J., de Wit, C.A., 2006. Levels and trends of brominated flame retardants in the European environment. Chemosphere 64, 187–208. McCrindle, R., Chittim, B., Konstantinov, A., Kolic, T., McAlees, A., MacPherson, K., Reiner, E., Potter, D., Tashiro, C., Yeo, B., 2004. Native and mass labeled [13C14]decabromodiphenylethane: characterization and use in determination of DBDPE in sewage sludge. Organohalogen Compd. 66, 3744–3750. Nylund, K., Eriksson, U., Haglund, M., Berggren, D., Kierkegaard, A., Allan, A., Asplund; L, deWit, C., 2002. Swedish EPA report no. 5188. Pulkrabová, J., Hajslová, J., Poustka, J., Hrádková, P., 2007. Brominated flame retardants in river sediments and sewage sludges collected in the Czech Republic. In: 4th International Workshop on Brominated Flame Retardants, Amsterdam. Qiu, X., Hites, R.A., 2008. Dechlorane plus and other flame retardants in tree bark from the northeastern United States. Environ. Sci. Technol. 42, 31–36. Ricklund, N., Kierkegaard, A., McLachlan, M., Wahlberg, C., 2008, accepted for publication. Mass balance of decabromodiphenyl ethane and decabromodiphenyl ether in a WWTP. Chemosphere, in press, doi:10.1016/j.chemosphere. 2008.09.054. Sellstroem, U., de Wit, C.A., Lundgren, N., Tysklind, M., 2005. Effect of sewage-sludge application on concentrations of higher-brominated diphenyl ethers in soils and earthworms. Environ. Sci. Technol. 39, 9064–9070. Sporring, S., Bjorklund, E., 2004. Selective pressurized liquid extraction of polychlorinated biphenyls from fat-containing food and feed samples influence of cell dimensions, solvent type, temperature and flush volume. J. Chromatogr. A 1040, 155–161. Stapleton, H.M., Dodder, N.G., 2008. Photodegradation of decabromodiphenyl ether in house dust by natural sunlight. Environ. Toxicol. Chem. 27, 306–312. Tasaki, T., Takasuga, T., Osako, M., Sakai, S.I., 2004. Substance flow analysis of brominated flame retardants and related compounds in waste TV sets in Japan. Waste Manage. 24, 571–580. Wang, Y., Jiang, G., Lam, P.K.S., Li, A., 2007a. Polybrominated diphenyl ether in the East Asian environment: a critical review. Environ. Int. 33, 963–973. Wang, Y., Zhang, Q., Lv, J., Li, A., Liu, H., Li, G., Jiang, G., 2007b. Polybrominated diphenyl ethers and organochlorine pesticides in sewage sludge of wastewater treatment plants in China. Chemosphere 68, 1683–1691.
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An international survey of decabromodiphenyl ethane (deBDethane) and decabromodiphenyl ether (decaBDE) in sewage sludge samples Niklas Ricklund *, Amelie Kierkegaard, Michael S. McLachlan Department of Applied Environmental Science (ITM), Stockholm University, SE-10691 Stockholm, Sweden
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Article history: Received 24 June 2008 Received in revised form 25 August 2008 Accepted 26 August 2008 Available online 14 October 2008 Keywords: DBDPE BDE209 Brominated flame retardant PBDE Waste water treatment plant
a b s t r a c t Decabromodiphenyl ethane (deBDethane) is an additive flame retardant marketed as a replacement for decabromodiphenyl ether (decaBDE). The structures of the two chemicals are similar, and hence deBDethane may also become an environmental contaminant of concern. Environmental data on deBDethane are scarce. Since sewage sludge is an early indicator of leakage of these chemicals into the environment, an international survey of deBDethane and decaBDE levels in sludge was conducted. Samples were collected from 42 WWTPs in 12 different countries and analyzed with GC/LRMS. DeBDethane was present in sludge from all countries and may therefore be a worldwide concern. The levels of deBDethane in sludge samples from the Ruhr area of Germany were the highest so far reported in the literature (216 ng g1 d.wt.). The [deBDethane]/[decaBDE] quotient for the whole data set ranged from 0.0018 to 0.83. High ratios were found in and around Germany where deBDethane imports are known to have been high and substitution of decaBDE with deBDethane is likely to have occurred. Low ratios were found in the USA and the UK, countries that have traditionally been large users of decaBDE. An estimate of the flux of deBDEthane from the technosphere via WWTPs to the environment within the European Union gave 1.7 ± 0.34 mg annually per person. The corresponding value for decaBDE was 41 ± 22 mg annually per person. Ó 2008 Elsevier Ltd. All rights reserved.
1. Introduction In the early 1990s, decabromodiphenyl ethane (deBDethane) was introduced as an alternative to its polybrominated diphenyl ether (PBDE) analogue, decabromodiphenyl ether (decaBDE). Over the past 20 years, PBDEs have been shown to be ubiquitously present and persistent in the environment (Hale et al., 2003; de Wit et al., 2006; Law et al., 2006; Wang et al., 2007a). PBDE usage has been voluntarily phased out in several countries or is restricted by law due to concerns regarding human and wildlife health. This has created a demand for alternative flame retardants. In 2003, deBDethane was discovered in the environment for the first time (Kierkegaard and Bjoerklund, 2003). It was identified in sewage sludge, sediment and indoor air. This work demonstrated that deBDethane, like decaBDE, is leaking out of the technosphere into the environment and accumulating there. Since then, deBDethane has been found in sludge from Spain (Eljarrat et al., 2005) and Canada (McCrindle et al., 2004), and also in tree bark (Qiu and Hites, 2008), and in a benthic food chain (Law et al., 2006) from North America. For many industrial chemicals, wastewater treatment plants (WWTPs) are major filters between the technosphere and the environment. Chemicals entering WWTPs may volatilize, be discharged * Corresponding author. Tel.: +46 86747565; fax: +46 86747637. E-mail address: [email protected] (N. Ricklund). 0045-6535/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2008.08.047
with the effluent, sequestrated into sewage sludge, or degraded. Data on degradation of deBDethane and decaBDE in WWTPs is scarce. However, it has been demonstrated by Gerecke et al. (2005, 2006) that decaBDE can undergo anaerobic degradation in sewage sludge under laboratory conditions. The behaviour of deBDethane and decaBDE in a WWTP in Stockholm, Sweden, serving 7.05 105 persons was recently investigated (Ricklund et al., 2008). The influent delivered 8.5 lg d1 person1 of deBDethane and 78 lg d1 person1 of decaBDE to the plant. In accordance with their hydrophobic and involatile properties, the chemicals associated primarily with the solids. As a result of the high solids removal efficiency in this WWTP (99.5%), <1% of the inflowing chemicals left the plant in the effluent; both deBDethane and decaBDE were almost completely sequestered into the sludge. Anaerobic degradation of the BFRs did not have a major influence on the overall mass balance. North (2004) reported a similar behaviour for decaBDE in a WWTP in California. In Ricklund et al. (2008), deBDethane was present in the digested sludge at 81 ng g1 d.wt., which was just ten times less than the concentration of decaBDE (800 ng g1 d.wt.). This indicates that environmental contamination with deBDethane may achieve a similar magnitude to decaBDE. Apart from a handful of measurements, it is currently not known how widespread the use of deBDethane is and to what extent it is being released to the environment. Concentrations in sludge can be used to achieve an overview of how much deBDethane is leaking
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out of the technosphere via wastewater. For this purpose, an international survey of deBDethane levels in sludge samples was conducted. DecaBDE was also analyzed to allow comparison of the leakage of the two flame retardants.
top. The analytes were eluted with n-hexane in the second fraction (4–7 mL). 13C-labeled 2,20 ,3,4,40 5,50 -heptachlorobiphenyl (2.1 ng) was added as a volumetric standard. Finally, the extracts were evaporated under nitrogen to approximately 250 lL prior to analysis with GC/LRMS.
2. Materials and methods 2.4. GC–LRMS analysis 2.1. Chemicals All chemicals were of analytical grade. Acetone, n-hexane, sodium sulphate and silica gel (0.063–0.200 mm) were obtained from Merck (Darmstadt, Germany); aminopropyl silica gel (0.040–0.070 mm) from Sorbent AB (V. Frölunda, Sweden); ethanol (99.5%) from Kemetyl AB (Stockholm, Sweden); potassium hydroxide (87.9%) from Eka Chemicals AB (Bohus, Sweden), sulfuric acid (98%) from Thermo Fischer Scientific (Waltham, MA, USA); 2,2,4trimethylpentane from Labscan Limited (Dublin, Ireland). Native and 13C-labeled deBDethane was obtained from Wellington Laboratories Inc. (Guelph, Ontario, Canada); native and 13C-labeled decaBDE and the volumetric standard, 13C-labeled 2,20 ,3,4,40 5,50 heptachlorobiphenyl, were obtained from Cambridge Isotopic Laboratories (CIL, Andover, MA, USA). 2.2. Sampling Sludge was collected from WWTPs around the world during the period between 1998 and 2006, whereby most of them were sampled during 2004 (countries and levels are presented in table s1, supplementary material). The plants employed different treatment techniques, but in most cases (in 20 out of 42 plants) the final product was anaerobically digested sludge. Collection was performed by WWTP staff on site or by research personal. Guidelines for sampling and a questionnaire were sent in advance to the person handling the sampling at each site. In the questionnaire, information about site specific technical and operational conditions was requested, e.g. the number of persons and any major industries connected, the wastewater flow, and the treatment processes. In addition, the contact persons were requested to document the drying method. In most cases the sludge was air dried in the dark and shipped in glass jars as specified in the sampling guidelines, but there were exceptions, and documentation was not complete in all cases (see Supplementary material, Table S2 for a summary of the questionnaire responses). Upon arrival at Stockholm University, the samples were immediately frozen (20 °C). 2.3. Extraction and cleanup The dried sludge was ground and between 0.4 and 1.8 g was extracted using an accelerated solvent extractor (ASE 300, Dionex). With some modifications the ASE cells (33 mL) were filled according to the method of Sporring and Bjorklund (2004). From the bottom of the cell the layers were: glass fibre filter, sodium sulphate, sulfuric acid treated silica gel (40% w/w), dried sludge spiked with 13 C-labeled decaBDE (60 ng), and finally sodium sulphate. The ASE parameters were set to 100 °C, two 5 min static cycles, 60% flush volume, and 60 s purge time with nitrogen gas. For additional cleanup, the extracts were transferred to new test tubes and evaporated to 2 mL under a gentle stream of nitrogen. Sulfur was removed by adding 2 mL potassium hydroxide (0.5 M) in ethanol (99%) and placing the extracts in a 45 °C water bath for 20 min. The alkaline treatment was interrupted by the addition of 4 mL water and the hexane phase was decanted to new test tubes. The water–ethanol phase was re-extracted twice with a small amount of hexane. The extracts were then evaporated to approximately 500 lL and fractionated on a column of 1 g preconditioned aminopropyl gel with 0.3 g acid silica (40%) added to the
The samples were analyzed with a GC (HP 5890 II, Agilent Technol.) equipped with a split/splitless injector. A 15 m, 0.25 mm i.d., 0.1 lm film thickness DB5MS column (J&W Scientific, Agilent Technologies Inc.) was employed. The GC temperature program was: start at 80 °C and hold for 2 min; ramp 20 °C min1 to 200 °C; ramp 6 °C min1 to 315 °C and hold for 10 min. The helium carrier gas flow was 1.4 mL min1. The GC was coupled to a Finnigan MAT SSQ 7000 mass spectrometer, operated in electron capture negative ionization (ECNI) mode with NH3 as reaction gas. For deBDethane the ions m/z = 78.9 and m/z = 80.9 were monitored. For decaBDE and 13C-decaBDE the ions m/z = 484.6; 486.6 and m/z = 494.6; 496.6 were used, respectively. 2.5. Identification and quantification The identification of native and labeled deBDethane and decaBDE was based on the retention time and the relative intensity of the fragment ions monitored. The relative intensities of the isotopes differed from the theoretical values by <10% in all samples except for 3, for which the difference was <15%. Quantification was performed using 8 point calibration curves of each native chemical. 13C-labeled decaBDE was used as an internal standard for both decaBDE and deBDethane. The deBDethane levels were corrected for its relative recovery compared to the internal standard. 2.6. Quality assurance Exposure of samples to UV-light was minimized by covering all lamps in the laboratory with UV-protective film. Procedural blanks (n = 7) that included the extraction and cleanup were analyzed in parallel to the samples. The samples were extracted in batches of 5. In addition to a procedural blank, each extraction batch included a reference matrix control sample (R-sample) and a spiked matrix control sample (S-sample). The R-samples were employed primarily to give information about the precision of the method. The R-samples were sub-sampled from a single sample of sludge from a WWTP in Stockholm, Sweden. The S-samples were included for determination of the relative recovery of deBDethane compared to decaBDE. Each S-sample was a duplicate randomly selected from the samples to be analyzed in the extraction batch. In 2 of the batches, the R-sample sludge was selected. The S-samples were spiked with a known quantity of unlabeled deBDethane prior to extraction. Following analysis, the amount of deBDethane determined in each unspiked duplicate sample was subtracted from the amount determined in the corresponding spiked sample, and the difference was divided by the spiked amount of deBDethane to give the relative recovery. By making the S-samples out of different sludge samples, the procedure yielded information on the influence of matrix variability on relative recovery. 3. Results and discussion 3.1. Quality control The data were examined for systematic errors related to the sampling and analytical procedures. The chemical concentrations
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in sewage sludge were plotted against different method variables such as sampling year, drying technique, recovery and extraction batch. No relationships were observed. The mean recovery of the surrogate standard in the final dataset, including blank samples, was 72%, but it varied considerably (CV 40%). 15 samples were re-extracted because of low recoveries, whereby additional quality assurance samples were also analysed. The recovery threshold for data acceptance was set at 20%. Four field samples and three quality control samples (1 S-sample, 1 Rsample and 1 blank sample) did not meet this criterion and were excluded from the dataset. The countries (Canada and Germany) that the excluded field samples originated from were already well represented in the data set. The reasons for the variable and occasionally insufficient recoveries could not be identified. No relationship was observed between recovery and extraction batch or sample size. The fact that the recovery was also poor in one of the blanks indicates that the losses were not primarily due to matrix effects. Degradation of BDE209 is known to occur during cleanup or through exposure to UV-light. However, in the sludge samples the recovery was only weakly correlated (R2 = 0.34) to the relative signal (at m/z = 496.6) of BDE209 to BDE207, a presumed degradation product. It is possible that degradation occurred via pathways that did not lead primarily to formation of debromination products, as was recently postulated by Stapleton and Dodder (2008). The deBDethane recovery was calculated from the spiked Ssamples. It was on average a factor of 1.2 (CV 27%) higher than the decaBDE recovery. In all samples, the deBDethane levels were corrected for this deviation, i.e. divided by 1.2. In 5 out of 7 of the procedural blank samples deBDethane was not detectable. In the same blank samples the decaBDE levels ranged between 0.34 and 1.2 ng. One of the remaining blank samples, was discarded because the recovery of the internal standard was <20%. In the other, relatively high levels of both BFRs were found, i.e. 2.7 ng of deBDethane and 59 ng of decaBDE. This blank was treated as an outlier, but there is a chance that a few of the samples could have been contaminated at this level. Nevertheless, there were only 7 samples for which the quantity of deBDethane in this blank was >20% of the quantity in the sample, while for decaBDE the corresponding number was 12 samples. The method limit of detection (LOD) and method limit of quantification (LOQ) for deBDethane were based on 3 and 5 times the detector noise in field samples, respectively. For decaBDE, the LOD and LOQ were calculated from the levels found in the blank samples and defined as the mean plus 3 and 10 times its standard deviation, respectively. The LOD and LOQ for deBDethane were 0.58–1.6 and 0.83–2.7 ng g1 d.wt., respectively. This corresponded to 1.4 and 2.3 ng per sample. The LOD and LOQ for decaBDE were 1.9 and 4.6 ng per sample, respectively. Good agreement was found between the R-sample replicates (n = 4). The CVs of deBDethane and decaBDE were 18 and 14% with mean levels of 54 and 786 ng g1 d.wt., respectively. In addition, duplicate determinations of decaBDE were available from the matrix (deBDethane-) spiked control samples and duplicate unspiked samples. The ratio of the decaBDE concentrations between the duplicates was in 3 cases between 0.97–1.1 and in 1 case higher (2.9).
3.2. Levels in sludge The levels and the international distribution of deBDethane and decaBDE in the sludge samples are illustrated in Figs. 1 and 2, while the data are tabulated in Supplementary material, Table S1. DeDBethane was found in all but 2 samples. It can be concluded that deBDethane is being used and emitted worldwide.
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DecaBDE was found in all samples. No relationships were observed between the levels of either of the two BFRs and the number of persons connected to the WWTP, in agreement with previous observations (Nylund et al., 2002; Kierkegaard et al., 2004; Tasaki et al., 2004). The levels were also not related to any of the other parameters documented in the sampling protocols. The level of deBDethane found in one sample from Germany is, at 220 ng g1 d.wt., the highest so far reported in the literature. It is a factor of 2.7 and 7.0 higher than the mean levels for the European samples (81 ng g1 d.wt.) and the North American samples (31 ng g1 d.wt.), respectively. The WWTP is located in a highly industrial area (the Ruhr Region) of Germany. According to the sampling protocol it receives water from the automobile industry. The automobile industry is a known user of BFRs (Gearhart et al., 2006). There were 3 other samples from the Ruhr Area containing deBDethane levels of 121, 74 and 70 ng g1 d.wt.. Two of these were also among the 10 highest in this study. The other 7 came from Switzerland, the Czech Republic, China, Singapore, and the USA. There was no information in the sampling protocols suggesting particular industrial sources. However, Germany was reported to account for a majority of the total import of deBDethane into Europe in 2001 (Kierkegaard, 2007). The high levels in sludge from Germany as well as Switzerland and the Czech Republic, which both have close economic ties to Germany, are consistent with the high imports. Unfortunately, more information on the import of deBDethane to the countries studied was not found. Two other studies have reported the presence of deBDethane in sewage sludge. In sludge from 8 Spanish WWTPs, deBDethane levels ranged between 0.2 and 15 ng g1 d.wt. (Eljarrat et al., 2005), while in 10 Canadian sludges it was between 6 and 30 ng g1 d.wt. (McCrindle et al., 2004). The levels in the Spanish sludge were more than five times lower than the European mean in this study, while the levels from Canada presented by McCrindle et al. (2004) were in the same range as the Canadian mean for this study. The highest levels of decaBDE were found in the USA and the United Kingdom; i.e. up to 19 000 and 12 000 ng g1 d.wt., respectively. For the USA these findings agree well with the fact that they had the world’s highest market demand for decaBDE in 2001(Law et al., 2006). The per capita market demand for decaBDE in the United Kingdom was suggested to be in line with that of North America due to the UK’s history of stringent fire regulations (Harrad et al., 2008). It was in samples from the UK that Harrad et al. (2008) found the highest ever recorded decaBDE levels in domestic or office dust, namely 520 and 100 ppm on dry weight basis. Relatively high decaBDE levels were also found in one sample from New Zealand and in one sample from China (9500 and 3300 ng g1 d.wt., respectively). Almost no existing data were found for these countries. One exception is the study by Wang et al. (2007b) that reported decaBDE levels between
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Fig. 1. Levels of deBDethane in sludge from different countries. Levels
used independently (Kierkegaard et al., 2004). In this study there were some indications that the levels of the two substances were not independent of each other, particularly for the samples grouped at the ends of the ratio range. Among the samples containing the 10 highest and 10 lowest ratios, an increasing ratio was accompanied by a concurrent increase in the deBDethane level (R2 = 0.42) and a decrease in the decaBDE level (R2 = 0.64) (see Fig. 3). This was less significant when plotting the whole data set (corresponding R2-values of 0.25 and 0.50). A similar pattern was previously indicated in a survey of Swedish sludge, where the highest [deBDethane]/[decaBDE] ratios were found in samples with low to medium levels of decaBDE (Kierkegaard et al. (2004). We interpret this observation to be partly a result of chemical substitution. As deBDethane emissions rise, a decrease in decaBDE emissions can be expected, because deBDethane is marketed as a replacement for decaBDE. Nevertheless, the decrease in decaBDE levels in Fig. 3 is very large compared to the increase in deBDethane levels (note the logarithmic scales), indicating there are other causal factors as well. Geographical patterns in the [deBDethane]/[decaBDE] ratio were also observed. All 3 samples from Switzerland were found in the high ratio group together with 3 out of 4 samples from the Czech Republic, 3 out of 5 samples from Germany, and 1 out of 3 samples from Singapore. In this high ratio group, 9 out of 10 samples originated from Germany or countries adjacent to Germany. All of the 5 samples from the USA were in the low ratio group together with both of the samples from England, 1 out of 3 samples from New Zeeland, 1 out of 4 samples from Australia, and 1 out of 9
samples from Canada. Only English speaking countries were represented in this group. Hence the geographical groupings of this ratio supports the interpretation that chemical substitution has occurred; the high ratios were found in and around Germany where deBDethane imports are known to have been high and substitution of decaBDE with deBDethane is likely to have progressed far, while the low ratios were found in countries that have traditionally been large users of decaBDE. From the flame retardant levels in sludge and data on sludge production, a rough estimate of deBDethane release from the technosphere via wastewater was made. It has been shown for both BFRs that virtually all of the chemical present in the wastewater stream is sequestered into sewage sludge (Ricklund et al., 2008), and hence the mass flow into the WWTP can be approximated by the mass flow in sludge. For samples that originated from EU states (n = 15; Czech Republic, England, Germany, Switzerland, Sweden), the level of deBDethane in sludge was 81 ± 16 ng g1 d.wt. (mean ± standard error). Multiplying this by the estimated annual production of sludge within the EU during 2005 (European Commission: the Directorate-General for the Environment, 1999) (8.3 million tonnes d.wt.), gives a total sequestration of 0.68 ± 0.13 tonnes of deBDethane annually. This is equivalent to 1.7 ± 0.34 mg annually per person. The corresponding estimates for decaBDE are 16 ± 8.6 tonnes annually and 41 ± 22 mg annually per person. The decaBDE usage within the EU was estimated to 8200 tonnes annually by the European Commission in a 2002 risk assessment report of decaBDE (European Commission: Joint Research Centre,
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Fig. 2. Levels of decaBDE in sludge from different countries. Levels
two BFRs. In this manner, the chemicals are being distributed in the environment. As has been shown for decaBDE (Sellstroem et al., 2005), there is a potential for bioaccumulation of this class of chemicals from sludge treated soils into food webs, thereby contributing to wildlife and human exposure. Acknowledgements
Fig. 3. Samples with the 10 highest and 10 lowest ratios. One sample with a deBDethane level between LOD and LOQ is included. Two samples with deBDethane levels
2002). Comparing this estimate to the total annual sequestration in sewage sludge from the present study suggests that the leakage of decaBDE from the technosphere via municipal wastewater is of the order of 0.2%. This is a small number, but not unexpected, since most of the decaBDE is expected to leave the technosphere via solid waste. It is notable that 19 of the sludges were used for land application or were so-called biosolids. Several of these samples were among the samples containing the 10 highest levels of one of the
Financial support was provided by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS). We greatly acknowledge the following persons for providing sludge samples and information: Jonathan Barber (Lancaster University), Les Burridge (Fisheries and Oceans Canada), Kai Bester (University of Duisburg-Essen), Cathleen Guo (ITT, Shanghai), Luke Chimuka (University of the Witwatersrand), Lao Choon Leng (Public Utilities Board, Singapore), Mark la Guardia (Virginia Institute of Marine Science), Harry Collins (Miramichi Environmental Assessment Committee), Dominique Grandjean (CECOTOX, Lausanne), Ivan Holoubek, Masaryk University), Jochen Müller (University of Queensland), Kuria Ndungu (Stockholm University), Olaf Päpke (Eurofins/ERGO, Hamburg), Erik Reiner (Ontario Ministry of the Environment), Sean Steller (Fisheries and Oceans Canada), Bryan S.F. Wong (Hong Kong), Veronica Ulfves (MWH Global, Dunedin NZ). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.chemosphere.2008.08.047.
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References De Wit, C.A., Alaee, M., Muir, D.C.G., 2006. Levels and trends of brominated flame retardants in the Arctic. Chemosphere 64, 209–233. Eljarrat, E., Labandeira, A., Martinez, A., Fabrellas, B., Barcelo, B., 2005. Occurrence of the ‘‘new” brominated flame retardant, decabromodiphenyl ethane, in sewage sludge from Spain. Organohalogen Compd. 67, 459–461. European Commission: Joint Research Centre, 2002. European union risk assessment report: bis(pentabromophenyl) ether. EUR 20402 EN. European Commission: The Directorate-General for the Environment, 1999. Workshop on problems around sludge. EUR 19657 EN. Gearhart, J., Posselt, H., Dempsey, D., Costner, P., Griffith, C., Juska, C., 2006. Toxic at any speed. Chemicals in cars and the need for safe alternatives. Ecology center report. Web site accessed June 2008:
Law, R.J., Allchin, C.R., de Boer, J., Covaci, A., Herzke, D., Lepom, P., Morris, S., Tronczynski, J., de Wit, C.A., 2006. Levels and trends of brominated flame retardants in the European environment. Chemosphere 64, 187–208. McCrindle, R., Chittim, B., Konstantinov, A., Kolic, T., McAlees, A., MacPherson, K., Reiner, E., Potter, D., Tashiro, C., Yeo, B., 2004. Native and mass labeled [13C14]decabromodiphenylethane: characterization and use in determination of DBDPE in sewage sludge. Organohalogen Compd. 66, 3744–3750. Nylund, K., Eriksson, U., Haglund, M., Berggren, D., Kierkegaard, A., Allan, A., Asplund; L, deWit, C., 2002. Swedish EPA report no. 5188. Pulkrabová, J., Hajslová, J., Poustka, J., Hrádková, P., 2007. Brominated flame retardants in river sediments and sewage sludges collected in the Czech Republic. In: 4th International Workshop on Brominated Flame Retardants, Amsterdam. Qiu, X., Hites, R.A., 2008. Dechlorane plus and other flame retardants in tree bark from the northeastern United States. Environ. Sci. Technol. 42, 31–36. Ricklund, N., Kierkegaard, A., McLachlan, M., Wahlberg, C., 2008, accepted for publication. Mass balance of decabromodiphenyl ethane and decabromodiphenyl ether in a WWTP. Chemosphere, in press, doi:10.1016/j.chemosphere. 2008.09.054. Sellstroem, U., de Wit, C.A., Lundgren, N., Tysklind, M., 2005. Effect of sewage-sludge application on concentrations of higher-brominated diphenyl ethers in soils and earthworms. Environ. Sci. Technol. 39, 9064–9070. Sporring, S., Bjorklund, E., 2004. Selective pressurized liquid extraction of polychlorinated biphenyls from fat-containing food and feed samples influence of cell dimensions, solvent type, temperature and flush volume. J. Chromatogr. A 1040, 155–161. Stapleton, H.M., Dodder, N.G., 2008. Photodegradation of decabromodiphenyl ether in house dust by natural sunlight. Environ. Toxicol. Chem. 27, 306–312. Tasaki, T., Takasuga, T., Osako, M., Sakai, S.I., 2004. Substance flow analysis of brominated flame retardants and related compounds in waste TV sets in Japan. Waste Manage. 24, 571–580. Wang, Y., Jiang, G., Lam, P.K.S., Li, A., 2007a. Polybrominated diphenyl ether in the East Asian environment: a critical review. Environ. Int. 33, 963–973. Wang, Y., Zhang, Q., Lv, J., Li, A., Liu, H., Li, G., Jiang, G., 2007b. Polybrominated diphenyl ethers and organochlorine pesticides in sewage sludge of wastewater treatment plants in China. Chemosphere 68, 1683–1691.