Polybrominated Diphenyl Ethers (PBDEs): Turning the Corner in Great

Article pubs.acs.org/est

Polybrominated Diphenyl Ethers (PBDEs): Turning the Corner in Great Lakes Trout 1980−2009 Bernard S. Crimmins,†,* James J. Pagano,‡ Xiaoyan Xia,§ Philip K. Hopke,§ Michael S. Milligan,∥ and Thomas M. Holsen† †

Department of Civil and Environmental Engineering, Clarkson University, 8 Clarkson Ave, Potsdam, New York 13699, United States Department of Chemistry, State University of New York at Oswego, 8C Snygg Hall, Washington Blvd, Oswego, New York 13126, United States § Center for Air Resources Engineering and Science, Clarkson University, 8 Clarkson Ave, Potsdam, New York 13699, United States ∥ Department of Chemistry, State University of New York at Fredonia, 218 Houghton Hall, Fredonia, New York 14063, United States ‡

S Supporting Information *

ABSTRACT: Lake trout and walleye composites were collected between 2004 and 2009 as part of the Great Lakes Fish Monitoring and Surveillance Program (GLFMSP) and analyzed for polybrominated diphenyl ethers (PBDEs). Yearly mean total PBDE concentrations (sum of congeners BDE47, BDE-99, BDE-100, BDE-153, BDE-154) ranged from 44−192, 28−113, 50−107, 37−111, and 11−22 ng/g wet wt. for Lakes Michigan, Huron, Ontario, and Superior lake trout, and Lake Erie walleye, respectively. A 1980− 2009 temporal record of PBDE concentrations in the Great Lakes’ top predator fish (lake trout and walleye) was assembled by integrating previous GLFMSP data (1980−2003) with current results (2004−2009). Temporal profiles show obvious breakpoints between periods of PBDE accumulation and decline in trout for Lakes Huron, Michigan and Ontario with a significant (p < 0.0001 and r = 0.55, 0.72, and 0.51, respectively) decrease in concentration after 2000−2001. A similar transition was observed in Lake Superior for the nearshore site accompanied by a less significant decreasing trend (p = 0.016, r = 0.33), suggesting concentrations are declining very slowly or have leveled off. In contrast, Lake Erie walleye concentrations began leveling off in the late 1990s and no statistically significant trend (increasing or decreasing) has been observed in recent years. A decrease in the BDE-47/BDE-153 ratio was also recently observed, suggesting a transition to more highly brominated PBDEs is occurring in Great Lakes trout. This study provides region-wide evidence that PBDE concentrations are generally declining in Great Lakes trout, although there are clear exceptions to this trend. Results from this study reflect the positive impact of the 2004 PentaBDE ban on macro-scale aquatic freshwater ecosystems.

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2001.3 Both mixtures have been phased out of the NA and EU markets8 while the DecaBDE mixture remains in NA commerce with a proposed phase out date of 2012. Health concerns from PBDE exposure arise from endocrine disruption and neurotoxicological effects on mammals, birds, and fish.9 In humans, PBDEs appear to pass freely from mother to fetus regardless of extent of bromine substitution.10 North American placental tissue levels are typically orders of magnitude higher than EU values10,11 reflecting the greater use of the PentaBDE formulation in North America. Recent evidence also suggests an inverse relationship between cord blood concentrations and neurodevelopment in children 12−48 and 72 months of age.12

INTRODUCTION The combustion process is essentially a radical driven chemical reaction. Polybrominated diphenyl ethers (PBDEs) were developed as effective radical scavengers and when added to materials, combustion retardation is observed as the bromine atoms quench radical formation (or reaction). Application of PBDEs has provided flame retardant properties to polymer matrices including plastics, polyurethane foam and circuit boards.1 The large usage of the PentaBDE mixture can be seen in the ubiquitous presence of the congeners BDE-47, BDE-99, and BDE-100 in freshwater2−4 and marine5,6 environments with North American (NA) concentrations typically >10-fold higher than European (EU) values. Prior to the voluntary U.S. industry phase out in 2004, the PentaBDE mixture was primarily used by NA industries, accounting for 95% of the total worldwide production in 2001 (7100−8300 t3,7). The OctaBDE mixture was consumed in lesser amounts (1500 t) with NA use accounting for 40% of its total production in © 2012 American Chemical Society

Received: Revised: Accepted: Published: 9890

June 15, 2012 August 13, 2012 August 28, 2012 August 28, 2012 dx.doi.org/10.1021/es302415z | Environ. Sci. Technol. 2012, 46, 9890−9897

Environmental Science & Technology

Article

Figure 1. Map of Great Lakes Fish Monitoring and Surveillance Program sampling sites.

analytical methods for each data set employed in this manuscript can be found in the Supporting Information (SI). Briefly, lake trout and walleye (Lake Erie only) were collected at two sites from each of the Great Lakes (Figure 1) in alternate years.4,19,20 Extracts from 2004 to 2009 fish were desiccated with cross-linked poly(acrylic acid) and extracted with dichloromethane using pressurized fluid extraction. Lipids were removed via gel permeation chromatography followed by fractionation over deactivated silica to separate polychlorinated biphenyls from select organochlorine pesticides, toxaphene and brominated diphenyl ethers. Quantification of the PBDE fraction was performed via gas chromatography with electron capture detection. Yearly mean surrogate recoveries ranged between 84 and 105%, 69 and 100%, 91 and 113%, and 80 and 107% for PCB-14, PCB-65, PCB-166, and PCT5 (pentachloroterphenyl), respectively. Currently, there is no Certified Reference Material for PBDEs in fish tissue. However, researchers from the National Institutes of Standards and Technology (NIST) published concentrations for several BDEs in the NIST lake trout Standard Reference Material (SRM 1946). Our yearly mean SRM 1946 recoveries (relative to ref 24) ranged 75−91%, 66−79%, 57−64%, 60−95%, and 36−63% for BDE-47, BDE-99, BDE-100, BDE-153, and BDE-154, respectively. A summary table for the NIST SRM 1946 and surrogates can be found in the SI. Interlaboratory Comparison. Results from three previous studies have been added to the current data set to provide a meaningful temporal trend of PBDE concentrations in Great Lakes trout. To assess potential interlaboratory bias between studies five lake trout composites from Lakes Superior and Michigan, collected in 2003, were analyzed by Carlson et al.19 and by our laboratory. No significant difference (t-test, p > 0.01) was observed for the sum of congeners 47, 99, 100, and 153 (t-BDE4, p = 0.33 and 0.04, respectively) at the 99% confidence interval. PBDE concentrations for trout collected in 2000 were reported by Zhu and Hites,4 Carlson et al.,19 and Batterman et al.20 for Lakes Erie, Michigan, Ontario, Superior,

The 10-fold increase in breast milk concentrations from 1992 to 200213 has been tempered by more recent NA studies suggesting human concentrations have leveled off.13 Doucet et al. 10 observed a 5-fold increase in fetal liver PBDE concentrations from 1998 to 2006 in Quebec, with congener patterns similar to the PentaBDE mixture DE-71. The majority of human milk PBDE concentration studies have found that NA values are typically an order of magnitude above levels in Europe and Asia.14−17 Canadian breast milk concentrations ranged over 3 orders of magnitude, suggesting significant exposure route differences in a given population that are not observed for PCBs and dioxins.17 Andersen et al.18 found household dust contributed strongly to PBDE exposure and also noted fish consumption was positively correlated to PBDE blood levels, but was not the dominant exposure pathway. The Great Lakes Fish Monitoring and Surveillance Program (GLFMSP, formerly the Great Lakes Fish Monitoring Program) dates back several decades and is tasked with documenting the health of the Great Lakes through the use of top predator species (lake trout and walleye) as biomonitors. Previous studies have investigated the temporal trends of polychlorinated biphenyls, organochlorine pesticides, mercury, and, more recently, brominated flame retardants.4,19,20 PBDE concentrations in the Great Lakes increased from 1980 to 2003.3,4,19,20 However, Ismail et al.21 observed a decrease in PBDEs in Lake Ontario trout collected in 2000 and 2004, respectively. This report describes the latest measured PBDE concentrations and contemporary trends for lake trout and walleye in the Great Lakes. Previous GLFMSP data sets were included4,19,20 to provide a history of PBDE concentrations, determine the current trends and sources, and project future concentrations of PBDEs in Great Lake trout and walleye.

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EXPERIMENTAL SECTION A discussion of sample collection has been presented previously.22,23 A description of the sample collection and 9891

dx.doi.org/10.1021/es302415z | Environ. Sci. Technol. 2012, 46, 9890−9897


Article

Table 1. PBDE Concentration Summary 2004−2009 year

a

location

n

47 a

99

100

153

154

t-BDEc

Lake Erie

2004 2005 2006 2007 2008 2009

Middle Bass Is. Dunkirk Middle Bass Is. Dunkirk Middle Bass Is. Dunkirk

6 10 10 10 10 10

13.5 6.4 8.5 10.1 10.5 8.1

[1.1] [1.3] [2.3] [2.9] [1.5] [1.4]

2.6 1.3 0.92 1.6 0.90 1.9

[0.6] [0.6] [0.29] [0.61] [0.22] [0.5]

4.0 2.1 2.12 2.37 2.17 1.6

[0.6] [0.5] [0.70] [0.99] [0.44] [0.3]

1.1 [0.2] 0.6 [0.1] LH > LM = LS > LE as compared to 2004, where the concentration hierarchy was LM > LH = LO = LS > LE. Lake Ontario exhibited the highest t-BDE 4 concentrations in 2009 due to a 2-fold increase from 2008 to 2009. 9892



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Figure 2. Temporal trends of t-BDE4 (sum BDE-47, BDE-99, BDE-100, and BDE-153) in Lake trout for Lakes Michigan, Huron, Superior, and Ontario. Pre-2000 data taken from Zhu and Hites (red triangles, ref 4) and Batterman et al. (circles, ref 20); 2000−2003 data from Carlson et al. (squares, ref 19) and 2003−2009 data from current study (diamonds). Points and error bars represent means and 1 standard deviation. Regression lines represent statistically significant correlations using the current data set 2004−2009. See text for details.

significant increase in t-BDE4 concentrations was observed relative to 2008 suggesting a continued concentration decline. Lake Ontario. In Lake Ontario t-BDE4 concentrations appear to level off between the late 1990s and 2001. The piecewise and peak regression analyses identified 1997 (r = 0.85, p < 0.0001) and 2000 (r = 0.82, p < 0.0001), respectively, as maximum concentration years. The 2004−2009 data set exhibited a significant (r = 0.51, p < 0.0001) decrease in t-BDE4 concentrations with a half-life of 5.0 ± 1.2 years. Similar to Lake Huron, the recent concentration decrease may be short-lived as t-BDE4 concentrations in 2009 were significantly greater than in 2008 and 2007 (t test, p < 0.0001). Lake Superior. No apparent site difference was observed in the Lake Superior pre-2000 data. PBDEs exhibited an increasing trend in Lake Superior up to 2000. After 2000, the nearshore site (Apostle Islands) exhibited significantly higher concentrations compared to the offshore site (Keweenaw Point, t-test, p < 0.0001). Lake Superior has the greatest water retention time of all the lakes (191 years, www.epa.gov/ greatlakes/atlas). Therefore, bathymetric differences between the two sites may be influencing feeding habits, sources, and likely the PBDE accumulation in lake trout. From 2000 to 2008 a slight decreasing trend was observed for the even year log normalized concentrations (p = 0.016) with a calculated halflife of 13 ± 5.3 years. No statistically significant trend was observed for the offshore site (odd years). Lake Erie. The peak and piecewise regression identified 2000 (r = 0.70, p < 0.0001) and 1996 (r = 0.80, p < 0.0001) as the t-BDE4 maximum concentration years, respectively. The discrepancy between these two algorithms is likely due to the relatively high t-BDE4 concentrations reported for 2000. Elevated concentrations in 2000 were independently reported by three groups suggesting that the collection or some kind of system anomaly, not analytical bias, was responsible for this apparent outlier. No statistically significant trend was observed for the 2004−2009 suggesting concentrations have leveled off in Lake Erie but have not begun to significantly decrease.

Great Lakes Fish Monitoring Program. All statistics were performed using individual data points (Sigma Plot 10.0, Systat Software, Inc.). Peak concentration years were determined using dynamic fitting nonlinear regression model (i.e., three parameter Gaussian peak model) and a two-segment piecewise regression22,25 using log transformed concentration data. A full description of each model and results for each lake are included in the SI. Agreement between these approaches provided an independent evaluation of maxima, breakpoints, and trends observed in the plots presented below. Lake Huron. When the three previous data sets4,19,20 are combined with the current analysis, t-BDE4 concentrations appear to begin leveling off in 1998 (Figure 2). The peak and piecewise regression results using log transformed data identified 1999 (r = 0.83, p < 0.0001) and 2002 (r = 0.82, p < 0.0001), respectively as the maximum concentration years. After 2004, the t-BDE4 concentrations decreased until 2009. Using the 2004−2009 data set, the calculated removal half-life was 3.8 ± 0.7 years. In 2009, the lake trout t-BDE 4 concentrations significantly (p < 0.0001, t-test) increased relative to 2008, but 2009 values were not significantly different from 2007. The sampling program alternates between two sampling sites each year. Therefore, it is unclear whether elevated concentrations measured in 2009 are due to differences in collection sites or a shift in the temporal trend of t-BDE4 concentrations in Lake Huron. Apparent site differences (odd vs even collection years) have been previously observed by Batterman et al. (ref 20, Figure 2) from 1990 to 1996. After 1996, Batterman et al. and Carlson et al.19 observed no difference in t-BDE4 lake trout concentrations among the two sites in Lake Huron. Lake Michigan. Lake Michigan t-BDE4 concentrations began to level off in the mid to late 1990s with a peak level in 1999 identified by both piecewise and peak regressions (p < 0.0001 and r = 0.90 and 0.92, respectively). Using the contiguous data set of 2004−2009 a half-life of 3.3 ± 0.4 years was calculated. Unlike Lake Huron no statistically 9893



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Figure 3. Temporal trend of the BDE-47/BDE-153 ratio for Lakes Ontario, Michigan, Huron, and Erie. Lines represent regressions using individual data points. See text for significance and resulting halflives (t1/2) and doubling times (t2). Pre-2000 data taken from Zhu and Hites (red triangles, ref 4) and Batterman et al. (circles, ref 20); 2000−2003 data from Carlson et al. (squares, ref 19) and 2003−2009 data from current study (diamonds). Points and error bars represent means and 1 standard deviation.

Herring gull egg PBDE concentrations26,27 have decreased between 2000 and 2006 near LM (3%, Gull Island), LS (54%, Agawa Rocks), and LO (37%, Toronto Harbor). During this period gull egg levels at Fishing Island (Detroit River) and Niagara Falls, near LE, increased 23 and 24%, respectively. This agrees with the observed increase for LE walleye from 2006 to 2008. Gull egg concentrations at the two LH sites exhibited a slight increase and decrease for Channel-Shelter Island and Chantry Island, respectively.26,27 Half-lives calculated for the herring gull eggs from 2000 to 2006 were greater (5.5−100 years26) than those calculated for the Lakes Huron, Michigan and Ontario lake trout. Park et al.28 reported a continued increase in peregrine falcon egg PBDE concentrations from 1985 to 2007 for urban, coastal and rural areas of California. From the reported slope (0.13 log [BDE]/year), the calculated doubling time of 2.3 years is similar to the accumulation rate in Great Lakes fish. Sources. Hites3 and Zhu and Hites4 utilized the ratio of congeners 47 + 99 + 100 to 153 + 154 to illustrate the temporal shift to lower brominated congeners in Great Lakes trout prior to 2000. More recent changes in herring gull and peregrine falcon egg concentrations were accompanied by a shift to higher brominated homologues.28,29 As mentioned above, BDE-154 was not reported in all the data sets compiled for this study. Therefore, we simplified the Zhu and Hites4 method to the ratio of BDE-47 to BDE-153. Using this ratio, we were able to perform a similar assessment of temporal bromine content shifts. As a reference, DE-71 and Bromkal PentaBDE mixtures were analyzed by La Guardia et al.30 resulting in BDE47/BDE-153 ratios of 6.98 and 8.04, respectively. BDE-47 was not detected in the DecaBDE formulation and only trace amounts (1.7% w/w) were observed in one of two OctaBDE formulations analyzed. An increase in this ratio represents the predominance of a PentaBDE mixture. This pattern may result from preferential bioaccumulation of congener 47 and/or an increased PBDE contribution from atmospheric (air/water

exchange) sources. Congener 153 has been identified as a potential debromination marker for BDE-20928,31 and is a native component of the OctaBDE mixture.32 Decreases in the BDE-47 to BDE-153 ratio would suggest an increased exposure to a higher brominated PBDE environmental mixture and/or simply decreased exposure to the PentaBDE mixture. Each lake exhibited a statistically significant log−linear increase of the BDE-47/BDE-153 ratio from 1990 - 2000 (Figure 3) consistent with Zhu and Hites’4 analyses with doubling times (47/153t2) ranging 4−15 years for Lakes Ontario (1980−2005, r = 0.34, p = 0.0015), Huron (1990−2007, r = 0.58, p < 0.0001), and Michigan (1980 − 2005, r = 0.74, p < 0.0001) peaking in 2005−2007. After 2007 the BDE-47/BDE153 ratio was decreasing in all the lakes. In contrast, Lake Erie log BDE-47/BDE-153 regressions exhibited a negative slope (r = 0.60, p < 0.0001) from 1990 to 2009. Congener 153 was below detection limits for all LE composites collected 2006 (Middle Bass Island). Using 1990− 2009 concentrations, the ratio of 47−153 decreases by a factor of 2 (47/153t1/2) every 9.1 ± 1.2 years. The two sites from Lake Superior exhibited inverse trends during the 2002−2008 collection years (Figure 4). A decreasing trend was observed for the Apostle Islands (even) site (47/153t1/2 = 5.3 ± 1.5 years, r = 0.55, p = 0.0003), whereas the BDE-47/BDE-153 ratio increased at the offshore (odd year) site from 2003 to 2007 (47/153t2 = 2 ± 0.2 years, r = 0.85, p < 0.0001). In 2009, the offshore BDE-47/BDE-153 ratio decreased by more than a factor of 2 relative to 2007. While these plots contain a limited number of time points per site (3 and 4), we suggest the dramatic decrease in the offshore site reflects the decreasing trend observed at the nearshore site in previous years. The offshore trend reversal suggests PBDE sources to the two Lake Erie sites are becoming more similar. While the current PentaBDE mixture signature is likely to have been released from products in use prior to the 2004 phase out, elevated levels of BDE-47 may also reflect the role of 9894



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the fact that the PentaBDE mixture was in use during the European studies. From the current analysis, it is apparent that the maxima, leveling off and decline of fish concentrations in the Great Lakes converge prior to the 2004 PentaBDE phase out. This may represent industry anticipation of PentaBDE regulation in NA. In fact, an industry sponsored paper in 199938 acknowledged pressure to restrict use of the PentaBDE mixture. Prior to this, a Voluntary Industrial Commitment (VIC) was reached between European and North American brominated flame retardant industry groups, and the OECD (Organization for Economic Co-operation and Development) in 1995.38 One aspect of the commitment prompted industry to reevaluate handling and disposal practices of PentaBDE to minimize fugitive emissions. It is unclear if preemptive removal of PentaBDE from the market, or improved handling and disposal practices can be credited with the declines in lake trout concentrations after 2000. The rapid collection of ambient and human measurements undoubtedly spurred changes in how PBDEs were viewed by the general public, resulting in changes in how raw materials are processed, and ultimately used. While the current study suggests the Great Lakes are beginning to recover from the use of PBDEs in consumer products, the shift to higher brominated BDEs observed in Lakes Michigan, Huron, Ontario, and Erie trout (this study), herring gull eggs26 and atmospheric samples collected as part of Integrated Atmospheric Deposition Network33 is cause for concern. All of these studies support the need to monitor highly brominated BDE congeners in all biological media. As DecaBDE continues to be used, abiotic and biotic debromination of this mixture may become a significant source of environmental mobile and bioaccumulative PBDEs to the Great Lakes Region.

Figure 4. The temporal trend of BDE-47/BDE-153 for Lake Superior during the 2002−2009 period. Empty and filled circle represent the even (nearshore) and odd (offshore) collection years. Year 2009 is identified by a filled triangle and was not included in the regression analyses. Duplicate data points in year 2003 represent means from Carlson et al. and the current study during laboratory intercalibration.

atmospheric sources to the lakes. The urban plume from Chicago is a significant source of BDE-47 to Lake Michigan.33 The statistically significant decrease observed for Lake Michigan between 2007 and 2009 is most likely due to the phase out in PentaBDE use. Cleveland has been identified as a source of PBDEs to Lake Erie with atmospheric levels enriched in BDE-209.33 This too is reflected in the decrease in the BDE47/BDE-153 ratio trend from 1990 to 2009. Recent declines and trend reversal of the BDE-47/BDE-153 ratio in Lakes Ontario and Huron may reflect the transition from PentaBDE to more highly brominated mixtures (or breakdown products). Site independent trends were observed for Lake Superior. An atmospheric influence (increasing BDE-47/BDE-153 ratio) and local sources (decreasing BDE-47/BDE-153) influence was observed at the offshore and nearshore sites, respectively, for years 2002 to 2008. Anderson et al.18 found a weak correlation between fish and human PBDE levels in the Great Lakes region suggesting alternative sources dominate PBDE exposure. In contrast, Turyk et al.34 reported an increase from 1994 to 1995 to 2001− 2003 but not from 2001−2003 to 2004−2005 in PBDE serum samples of Great Lakes fish consumers. This trend resembles lake trout temporal profiles reported here for LM, LH, and LO. Kierkegaard et al.35 measured five BDEs in pike from Lake Bolmen, Sweden from 1960 to 2000 and observed a maximum in the mid-1980s with declining concentrations from ∼1990 to 2000. The authors noted the decrease in pike concentrations was markedly slower than a companion Guillemot egg study performed at a Baltic Sea site.36 These differences were attributed to potential terrestrial sources impacting pike more than guillemot populations. In contrast, Great Lakes herring gull egg concentration decreases29 appear to lag lake trout concentration changes reported here. This may be explained by a terrestrial scavenging component in herring gull diets. Regardless, it is likely that alternate food sources (terrestrial vs aquatic) of the herring gull and guillemot explain the differences in PBDE declines relative to regional fish species. Other differences seen in regional PBDE concentration trends include a 10 year lag observed between peak environmental and human milk concentrations in Sweden.33,37 Interestingly, this delay is not apparent in the Great Lakes system if fish samples and NA serum samples are compared.34 The temporal response difference may be due to shifts in exposure routes, a decreased residence time in serum compared with PBDE remobilization during breast milk production, or

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ASSOCIATED CONTENT

S Supporting Information *

A brief description of the fish collection procedure, summary of the analytical methods and description of trend fitting models and additional plots of the regression models for each, including summary statistics are included in the Supporting Information. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This project was partially funded by United States Environmental Protection Agency Grant No. GL 96594201. We thank Elizabeth Murphy from the Great Lakes National Program Office for her support and Heather Stapleton from Duke University for providing the individual PBDE standards used in this study. Although the research described in this article has been partly funded by the U.S. EPA, it has not been subjected to the agency’s required peer and policy review and therefore, does not necessarily reflect the views of the agency and no official endorsement should be inferred. 9895



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