Environmental Pollution 214 (2016) 627e634

Contents lists available at ScienceDirect

Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Statewide surveillance of halogenated ame retardants in sh in

Illinois, USA*
Margaret Widelka a, Michael J. Lydy b, Yan Wu a, Da Chen a, *
a
Cooperative Wildlife Research Laboratory and Department of Zoology, Southern Illinois University, Carbondale, IL 62901, United States
b
Center for Fisheries, Aquaculture and Aquatic Sciences and Department of Zoology, Southern Illinois University, Carbondale, IL 62901, United States

a r t i c l e i n f o a b s t r a c t

Article history: In order to better understand the exposure of aquatic systems to halogenated ame retardant con-
Received 6 February 2016 taminants, the present study investigated a variety of legacy and emerging ame retardants in common
Received in revised form carp and largemouth bass collected from 58 stations across Illinois (United States). The data revealed that
15 April 2016
polybrominated diphenyl ethers (PBDEs) generally dominated the ame retardant residues in Illinois
Accepted 18 April 2016
sh. Concentrations of SPBDEs (including all detectable PBDE congeners) ranged from 24.7 to 8270 ng/g
lipid weight (median: 135 ng/g lw) in common carp and 15e3870 ng/g lw (median: 360 ng/g lw) in
largemouth bass. In addition to PBDEs, Dechlorane analogues (i.e. Dec-603, Dec-604, and Chlordane Plus)
Keywords:
Polybrominated ame retardants
were also frequently detected. Median concentrations of SDechloranes (including all detected Dech-
Dechlorane analogues lorane analogues) were 34.4 and 23.3 ng/g lw in common carp and largemouth bass, respectively. Other
Common carp emerging ame retardants, including tetrabromo-o-chlorotoluene (TBCT), hexabromobenzene (HBBZ), 2-
Largemouth bass ethylhexyltetrabromobenzoate (EH-TBB), and bis(2-ethylhexyl)-3,4,5,6-tetrabromo-phthalate (BEH-
Illinois TEBP), were also detected in 40e78% of the sh at the monitored stations. Spatial analysis revealed
signicantly greater PBDE concentrations in sh living in impaired urban streams and lakes compared to
those from the impaired agricultural and unimpaired agricultural/urban waters, demonstrating a sig-
nicant urban inuence on PBDE contamination. Future studies and environmental monitoring are
recommended to focus on temporal trends of PBDEs and alternative ame retardants, as well as human
exposure risks via edible shes, in the identied Areas of Concern within Illinois.
2016 Published by Elsevier Ltd.

1. Introduction et al., 2003; Watanabe and Sakai, 2003). As a consequence of sub-

Flame retardants are chemicals added to textiles, polyurethane
foams, thermoplastics, electronic products, and building materials
to increase their re resistance (Alaee et al., 2003; de Wit et al.,
2010; Covaci et al., 2011). To date, more than 75 different ame-
retardant substances have been commercially manufactured
(Birnbaum and Staskal, 2007; Covaci et al., 2011). Flame retardant
substances can be divided into two classes, additive or reactive,
depending on how they are added to the polymer (Alaee et al.,
2003). Additive halogenated ame retardants, which include pol-
ybrominated diphenyl ethers (PBDEs) as the most often used ad-
ditives, are not chemically blended in the polymer, and are more
likely to leach out of consumer products than reactive types (Alaee
* Flame retardants may enter aquatic systems through releases in
This paper has been recommended for acceptance by Charles Wong.
* Corresponding author.
E-mail address: dachen@siu.edu (D. Chen).
stantial, long-term use, PBDEs are ubiquitous in the environment,
and have been measured in air, water, sh, birds, marine mammals,
and humans, even in remote areas (Hites, 2004; Law et al., 2014;
Letcher et al., 2010; de Wit et al., 2010). Although all three com-
mercial mixtures of PBDEs (i.e. PentaBDE, OctaBDE, and DecaBDE)
were phased out in North America by 2013, they are still present in
many currently in-use or discarded consumer products (Law et al.,
2014). Leaching from the in-use and discarded products may
continue for decades (Chen et al., 2013). In addition, some PBDE
congeners are persistent, bioaccumulative, and toxic (Hites, 2004;
Darnerud, 2003). Toxicological studies suggest that PBDEs may
impact thyroid hormone levels; thyroid, liver, and kidney
morphology; liver ethoxyresorun-O-deethylase activity; neuro-
development; reproductive success; and, fetal toxicity/teratoge-
nicity (Darnerud, 2003).
municipal or industrial wastewater treatment plant efuents and

rez-Fuentetaja et al., 2010; Chen
surface runoff (Song et al., 2006; Pe

http://dx.doi.org/10.1016/j.envpol.2016.04.063
0269-7491/ 2016 Published by Elsevier Ltd.
628 M. Widelka et al. / Environmental Pollution 214 (2016) 627e634
et al., 2011). In addition to aquatic wildlife exposure, humans may
be at risk via intake of contaminated shes (Hites, 2004; Cruz et al.,
2015). Water quality in Illinois has been monitored by projects,
such as the Illinois Fish Contaminant Monitoring Program (FCMP).
To date, these projects have largely focused on heavy metals, pes-
ticides, and polychlorinated biphenyls (PCBs). Information on the
spatial and temporal distributions of halogenated ame retardants
in Illinois waters remained extremely limited. Additionally, re-
strictions on PBDE applications have resulted in increased use of
alternative ame-retardant chemicals to meet ammability stan-
dards. For example, decabromodiphenylethane (DBDPE) and 1,2-
bis(2,4,6-tribromophenoxy)ethane (BTBPE) were considered as
potential DecaBDE or OctaBDE replacements, whereas 2-
ethylhexyltetrabromobenzoate (EH-TBB) and bis(2-ethylhexyl)-
3,4,5,6-tetrabromo-phthalate (BEH-TEBP) were suggested as Pen-
taBDE replacements (Covaci et al., 2011; United States
Environmental Protection Agency, 2014). However, nothing is
known about the levels and distributions of the alternative ame
retardants in Illinois water.
The present study aimed to investigate the contamination status
of a suite of halogenated ame retardants in rivers and lakes across
the state of Illinois via the analysis of sh llet tissues. Specic
objectives were to: (1) determine the levels and composition of
halogenated ame retardant substances in Illinois sh; and, (2)
elucidate the differences in ame retardant exposure among
different water use types across the State of Illinois and identify the
Areas of Concern.
2. Materials and methods
2.1. Chemical and reagents
Reference standards for the 20 PBDE congeners (Table S1) were
purchased from AccuStandard (New Haven, CT, USA). Reference
standards of syn- and anti-Dechlorane Plus (DP) and other Dech-
lorane analogues were purchased from Wellington Laboratories
(Guelph, ON, Canada), including syn- and anti-DP, mono-
dechlorinated DP (C11-DP), didechlorinated DP (C10-DP), Dech-
lorane 601 (Dec-601), Dec-602, Dec-603, Dec-604, Dec-604
Component B (Dec-604CB), and Chlordane Plus (CPlus). Additional
ame retardant chemicals, including pentabromobenzene (PBBZ),
pentabromobenzyl bromide (PBBB), pentabromoethyl benzene
(PBEB), hexabromobenzene (HBBZ), tetrabromo-o-chlorotoluene
(TBCT), BTBPE, DBDPE, BEH-TEBP and EH-TBB, were purchased
from AccuStandard or Wellington Laboratories. Surrogate stan-
dards, including 2,4,6-tribromodiphenyl ether (BDE-30),
2,3,30 ,4,40 ,5-hexabromodiphenyl ether (BDE-156) and
2,20 ,3,30 ,4,5,50 ,6,60 -nonabromo-40 -chlorodiphenyl ether (4PC-BDE-
208), as well as an internal standard, decachlorodiphenyl ether
(DCDE), were purchased from AccuStandard. Diatomaceous earth
and sodium sulfate (10e60 mesh) were purchased from Fisher
Scientic (Hanover Park, IL, USA) and treated in a mufe furnace at
600  C overnight (>12 h) prior to use. Copper (50 mesh, granular,
reagent grade) and high-performance liquid chromatography grade
solvents were purchased from Fisher Scientic. Isolute silica sor-
bent (average pore size: 60) was purchased from Biotage Inc.
(Charlotte, NC, USA) and baked at 130  C prior to use.
2.2. Samples
Fishes (common carp, Cyprinus carpio; largemouth bass, Micro-
pterus salmoides) were collected at 58 stations located in a number
of streams and lakes across the state of Illinois in 2013e2014
(Fig. 1). Fish collection was conducted by the Illinois FCMP.
Depending on water use type, stations were classied by the Illinois
FCMP into three categories, including unimpaired rural, agricul-
tural, or urban streams and lakes (N 25; Type 1), impaired agri-
cultural streams and lakes (N 12; Type 2), and impaired urban
streams and lakes (N 21; Type 3) (Rousey, 2013). Type 1 stations
represent aquatic systems not known to have received pollution
from any agricultural or urban sources. Type 2 stations represent
the aquatic systems receiving known inuences from agricultural
activities. Type 3 stations represent aquatic systems near or within
metropolitan regions and receiving known inuences from urban
sources (e.g. wastewater treatment discharges or urban runoff). At
each station, a minimum of three (and preferably ve) sh, with the
smallest sh being at least 75% of the length of the largest sh, were
collected and comprised for each composite llet sample (Rousey,
2013). The average (standard deviation) lengths were
57.9 7.2 cm and 35.2 5.5 cm for common carp and largemouth
bass, respectively. The composite llet samples were prepared by
removing scales and leaving skin on the sh. The sh were then
lleted to remove bones and ground into a composite. Fish com-
posite samples were stored at 20  C prior to chemical analysis.
2.3. Analysis
The extraction and cleanup procedures were based on Chen
et al. (2011) and Chen et al. (2013) with modication. In brief,
one to three grams of sh composite were ground with diatoma-
ceous earth. After spiking with surrogate standards (BDE-30, BDE-
156, and 4-PC-BDE208), the sample was subject to accelerated
solvent extraction (ASE350; Thermo Scientic, Sunnyvale, CA, USA)
with dichloromethane (DCM) at 100  C and 1500 psi. The extract
was subject to gravimetric determination of lipid content by using
10% of the extract (Chen et al., 2011). The remaining extract was
puried by gel permeation chromatography (GPC) (CO100 GPC
Column, J2 Scientic, Inc.; Columbia, Missouri, USA) to remove bulk
lipids; then further puried on a 2-g silica gel solid phase extraction
(SPE) cartridge. The rst fraction collected from the SPE cartridge
was eluted with 3 mL of hexane and discarded. The second fraction
was eluted with 6.5 mL of a 60:40 hexane/DCM mixture (v/v) fol-
lowed by 7 mL of DCM. The second fraction contained all con-
taminants of interest and was concentrated for instrumental
analysis. The internal standard DCDE (100 ng) was added prior to
instrumental analysis.
All ame retardants of interest were analyzed on an Agilent
6890N gas chromatography coupled to a 5973 mass spectrometry
(GC-MS, Agilent Technologies, Palo Alto, CA, USA) in electron cap-
ture negative ionization (ECNI) mode. The column was a 15-m DB-
5HT column (0.25 mm i.d., 0.1 mm lm thickness, J&W Scientic,
Folsom, CA, USA). The injector was operated in pulsed-splitless
mode, held at 240  C. Injection volume was 1 mL. The initial col-
umn temperature was held at 50  C for 3 min; increased to 300 at
10  C/min and held for 15 min. The GC and MS interface temper-
ature was set at 280  C. Identication and quantication of FR
substances on GC-MS was achieved via selected ion monitoring
(SIM) of characteristic ions (Table S1; Supplemental material).
2.4. Quality assurance and control
Several measures were employed to ensure QA/QC for the pre-
sent study, including matrix spiked experiments, analysis of Stan-
dard Reference Materials (SRMs), process of procedural blanks, and
examination of surrogate standard recoveries. Known amounts
(20e100 ng) of ame retardant analytes of interest were spiked
into a composite of sh (Tilapia, Oreochromis niloticus) llets pur-
chased from local supermarket and analyzed using the methodol-
ogy described above to determine the analyte recoveries
throughout the analysis. These sh llets were tested prior to the
 M. Widelka et al. / Environmental Pollution 214 (2016) 627e634 629

Fig. 1. Sampling stations in the Illinois (U.S.) aquatic systems. Stations were grouped into three categories according to water use types: unimpaired rural/agricultural/urban streams
and lakes (N 25), impaired agricultural streams and lakes (N 12), and impaired urban streams and lakes (N 21).

spiking experiments, and conrmed to be free of all of the target
ame retardants. The mean (standard deviation) of recoveries of
individual ame retardant analytes ranged from 78 10.5% to
104 7.5% in six replicates. The analyses of the National Institute of
Standards Technology SRM 1947 Lake Michigan Fish (n 5)
revealed mean recovery efciencies of PBDE congeners ranging
from 89 to 97% of the certied concentrations. A procedural blank
was run with every ve samples to check for laboratory contami-
nation. None of the ame retardant analytes were detected in the
procedural blanks, except for BDE-47 which was detected in 45% of
blanks but its concentrations were all below the limit of quanti-
cation (LOQ). Recoveries of surrogate standards BDE-30, BDE-156,
and 4PC-BDE208 ranged from 73.4% to 93.2%, 77.9%e105.2%, and
65.2%e84.6%, respectively, in Illinois sh samples. The LOQs of
ame retardants, estimated as an analyte response 10 times the
standard deviation of the noise during instrumental analyses,
ranged from 0.5 to 3.5 ng/g lipid weight (lw) (Table S1).
2.5. Data analysis
For measurements below LOQs, a regression plotting method
was applied to assign values for statistical analysis (Newman, 1995).
All concentrations were lipid-normalized and expressed as ng/g lw,
unless otherwise noted. Lipid contents of common carp and bass
were 9.6 7.8% and 8.1 6.7%, respectively. The residue levels were
corrected based on BDE-156 recoveries, except for BDE-209 and
DBDPE which were adjusted based on the recovery of 4PC-BDE208.
Non-normally distributed data were logarithmically transformed to
approximate a normal distribution before being subjected to
Analysis of Covariance (ANCOVA) and Scheffe's post hoc analysis
(PASW Statistics 18.0; IBM Inc.). The level of signicance was set at
a 0.05.
3. Results and discussion
3.1. PBDEs in Illinois sh
Of the 20 PBDE congeners that were screened, seven com-
pounds, including BDE-28, -47, -49, -99, -100, -153, and -154, were
detected above quantitation limits in all sh samples. Concentra-
tions of SPBDEs (including all detectable PBDE congeners) ranged
from 24.7 to 8270 ng/g lw (median: 135 ng/g lw) in carp and
15e3870 ng/g lw (median: 360 ng/g lw) in largemouth bass (Fig. 2).
Wide presence of PBDEs in Illinois aquatic systems may be due to
their long-term, extensive use in various consumer products.
Global market demand for commercial PentaBDE, OctaBDE and
630 M. Widelka et al. / Environmental Pollution 214 (2016) 627e634

Hale, 2010; Law et al., 2014). For years in which data are available,
the North American market has encompassed the bulk of the
world's PentaBDE production, i.e. 95% in 2001 and 98% in 2003
(Chen and Hale, 2010). Hence, the amounts of major PentaBDE
constituents (i.e. BDE-47, -99, and -100) released into the North
American environment, and therefore readily available to the
aquatic organisms, would be expected to be substantially higher
than elsewhere in the world (Chen and Hale, 2010).

3.2. Dechlorane-related compounds

Selected Dechlorane analogues were also frequently detected in

Illinois shes. Dec-603, Dec-604, and CPlus had detection fre-
quencies over 60%, whereas the other analogues were generally
non-detectable or at low detection frequencies (i.e. < 10%). A
consistent composition prole was observed across stations, in
which Dec-604 and Dec-603 dominated, followed by Dec 604CB
Fig. 2. Median concentrations of SPBDEs (summed concentration of all detectable and CPlus (Fig. 3B). Concentrations of SDechloranes (including all
PBDE congeners), SDechloranes (summed concentration of Dechlorane Plus and its
Dechlorane analogues) ranged from 1.6 to 372 ng/g lw (median:
analogues), TBCT, HBBZ, and EH-TBB in common carp and largemouth bass from all
stations. Error bars represent 75 and 25 percentiles. 34.4 ng/g lw) in carp and non-detected (nd) to 150 ng/g lw (me-
dian: 23.3 ng/g lw) in largemouth bass.
Hoh et al. (2006) rst reported on the environmental occurrence
DecaBDE mixtures reached 67,390 metric tons in 2001, while the
of DP in the Great Lakes of North America, where it has been
demand for DecaBDE alone reached 65,700 and 56,400 metric tons
manufactured by a plant in Niagara Falls, New York for more than
in 2002 and 2003, respectively (de Wit et al., 2006). PBDEs may
40 years. Dechlorane Plus is used as a ame retardant in electrical
enter aquatic systems and accumulate in sediments and biological
hard plastic connectors in televisions and computer monitors, wire
tissues from point (e.g. wastewater discharges) and non-point
coatings, and furniture; and identied as a High Production Volume
sources (e.g. air deposition) (Hites, 2004; Law et al., 2014).
chemical by the U.S. EPA (Betts, 2006; Sverko et al., 2011). Studies
Bioavailability of PBDEs has been demonstrated in both laboratory
after Hoh et al. (2006) also reported the presence of DP in envi-
and eld studies (Law et al., 2014). A number of PBDE congeners are
ronmental (e.g. sediments, air, and indoor dust) and biological
also resistant to environmental degradation and subject to long-
samples (e.g. sh and bird eggs) from other regions of the world,
distance transport via air or water (Law et al., 2014). Conse-
indicating that DP is a worldwide pollutant (Sverko et al., 2011). In
quently, environmental monitoring via sh and other aquatic or-
addition to DP, several other structurally similar Dechlorane ana-
ganisms has demonstrated global contamination by PBDEs,
logues, such as Dec-602, -603, and -604, were recently discovered
including Arctic and Antarctic regions (Law et al., 2014; de Wit
in the Great Lakes basin (Shen et al., 2011a). As DP does not meet
et al., 2010; Letcher et al., 2010). The PBDE congener composition
the specic voltage leakage and thermal standards in certain ap-
of Illinois sh was dominated by BDE-47, followed by BDE-100,
plications, a mixture of Dec-602 and Dec-604 has been used instead
BDE-99, and then BDE-154, BDE-153, and BDE-183 (Fig. 3A).
(Krackeler and Biddell, 1976). The Dec-602 is also used in
Except for BDE-183, PBDE congeners substituted with more than
Fiberglass-Reinforced Nylon-6 at 18% by weight, while Dec-604 is
seven bromine atoms were not detected or quantied in any of the
used at 10e30% by weight in Molykote AS-810 Silicone Grease for
analyzed sh samples. This pattern resembled the congener com-
lubrication of metal-to-metal and metal-to-plastic substrates in
positions found in a majority of studies on sh and other aquatic
electro-mechanical applications (Sverko et al., 2011). Dechlorane
species worldwide, which reected congener-specic bio-
analogues have also been found as impurities in
accumulation or biomagnication potencies (Hites, 2004; Chen and
hexachlorocyclopentadiene-derived pesticides. Dec-603 was
Hale, 2010). By contrast, more brominated congeners, such as BDE-
detected in aldrin and dieldrin, while CPlus was detected in
153 and BDE-154, were usually dominant in terrestrial predators
chlordane and chlordene (Shen et al., 2011b).
(Chen and Hale, 2010).
In contrast with the numerous DP studies (Sverko et al., 2011),
Fishes, particularly carp, have been frequently used to monitor
data on other Dechlorane analogues remain relatively limited
environmental pollution in freshwater systems worldwide. The
worldwide. Available studies were mainly focused in the Great
statewide median SPBDE concentration in common carp (135 ng/g
Lakes basin (Houde et al., 2014; Jobst et al., 2013; Shen et al., 2010,
lw or 14.6 ng/g wet weight or ww) from Illinois waters was
2014). Field studies have suggested that Dechlorane analogues are
generally lower than the concentrations (mean: 13e74 ng/g ww in
bioavailable to the Great Lakes trout and whitesh with Dec-602
2009) in lake trout (Salvelinus namaycush) from the Great Lakes of
and Dec-604 concentrations as high as 34 and 1.2 ng/g lw,
North America (Crimmins et al., 2012). It is also in the lower end of
respectively (Shen et al., 2010). Concentrations of Dec-602 and Dec-
the concentration range reported in carps from other U.S. waters
604CB were reported to be 23.7 20.1 and 139 130 ng/g lw,
(Table 1). For example, median concentrations of SPBDEs were
respectively, in muskellunge (Esox muskellunge) from the St. Law-
reported to be 9140, 1180, and 1340 ng/g lw in common carp from
rence River system (Houde et al., 2014). Dec-604CB was also
the Hyco, Dan, and Roanoke Rivers (Virginia, U.S.), respectively
detected in Lake Ontario sh at concentrations of 10e60 ng/g lw,
(Chen et al., 2011). Concentrations ranged from 191 to 84,044 ng/g
approximately 50e200 times greater than concentrations of
lw in common carp composites from the Gila River (Arizona, US)
Dec604 (Shen et al., 2014). This pattern was different from the
(Echols et al., 2013). When compared to the studies from other
analogue composition in the Illinois sh analyzed in the present
regions of the world, elevated PBDE concentrations were generally
study, where Dec-604CB was generally less abundant than Dec-603
seen in the U.S. shes. This agrees with the ndings in bird and
and Dec-604 (Fig. 3B). The discrepancy may reect the differences
marine mammal studies, where some of the highest PBDE con-
in contamination sources among aquatic systems or the species-
centrations were seen in the North American organisms (Chen and
specic bioaccumulation/biotransformation potential.
 M. Widelka et al. / Environmental Pollution 214 (2016) 627e634 631

Fig. 3. Composition proles of PBDE congeners (A) and Dechlorane analogues (B) in sh (including common carp and largemouth bass) from all stations. Error bars represent
standard deviations.

Table 1
Comparison of PBDE concentrations (ng/g lipid weight) in carp among various studies.

Species Scientic name Country Region Year Concentrationa Reference

Common carp Cyprinus carpio U.S Illinois 2013e2014 135 This study
Common carp Cyprinus carpio U.S Hyco River, Virginia 2006e2007 9140 Chen et al., 2011
Common carp Cyprinus carpio U.S Dan River, Virginia 2006e2007 1180 Chen et al., 2011
Common carp Cyprinus carpio U.S Roanoke River, Virginia 2006e2007 1340 Chen et al., 2011
Common carp Cyprinus carpio U.S Gila River, Hayden, Arizona 2003 191b Echols et al., 2013
Common carp Cyprinus carpio U.S Gila River, Phoenix, Arizona 2003 84,044b Echols et al., 2013
Common carp Cyprinus carpio U.S Gila River, Arlington, Arizona 2003 453b Echols et al., 2013
Common carp Cyprinus carpio U.S Des Plaines River, Illinois 1999 161 Rice et al., 2002
Common carp Cyprinus carpio U.S Detroit River, Michigan 1999 38 Rice et al., 2002
Common carp Cyprinus carpio U.S Eastern Lake Erie 2006 17.5
rez-Fuentetaja et al., 2010
Pe
Common carp Cyprinus carpio Spain Anoia River 2000 113 Labandeira et al., 2007
Common carp Cyprinus carpio Spain Cardener River 2000 260 Labandeira et al., 2007
Common carp Cyprinus carpio Turkey Kahramanmaras 2003 39 Erdogrul et al., 2005
Common carp Cyprinus carpio South Africa Vaal River 2013 20 Chokwe et al., 2015
Common carp Cyprinus carpio China Yangtze River 2006 31 Xian et al., 2008
Common carp Cyprinus carpio China Taihu Lake 2010 16.5 Su et al., 2014
Mud carp Cirrhina molitorella China Dongjiang River 2010 183 He et al., 2012
a
Median or mean concentrations.
b
Concentrations in sh composites.

Nonetheless, the frequent detection of Dechlorane analogues in
Illinois sh in the present study indicated their wide presence in
the Midwestern U.S. freshwater systems. In general the median
concentration of SDechloranes across all studied steams and lakes
was one order of magnitude lower than that of SPBDEs (Fig. 2).
However, concentrations of SDechloranes have surpassed those of
SPBDEs in sh collected from eight of the sampled stations. As
PBDEs have been phased out, alternative ame retardants,
including Dechlorane analogues, may be subject to increasing use
to meet ammability standards.
3.3. Other brominated ame retardants
Among the variety of non-PBDE brominated ame retardants,
TBCT, HBBZ, EH-TBB, and BEH-TEBP were detected in 40e78% of the
sh from the monitored stations; whereas, the others were non-
632 M. Widelka et al. / Environmental Pollution 214 (2016) 627e634
detected or detected at a very low frequency. It should be noted that
the present study did not include hexabromocyclododecane
(HBCD) into the target analyte list. Previous studies have reported a
wide distribution of HBCD in global environment, along with its
bioaccumulative and toxic potencies (Covaci et al., 2006). Conse-
quently it is currently on track for global phase-out of production
and use. Concentrations of TBCT, HBBZ, EH-TBB, and BEH-TEBP
were nd-30 ng/g lw (median: 2.1), nd-90 ng/g lw (median: 5.8),
nd-73 ng/g lw (median: 1.2), and nd-64 ng/g lw (median: <LOQ) in
carp, and nd-36 ng/g lw (median: 1.2), nd-286 ng/g lw (median:
3.2), nd-225 ng/g lw (median: 1.5), and nd-122 ng/g lw (median:
<LOQ) in largemouth bass, respectively (Fig. 2). Hex-
abromobenzene has been used as an additive ame retardant in
paper, plastic, and electronic goods (Watanabe and Sakai, 2003).
Both EH-TBB and BEH-TEBP are major components of the com-
mercial ame retardant mixtures Firemaster 550, Firemaster BZ-54,
and DP-45 (BEH-TEBP only), and are suggested as PentaBDE re-
placements (Ma et al., 2012). A review by Howard and Muir (2010)
identied EH-TBB and BEH-TEBP as high priority chemicals with
persistence and bioaccumulation potential. They have been re-
ported in air, dust, sewage sludge, sh, and marine mammals
(Klosterhaus et al., 2012; La Guardia et al., 2010; Lam et al., 2009;
Ma et al., 2012; Stapleton et al., 2008). Their detection in fresh-
water sh in the present study may indicate the release of these
chemicals from point or non-point sources to Illinois aquatic sys-
tems. In addition to the analytes frequently detected in the present
work, other alternative ame retardants, such as BTBPE and DBDPE,
were also reported in sh from the Great Lakes basin and other
regions of North America (Hoh et al., 2005; Law et al., 2006; Ismail
et al., 2009). Although their current concentrations are generally
lower than PBDEs, continuous application as emerging ame re-
tardants may lead to elevated environmental levels and risk to
ecosystems in the future.
3.4. Contamination differences among water use types
In order to elucidate spatial distribution of halogenated ame
retardants and identify impaired water systems in Illinois, we
compared concentrations of SPBDEs and SDechloranes in carp and
largemouth bass among different water use types, including un-
impaired agricultural and urban streams and lakes, impaired agri-
cultural streams and lakes, and impaired urban streams and lakes
(Fig. 4). The results revealed signicantly greater SPBDE concen-
trations in impaired urban water compared to the impaired agri-
cultural and unimpaired agricultural/urban waters (F2,77 37.49,
p < 0.0001). Stations at impaired urban rivers were usually located
near large metropolitan areas and subject to substantial human
inuence. Areas of Concern were identied as stations where sh
PBDE residue levels reached or surpassed the Environment Canada
Federal Environmental Quality Guidelines (FEQGs) for PBDEs, i.e.
120 ng/g ww for triBDE, 88 ng/g ww for tetraBDE, and 420 ng/g ww
for hexaBDE (Environment Canada, 2013). The identied Areas of
Concern included the stations located in the Mississippi River near
Davenport (Iowa) (81e286 ng/g ww of SPBDEs in carp and bass), in
the Calumet Sag Channel and Little Calumet River near Chicago
(Illinois) (125e420 ng/g ww), and in the harbors of Lake Michigan
(95e584 ng/g ww). Regions with higher human population den-
sities (i.e. metropolitan areas) may have more use of and subse-
quent emissions from PBDE-containing products; thereby,
releasing greater amounts of PBDEs into surrounding waterways
through wastewater discharges and other pathways (e.g. atmo-
spheric deposition), and consequently leading to greater PBDE
exposure to aquatic species. Atmospheric deposition of ame re-
tardants to the Great Lakes basin has been investigated and
demonstrated by a number of studies (Salamova and Hites, 2011a,
2011b; Robson et al., 2013). In a pan-Canadian study, a signicant
positive correlation was observed between SPBDE concentrations
in gull eggs and human population density of the nearest metro-
politan area located within a radius of 100 km distance from each
gull colony (Chen et al., 2012). In the Columbia basin (U.S.), osprey
eggs usually had the greatest PBDE concentrations at locations with
low river ow and high populations where wastewater dilution was
low (Henny et al., 2011). A similar pattern was also observed in
terrestrial ecosystems. For example, concentrations of SPBDEs in
eggs of peregrine falcon (Falcon peregrinus) from the northeastern
U.S. exhibited a signicant positive correlation with the human
population density of the towns where peregrine nests were
located (Chen et al., 2008). These studies demonstrated a signi-
cant urban inuence on environmental PBDE concentrations.
The spatial distribution of Dechlorane analogues exhibited a
pattern unlike that of PBDEs. No statistical difference was observed
among the three water use types (F2,77 1.36, p 0.262). The lack
of signicant urban inuence on Dechlorane contamination may be
due to the fact that several Dechlorane analogues have been used to
replace Mirex and were present as impurities in pesticide products,
such as aldrin, dieldrin, chlordane and chlordene (Shen et al.,
2011b). Shen et al. (2011b) also reported greater sediment con-
centrations of Dec-603 collected near the mouths of agricultural
watersheds in the Great Lakes region (along Lake Erie) than in other
regions, demonstrating an agricultural inuence. Therefore, the
contamination and distribution of Dechlorane analogues may
reect a combined signature of agricultural and consumer product-
related sources. By contrast, PBDE contamination was mainly
attributed to releases from consumer products; thus, an urban in-
uence would be more signicant.
3.5. Implications for future research and environmental monitoring
The present study addressed the spatial distribution of haloge-
nated ame retardants in aquatic systems across the State of Illinois
and identied a number of impaired urban waters as the Areas of
Concern based on the Environment Canada FEQGs for PBDEs.
Although there is low likelihood of adverse effects on aquatic life or
the predator species where the FEQG is met, the FEQG benchmarks
aid in pollution prevention by identifying target pollutants and
evaluating the signicance of pollutant concentrations found in the
environment (Environment Canada, 2013). Future studies and
environmental monitoring are advised to focus on these Areas of
Concern for further investigation, including the temporal changes
of PBDE contamination, the shift of ame retardant contamination
proles, and human exposure risks. The Areas of Concern are
subject to signicant human inuences and the information from
these sites may sensitively reect changes of anthropogenic inputs.
Available studies have revealed that PBDE contamination has begun
to decline or level off since the early 2000's in some North Amer-
ican aquatic systems. For instance, Ismail et al. (2009) reported the
concentrations of dominant PBDE congeners in lake trout from Lake
Ontario (Canada) peaked around the mid-1990s and then either
leveled off or decreased signicantly between 1998 and 2004. A
further study by Crimmins et al. (2012) reported that PBDE con-
centrations declined signicantly in lake trout (1980e2009) from
Lakes Huron, Michigan, and Ontario of the Laurentian Great Lakes
of North America after 2000e2001. Declining trends were also re-
ported in herring gull (Larus argentatus) eggs from the Great Lakes
(Chen et al., 2012; Gauthier et al., 2008). In the San Francisco Bay,
PBDE concentrations have declined by approximately half in sport
sh and 74e95% in bivalves and bird eggs since 2002 (Sutton et al.,
2015). These trends apparently corresponded to recent phase-out
of the production and application of PBDE mixtures in North
America. However, to date, information on the temporal trend of
 M. Widelka et al. / Environmental Pollution 214 (2016) 627e634
Fig. 4. Median concentrations of SPBDEs (top) and SDechloranes (bottom) in common carp and largemouth bass collected from three different types of stations: unimpaired rural/
agricultural/urban streams and lakes (A), impaired agricultural streams and lakes (B), and impaired urban streams and lakes (C). Error bars represent 75 and 25 percentiles.
PBDE contamination in the mid-western U.S. environments is
lacking. Along with the phase-out of PBDE mixtures, additional
halogenated ame retardants (including the chemicals detected in
the present study), as well as the phosphate-based ame re-
tardants, may be subject to increasing market demands. Organo-
phosphate ame retardants have been widely reported in
environmental compartments and humans, suggesting contem-
porary applications and subsequent pollution (van der Veen and de
Boer, 2012). Therefore, future investigations are needed to assess
the shift of ame retardant contamination proles along with time.
Additionally, given that the identied Areas of Concern are subject
to elevated contamination in sh, human health risks via edible sh
should be evaluated therein.
4. Conclusion
Although commercial PBDE mixtures have been phased out in
the U.S., PBDEs are still present as the most dominant halogenated
ame retardants in the Illinois aquatic systems. Through the
statewide surveillance effort, our data demonstrated the wide
distribution of PBDEs in Illinois waters. A comparison among
different water use types revealed signicantly greater SPBDE
concentrations in impaired urban streams and lakes versus
impaired agricultural rivers or unimpaired waters, demonstrating a
substantial urban inuence. The frequent detection of Dechlorane
analogues, as well as the presence of other alternative halogenated
ame retardant substances in some rivers or lakes, raises a concern
on the selected emerging ame retardants currently in use. These
emerging substances may be subject to increasing applications due
to the phase-out of PBDE mixtures. Knowledge on the environ-
mental distribution, behavior, fate, and toxicity of most emerging
ame retardants remains limited in general. Thus, more studies are
needed to better elucidate their potential risks to human and
wildlife health worldwide.
633
Acknowledgements
The present study was nancially supported by the Illinois
Water Research Center (Award No. 2011-03502-02). The authors
thank the Illinois EPA for providing sh samples for chemical
analysis and the support from Dr. Thomas Hornshaw, Ms. Celeste
Crowley, and Mr. Matthew Neely (Illinois EPA). We also thank the
Cooperative Wildlife Research Laboratory and the Department of
Zoology at Southern Illinois University-Carbondale.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.envpol.2016.04.063.
References
din, A., Bergman, ., 2003. An overview of commercially used
Alaee, M., Arias, P., Sjo
brominated ame retardants, their applications, their use patterns in different
countries/regions and possible modes of release. Environ. Int. 29, 683e689.
Betts, K.S., 2006. A new ame retardant in the air. Environ. Sci. Technol. 40,
1090e1091.
Birnbaum, L.S., Staskal, D.F., 2007. Brominated ame retardants: cause for concern?
Environ. Health Persp 112, 9e17.
Chen, D., La Guardia, M.J., Harvey, E., Amaral, M., Wohlfort, K., Hale, R.C., 2008.
Polybrominated diphenyl ethers in peregrine falcon (Falco peregrinus) eggs
from the northeastern U.S. Environ. Sci. Technol. 42, 7594e7600.
Chen, D., Hale, R.C., 2010. A global review of polybrominated diphenyl ether ame
retardant contamination in birds. Environ. Int. 36, 800e811.
Chen, D., La Guardia, M.J., Luellen, D.R., Harvey, E., Mainor, T.M., Hale, R.C., 2011. Do
temporal and geographical patterns of HBCD and PBDE ame retardants in U.S.
sh reect evolving industrial usage? Environ. Sci. Technol. 45, 8254e8261.
Chen, D., Letcher, R.J., Burgess, N.M., Champoux, L., Elliott, J.E., Hebert, C.E.,
Martin, P., Wayland, M., Weseloh, D.V.C., Wilson, L., 2012. Flame retardants in
eggs of four gull species (Laridae) from breeding sites spanning Atlantic to
Pacic Canada. Environ. Pollut. 168, 1e9.
Chen, D., Martin, P., Burgess, N.M., Champoux, L., Elliott, J.E., Forsyth, D.J., Idrissi, A.,
Letcher, R.J., 2013. European starlings (Sturnus vulgaris) suggest that landlls are
an important source of bioaccumulative ame retardants to Canadian terrestrial
ecosystems. Environ. Sci. Technol. 47, 12238e12247.
Chokwe, T.B., Okonkwo, J.O., Sibali, L.L., Ncube, E.J., 2015. Alkylphenol ethoxyates
and brominated ame retardants in water, sh (carp) and sediment samples
from the Vaal River, South Africa. Environ. Sci. Pollut. Res. 22, 11922e11929.
634 M. Widelka et al. / Environmental Pollution 214 (2016) 627e634
Covaci, A., Gerecke, A.C., Law, R.J., Voorspoels, S., Kohler, M., Heeb, N.V., Leslie, H.,
Allchin, C.R., de Boer, J., 2006. Hexabromocyclododecanes (HBCDs) in the
environment and humans: a review. Environ. Sci. Technol. 40, 3679e3688.
Covaci, A., Harrad, S., Abdallah, M.A.-E., Ali, N., Law, R.J., Herzke, D., de Wit, C.A.,
2011. Novel brominated ame retardants: a review of their analysis, environ-
mental fate and behavior. Environ. Int. 37, 532e556.
Crimmins, B.S., Pagano, J.J., Xia, X., Hopke, P.K., Milligan, M.S., Holsen, T.M., 2012.
Polybrominated diphenyl ethers (PBDEs): turning the corner in Great Lakes
trout 1980e2009. Environ. Sci. Technol. 46, 9890e9897.
Cruz, R., Cunha, S.C., Casal, S., 2015. Brominated ame retardants and seafood
safety: a review. Environ. Int. 77, 116e131.
Darnerud, P.O., 2003. Toxic effects of brominated ame retardants in man and in
wildlife. Environ. Int. 29, 841e853.
de Wit, C.A., Alaee, M., Muir, D.C.G., 2006. Levels and trends of brominated ame
retardants in the Arctic. Chemosphere 64, 209e233.
de Wit, C.A., Herzke, D., Vorkamp, K., 2010. Brominated ame retardants in the
Arctic environment e trends and new candidates. Sci. Total Environ. 408,
2885e2918.
Echols, K.R., Peterman, P.H., Hinck, J.E., Orazio, C.E., 2013. Polybrominated diphenyl
ether metabolism in eld collected sh from the Gila River, Arizona, USA e
levels, possible sources, and patterns. Chemosphere 90, 20e27.
Environment Canada, 2013. Canadian Environmental Protection Act, 1999 Federal
Environmental Quality Guidelines Polybrominated diphenyl ethers (PBDEs).
Available at: https://www.ec.gc.ca/ese-ees/default.asp?langEn&n05DF7A37-
1 (accessed April 2016).
Erdogrul, O., Covaci, A., Schepens, P., 2005. Levels of organochlorine pesticides,
polychlorinated biphenyls and polybrominated diphenyl ethers in sh species
from Kahramanmaras. Turkey. Environ. Int. 31, 703e711.
Gauthier, L.T., Hebert, C.E., Weseloh, D.V.C., Letcher, R.J., 2008. Dramatic changes in
the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull
eggs from the Laurentian Great Lakes: 1982e2006. Environ. Sci. Technol. 42,
1524e1530.
He, M., Luo, X., Chen, M., Sun, Y., Chen, S., Mai, B., 2012. Bioaccumulation of poly-
brominated diphenyl ethers and decabromodiphenyl ethane in sh from a river
system in a highly industrialized area, South China. Sci. Total Environ. 419,
109e115.
Henny, C.J., Grove, R.A., Kaiser, J.L., Johnson, B.L., Furl, C.V., Letcher, R.J., 2011.
Wastewater dilution index partially explains observed polybrominated
diphenyl ether ame retardant concentrations in osprey eggs from Columbia
River Basin, 2008e2009. Ecotoxicology 20, 682e697.
Hites, R.A., 2004. Polybrominated diphenyl ethers in the environment and in peo-
ple: a meta-analysis of concentrations. Environ. Sci. Technol. 38, 945e956.
Hoh, E., Zhu, L., Hites, R.A., 2005. Novel ame retardants, 1,2-bis(2,4,6-
tribromophenoxy)ethane and 2,3,4,5,6-pentabromoethylbenzene, in United
States' environmental samples. Environ. Sci. Technol. 39, 2472e2477.
Hoh, E., Zhu, L., Hites, R.A., 2006. Dechlorane plus, a chlorinated ame retardant, in
the Great lakes. Environ. Sci. Technol. 40, 1184e1189.
Houde, M., Berryman, D., de Lafontaine, Y., Verreault, J., 2014. Novel brominated
ame retardants and dechloranes in three sh species from the St. Lawrence
River, Canada. Sci. Total Environ. 479e480, 48e56.
Howard, P.H., Muir, D.C.G., 2010. Identifying new persistent and bioaccumulative
organics among chemicals in commerce. Environ. Sci. Technol. 44, 2277e2285.
Ismail, N., Gewurtz, S.B., Pleskach, K., Whittle, D.M., Helm, P.A., Marvin, C.H.,
Tomy, G.T., 2009. Brominated and chlorinated ame retardants in Lake Ontario,
Canada, lake trout (Salvelinus namaycush) between 1979 and 2004 and possible
inuences of food-web changes. Environ. Tox. Chem. 28, 910e920.
Jobst, K.J., Shen, L., Reiner, E.J., Taguchi, V.Y., Helm, P.A., McCrindle, R., Backus, S.,
2013. The use of mass defect plots for the identication of (novel) halogenated
contaminants in the environment. Anal. Bioanal. Chem. 405, 3289e3297. Kelly,
B.C., Ikonomou, M.G., Blair, J.D., Morin, A.E., Gobas, F.A.P.C., 2007. Food web-
specic biomagnication of persistent organic pollutants. Science 317, 236-239.
Klosterhaus, S.L., Stapleton, H.M., La Guardia, M.J., Greig, D.J., 2012. Brominated and
chlorinated ame retardants in San Francisco Bay sediments and wildlife. En-
viron. Int. 47, 56e65.
Krackeler, J.P., Biddell, W.G., 1976. Insulated high voltage wire coated with a ame
retardant composition. U.S. Patent No. 3,900,533.
Labandeira, A., Eljarrat, E., Barcelo
, D., 2007. Congener distribution of poly-
brominated diphenyl ethers in feral carp (Cyprinus carpio) from the Llobregat
River. Spain. Environ. Pollut. 146, 188e195.
La Guardia, M.J., Hale, R.C., Harvey, E., Chen, D., 2010. Flame-retardants and other
organohalogens detected in sewage sludge by electron capture negative ion
mass spectrometry. Environ. Sci. Technol. 44, 4658e4664.
Lam, J.C.W., Lau, R.K.F., Murphy, M.B., Lam, P.K.S., 2009. Temporal trends of hex-
abromocyclododecanes (HBCDs) and polybrominated diphenyl ethers (PBDEs)
and detection of two novel ame retardants in marine mammals from Hong
Kong, South China. Environ. Sci. Technol. 43, 6944e6949.
Law, K., Halldorson, T., Danell, R., Stern, G., Gewurtz, S., Alaee, M., Marvin, C.,
Whittle, M., Tomy, G., 2006. Bioaccumulation and trophic transfer of some
brominated ame retardants in a Lake Winnipeg (Canada) food web. Environ.
Tox. Chem. 25, 2177e2186.
Law, R.J., Covaci, A., Harrad, S., Herzke, D., Abdallah, M.A.-E., Fernie, K., Toms, L.L.,
Takigami, H., 2014. Levels and trends of PBDEs and HBCDs in the global envi-
ronment: status at the end of 2012. Environ. Int. 65, 147e158.
Letcher, R.J., Bustnes, J.O., Dietz, R., Jenssen, B.M., Jrgensen, E.H., Sonne, C.,
Verreault, J., Vijayan, M.M., Gabrielsen, G.W., 2010. Exposure and effects
assessment of persistent organohalogen contaminants in arctic wildlife and
sh. Sci. Total Environ. 408, 2995e3043.
Ma, Y., Venier, M., Hites, R.A., 2012. 2-ethylhexyl tetrabromobenzoate and bis(2-
ethylhexyl) tetrabromophthalate ame retardants in the Great Lakes atmo-
sphere. Environ. Sci. Technol. 46, 204e208.
Newman, M.C., 1995. Quantitative Methods in Aquatic Ecotoxicology. Lewis Pub-
lishers, Inc., Boca Raton, pp. 21e40.

rez-Fuentetaja, A., Lupton, S., Clapsadl, M., Samara, F., Gatto, L., Biniakewitz, R.,
Pe
Aga, D.S., 2010. PCB and PBDE levels in wild common carp (Cyprinus carpio)
from eastern Lake Erie. Chemosphere 81, 541e547.
Rice, C.P., Chernyak, S.M., Begnoche, L., Quintal, R., Hickey, J., 2002. Comparisons of
PBDE composition and concentration in sh collected from the detroit river, MI
and Des plaines river, IL. Chemosphere 49, 731e737.
Robson, M., Melymuk, L., Bradley, L., Treen, B., Backus, S., 2013. Wet deposition of
brominated ame retardants to the Great Lakes basin e status and trends.
Environ. Pollut. 182, 299e306.
Rousey, M., 2013. Quality Assurance Project Plan: Study of Peruorinated Com-
pounds in Fish Tissue and Surface Water Samples. Illinois Environmental Pro-
tection Agency IEPA BOW QAPP001-00-0511.
Salamova, A., Hites, R.A., 2011a. Discontinued and alternative brominated ame
retardants in the atmosphere and precipitation from the Great Lakes basin.
Environ. Sci. Technol. 45, 8698e8706.
Salamova, A., Hites, R.A., 2011b. Dechlorane plus in the atmosphere and precipi-
tation near the Great Lakes. Environ. Sci. Technol. 45, 9924e9930.
Shen, L., Reiner, E.J., MacPherson, K.A., Kolic, T.M., Sverko, E., Helm, P.A., Bhavsar, S.P.,
Brindle, I.D., Marvin, C.H., 2010. Identication and screening analysis of halo-
genated norbornene ame retardants in the Laurentian Great Lakes: dechlor-
anes 602, 603, and 604. Environ. Sci. Technol. 44, 760e766.
Shen, L., Reiner, E.J., Helm, P.A., Marvin, C.H., Hill, B., Zhang, X., MacPherson, K.A.,
Kolic, T.M., Tomy, T.M., Brindle, I.D., 2011a. Historic trends of dechloranes 602,
603, 604, Dechlorane Plus and other norbornene derivatives and their bio-
accumulation potential in Lake Ontario. Environ. Sci. Technol. 45, 3333e3340.
Shen, L., Reiner, E.J., MacPherson, K.A., Kolic, T.M., Helm, P.A., Richman, L.A.,
Marvin, C.H., Burniston, D., Hill, B., Brindle, I.D., McCrindle, B., Chittim, B.G.,
2011b. Dechloranes 602, 603, 604, dechlorane plus and chlordene plus, a newly
detected analogue, in tributary sediments of the Laurentian Great lakes. Envi-
ron. Sci. Technol. 45, 693e699.
Shen, L., Jobst, K.J., Reiner, E.J., Helm, P.A., McCrindle, R., Taguchi, V.Y., Marvin, C.H.,
Backus, S., MacPherson, K.A., Brindle, I.D., 2014. Identication and occurrence of
analogues of dechlorane 604 in Lake Ontario sediment and their accumulation
in sh. Environ. Sci. Technol. 48, 11170e11177.
Song, M., Chu, S., Letcher, R.J., Seth, R., 2006. Fate, partitioning, and mass loading of
polybrominated diphenyl ethers (PBDEs) during the treatment processing of
municipal sewage. Environ. Sci. Technol. 40, 6241e6246.
Stapleton, H.M., Allen, J.G., Kelly, S.M., Konstantinov, A., Klosterhaus, S., Watkins, D.,
McClean, M.D., Webster, T.F., 2008. Alternate and new brominated ame re-
tardants detected in U.S. house dust. Environ. Sci. Technol. 42, 6910e6916.
Su, G., Saunders, D., Yu, Y., Yu, H., Zhang, X., Liu, H., Giesy, J.P., 2014. Occurrence of
additive brominated ame retardants in aquatic organisms form Tai Lake and
Yantze River in Eastern China, 2009e2012. Chemosphere 114, 340e346.
Sutton, R., Sedlak, M.D., Yee, D., Davis, J.A., Crane, D., Grace, R., Arsem, N., 2015.
Declines in polybrominated diphenyl ether contamination of San Francisco Bay
following production phase-out and bans. Environ. Sci. Technol. 49, 777e784.
Sverko, E., Tomy, G.T., Reiner, E.J., Li, Y., McCarry, B.E., Arnot, J.A., Law, R.J., Hites, R.A.,
2011. Dechlorane Plus and related compounds in the environment: a review.
Environ. Sci. Technol. 45, 5088e5098.
United States Environmental Protection Agency, 2014. An Alternative Assessment
for the Flame Retardant Decabromodiphenyl Ether (DecaBDE). Available from:
htttp://www.epa.gov/dfe/pubs/projects/decaBDE/deca-report-complete.pdf
(accessed January 2016).
van der Veen, I., de Boer, J., 2012. Phosphorus ame retardants: properties, pro-
duction, environmental occurrence, toxicity and analysis. Chemosphere 88,
1119e1153.
Watanabe, I., Sakai, S., 2003. Environmental release and behavior of brominated
ame retardants. Environ. Int. 29, 665e682.
Xian, Q., Ramu, K., Isobe, T., Sudaryanto, A., Liu, X., Gao, Z., Takahashi, S., Yu, H.,
Tanabe, S., 2008. Levels and body distribution of polybrominated diphenyl
ethers (PBDEs) and hexabromocyclododecanes (HBCDs) in freshwater shes
from the Yangtze River, China. Chemosphere 71, 268e276.