Journal of Environmental Sciences 2011, 23(1) 133–138
Polybrominated diphenyl ethers in chicken tissues and eggs from an electronic
waste recycling area in southeast China
Xiaofei Qin1, Zhanfen Qin1,∗, Yan Li1, Yaxian Zhao1, Xijuan Xia1, Shishuai Yan1,
Mi Tian1, Xingru Zhao2, Xiaobai Xu1, Yongjian Yang3
1. State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-environmental Sciences,
Chinese Academy of Sciences, Beijing 100085, China. E-mail: email@example.com
2. Chinese Research Academy of Environmental Sciences, Beijing 100012, China
3. Taizhou No. 1 Middle School, Taizhou 318000, China
Received 03 March 2010; revised 06 April 2010; accepted 03 June 2010
The levels and distributions of polybrominated diphenyl ethers (PBDEs) in chicken tissues from an electronic waste (e-waste)
recycling area in southeast China were investigated. Human dietary intake by local residents via chicken muscle and eggs was estimated.
The mean PBDEs concentrations in tissues ranged from 15.2 to 3138.1 ng/g lipid weight (lw) and in egg the concentration was 563.5
ng/g lw. The results showed that the level of total PBDEs (?PBDEs) in the chicken tissue was 2–3 orders of magnitude higher than
PBDEs in tissues depend on tissue-specificity rather than the “lipid-compartment”. BDE-209 was the predominant congener (82.5%–
94.7% of?PBDEs) in all chicken tissues except in brain (34.7% of?PBDEs), which indicated that deca-BDE (the major commercial
terrestrial animals. The dietary PBDEs intake of the local residents from chicken muscle and egg, assuming only local bred chickens
and eggs were consumed, ranged from 2.2 to 22.5 ng/(day·kg body weight (bw)) with a mean value of 13.5 ng/(day·kg bw), which was
one order of magnitude higher than the value reported in previous studies for consumption of all foodstuffs.
those reported in the literature. The large difference of?PBDEs concentrations between tissues confirmed that the distribution of
PBDE formulation comprising 65%–70% of total production) was major pollution source in this area and could be bioaccumulated in
Key words: polybrominated diphenyl ethers; chicken; egg; bioaccumulation; tissue distribution; exposure risk
Citation: Qin X F, Qin Z F, Li Y, Zhao Y X, Xia X J, Yan S S et al., 2011. Polybrominated diphenyl ethers in chicken tissues and eggs
from an electronic waste recycling area in southeast China. Journal of Environmental Sciences, 23(1): 133–138.
Rapid technology change has resulted in a fast-growing
surplus of electronic waste (e-waste) around the globe.
Recently, e-wastes are becoming a major environmental
concern, particularly in developing countries where e-
wastes are mainly imported from developed countries
(Schwarzeret al.,2005; Leung etal., 2007). Itwasreported
that 50%–80% of the global e-wastes are legally or illegal-
ly imported to Asia. In the process of primitive recycling
treatment of e-wastes, the released hazardous chemicals
resulted in serious pollution problem in local area and
surrounding regions (Chan et al., 2007; Leung et al.,
2008; Zheng et al., 2008). Among these pollutants, poly-
brominated diphenyl ethers (PBDEs), as additive flame
retardants in electronic equipments, are one class pollutant
of the most concerns due to persistence, bioaccumulation
and potential toxicity (Darnerud and Sinjari, 1996; Eriks-
son et al., 1999, 2002).
* Corresponding author. E-mail: firstname.lastname@example.org
Wenling is located in Taizhou City, southeast coast of
China. As well as Guiyu of Guangdong Province, the
region near Wenling is one of the largest e-wastes recycle
process areas (Wang et al., 2005; Bi et al., 2007; Leung et
al., 2007). In this area many small family-run workshops
have devoted to processing discarded electronic waste,
known as e-waste, for ten years. They disassembled and
shattered e-waste into powder to select the usable materi-
of PBDEs in soils, sediments and biotic samples from this
PBDEs-polluted area (Liang et al., 2008; Yang et al., 2008,
2009), information on PBDEs pollution status in this area
is scarce, and data on exposure risk of PBDEs for local
residents are limited.
Birds have been applied as sentinel species for moni-
toring PBDEs pollution status on relative large geographic
scales (Naert et al., 2007; Chen et al., 2007; Voorspoels et
of PBDEs levels in bird tissues and eggs, in past decades,
is coincident with that observed for other animals and
human being (Nortstrom et al., 2002; Hites, 2004). There
134 Journal of Environmental Sciences 2011, 23(1) 133–138 / Xiaofei Qin et al. Vol. 23
is potential exposure risk of PBDEs for local residents via
poultry meat and eggs, which are common constituents of
The main objectives of the present study were to
measure the levels of PBDEs in chickens and eggs from
Wenling and to estimate dietary uptake of PBDEs by local
congener patterns of PBDEs in chicken tissues were also
1 Materials and methods
Polychlorinated biphenyl (PCB) 209 used as surrogate
was obtained from Supelco (USA). A standard solu-
tion of PBDE congeners (EO-5278) was obtained from
Cambridge Isotope Laboratories, Inc. (USA); n-hexane,
methylene dichloride, and nonane at pesticide grade were
from Tedia (USA); and anhydrous sodium sulfate, sulfuric
acid, sodium hydroxide, and anhydrous ethanol at analyti-
cal grade were from Beijing Chemical Factory (China).
1.2 Study area and sampling
Wenling area is located in the south of Taizhou, east of
Zhejiang Province, with population of about one million.
In this area, family-run workshops for e-waste recycling
process are very popular. For many families it is the
main familiar income. In addition, traditional agriculture,
such as rice growing, vegetables planting, fish farming,
and poultry breed, also plays an important role in the
local economic system. Sanhuang (SH) chicken, a popular
Chinese indigenous breed, is among the most consumed
meat in Chinese market. In this investigation SH chickens
(n = 4, about 3–4 months old) and eggs (n = 15) were
obtained from an e-wastes recycling village in Wenling
area. Various tissues of chickens were excised and all the
tissues were cleaned with deionized water, wrapped in
aluminum foil, and sealed in plastic bags to minimize the
possibility of contamination after sampling. Grain used to
feed the chickens and soil samples from location where the
chickens roamed were also collected. Then, tissue, grain
and soil samples were transported to analysis laboratory in
an ice box and stored in freezer at –20°C until analysis.
Eggs were transported at room temperature and stored in
refrigerator at 4°C until analysis.
1.3 Extraction and cleanup
The samples were freeze-dried and homogenized with
anhydrous sodium sulfate, 1 ng PCB 209 were spiked
into the sample as surrogate and equilibrated for 2 hr in
desiccator. Then, the sample was ultrasonic extracted for
4 min with 30 mL of hexane/dichloromethane (1:1, V/V).
After centrifuged (3000 ×g for 3 min) the supernatant was
transferred to a flask. The extraction process was repeated
3 times and the extracts were combined. The lipids con-
tent was determined gravimetrically after evaporating the
extract to dryness. The sample was then reconstituted in
1 mL hexane and was cleaned up with multilayer silica gel
column (0.2 m × 15-mm internal diameter) packed with 1
gel, 4 g acid silica gel (44% concentrated sulfuric acid,
W/W), 4 g acid silica gel (22% concentrated sulfuric acid,
W/W), 1 g activated silica gel and 2 g anhydrous sodium
sulfate. PBDE fraction was eluted from the column with
100 mL hexane. The eluent was concentrated to about 2
mL in a rotary evaporator. Then the sample solution was
transferred to a vial and reduced to a volume of 20 µL
under a gentle stream of N2.
1.4 Analysis of PBDEs
The analysis of PBDEs was performed using an Agilent
6890 series gas chromatograph equipped with Agilent
5973 mass spectrometer (Agilent Technologies, USA)
operated in electron capture negative ionization (ECNI)
mode. The gas chromatography column was a 15 m × 0.25
mm i.d. DB-5 MS capillary column with a film thickness
of 0.25 µm. The injector and interface temperatures were
290 and 300°C, respectively. A 1 µL aliquot of sam-
ple solution was injected with pulsed splitless injection
mode. Helium was used as carrier gas at constant flow
(1.0 mL/min) and methane was used as reagent gas. The
ion source and quadrupole temperatures were 150°C. The
oven temperature was programmed from 80°C (held for 1
min) to 200°C at a rate of 10°C/min and then from 200 to
300°C (held for 15 min) at a rate of 20°C/min. The mass
spectrometer was operated in the selected ion monitoring
(SIM) mode and ions of m/z 79 and 81 were monitored for
BDE-47, 100, 99, 154, 153, 183 and m/z 486.7 and 488.7
Identification of analyte was based on comparison of
retention time and mass spectrum with appropriate stan-
dards. Quantification was performed by external standard
method with multi-level calibration curve spanning the
range of anticipated analyte concentrations in the samples.
1.5 Quality assurance/quality control
To avoid the potential sample contamination and PBDE
degradation, the proper handling was adopted from sample
collection to chemical analysis. The method precision and
recovery were determined by analyzing fish tissue that was
spiked with PBDEs standard. The recoveries for target
deviation of 20%. One procedural blank was run for every
batch of nine samples to check the potential contamination
in analysis process. The recoveries of surrogate in all
samples ranged from 85% to 110%. The limit of detection
(LOD) was defined as the concentration of analyte in the
sample producing a peak with the ratio of signal to noise
of 3 (peak-to-peak). LODs ranged from 0.001 to 0.05 ng/g
for BDE-47 to BDE-183 and 0.1 ng/g for BDE-209.
1.6 EDI of PBDEs through chicken and eggs consump-
The daily dietary intake of PBDEs was estimated de-
pending on PBDEs concentration in food and the daily
food consumption. In addition, the body weight of the
human can influence the tolerance of pollutants. Estimated
No. 1 Polybrominated diphenyl ethers in chicken tissues and eggs from an electronic waste recycling area in southeast China135
daily intake (EDI) was calculated assuming that the local
residents consume only local bred chickens and eggs. EDI
was calculated as follows:
EDI =C × Cons
where, C (ng/g lw) is the concentration of PBDEs in
daily average consumption of chicken muscle and eggs in
this region, and BW represents the body weight. Average
body weight of the adult residents in this area was 60 kg
in the present study. Based on the dietary nutrition intake
level survey by Zhong et al. (2006), poultry meat (chicken
as the dominant) was one of the staple foods for daily
consumption, and the adult residents in this area have an
average daily intake of 23 g poultry meat and 17.6 g eggs
1.7 Statistical analyses
All the statistical analysis was performed using SPSS
software version 13.0 (SPSS Inc., Chicago, USA). Signifi-
cant difference among the congener in the same tissue was
analyzed using one-way analysis of variance. Significant
difference concentration of total PBDEs (?PBDEs) be-
A value of α = 0.05 was chosen to give a significant
tween tissues was analyzed using Mann-Whitney U test.
2 Results and discussion
2.1 PBDEs levels and tissue distribution
Table 1 and Fig. 1 show lipid-normalized concentrations
(lipid weight, lw) of individual PBDE congeners and
?PBDEs in various tissues of chickens, including blood,
The mean concentrations of?PBDEs in various tissues
2476.93) ng/g lw in fat. The concentrations of?PBDEs in
much higher than those in chicken breast from markets of
U.S. (0.3 ng/g ww) (Schecter et al., 2004) and Belgium
(0.03 ng/g ww) (Voorspoels et al., 2007b). The mean
concentrations of?PBDEs in the chicken muscle and liver
lw) were about 100 times higher than those reported in
male chickens (muscle: 66 ng/g lw; liver: 41 ng/g lw)
and male ducks (muscle: 6.6 ng/g lw; liver: 8.5 ng/g lw)
collected from an e-waste recycling site in Guangdong
Province, South China (Luo et al., 2009). Concentration of
fat, intestine, liver, muscle, kidney, lung, testis and brain.
ranged from (15.23 ± 8.27) ng/g lw in brain to (3138.06 ±
chicken muscle (5.90 ± 2.54 ng/g wet weight (ww)) were
samples (muscle: 1092.42 ng/g lw; liver: 1077.81 ng/g
Tissue distribution of total polybrominated diphenyl ethers.
?PBDEs in eggs averaged (563.51 ± 339.82) ng/g lw and
contamination level was two orders of magnitude higher
than those in Belgian home-produced eggs (7.8 ng/g lw)
(Covaci et al., 2009) and eggs (0.5 ng/g lw) from markets
of Spain (Bocio et al., 2003).
The concentration of?PBDEs decreased in the follow-
muscle ? liver > kidney ? lung > testis > brain (Fig.
1). Statistical analysis revealed that the concentration of
?PBDEs in muscle and liver were not different. Also, no
tween kidney and lung was found. However, brain showed
lower levels than the other tissues. Matthews and Dedrick
tissues. If so, concentrations of PBDEs, as a class of
lipophilic compounds, on a lipid-weight basis might be
similar in all the tissues. Our results showed that lipid-
normalized concentrations of?PBDEs in some tissues
reports (Voorspoels et al., 2006; Liang et al., 2008).
Some researchers suggested that the difference dis-
tribution of?PBDEs in tissues resulted from different
spoels et al. (2006) reported concentration of?PBDEs
species and suggested that relatively higher metabolic
activity in liver than in muscle could explain this phe-
nomenon. Luo et al. (2009) also explained their results
in chickens using this hypothesis. However, some studies
(38.31 ± 42.31 ng/g ww) in the present study. This PBDEs
ing order in the present study: fat > blood > intestine >
significant difference in the concentration of?PBDEs be-
were very different. This result is in consistent with other
metabolic activities in different tissues. For example, Voor-
in muscle were higher than that in liver for several bird
Levels of individual PBDE congeners in various tissues of chickens (n = 4) from an e-wastes recycling area in Southeast China*
Level of individual PBDE congeners (ng/g lipid weight)
Fat TestisKidney LungMuscle IntestineLiver Blood Brain
25.24 ± 11.83
9.05 ± 6.70
31.34 ± 17.87
7.60 ± 6.31
39.90 ± 27.61
54.57 ± 57.13
2971.65 ± 2454.27
6.84 ± 4.52
1.93 ± 1.77
5.88 ± 4.19
0.97 ± 0.84
5.09 ± 2.79
7.22 ± 5.38
131.22 ± 121.95
6.99 ± 3.83
3.19 ± 1.27
6.14 ± 2.42
1.45 ± 0.43
7.95 ± 3.83
14.52 ± 19.61
443.34 ± 161.50
7.34 ± 5.45
1.94 ± 0.72
6.80 ± 4.03
1.47 ± 0.75
6.53 ± 8.10
17.64 ± 19.31
402.67 ± 88.76
20.10 ± 28.84
3.32 ± 2.54
14.25 ± 17.06
2.10 ± 1.77
10.14 ± 8.43
8.66 ± 6.11
1033.86 ± 729.58
37.85 ± 39.20
8.90 ± 6.93
41.83 ± 48.93
4.98 ± 3.96
28.72 ± 20.74
42.44 ± 59.24
1491.31 ± 1120.27
21.27 ± 15.04
7.69 ± 4.52
15.45 ± 11.60
2.04 ± 2.15
16.27 ± 13.38
35.72 ± 62.13
979.38 ± 643.38
25.98 ± 13.95
14.69 ± 6.22
26.63 ± 12.79
9.35 ± 4.74
29.83 ± 15.37
62.12 ± 73.07
2491.16 ± 3019.06
1.90 ± 1.28
0.67 ± 0.51
1.72 ± 1.23
0.43 ± 0.41
2.50 ± 1.43
2.72 ± 2.09
5.29 ± 3.22
* Data are presented as mean ± SD (standard deviation).
reported that no significant difference of?PBDEs concen-
birds (Chen et al., 2007). In the present study, our results
also showed that there was no significant difference of
?PBDEs concentration found between liver and muscle.
not completely explain this phenomenon.
It was reported that PBDEs and their metabolites like
other lipophilic compounds could bind to some proteins
or lipoproteins, such as thyroid hormone transport protein,
retinol binding protein, fatty acid binding protein (G´ omez-
Catal´ an et al., 1991; Marsh et al., 1998; Cheek et al.,
1999; Meerts et al., 2000). Maybe, these proteins or other
proteins involve in the tissue distribution of PBDEs in
In the present study, the concentrations of?PBDEs in
(e.g., muscle and liver)of chickens.This wasalso observed
in birds of prey and wild rodents (Voorspoels et al., 2006,
2007a), suggesting that the efficiency of the blood-brain
barrier was probably protecting the brain from accumu-
lation of PBDEs (Bachour et al., 1998; Voorspoels et al.,
2006). Considering potential developmental neurotoxicity
of PBDEs (Branchi et al., 2003; Viberg et al., 2003),
the presence of PBDEs in animal brains should be paid
much attention. In addition, this study reported for the
first time PBDEs bioaccumulation in testis of animals.
Several studies showed that PBDEs have potential adverse
effects on spermatogenesis, such as the decrease in sperm
and spermatid counts (Kuriyama et al., 2005; Lilienthal et
al., 2006). Although very low concentrations of pollutants
might not cause any obvious damage, our results indicated
that the potential damage of PBDEs to animal spermatoge-
nesis should arouse much attention.
Journal of Environmental Sciences 2011, 23(1) 133–138 / Xiaofei Qin et al.Vol. 23
tration was found between liver and muscle of terrestrial
It seems that different metabolic activities in tissues can
brain were significantly lower than those in other tissues
2.2 Congener patterns in chickens
The congener pattern of PBDEs detected in chicken
tissues, grain and soil from this area is shown in Fig.
2. BDE-209 contributed up to 48.04% and 60.64% of
?PBDEs in grain and soil, indicating that main PBDE
BDE-209 was also the dominant congener among detected
PBDE congeners in all chicken tissues (Table 1), and
contributed up to 82.46%–94.70% of?PBDEs except
abundant congener in chicken tissues. In early study, it was
suggested that high brominated congeners could not be
bioaccumulated in biotic tissues due to its large molecular
size and high octanol-water partition coefficient (Boon
et al., 2002). However, with increasing finding of BDE-
209 in many biotic samples, it was shown that all PBDE
congeners were bioavailable (Sj¨ odin et al., 1999; Eljarrat
et al., 2007). Our results also showed that high brominated
congeners (e.g., BDE-209 and BDE-183) could be bioac-
cumulated in terrestrial animals. Generally, BDE-47 was
congeners were relatively less (Law et al., 2003; Jaspers
et al., 2006; Naert et al., 2007). However, in the present
study, BDE-47 only contributed up to 0.63%–13.66% of
pollution source in Taizhou region was deca-BDE mixture.
for brain samples (Fig. 2). BDE-183 was the second
Fig. 2 Congenerpatternsofpolybrominateddiphenylethersinsoil,grain
as chicken food and various tissues of chickens (n = 4) from an e-wastes
recycling area in Southeast China.
?PBDEs in chicken tissues (Fig. 2). It is well known that
BDE) were produced in large volumes in the world. Penta-
and octa-BDE mixtures were the major commercial PBDE
formulation before they were banned in some countries
about ten years ago. However, deca-BDE mixture (com-
prising 65%–70% of total production) is still produced and
used. This might result in that the pattern of PBDEs in
some situation shifted to higher brominated congeners. We
suggest that low levels of BDE-209 in terrestrial birds in
previous studies (Voorspoels et al., 2006) might be due to
low exposure of BDE-209 but not to poor accumulation of
In brain samples, BDE-209 contributed up to 34.73%
of the total PBDEs, which was lower than those (82.46%–
94.70%) in other tissues. Correspondingly, the percentages
of lower brominated congeners such as BDE-47 and
BDE-99 in brain were slightly higher than those in other
tissues. Therefore, we suggest that the brain might be
protected more effectually from accumulation of the higher
brominated congeners (BDE-209) than the lower bromi-
nated congeners, such as BDE-47 and BDE-99.
three technical PBDE formulations (penta, octa, and deca-
2.3 Dietary exposure risk of PBDEs
en muscle and egg samples (Table 2), which ranged from
2.21 to 22.48 ng/(day·kg body weight (bw)). The mean
estimated daily intake (MEDI) value (13.51 ng/(day·kg
bw)) in the present study was one order of magnitude
higher than that (1.1 ng/(day·kg bw), summation of 16
PBDE congeners) from intakes of chicken and duck
consumption in a recent survey for consumed free-range
domestic fowl collected from an e-waste recycling site in
Guangdong Province, South China (Luo et al., 2009). In a
previous study on EDI of PBDEs, the calculated exposure
levels ranged from 35 to 97 ng/day (0.6–1.6 ng/(day·kg
bw)) based on the average daily food consumption in
Belgium and varied geographically (Voorspoels et al.,
No. 1 Polybrominated diphenyl ethers in chicken tissues and eggs from an electronic waste recycling area in southeast China137
recycling area in Southeast China and the mean estimated daily intake of PBDEs through muscle and egg consumption by a 60 kg body weight person
Levels of individual PBDE congeners and total PBDEs (ng/g wet weight) in chicken muscle (n = 4) and eggs (n = 15) from an e-wastes
SD: standard deviation.
MEDI: mean estimated daily intake, which is calculated from the mean concentrations of PBDEs in chicken muscle and eggs; MinI and MaxI: estimated
minimum and maximum daily intake, which are calculated from the minimum and maximum concentrations, respectively, of PBDEs in chicken muscle
2007b), which was also lower than that estimated in the
It should be mentioned that in some previous studies the
data calculated for dietary PBDE intake did not include
the high brominated congeners (e.g., BDE-209), which
might underestimate the total PBDEs exposure. In the
present study, the MEDI value of BDE-209 from chicken
muscle and eggs was 7.24 ng/(day·kg bw). The EDI
maximum value of BDE-209 from chicken muscle and
eggs was 10.93 ng/(day·kg bw) in this e-wastes recycling
area. Therefore, the exposure risk of BDE-209 is of great
concern for residents in this e-wastes recycling area.
The concentrations of PBDEs in chickens and eggs from
this e-waste recycling process area were 2–3 orders of
magnitude higher than those reported in the literature,
suggesting PBDEs pollution was serious in this area. PB-
DEs daily dietary intake through chicken muscle and eggs
consumption for residents in this area was one order of
ies. The large difference in PBDEs concentrations between
different tissues suggested that distribution of PBDEs
in tissues might depend on tissue-specificity rather than
the “lipid-compartment”, which mean uniform distribution
in lipid. BDE-209 was the predominant congener in all
chicken tissues, which indicated that BDE-209 was major
pollutant source in this area and can be bioaccumulated in
terrestrial animals. In addition, low PBDEs levels in brain
relative to other tissues suggest that the blood-brain barrier
might protect the brain from accumulation of PBDEs,
and the brain might be protected more effectually from
accumulation of the higher brominated congeners than the
lower brominated congeners.
This work was supported by the Knowledge In-
novation Program of Chinese Academy of Sciences
(No. KZCX2-YW-420-3, KZCX2-YW-Q-02-05) and the
National Natural Science Foundation of China (No.
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