Chemosphere 90 (2013) 23652371

Contents lists available at SciVerse ScienceDirect

Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Soil contamination by brominated ame retardants in open waste dumping sites

in Asian developing countries
Akimi Eguchi a, Tomohiko Isobe a,b, Karri Ramu a, Nguyen Minh Tue a, Agus Sudaryanto a,c,
Gnanasekaran Devanathan a, Pham Hung Viet d, Rouch Seang Tana e, Shin Takahashi a,
Annamalai Subramanian a, Shinsuke Tanabe a,
a

Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan
Senior Research Fellow Center, Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, Japan
Technology Center for Marine Survey, Agency for the Assessment and Application of Technology (BPPT), Jl. M.H. Thamrin 8, Jakarta, Indonesia
d
Centre for Environmental Technology and Sustainable Development, Hanoi University of Science, 334 Nguyen Trai, Hanoi, Viet Nam
e
Economic, Social and Cultural Observation Unit, Ofce of the Council of Minister, Sahapoan Russi Blvd., Phnom Penh, Cambodia
b
c

h i g h l i g h t s
" PBDE levels in municipal dumping sites were higher than those in reference sites.
" HBCD levels in municipal dumping sites and reference sites were comparable.
" BDE-209 was the dominant PBDE congener, while

c-HBCD was the dominant isomer.

a-HBCD.

" Waste burning may be causing the elevated ratios of octa- and nona-BDEs, and
" PBDE level and the TOC content of soils at dumping sites were not correlated.

a r t i c l e

i n f o

Article history:
Received 12 January 2012
Received in revised form 29 September 2012
Accepted 17 October 2012
Available online 11 November 2012
Keywords:
Polybrominated diphenyl ethers (PBDEs)
Hexabromocyclododecanes (HBCDs)
Municipal waste dumping sites
Soil
Asian developing countries

a b s t r a c t
In Asian developing countries, large amounts of municipal wastes are dumped into open dumping sites
each day without adequate management. This practice may cause several adverse environmental consequences and increase health risks to local communities. These dumping sites are contaminated with
many chemicals including brominated ame retardants (BFRs) such as polybrominated diphenyl ethers
(PBDEs) and hexabromocyclododecanes (HBCDs).
BFRs may be released into the environment through production processes and through the disposal of
plastics and electronic wastes that contain them.
The purpose of this study was to elucidate the status of BFR pollution in municipal waste dumping sites
in Asian developing countries. Soil samples were collected from six open waste dumping sites and ve
reference sites in Cambodia, India, Indonesia, Malaysia, and Vietnam from 1999 to 2007. The results suggest that PBDEs are the dominant contaminants in the dumping sites in Asian developing countries,
whereas HBCD contamination remains low. Concentrations of PBDEs and HBCDs ranged from ND to
180 lg/kg dry wt and ND to 1.4 lg/kg dry wt, respectively, in the reference sites and from 0.20 to
430 lg/kg dry wt and ND to 2.5 lg/kg dry wt, respectively, in the dumping sites. Contamination levels
of PBDEs in Asian municipal dumping sites were comparable with those reported from electronic waste
dismantling areas in Pearl River delta, China.
2012 Elsevier Ltd. All rights reserved.

1. Introduction
Environmental contamination by brominated ame retardants
(BFRs), such as polybrominated diethyl ethers (PBDEs) and hexabromocyclododecanes (HBCDs), has received increasing public
Corresponding author.
E-mail address: shinsuke@agr.ehime-u.ac.jp (S. Tanabe).
0045-6535/$ - see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.chemosphere.2012.10.027

attention because of the persistence, bioaccumulation potential,

and possible adverse effects of these chemicals on humans and
wildlife (Hites, 2004; Covaci et al., 2006).
PBDEs can have adverse in vitro and in vivo physiological effects,
including endocrine disruption and interference with neurobehavioral development (Darnerud, 2003; Birnbaum and Staskal, 2004;
Herbstman et al., 2010). Several studies have shown that effects
of PBDEs are similar to those of organohalogen compounds, such

2366

A. Eguchi et al. / Chemosphere 90 (2013) 23652371

as reduction in serum thyroid hormone levels (Hallgren et al.,

2001). Reported toxicities of HBCDs include developmental neurotoxic effects such as aberrations in spontaneous behavior, learning,
and memory functions (Eriksson et al., 2002, 2004). HBCDs also alter the normal transport of neurotransmitters in rat brain (Mariussen and Fonnum, 2003; Ibhazehiebo et al., 2011).
PBDEs and HBCDs are used as ame-retardant additives in a wide
variety of commercial and household products such as plastics, textiles, and electronic appliances including computers and televisions
(Kemmlein et al., 2009). In 2001, global consumption of the technical PBDE mixtures penta-, octa-, and deca-BDE and HBCDs was
7500, 3800, 56 000, and 15 900 tons, respectively. In Asia, the total
consumption volumes of penta-, octa-, deca-BDEs and HBCDs were
150, 2000, 23 000, and 3900 tons, respectively, during 2001 (BSEF,
2003; Watanabe and Sakai, 2003). This widespread usage and bioaccumulation potential of BFRs resulted in both classes of these chemicals being present in air, water, sh, birds, marine mammals, and
humans throughout the world (Law et al., 2008).
In Asian developing countries, the majority of the municipal solid waste, which consists of a wide variety of materials such as food
waste, paper, plastics, building material, metal wastes, and ash
(Gullett et al., 2010; Fiedler and Solorzano Ochoa, 2010), were disposed directly into open waste dumping sites without appropriate
processes (Minh et al., 2003). Apart from the enormous amounts of
waste dumped in such areas, not much information on their quality and quantity is available from Asian developing countries. As a
result, these open dumping sites could be a major source of contaminant emission on the environment and human exposure route.
This practice has led to public concerns over potential impacts on
the environment and local communities. These concerns were justied by more recent intensive studies that demonstrated an increased human health risk caused by exposure to toxic chemicals
such as persistent organic pollutants (POPs) from dumping sites
(Minh et al., 2006). However, previous studies on BFRs in soil samples from Asian developing countries were conned to Chinese
e-waste recycling sites and Indonesian municipal waste dumping
sites (Leung et al., 2007; Zou et al., 2007; Ilyas et al., 2011). A comprehensive survey monitoring BFRs in background soils in Asian
developing countries has not yet been conducted. Thus, the present
study investigated BFR contamination of soils from municipal
waste dumping sites and background areas in ve Asian developing countries to elucidate the role of municipal waste dumping
sites as potential sources of BFR pollution in these countries.

2. Materials and methods

2.1. Sample collection
Soil samples were collected from municipal waste dumping
sites and reference sites in India, Vietnam, Malaysia, Indonesia,
and Cambodia between 1999 and 2007 (Fig. S1) and stocked in
the es-Bank of Ehime University (Tanabe, 2006), Japan were used
for the present study. Sampling was made in the municipal dumping sites and uncontaminated sites in many Asian developing
countries under our various research programs for about a decade
starting from the late 1990s. At each location, samples were collected at depths of 010 cm at ve points within an area of approximately 25 m2 and then combined together and treated as a
representative sample for the respective location. The frozen samples were transported to the Environmental Specimen Bank for
Global Monitoring (es-BANK) (Tanabe, 2006) at Ehime University
with permission from the Ministry of Agriculture, Forestry and
Fisheries, Japan. Samples were sieved through a 2-mm sieve, air
dried, packed in polyethylene bags, and stored at 25 C until
chemical analysis.

2.2. Chemical analysis

PBDEs were analyzed according to a previously published method (Eguchi et al., 2011) with slight modication. In brief, 5 g of each
air-dried soil sample was extracted using a mixture of hexane and
acetone (50:50, v:v, 50 mL), initially with an electric shaker for
15 min, (SR-2W model, TAITEC, Japan) and then twice using an
ultrasonic bath (AU-80C model, EYELA, Japan) for 15 min each time.
An aliquot of the combined extract was spiked with 13C12-labeled
BDE-3, -15, -28, -47, -99, -153, -154, -183, -197, -207, and -209
(5 ng each) and 13C12-labeled a-, b-, and c-HBCD (10 ng each)
before being passed through a multilayer silica gel column. The
extract was treated with sulfuric acid and loaded onto a gel permeation chromatography column (GPC). The GPC fraction containing
the target compounds was concentrated and puried by passage
though a column containing 4 g of activated silica gel (Wakogel
DX, Wako Pure Chemical Industries Ltd., Japan). The rst fraction,
eluted with 5% dichloromethane in hexane (v/v), contained PBDEs,
whereas the second fraction, eluted with 25% dichloromethane in
hexane, contained HBCDs. The PBDE fraction was treated with activated copper to remove any sulfur and it was spiked with 13C12BDE-139 to be used as an internal standard. Fourteen major PBDE
congeners (BDE-3, -15, -28, -47, -99, -100, -153, -154, -183, -196,
-197, -206, -207, and -209) were quantied using a gas chromatography (GC) system (Agilent 7890A) equipped with a mass spectrometer (MS, Agilent 5975C) using electron ionization with
selective ion monitoring mode. The GC columns used for quantication were DB-1MS fused silica capillaries (J&W Scientic Inc.) measuring 30 m length  0.25 mm i.d. with 0.25 lm lm thickness for
di- to hepta-BDEs, and 15 m  0.25 mm with 0.1 lm lm thickness
for octa- to deca-BDEs. All the congeners were quantied using the
isotope dilution method for the corresponding labeled congeners.
Recovery of labeled BDEs ranged between 60% and 120%. The HBCD
fraction of silica gel column was evaporated and redissolved in a
solution of labeled HBCD (a-, b-, and c-HBCD-d18) before liquid
chromatographytandem mass spectrometry (LCMS/MS) analysis.
The diastereomeric analysis of HBCDs was performed by LCMS/
MS, according to a previously published method (Isobe et al.,
2007). Samples were analyzed using ACQUITY UPLC (Waters, Tokyo,
Japan) equipped with a Quattro Micro API triple quadrupole mass
spectrometer (Waters/Micromass, Tokyo, Japan). HBCD isomers
(a-, b-, and c-) were separated using an Extend-C18 column
(2.1 mm i.d., 100 mm, 1.8 lm particle size, Agilent, Tokyo, Japan).
The mobile phase comprised water/acetonitrile/methanol
(20:20:60) at 0.2 mL/min initially for 5 min, before ramping up
methanol for 2 min, and then water/acetonitrile/methanol
(20:20:60) for 3 min. The MS/MS analysis was operated in negative
electrospray ionization mode and was performed in multiple reaction monitoring mode (MRM). Quantication of native HBCDs was
based on the mean value of the response of two MRM transitions
(i.e., m/z 640 > 81, m/z 642 > 81), which was corrected with the
MRM transition response for 13C12-HBCDs (i.e., m/z 652 > 81).
Recovery of 13C12-HBCDs spiked in the sample extracts was always
in the range of 50%120%. Concentrations of BFRs were calculated
by isotope dilution procedure. For total organic carbon (TOC) analysis, approximately 2 g of dried and homogenized soil sample was
treated with 6 M HCl to remove inorganic carbon, washed with
Milli-Q water ve times, and dried overnight at 40 C. TOC was then
determined using a Yanaco CHN corder MT-5. Acetanilide, antipyrine, and 4-nitroaniline were used as external standards.
2.3. Quality control and assurance
A certied sediment sample (NIES CRM Air Dried Sediment#1)
that was prepared for a previous interlaboratory calibration exercise (Takahashi et al., 2004) was analyzed to determine specic

A. Eguchi et al. / Chemosphere 90 (2013) 23652371

PBDEs and HBCDs. The data produced by our laboratory were in

good agreement with the certied concentrations (relative standard deviation < 10%). The limit of detection (LOD) for the target
compounds was based on a signal-to-noise ratio (S/N) of >3 for
the chromatogram of the actual sample, while the limit of quantication (LOQ) was dened as the amount of target compounds
with a S/N of 10. The LODs were 0.003, 0.005, and 0.005 lg/kg
dry wt for mono- to hepta-BDEs, octa- to deca-BDEs, and HBCDs,
respectively. A procedural blank sample was analyzed with every
batch of seven samples. No peaks were detected in the chromatograms of the blank samples.
2.4. Statistical analysis
Statistical analyses were performed with the R program, Ver.
2.12.0. The Wilcoxon rank-sum test was used to determine any differences in the concentrations of PBDEs and HBCDs between the
municipal waste dumping sites and the reference sites. Spearmans
rank correlation test was used to test the signicance of correlation
between the concentration of BFR and organic carbon. Principal
component analysis (PCA) was employed to categorize PBDE congeners according to variations in the patterns of their proportions in
the total PBDEs. This analysis included only the congeners that
were detected in at least 75% of the samples. A p value of <0.05
was considered to be statistically signicant. Results below LOQ
were given a value of 0.5 LOQ.
3. Results and discussion
3.1. Contamination levels
3.1.1. BFR contamination in reference sites
BFR soil levels in Asian developing countries have only been reported by a limited number of studies from contamination hotspots, such as e-waste recycling sites in China (Leung et al.,
2007; Zou et al., 2007) and municipal waste dumping sites in Indonesia (Ilyas et al., 2011). In this study, 27 soil samples from urban
and agricultural sites in India, Vietnam, Malaysia, Indonesia, and
Cambodia were analyzed as reference sites. PBDEs were detected
in 25 samples and HBCDs were detected in 21 samples. The PBDE
and HBCD concentrations were signicantly higher (p < 0.05) in
Cambodian reference sites than in soil samples from other reference sites (Table 1). As shown in Table 2, the PBDE levels in soils
from other Asian developing countries were comparable to the
background levels in Japan and Pearl River delta, China, whereas
the levels in Cambodian soils were 210 times higher (Hayakawa
et al., 2004; Sellstrom et al., 2005; Leung et al., 2007; Zou et al.,
2007). The higher levels observed in Cambodia may be related to
the proximity of some collection points to roads. The levels of total
HBCDs from most reference sites were comparable to those reported in urban areas in Guangzhou, China (Yu et al., 2008) and
background areas in Surabaya, Indonesia (Ilyas et al., 2011). This
indicates that signicant and ubiquitous BFR pollution sources
are present in Asian developing countries.
3.1.2. BFR contamination in municipal waste dumping sites
Since, contamination levels of PBDEs and HBCDs in Indonesian
waste dumping sites were not signicantly different between
20022003 and 2007, these samples were merged. Recent studies
have demonstrated that open waste dumping sites found in Asian
developing countries may be hotspots for toxic chemicals, such as
PCBs and dioxin-like compounds, and exposure to these contaminants may have adverse effects on the health of people living in
affected areas (Minh et al., 2003, 2006). However, only one previous study has reported the BFR contamination level of soil from a

2367

dumping site which was in Surabaya, Indonesia (Ilyas et al.,

2011). The current study detected PBDEs in all dumping site soils
at signicantly higher levels than that in their respective reference
sites (Table 1, p < 0.05), suggesting that municipal waste dumping
sites are a potential source of PBDEs in Asian developing countries.
The levels were highest in Vietnam (mean: 95 lg/kg dry wt, range:
1.2430 lg/kg dry wt), followed by Indonesia, Cambodia, India,
and Malaysia (mean: 6.232 lg/kg dry wt, range: 0.12260 lg/kg
dry wt) (Table 1). However, these levels were one to two orders
of magnitude lower than that found in soils from contamination
hotspots in other countries such as sludge application areas in
Sweden, (mean: 350 lg/kg dry wt) (Sellstrom et al., 2005) and
e-waste recycling sites in China (27194250 lg/kg dry wt) (Leung
et al., 2007).
HBCDs were detected in 30/45 samples and the HBCD levels
were not signicantly different between municipal waste dumping
sites and reference sites in all countries (Table 1), indicating that
municipal waste dumping sites may not be a major source of HBCDs
in Asian developing countries. The HBCD levels in soil samples from
municipal waste dumping sites (mean: 0.29 lg/kg dry wt, range:
<0.052.4 lg/kg dry wt) were two to six orders of magnitude lower
than the levels reported for near point sources in Sweden (mean:
810 lg/kg dry wt) (Remberger et al., 2004) and other European
countries (mean: 4300 lg/kg dry wt) (Malte et al., 2004) (Table
2). Moreover, the HBCD concentrations were one to two orders of
magnitude lower than those of PBDEs at all locations. These results
suggest that HBCDs have not been used extensively in Asian developing countries. Indeed, statistical data on BFR consumption indicates a lower usage of HBCDs in Asia, when compared with PBDEs
(Watanabe and Sakai, 2003). The low levels of HBCDs could also
be due to the high levels of transformation processes for these compounds, via biotic and/or abiotic mechanisms in the soil medium.
For example, signicant decomposition of HBCDs in aerobic (75%
in 119 d) and anaerobic (92% in 21 d) soils was reported in a microcosm study (Davis et al., 2005). However, there are currently no regulations on the production and usage of HBCDs, so it is anticipated
that the environmental levels may rise in the near future. Thus, further monitoring of the HBCD levels and alternative compounds that
were introduced after restrictions on PBDE mixtures are needed in
order to determine their contamination status and provide future
risk assessments.
3.2. Congener and isomer proles
Principal component analysis (PCA) was employed to categorize
PBDE congeners according to the variation in the patterns of their
relative proportions (%) in total PBDEs. Based on the results, soil
samples were divided into three categories as lower brominated
BDEs (36Br), 79Br BDEs, and BDE-209 (Fig. 1). Deca-BDE was
aligned with the rst principal component (PC1, accounting for
39.2% of total variance). 79Br-congeners, and lower brominated
PBDEs contributed to both PCs, but in an opposite manner in PC2
(23.5% of variance). Most soil samples aligned with BDE-209,
reecting its high abundance (4893% of total PBDEs) in those particular samples. This predominance was consistent with the high
volume of consumption of deca-BDE technical mixtures (Watanabe
and Sakai, 2003) in Asia and the strong binding afnity of BDE-209
with soil particles. Some samples from municipal waste dumping
sites aligned with 79Br-BDEs, especially in Vietnam and Indonesia,
indicating the higher abundance of these congeners compared with
samples from the reference sites (Table 1). Lower brominated BDEs
were aligned with samples from the reference sites and the
Cambodian municipal waste dumping site. The proportion of
octa- and nona-BDE congeners in samples from dumping sites
(7.830%) was higher than that in deca-BDE technical mixtures
(2.49.3%) (La Guardia et al., 2006), possibly due to a higher degree

a
b
c

Cambodia, mean (minmax)

India, mean (minmax)

Indonesia, mean (minmax)

Malaysia, mean (minmax)

Vietnam, mean (minmax)

Reference site

Dumping site

Reference site

Dumping site

Reference site
20022003

Dumping site 2002 Dumping site 2007

2003

Reference site

Dumping site

Reference site

1.1 (0.02.7)

7.7 (0.4424)

0.80 (0.341.1)

4.9 (0.9810)

8.4 (0.9215)

11 (1.127)

7.9 (0.9727)

1.9 (0.363.4)

4.5 (3.35.7)

6.7 (0.2824)

8.7 (1.415)

<0.003
<0.003
0.01 (<0.0030.02)
0.34 (<0.0031.2)
0.48 (<0.0031.5)
0.04 (<0.0030.18)
0.07 (<0.0030.2)
0.03 (<0.0030.09)
0.10 (<0.0030.33)
0.30 (<0.0031.08)
0.05 (<0.0030.17)
0.63 (<0.0032.9)
0.40 (<0.0031.8)
35 (<0.003170)
1.1 (<0.0035.2)
38 (<0.003180)

<0.003
0.13 (<0.0030.71)
0.98 (0.0095.6)
3.5 (0.0818)
1.8 (0.117.5)
0.20 (<0.0030.65)
0.48 (0.021.5)
0.17 (0.010.54)
1.1 (0.035.5)
0.20 (0.010.81)
0.28 (0.011.3)
1.1 (0.024.9)
0.80 (0.023.6)
21 (0.1671)
8.3 (0.3135)
32 (0.5491)

<0.003
<0.003
<0.003
0.01 (<0.0030.02)
0.01 (<0.0030.05)
<0.003
<0.003
<0.003
<0.003
<0.003
<0.003
<0.003
<0.003
0.05 (<0.0030.18)
0.02 (<0.0030.06)
0.07 (<0.0030.18)

<0.003
0.01 (<0.0030.05)
0.01 (<0.0030.05)
0.19 (0.050.50)
0.33 (0.100.86)
0.05 (<0.0030.24)
0.05 (<0.0030.23)
0.01 (<0.0030.05)
0.15 (<0.0030.29)
0.07 (0.020.20)
0.04 (<0.0030.18)
0.41 (0.021.9)
0.63 (0.042.7)
5.4 (0.4816)
0.81 (0.181.7)
7.3 (0.8219)

<0.003
0.004 (<0.0030.01)
0.002 (<0.0030.01)
0.18 (0.050.71)
0.14 (<0.0030.33)
0.01 (<0.0030.05)
0.02 (<0.0030.11)
0.01 (<0.0030.03)
0.20 (0.040.44)
0.15 (0.020.45)
0.12 (0.0080.26)
0.60 (0.082.5)
0.52 (0.081.7)
8.3 (0.4838)
0.57 (0.151.3)
10 (0.9944)

<0.003
0.02 (<0.0030.06)
0.06 (<0.0030.29)
0.79 (<0.00310)
0.99 (<0.00314)
0.08 (<0.0030.46)
0.37 (<0.0034.3)
0.24 (<0.0032.7)
0.63 (<0.0034.1)
1.1 (0.0058.7)
0.91 (0.017.3)
2.1 (<0.00313)
2.8 (0.00927)
31 (0.07250)
3.2 (<0.00335)
41 (0.12260)

<0.003
<0.003
0.01 (<0.0030.05)
0.28 (0.100.77)
0.36 (<0.0030.94)
0.05 (<0.0030.23)
0.10 (<0.0030.40)
0.05 (<0.0030.17)
0.23 (<0.0031.1)
0.25 (<0.0031.0)
0.26 (<0.0031.0)
0.44 (<0.0031.7)
0.57 (0.121.9)
9.9 (1.049)
1.1 (0.103.7)
13 (2.458)

<0.003
0.003 (<0.0030.006)
<0.003
0.02 (0.02)
0.01 (0.010.02)
0.008 (0.0070.01)
0.005 (<0.0030.01)
0.01 (0.0080.02)
0.02 (0.020.03)
0.01 (0.0060.02)
0.02 (0.010.03)
0.07 (0.050.09)
0.08 (0.050.1)
2.1 (1.13.0)
0.09 (0.070.11)
2.4 (1.33.4)

<0.003
0.12 (0.0070.24)
0.32 (0.020.62)
0.41 (0.290.54)
0.36 (0.250.48)
0.03 (<0.0030.05)
0.02 (<0.0030.05)
0.44 (0.020.85)
0.53 (0.090.97)
0.18 (0.040.32)
0.33 (0.010.65)
0.21 (0.140.28)
0.29 (0.140.43)
3.0 (2.43.5)
2.2 (0.783.7)
6.2 (4.67.8)

<0.003
<0.003
<0.003
0.01 (<0.0030.05)
0.01 (<0.0030.08)
0.02 (<0.0030.14)
<0.003
<0.003
0.01 (<0.0030.02)
0.01 (<0.0030.03)
0.01 (<0.0030.05)
<0.003
0.01 (<0.0030.04)
0.14 (<0.0030.27)
0.05 (<0.0030.28)
0.22 (0.020.42)

<0.003
0.03 (<0.0030.05)
0.07 (<0.0030.30)
0.14 (<0.0030.34)
0.66 (<0.0032.4)
0.10 (<0.0030.50)
1.6 (<0.0036.1)
0.97 (<0.0034.9)
7.3 (<0.00328)
4.1 (0.0216)
5.6 (0.0225)
5.1 (0.0624)
14 (0.0564)
56 (1.0260)
11 (<0.00343)
95 (1.2430)

0.03
0.03
0.49
0.54

0.12
0.02
0.05
0.20

0.01
0.01
0.06
0.09

0.37 (<0.0050.94)
0.14 (<0.0050.35)
0.56 (<0.0051.3)
1.1 (<0.0052.4)

0.09 (0.040.19)
0.008 (<0.0050.02)
0.01 (<0.0050.02)
0.11 (0.060.21)

0.07
0.02
0.11
0.23

0.02 (<0.0050.21)
0.004 (<0.0050.04)
0.02 (<0.0050.07)
0.04 (<0.0050.31)

0.007 (<0.0050.01)
<0.005
0.04 (<0.0050.08)
0.05 (<0.0050.10)

0.06 (<0.0050.12)
0.009 (<0.0050.02)
0.03 (<0.0050.06)
0.10 (<0.0050.20)

0.03
0.02
0.18
0.23

0.03
0.02
0.09
0.14

(<0.0050.15)
(<0.0050.08)
(<0.0051.2)
(<0.0051.4)

(<0.0050.41)
(<0.0050.06)
(<0.0050.16)
(<0.0050.40)

(<0.0050.06)
(<0.0050.04)
(<0.0050.30)
(<0.0050.40)

(<0.0050.38)
(<0.0050.09)
(<0.0050.51)
(<0.0050.83)

(<0.0050.22)
(<0.0050.13)
(<0.0050.95)
(<0.0051.3)

Dumping site

(<0.0050.05)
(<0.0050.04)
(<0.0050.2)
(<0.0050.3)

Sum of mono- to hepta-BDE congeners (BDE3, 15, 28, 47, 99, 100, 153, 154 and 183).
Sum of mono- to deca-BDE congeners (BDE3, 15, 28, 47, 99, 100, 153, 154, 183, 196, 197, 206, 207 and 209).
Sum of a-, b- and c-HBCDs.

of debromination of deca-BDE to nona- and octa-BDEs during open

waste burning (Weber and Kuch, 2003) and photolytic debromination (Soderstrom et al., 2004) in dumping sites. In most samples, the
BDE-47 to BDE-99 ratio was around 1:1 while BDE-153 to BDE-154
was around 2:1, which was similar to that found in the commercial
penta-BDE mixture Bromkal 70-5DE (La Guardia et al., 2006; Yun
et al., 2008). This suggests that the major source of contamination
for tetra- to hexa-BDE congeners is penta-BDE mixtures. Interestingly, a higher proportion of BDE-183 was detected in Vietnamese
municipal waste dumping sites (67% of monohepta-BDEs in
average) while BDE-100 was the predominant congener in
Vietnamese reference sites. BDE-183 may be considered to be a
marker for the octa-BDE mixture because only trace quantities of
this congener are present in the penta-BDE mixture and it is not
found in deca-BDE (La Guardia et al., 2006). Thus, the higher
percentage of BDE-183 in Vietnamese municipal waste dumping
sites suggests that disposed consumer products had a higher
octa-BDE content in Vietnam.
The average contributions of a-, b-, and c-HBCD isomers to the
total HBCDs were 32%, 17%, and 51% in reference site and 39%, 9.0%,
and 52% in dumping site, respectively (Table.1). The predominance
of c-HBCD in the soil samples reects its high proportion in technical HBCD products (80% of total HBCDs) (Covaci et al., 2006) and
its stronger binding afnity with soil particles (Davis et al., 2005).
However, the percentages of a-HBCD in soils from municipal waste
dumping sites are greater than in soils from reference site. It was
reported that HBCDs undergo thermal rearrangements at temperatures above 160 C, resulting in a specic mixture of 78% a, 13%
b, and 9% c (Barontini et al., 2001). Compared with c-HBCD,
a-HBCD also has a higher water solubility and lower afnity for
particles, which implies it can move easily between different
environmental matrices (Davis et al., 2005; Covaci et al., 2006). It
remains unclear whether this difference in the composition of
the HBCD stereoisomers among some soils and technical HBCD
products is caused by isomerization during the thermal processing
of HBCD-containing products, or during open waste burning in the
dumping sites, or by isomer-specic partition and distribution in
the environment. However, as the data size was small and levels
of contaminations were quite low in this study, clear monitoring
of contamination of BFRs and their proles is needed in Asian
developing countries.

3.3. Correlation with total organic carbon (TOC)

The relationship between BFR concentrations and soil TOC was

examined using Spearmans correlation test. As shown in Table 3,
signicant correlation was found between TOC and mono
hepta-BDEs, as well as deca-BDE/BDE-209 in soils from the whole
sample set and reference sites. However, these correlations were
not found in the sample subset from the dumping sites. HBCD concentrations did not have any correlation with TOC in any sample set.
Organic carbon in soils and sediments is recognized as a primary
sorbent for hydrophobic compounds including POPs and PBDEs
(Meijer et al., 2002; Gouin and Harner, 2003). Thus, soils with a high
TOC content may retain more hydrophobic contaminants from
short- and long-range atmospheric transport, depending on their
proximity to the sources and the extent of airsurface exchange
of these compounds (Nam et al., 2008). In this study, the positive
correlation between PBDE levels and the TOC contents of soils from
the reference sites indicated the inuence of organic matter loading
on the accumulation of these compounds in soils. Therefore, the
distribution of PBDEs in background soils may be governed by the
atmospheric deposition of particles containing organic matter. In
contrast, the lack of correlation in soils from dumping sites
indicated that the soil contamination levels in these sites were
more inuenced by their proximity to heterogeneously distributed

A. Eguchi et al. / Chemosphere 90 (2013) 23652371

TOC (%)
PBDEs
BDE3
BDE15
BDE28
BDE47
BDE99
BDE100
BDE153
BDE154
BDE183
BDE196
BDE197
BDE206
BDE207
BDE209
P
PBDEsa
P9
PBDEsb
HBCDs
a-HBCD
b-HBCD
c-HBCD
P
HBCDsc

2368

Table 1
Concentrations (lg/kg, dry weight) of PBDEs and HBCDs in soils from Asian developing countries.

Table 2
Concentrations (lg/kg, dry weight) of PBDEs and HBCDs in soils from Asian developing countries in the present study and those from other countries reported.
Japan

China, Pearl river delta

China, Guiyu

Reference site

Dumping site

Background

Surface

Point-source

Background

Near acid bath

Sweden
Background

Sludge application soil

Background

Europian countries
Near HBCD processing plant

<0.003
<0.003
0.01
0.19
0.25
0.07
0.09
0.04
0.14
0.23
0.11
0.68
0.46
9.16
0.38
10.2

<0.003
0.09
0.27
0.80
0.81
0.15
0.53
0.30
1.26
0.81
0.91
1.45
2.43
20.6
3.31
29.5

n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
9.6

n.a.
n.a.
0.04
0.63
0.14
0.03
0.05
0.03
0.08
n.a.
n.a.
n.a.
n.a.
13.8
n.a.
n.a.

n.a.
n.a.
0.08
1.05
1.6
0.21
0.85
0.35
3.7
n.a.
n.a.
n.a.
n.a.
70.5
n.a.
n.a.

ND
0.008
0.026
0.24
0.2
0.039
0.053
0.035
0.066
n.a.
0.051
n.a.
0.1
2.8
n.a.
n.a.

8.6
10
36.3
74
150
22
66
54
72
n.a.
51
n.a.
130
1270
n.a.
n.a.

n.a.
n.a.
0.04
0.01
0.05
0.01
0.01
0.1
0.01
n.a.
n.a.
n.a.
n.a.
0.48
n.a.
n.a.

n.a.
n.a.
75
1
99
20
8.7
7.7
0.51
n.a.
n.a.
n.a.
n.a.
370
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.

0.04
0.016
0.15
0.21

0.11
0.03
0.15
0.29

n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
n.a.

n.a.
n.a.
n.a.
810

620
320
3400
4300

HBCDs

a-HBCD
b-HBCD
c-HBCD
P
HBCDsc
a
b
c

A. Eguchi et al. / Chemosphere 90 (2013) 23652371

PBDEs
BDE3
BDE15
BDE28
BDE47
BDE99
BDE100
BDE153
BDE154
BDE183
BDE196
BDE197
BDE206
BDE207
BDE209
P
PBDEsa
P9
PBDEsb

Asian developing countries

Sum of mono- to hepta-BDE congeners (BDE3, 15, 28, 47, 99, 100, 153, 154 and 183).
Sum of mono- to deca-BDE congeners (BDE3, 15, 28, 47, 99, 100, 153, 154, 183, 196, 197, 206, 207 and 209).
Sum of a-, b- and c-HBCDs.

2369

2370

A. Eguchi et al. / Chemosphere 90 (2013) 23652371

dumping sites indicated that the contamination was affected by

the proximity of waste materials rather than atmospheric
transport.
Acknowledgments
This study was supported by Global COE Program, Grantsin-Aid for Scientic Research (S) (No. 20221003) from the Ministry
of Education, Culture, Sports, Science and Technology, Japan
(MEXT) and Japan Society for the Promotion of Science (JSPS) and
the Waste Management Research Grant (K2062, K2129, K2121)
from the Ministry of Environment, Japan. We also acknowledge
the JSPS Research Fellowships for Young Scientists (DC1) in Japan
provided to Mr. A. Eguchi (226331).
Appendix A. Supplementary material
Fig. 1. PCA biplot of PBDE percentage in soil samples. The factor scores for each
location are presented as plots, while factor loadings for the different compounds
are presented as red arrows. Open and closed circles indicate samples from
reference sites and municipal dumping sites, respectively. Blue, red, orange, purple
and green circles show samples from Cambodia, India, Vietnam, Indonesia and
Malaysia. (For interpretation of the references to color in this gure legend, the
reader is referred to the web version of this article.)

Table 3
Correlation between concentrations of BFRs and TOC in reference and dumping sites.
aP
9PBDEs
BDE209
HBCDs
All samples
r-Value
p-Value
Dumping site
r-Value
p-Value
Reference site
r-Value
p-Value

0.22
0.046
0.07
0.59
0.39
0.049

0.32
0.003

0.03
0.773

0.03
0.81

0.02
0.87

0.4
0.045

0.14
0.51

a
Sum of mono- to hepta-BDE congeners (BDE3, 15, 28, 47, 99, 100, 153, 154 and
183).

waste materials containing PBDEs. HBCD concentrations had no

signicant relationship with the TOC contents in reference or
dumping sites, possibly due to low contamination levels and the
different chemical properties of HBCDs compared with PCBs and
PBDEs.
4. Conclusions
This study demonstrated ubiquitous BFR contaminations in
Asian developing countries, especially in municipal waste dumping
sites. PBDE levels in municipal waste dumping sites were higher
than those in reference sites, indicating the presence of prominent
sources of PBDE contaminations in municipal waste dumping sites.
Recycling and disposing of PBDE-containing materials in Asian
developing countries may lead to serious environmental contaminations at those sites. HBCD levels at all locations were relatively
low indicating the minimum pollution. No signicant difference
in the HBCD levels were found between municipal waste dumping
sites and reference sites, possibly due to HBCD usage remains lower than that of PBDEs. BDE-209 was the dominant PBDE congener,
while c-HBCD was the dominant isomer in soils from Asian developing countries. However, waste burning may be responsible for
the elevated proportions of octa- and nona-BDEs, and a-HBCD in
dumping sites. Unlike the reference site soils, the lack of correlation between the PBDE levels and the TOC contents of soils at

Supplementary data associated with this article can be found, in

the online version, at http://dx.doi.org/10.1016/j.chemosphere.2012.
10.027.
References
Barontini, F., Cozzani, V., Cuzzola, A., Petarca, L., 2001. Investigation of
hexabromocyclododecane
thermal
degradation
pathways
by
gas
chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 15,
690698.
Birnbaum, L.S., Staskal, D.F., 2004. Brominated ame retardants: cause for concern?
Environ. Health Perspect. 112, 917.
BSEF, 2003. <http://www.bsef.com>.
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, 36793688.
Darnerud, P.O., 2003. Toxic effects of brominated ame retardants in man and in
wildlife. Environ. Int. 29, 841853.
Davis, J.W., Gonsior, S., Marty, G., Ariano, J., 2005. The transformation of
hexabromocyclododecane in aerobic and anaerobic soils and aquatic
sediments. Water Res. 39, 10751084.
Eguchi, A., Isobe, T., Ramu, K., Tanabe, S., 2011. Optimisation of the analytical
method for octa-, nona- and decabrominated diphenyl ethers using gas
chromatographyquadrupole mass spectrometry and isotope dilution. Int. J.
Environ. Anal. Chem. 91, 348356.
Eriksson, P., Viberg, H., Fischer, C., Wallin, M., Frederiksson, A., 2002. A comparison
on developmental neurotoxic effects of hexabromocyclododecane, 2,20 ,4,40 ,5,50 hexabromodiphenylether (PBDE 153) and 2,20 ,4,40 ,5,50 -hexachlorobiphenyl
(PCB 153). Organohalogen Compd. 57, 389390.
Eriksson, P., Johansson, N., Viberg, H., Fischer, C., Wallin, M., Fredriksson, A., 2004.
Comparative developmental neurotoxicity of ame retardants, polybrominated
ame retardants and organophosphorous compounds, in mice. Organohalogen
Compd. 66, 31633165.
Fiedler, H., Solorzano Ochoa, G., Yu, G., Zhang, T., Marklund, S., Lundin, L., 2010.
Hazardous Chemicals from Open Burning of Waste in Developing Countries
Final Report. United Nations Environment Programme, Division of Technology,
Industry and Economics, Chemicals Branch.
Gouin, T., Harner, T., 2003. Modelling the environmental fate of the polybrominated
diphenyl ethers. Environ Int 29, 717724.
Gullett, B.K., Wyrzykowska, B., Grandesso, E., Touati, A., Tabor, D.G., Ochoa, G.S.,
2010. PCDD/F, PBDD/F, and PBDE emissions from open burning of a residential
waste dump. Environ. Sci. Technol. 44, 394399.
Hallgren, S., Sinjari, T., Hakansson, H., Darnerud, P.O., 2001. Effects of
polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls
(PCBs) on thyroid hormone and vitamin A levels in rats and mice. Arch.
Toxicol. 75, 200208.
Hayakawa, K., Takatsuki, H., Watanabe, I., Sakai, S., 2004. Polybrominated diphenyl
ethers (PBDEs), polybrominated dibenzo-p-dioxins/dibenzofurans (PBDD/Fs)
and
monobromo-polychlorinated
dibenzo-p-dioxins/dibenzofurans
(MoBPXDD/Fs) in the atmosphere and bulk deposition in Kyoto, Japan.
Chemosphere 57, 343356.
Herbstman, J.B., Sjodin, A., Kurzon, M., Lederman, S.A., Jones, R.S., Rauh, V.,
Needham, L.L., Tang, D., Niedzwiecki, M., Wang, R.Y., Perera, F., 2010. Prenatal
exposure to PBDEs and neurodevelopment. Environ. Health Perspect. 118, 712
719.
Hites, R.A., 2004. Polybrominated diphenyl ethers in the environment and in
people: a meta-analysis of concentrations. Environ. Sci. Technol. 38, 945956.
Ibhazehiebo, K., Iwasaki, T., Xu, M., Shimokawa, N., Koibuchi, N., 2011. Brain-derived
neurotrophic factor (BDNF) ameliorates the suppression of thyroid hormoneinduced granule cell neurite extension by hexabromocyclododecane (HBCD).
Neurosci. Lett. 493, 17.

A. Eguchi et al. / Chemosphere 90 (2013) 23652371

Ilyas, M., Sudaryanto, A., Setiawan, I.E., Riyadi, A.S., Isobe, T., Ogawa, S., Takahashi, S.,
Tanabe, S., 2011. Characterization of polychlorinated biphenyls and brominated
ame retardants in surface soils from Surabaya, Indonesia. Chemosphere 83,
783791.
Isobe, T., Ramu, K., Kajiwara, N., Takahashi, S., Lam, P.K., Jefferson, T.A., Zhou, K.,
Tanabe, S., 2007. Isomer specic determination of hexabromocyclododecanes
(HBCDs) in small cetaceans from the South China SeaLevels and temporal
variation. Mar. Pollut. Bull. 54, 11391145.
Kemmlein, S., Herzke, D., Law, R.J., 2009. Brominated ame retardants in the
European chemicals policy of REACH-Regulation and determination in
materials. J. Chromatogr. A 1216, 320333.
La Guardia, M.J., Hale, R.C., Harvey, E., 2006. Detailed polybrominated diphenyl
ether (PBDE) congener composition of the widely used penta-, octa-, and decaPBDE technical ame-retardant mixtures. Environ. Sci. Technol. 40, 62476254.
Law, R.J., Herzke, D., Harrad, S., Morris, S., Bersuder, P., Allchin, C.R., 2008. Levels and
trends of HBCD and BDEs in the European and Asian environments, with some
information for other BFRs. Chemosphere 73, 223241.
Leung, A.O., Luksemburg, W.J., Wong, A.S., Wong, M.H., 2007. Spatial distribution of
polybrominated diphenyl ethers and polychlorinated dibenzo-p-dioxins and
dibenzofurans in soil and combusted residue at Guiyu, an electronic waste
recycling site in southeast China. Environ. Sci. Technol. 41, 27302737.
Malte, P., Steohan, H., Angela, S., Ulrich, E., 2004. Comparative GC/MS and LC/MS
detection of hexabromocyclododecane (HBCD) in soil and water samples.
Organohalogen Compd. 66, 224231.
Mariussen, E., Fonnum, F., 2003. The effect of brominated ame retardants on
neurotransmitter uptake into rat brain synaptosomes and vesicles. Neurochem.
Int. 43, 533542.
Meijer, S.N., Steinnes, E., Ockenden, W.A., Jones, K.C., 2002. Inuence of
environmental variables on the spatial distribution of PCBs in Norwegian and
U.K. soils: implications for global cycling. Environ Sci Technol 36, 21462153.
Minh, N.H., Minh, T.B., Watanabe, M., Kunisue, T., Monirith, I., Tanabe, S., Sakai, S.,
Subramanian, A., Sasikumar, K., Pham, H.V., Bui, C.T., Tana, T.S., Prudente, M.S.,
2003. Open dumping site in Asian developing countries: a potential source of
polychlorinated dibenz-p-dioxins and polychlorinated dibenzofurans. Environ.
Sci. Technol. 37, 14931502.
Minh, N.H., Minh, T.B., Kajiwara, N., Kunisue, T., Subramanian, A., Iwata, H., Tana,
T.S., Baburajendran, R., Karuppiah, S., Viet, P.H., Tuyen, B.C., Tanabe, S., 2006.

2371

Contamination by persistent organic pollutants in dumping sites of Asian

developing countries: implication of emerging pollution sources. Arch. Environ.
Contam. Toxicol. 50, 474481.
Nam, J.J., Thomas, G.O., Jaward, F.M., Steinnes, E., Gustafsson, O., Jones, K.C., 2008.
PAHs in background soils from Western Europe: inuence of atmospheric
deposition and soil organic matter. Chemosphere 70, 15961602.
Remberger, M., Sternbeck, J., Palm, A., Kaj, L., Stromberg, K., Brorstrom-Lunden, E.,
2004. The environmental occurrence of hexabromocyclododecane in Sweden.
Chemosphere 54, 921.
Sellstrom, U., de Wit, C.A., Lundgren, N., Tysklind, M., 2005. Effect of sewage-sludge
application on concentrations of higher-brominated diphenyl ethers in soils and
earthworms. Environ. Sci. Technol. 39, 90649070.
Soderstrom, G., Sellstrom, U., de Wit, C.A., Tysklind, M., 2004. Photolytic
debromination of decabromodiphenyl ether (BDE 209). Environ. Sci. Technol.
38, 127132.
Takahashi, S., Sakai, S.I., Watanabe, I., 2004. A small scale intercalibration study on
organobromine compounds in Japan: results on brominated dioxins, mixed
halogenated dioxins and brominated ame retardants. Organohalogen Compd.
66, 541545.
Tanabe, S., 2006. Environmental Specimen Bank in Ehime University (es-BANK),
Japan for global monitoring. J. Environ. Monit. 8, 782790.
Watanabe, I., Sakai, S., 2003. Environmental release and behavior of brominated
ame retardants. Environ. Int. 29, 665682.
Weber, R., Kuch, B., 2003. Relevance of BFRs and thermal conditions on the
formation
pathways
of
brominated
and
brominated-chlorinated
dibenzodioxins and dibenzofurans. Environ. Int. 29, 699710.
Yu, Z., Peng, P., Sheng, G., Fu, J., 2008. Determination of hexabromocyclododecane
diastereoisomers in air and soil by liquid chromatographyelectrospray tandem
mass spectrometry. J. Chromatogr. A 1190, 7479.
Yun, S.H., Addink, R., McCabe, J.M., Ostaszewski, A., Mackenzie-Taylor, D., Taylor,
A.B., Kannan, K., 2008. Polybrominated diphenyl ethers and polybrominated
biphenyls in sediment and oodplain soils of the Saginaw River watershed,
Michigan, USA. Arch. Environ. Contam. Toxicol. 55, 110.
Zou, M.Y., Ran, Y., Gong, J., Mai, B.X., Zeng, E.Y., 2007. Polybrominated diphenyl
ethers in watershed soils of the Pearl River Delta, China: occurrence, inventory,
and fate. Environ. Sci. Technol. 41, 82628267.