Science of the Total Environment 408 (2010) 21552162

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Science of the Total Environment

j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / s c i t o t e n v

Accumulation of polychlorinated biphenyls and brominated ame retardants in

breast milk from women living in Vietnamese e-waste recycling sites
Nguyen Minh Tue a, Agus Sudaryanto b, Tu Binh Minh c, Tomohiko Isobe b, Shin Takahashi a,,
Pham Hung Viet c, Shinsuke Tanabe a
a
b
c

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
Centre for Environmental Technology and Sustainable Development, Hanoi University of Science, 334 Nguyen Trai, Hanoi, Vietnam

a r t i c l e

i n f o

Article history:
Received 28 October 2009
Received in revised form 6 January 2010
Accepted 8 January 2010
Available online 8 February 2010
Keywords:
Breast milk
E-waste
Exposure pathway
HBCD
PBDE
PCB

a b s t r a c t
This study investigated the contamination status of PCBs, PBDEs and HBCDs in human and possible exposure
pathways in three Vietnamese e-waste recycling sites: Trang Minh (suburb of Hai Phong city), Dong Mai and
Bui Dau (Hung Yen province), and one reference site (capital city Hanoi) by analysing human breast milk
samples and examining the relationships between contaminant levels and lifestyle factors. Levels of PBDEs,
but not PCBs and HBCDs, were signicantly higher in Trang Minh and Bui Dau than in the reference site. The
recyclers from Bui Dau had the highest levels of PBDEs (20250 ng g 1 lipid wt.), higher than in the
reference group by two orders of magnitude and more abundant than PCBs (2859 ng g 1 lipid wt.), and
were also the only group with signicant exposure to HBCDs (1.47.6 ng g 1 lipid wt.). A specic accumulation, unrelated to diet, of low-chlorinated PCBs and high-brominated PBDEs was observed in e-waste
recyclers, suggesting extensive exposure to these compounds during e-waste recycling activities, possibly
through inhalation and ingestion of dust. The estimated infant intake dose of PBDEs from breast milk of some
mothers occupationally involved in e-waste recycling were close to or higher than the reference doses issued
by the U.S. EPA.
2010 Elsevier B.V. All rights reserved.

1. Introduction
Waste electrical and electronic equipment, also known as e-waste,
refers to end-of-life products encompassing information-communication devices, consumer electronics and household appliances. Owing
to the short life span of devices such as computers, television sets,
stereo systems, printers and cell phones, e-waste is generated in large
amounts, with an annual volume of 2050 million tonnes world-wide
and increases rapidly at a rate of 35% per year (UNEP, 2005). The
hazard of e-waste lies in the high content of many toxic substances
(BAN and SVCT, 2002) including heavy metals (lead, mercury,
cadmium, etc.) and persistent organohalogen compounds such as
polychlorinated biphenyls (PCBs) and brominated ame retardants
(BFRs). PCBs are present in older electrical capacitors and transformers
as coolants and dielectrics whereas BFRs are additives found in most
polymeric parts (printed circuit boards, cable coatings, plastic casings,
etc.). There are increasing evidences that BFRs, such as polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecanes
(HBCDs), exhibit a range of toxic effects similar to PCBs, including

Corresponding author. Tel./fax: + 81 89 927 8196.

E-mail address: [email protected] (S. Takahashi).
0048-9697/$ see front matter 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.scitotenv.2010.01.012

endocrine disruption as well as reproductive and neurodevelopmental

toxicity (Legler and Brouwer, 2003; Birnbaum and Staskal, 2004).
Uncontrolled e-waste recycling has become a topic of serious
concern in recent years. It is estimated that up to 80% of e-waste from
industrialised countries is exported to Asian developing countries for
recycling, exploiting the inexpensive cost of labour and weak
enforcement of environmental laws (BAN and SVCT, 2002). Large
scale waste processing operations employing primitive practices such
as uncontrolled dismantling, acid stripping and open burning in
Chinese e-waste recycling sites (EWRSs) have resulted in severe
environmental contamination (Wong et al., 2007). The human
exposure levels to PCBs in Taizhou region (Zhao et al., 2007) and to
PBDEs in Guiyu town (Bi et al., 2007) are two of the highest ever
reported. In other Asian developing countries such as Cambodia, India,
Philippines and Viet Nam, although open waste disposal sites have
been identied as potential sources of PCBs and dioxin-like compounds (Minh et al., 2003), information on EWRS are lacking. Available data, albeit limited, indicate that the levels of PCBs and BFRs in
the general populations from these countries are lower than those
from developed countries (Schecter et al., 2004; Sudaryanto et al.,
2005, 2008a; Malarvannan et al., 2009); nevertheless EWRSs are
suspected as potential hotspots of these contaminants. In this context,
the present study was carried out to assess the human exposure to
persistent organohalogen compounds related to e-waste recycling in

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N.M. Tue et al. / Science of the Total Environment 408 (2010) 21552162

Viet Nam. Breast milk was selected as bioindicator on account of the

simple and non-invasive sampling, relatively high content of lipid and
lipophilic contaminants, and relevance to infants' health. PCBs, PBDEs
and HBCDs were determined in human breast milk collected from
three EWRSs and a reference site in view of contamination levels,
congener patterns, inuence of lifestyle factors and potential health
risk for breastfeeding infants.
2. Materials and methods
2.1. Study locations
End-of-life electrical and electronic equipment in Viet Nam are
often picked up by scrap collectors, through purchase from their
former owners or by scavenging domestic waste disposal sites. The
wastes are then transported to trade villages specialised in recycling.
The present study investigated three e-waste recycling sites located in
the Red River delta region, in the northern part of the country; Dong
Mai (DM, Hung Yen province, battery recycling), Trang Minh (TM,
suburb of Hai Phong City, e-waste dismantling) and Bui Dau (BD,
Hung Yen province, e-waste dismantling). All study locations were
small villages with approximately 80 households or less. E-waste
recycling as a trade started in these villages very recently at the
beginning of the decade, except in the case of DM where the recycling
of lead from batteries has been occurring for almost four decades.
Most businesses are family-based and e-waste is recycled in the
backyard of the house. The waste processing often consists of only
dismantling, retrieval of easily accessible metals and grinding plastic
casings intro reusable pellets. Circuit boards are not processed and
instead sold to foreign buyers. Alongside these recent recycling
activities, the villages still maintain traditional crop production. A
minority of the families also raise livestock or aqua-culture sh in
limited quantities in-house, but the main supplies of livestock
produces and sh for all the three communities are from the
neighbouring communes.
2.2. Sample collection
The sampling survey was conducted in August 2007. In each of the
three recycling sites, the number of nursing mothers was limited to
around 20 or less. Four breast milk samples from DM, eleven from TM
and nine from BD were collected from the mothers who agreed to
donate. As reference, another nine samples were collected from the
capital Hanoi (HN), a typical urban area. Informed consents were
obtained from all donors. Questionnaire survey was also conducted to
acquire personal information on age, height and weight measurements, number of deliveries and duration of nursing periods,
occupation (recyclers or non-recyclers), period of involvement in
recycling activities and dietary habit (Table 1). All donors were nonsmokers and appeared healthy. Breast milk was expressed by the
donor or with the help of a midwife into a solvent-precleaned glass
container with Teon-lined screw caps. The samples were kept in
gel ice immediately after collection and then sent within 8 h to our

laboratory in Viet Nam and frozen at 20 C. Later the frozen samples

were air-transported with gel ice to the Environmental Specimen
Bank (es-BANK, Ehime University, Japan) and stored at 25 C in
until analysis.
2.3. Chemical analyses
Approximately 40 g of sample was freeze-dried and then Soxhletextracted with 300 ml diethyl ether and 100 ml hexane for 7 h. About
10% of the extract was used for determination of the lipid content
using the gravimetric method. The remaining extract was spiked with
13
C12PCBs, 13C12PBDEs (5 ng each) and 13C12HBCDs (10 ng each)
as standard surrogates, subjected to gel permeation chromatography
(packed Bio-Bead S-X 3, Bio-Rad Laboratories, USA) for lipid removal
using a hexane/dichloromethane (DCM) mixture (1:1 v/v) as eluant.
The cleaned-up extract was then concentrated and passed through 4 g
of activated silica gel (Wakogel DX, Wako, USA) packed in a glass
column for separation of HBCDs from PCBs and PBDEs. The rst
fraction containing PCBs and PBDEs, eluted with a mixture of hexane/
DCM (95:5 v/v, 80 ml), was spiked with 5 ng 13C12BDE-139 as
internal standard and solvent-exchanged into iso-octane. The HBCD
fraction, eluted with another mixture of hexane/DCM (75:25 v/v,
100 ml), was concentrated until dryness and then redissolved in a
methanol solution containing deuterium-labelled HBCDs-d18 (10 ng
each) as internal standards.
PCBs (62 congeners) and PBDEs (14 congeners commonly found in
abundance in the technical PBDE mixtures (La Guardia et al., 2006),
namely BDE-3, -15, -28, -47, -99, -100, -153, -154, -183, -196, -197,
-206, -207, and -209) were quantied using a gas chromatograph
(Agilent 7890 series) equipped with a mass-selective detector
(Agilent 5975 series) and a DB-1 fused silica column (J&W Scientic)
having 0.25 mm i.d. 30 m 0.25 m lm thickness for PCBs and
mono- to hepta-BDEs or 0.25 mm i.d. 15 m 0.1 m lm thickness
for octa- to deca-BDEs. The GC oven temperature program for PCBs
was: from 120 C to 180 C at 20 C min 1, 2 C min 1 to 260 C,
5 C min 1 to 300 C and held for 4 min. PCBs were monitored in
selective ion monitoring mode (EI-SIM) at masses of [M]+ and [M+ 2]+
for mono- to tetra-CBs, [M+ 2]+ and [M+ 4]+ for penta- to nona-CBs
and [M+ 4]+ and [M+ 6]+ for deca-CB. The instrumental set-up for
PBDE analysis has been described previously (Sudaryanto et al.,
2008b). HBCDs (, and isomers) were quantied by LC-MS/MS
according to the methods described elsewhere (Isobe et al., 2007).
Procedural blanks were analysed simultaneously with samples to
check for interferences and contamination. Detection limits were
calculated as three times the procedural blank, and were in the range
of 0.010.05 ng g 1 lipid wt. for all target compounds. Recoveries of
13
C-labelled surrogates were in the range of 57%107% for PCBs, 63%
110% for PBDEs and 84%113% for HBCDs. The analysis of human
breast milk described above followed our common procedure
employed for animal tissues. For quality assurance and control, our
laboratory participated in an intercalibration exercise on BFRs using
the blubber of a marine animal as the reference material and our data
were in good agreement with those reported by other laboratories

Table 1
General characteristics of the donors of breast milk.
Parameters

Hanoi (n = 9)

Dong Mai (n = 4)

Trang Minh (n = 11)

Bui Dau (n = 9)

Age (year)
Weight (kg)
Height (cm)
Body mass index (kg m 2)
Number of children
Total nursing time (month)
Occupation

2335 (28.2)
4662 (54.3)
155167 (160.9)
16.525.4 (21.1)
12 (1.67)
4.525 (12)
89% ofce worker
11% housewife

2531 (28.3)
4252 (46.0)
153155 (154.5)
17.921.6 (19.3)
14 (2.3)
457 (26)
25% recycler
75% farmer

1826 (23.6)
4150 (45.5)
150160 (154.6)
16.421.3 (19.1)
12 (1.55)
1.524 (12)
55% recycler
45% housewife

2435 (29.3)
4046 (44.0)
150155 (154.0)
16.721.6 (19.1)
14 (2.2)
9.579 (34)
55% recycler
45% others

Values between parentheses are arithmetic means.

N.M. Tue et al. / Science of the Total Environment 408 (2010) 21552162

2157

HBCDs were calculated using RfD values of 1 (Oostdam et al., 1999),

0.1, 0.1, 0.2 (EPA, 2008) and 0.2 g kg 1 day 1 (European Chemicals
Bureau, 2007), respectively.

(Isobe et al., 2007). Concentrations were expressed on a lipid weight

basis unless otherwise specied.
2.4. Statistical analyses

3. Results
The Wilcoxon rank sum test was used for assessing whether the
contaminant levels between groups were signicantly different. In
this analysis, non-detectable levels were set to zero. Principal
component analysis (PCA) was employed to categorise PCB and
PBDE congeners according to their variation patterns. This analysis
included only the congeners detected in at least 70% of the samples.
The inuence of socio-demographic parameters on the total concentration of each category was then analysed qualitatively using
multiple linear regressions. The parameters used as independent
variables included: age, body mass index (BMI), total duration of
nursing, period of involvement in recycling activities and consumption rate of food from animal origin (total rate of meat, sh and dairy
products, servings per week). Other location-specic factors were
assumed to be negligible and not considered. Parameters with a pvalue of less than 0.05 were considered as having signicant
relationship with contamination level. In these later two statistical
analyses, non-detectable concentrations were set to half of the
detection limit and then all concentrations were log-transformed to
bring the data distribution closer to normality. All calculations were
performed using the statistical software package R version 2.9.0.

PCBs, PBDEs and HBCDs were detected in all the samples analysed
(Table 2). In terms of total concentrations, PCBs were more abundant
than PBDEs and HBCDs by one order of magnitude or higher in majority
of the samples. However, PBDEs were more abundant than PCBs in three
donors who were involved in the recycling of e-waste in BD.
Total PCB levels were statistically comparable among locations but
signicant differences were observed with individual PCB congeners.
The residents of the three recycling sites had statistically lower
(p < 0.05) levels of high-chlorinated congeners such as CB-138, -153
and -180 but somewhat higher levels of tri- and tetra-chlorinated
congeners (tri- and tetra-CBs) than those of the urban reference site.
CB-28 was detected at signicantly higher (p < 0.05) levels in TM and
BD (recyclers only) than in HN, and the highest levels of CB-28 and
CB-74 were found in battery recyclers from DM. In each recycling site,
the total levels of tri- and tetra-CBs were higher in the recycler group
than in the non-recycler group, with the median being 30 vs 10, 6.7 vs
4.9 and 5.0 vs 2.8 ng g 1 lipid wt. in DM, TM and BD, respectively.
However, these differences were not statically signicant (p > 0.05),
probably due to the limited number of samples. The preferential
accumulation of these low-chlorinated biphenyls in the recycling sites
resulted in distinctive PCB congener proles. As seen in Fig. 1, the
prole in the reference site followed the order of CB-138 > CB153 > CB-118 > CB-180 > CB-99 > CB-74 > CB-28 whereas in TM and
BD, CB-28 and CB-74 were as abundant as CB-99 and more than CB180. In DM, the battery recycling site, CB-28 and CB-74 were the
dominant congeners. Based on the PCA results PCB congeners were
divided into three categories (Fig. 2): (a) high-chlorinated PCBs
(HighCB), including hepta to deca congeners and two hexa congeners
(CB-138 and CB-153), aligned with the rst principal component
(PC1) which accounted for 57% of the total variance; (b) low-

2.5. Risk assessment

The risk for infants exposed to contaminants in mother milk was
assessed using hazard quotients (HQs). An HQ is dened as the ratio of
the estimated daily intake dose (DI) of the compound via breastfeeding to the corresponding maximum acceptable oral dose for human, or
reference dose (RfD). A value of HQ higher than 1 indicates potential
risk. The DIs were calculated based on the assumption that an infant in
average weighs 5 kg and consumes 700 g mother milk daily (Oostdam
et al., 1999). HQs of total PCBs, BDE-47, BDE-99, BDE-153 and total

Table 2
Concentrations (ng g 1 lipid wt.) of major PCB congeners, PBDE congeners and HBCD isomers in human breast milk collected from Hanoi and Vietnamese e-waste recycling sites.
Compound

CB-28
CB-74
CB-99
CB-118
CB-138
CB-153
CB-180
PCBs
BDE-15
BDE-28
BDE-47
BDE-99
BDE-100
BDE-153
BDE-154
BDE-183
BDE-196
BDE-197
BDE-206
BDE-207
BDE-209
PBDEs
-HBCD
-HBCD
-HBCD
HBCDs

Bui Dau non-recyclers

Bui Dau recyclers

Median

Hanoi
Range

Median

Dong Mai
Range

Median

Range

Median

Range

Median

Range

1.1
2.8
2.9
4.8
9.7
8.2
3.7
46
0.040
0.029
0.13
0.057
0.040
0.098
n.d.
0.029
0.010
0.045
n.d.
0.025
n.d.
0.57
0.33
n.d.
n.d.
0.33

0.427.6
1.36.0
1.27.3
2.013
3.817
3.816
1.95.5
20100
0.0140.073
0.0170.067
0.0700.25
n.d.0.12
n.d.0.10
0.0620.14
n.d.0.037
n.d.0.038
n.d.0.015
0.0160.11
n.d.0.027
n.d.0.057
n.d.
0.240.8
0.0661.4
n.d.
n.d.0.13
0.0701.4

5.6
5.9
2.5
3.5
4.0
3.5
1.0
50
0.011
0.010
0.097
n.d.
n.d.
0.10
n.d.
0.050
0.010
0.046
0.024
0.030
0.17
0.73
0.43
n.d.
n.d.
0.42

1.034
1.215
0.884.6
1.28.3
2.111
1.79.0
0.513.5
1169
0.0100.032
n.d.0.044
0.0410.20
n.d.0.028
n.d.
0.0610.25
n.d.
0.0290.11
n.d.0.018
0.0260.14
n.d.0.10
0.0110.11
0.0690.50
0.261.1
0.110.97
n.d.
n.d.
0.110.97

2.0
2.7
2.1
3.3
5.8
5.7
1.8
33
0.030
0.074
0.40
0.11
0.082
0.40
0.021
0.13
0.036
0.26
0.05
0.10
0.42
2.3a
0.38
n.d
n.d.
0.38

0.7210
0.427.6
0.604.3
1.06.9
1.911
1.811
0.714.3
1173
0.0100.34
0.0241.0
0.111.8
0.0320.51
0.0220.21
0.0211.5
n.d.0.069
0.0221.2
n.d.0.14
0.0320.78
0.0120.23
0.0410.41
0.127.3
0.5513
0.123.3
n.d.0.051
n.d.0.27
0.113.3

0.85
1.6
1.7
2.8
4.8
3.6
1.4
24a
0.057
0.21
0.81
0.38
0.13
0.65
n.d.
0.14
0.037
0.47
0.014
0.15
0.11
3.2a
0.36
n.d.
n.d.
0.36

0.4214
0.563.7
0.602.0
1.03.3
1.76.0
1.55.2
0.502.1
8.428
0.0220.075
0.130.27
0.631.0
0.220.56
0.0831.6
0.271.0
n.d.0.035
0.0530.22
0.0270.056
0.170.61
n.d.0.03
0.100.18
n.d.0.16
2.04.0
0.291.2
n.d.
n.d.
0.291.2

1.9
2.7
2.8
4
5.5
4.6
1.6
34
0.35
0.96
4.8
3.2
0.80
4.4
0.39
1.2
0.59
7.5
0.26
3.5
4.1
84a
1.9
n.d.
0.045
2.0a

1.514
1.68.6
1.93.6
3.65.6
4.66.7
3.65.6
1.31.7
2859
0.161.5
0.828.2
3.532
2.215
0.543.1
2.123
0.272.1
0.492.7
0.255.1
3.129
0.164.5
1.351
0.8796
20250
1.47.5
n.d.
n.d.0.099
1.47.6

n.d.: not detected.

a
Signicantly different from reference site (p < 0.05).

Trang Minh

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N.M. Tue et al. / Science of the Total Environment 408 (2010) 21552162

chlorinated PCBs (LowCB), consisting of mainly tri and tetra

congeners, aligned with PC2 (17% of variance); and (c) others
(MediumCB), mostly penta and a few hexa congeners including CB99, -101, -118, -128, etc., contributing to both PCs.
PBDE levels in the battery recycling site DM were comparable with
those in the reference site HN whereas the levels in the two e-waste
dismantling sites, TM and BD, were statistically higher (Table 2). In TM,
the recycler and non-recycler groups had similar levels of total PBDEs,
with an overall median higher than in the reference group by a factor of 4.
In BD, although the levels in the non-recycler group were only
comparable to those in TM, the recycler group had the highest PBDE
levels of all donors, approximately two orders of magnitude higher than
those in the residents of HN. In the reference site, BDE-47 and BDE-153

were the dominant PBDE congeners whereas BDE-209 was at nondetectable levels (Fig. 1). BDE-209 was detected in most of the samples
collected from the recycling sites with varying proportions up to 50%.
Octa to nona congeners were also observed at higher percentages. BDE197 and -207 were prominent in samples from recyclers living in BD,
with levels comparable to BDE-47. PCA of PBDE congeners indicated that
these compounds could be considered as a single category because 86% of
the variance could be represented by PC1 (Fig. 2), suggesting a high
degree of correlation among congeners with the exception of BDE-209,
main contributor to PC2 (only 7.4% of the variance).
HBCDs levels were not statistically different among residents of HN,
DM and TM (both recyclers and non-recyclers) and BD (non-recyclers).
Recyclers from BD had signicantly higher levels than the other groups,

Fig. 2. PCA loading plot of individual congeners of PCBs (left) and PBDEs (right). Numbers represent IUPAC numbers of PCB/PBDE congeners.

N.M. Tue et al. / Science of the Total Environment 408 (2010) 21552162

2159

Table 3
Coefcients () and p-values of socio-demographic parameters in linear models of contaminant concentrations.
Parameters

Age
BMI
Nursing time
Recyclinga
Dietb

Model
a
b

LowCB

MediumCB

HighCB

PBDEs

HBCDs

0.028
0.062
0.008
0.145
0.008

0.19
0.36
0.11
0.009
0.85

0.015
0.046
0.002
0.076
0.070

0.23
0.09
0.49
0.022
0.013

0.007
0.023
0.0074
0.061
0.080

0.51
0.22
0.007
0.34
0.002

0.005
0.073
0.013
0.180
0.037

0.88
0.25
0.12
0.029
0.64

0.020
0.051
0.009
0.101
0.003

0.45
0.25
0.13
0.13
0.96

R2

R2

R2

R2

R2

0.40

0.013

0.37

0.023

0.48

0.002

0.38

0.018

0.24

0.17

Period of involvement in recycling activities (years).

Consumption rate of food from animal origin (total rate for meat, sh and dairy products, servings per week).

former were not major sources of PCBs. Total PCB levels in Vietnamese
human breast milk were in comparable ranges with those reported in
other Asian developing countries and lower than in developed nations
(Table 4). The levels observed in this study were similar to the serum
PCB levels in the residents of Guiyu (median 52 ng g 1 lipid wt.), the
largest recycling site of electronic waste in China, reported by Bi et al.
(2007). These authors also did not nd any signicant difference
between the exposed and the reference populations. Thus e-waste
related PCB contamination is believed to involve old electric materials,
especially transformers, rather than electronic waste. The case of
Luqiao, the largest Chinese disassembly site of electrical waste, is an
example where very high PCB levels in human breast milk associated
with e-waste recycling were reported (median 359 ng g 1 lipid wt.,
Zhao et al., 2007). The absence of substantial PCB contamination
suggests that in the Vietnamese recycling sites, the occurrence of
waste materials containing PCBs may be uncommon and the recycling
of these materials is of limited scale.
Signicant exposure to PBDEs was observed in the two e-waste
dismantling sites, TM and BD, especially in BD recyclers. Compared
with the levels reported by other studies, the PBDE levels in the

with a 6-fold difference compared with the reference group (Table 2).
-HBCD was the dominant isomer in all the samples, accounting for
more than 90% of the total HBCD levels. -HBCD was detected in eight
samples with a proportion of less than 10% and -HBCD was detected in
only one sample.
Results from the tting of chemical concentrations to multiple
linear regression models of socio-demographic parameters (Table 3)
showed that LowCB and PBDEs were associated only with involvement period in recycling activities, HighCB correlated positively with
consumption of food from animal origin but negatively with nursing
time whereas MediumCB had positive associations with both food
consumption and recycling activities. Age and BMI did not show any
signicant inuence on contaminant concentrations.
4. Discussion
4.1. Contamination levels
The similarity in PCB levels in the three Vietnamese e-waste
recycling sites as also seen in the reference site indicates that the
Table 4
Comparison of PCBs and BFRs in human breast milk from Viet Nam with other countries.
Country

Survey year

PCBs
206

7.1

India

20032005
2004
2007
20022003

34

0.6a

Indonesia
Philippines
Vietnam (HN)
Vietnam (DM)
Vietnam (TM)
Vietnam (BD non-recylers)
Vietnam (BD recyclers)

20012003
2004
2007
2007
2007
2007
2007

27
60
46
51
33
28
34

1.5
3.8
0.57
0.73
2.3
3.2
84

65

1.54

Belgium
Norway
Russia
Spain

2004
2006
2006
20002002
2002
20032004

123
165
175
111

2.01
3.19
0.96
6.1

1.5
0.13
0.62
27

Sweden
United Kingdom
United States

20062007
20022003
20012003
20022003

111
180
126

2.93a
6.3b
50.4

0.35

Asian developing countries

China

Other countries
Japan

PBDEs

HBCDs
0.86

0.62
0.33
0.42
0.38
0.36
2.0

1.44.0c

0.5

Concentrations are given as median if available (or arithmetic mean otherwise) and expressed in nanogram per gram lipid wt.
a
Mono- to hepta-BDEs only.
b
Mono- to hexa-BDEs only.
c
Pooled values.

References
Zhao et al. (2007)
Sudaryanto et al. (2008b)
Shi et al. (2009)
Subramanian et al. (2007),
Sudaryanto et al. (2005)
Sudaryanto et al. (2008a)
Malarvannan et al. (2009)
This study
This study
This study
This study
This study

Inoue et al. (2006)

Kakimoto et al. (2008)
Colles et al. (2008)
Polder et al. (2008b)
Polder et al. (2008a)
Bordajandi et al. (2008),
Gmara et al. (2007),
Eljarrat et al. (2009)
Lignell et al. (2003)
Kalantzi et al. (2004)
Ryan et al. (2006), She et al. (2007)

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reference group in this study (HN) were among the lowest in the
world (Table 4), consistent with the ndings of Schecter et al. (2004).
Levels in TM and BD non-recyclers were higher in Indonesia and Japan
and close to those in European countries whereas levels in BD
recyclers were in the same range with American levels which are the
highest reported among non-occupationally exposed populations.
The differences in waste materials, workload and processing methods
may contribute to the variation of PBDE contamination levels in the
Vietnamese recycling sites. For instance, PBDEs may be minor contaminants in waste batteries as suggested by the low levels accumulated in the battery recyclers in DM. On the other hand, the
elevated levels in recyclers from BD may be the result of processing
large amounts of waste materials with high PBDE contents using
methods which facilitate the release of these contaminants from the
waste matrices, such as burning and other thermal processes. It is also
remarkable that in BD recyclers, the PBDEs levels exceeded those of
PCBs, despite the long legacy of the latter compounds. This unusual
feature (comparison in Table 4) has so far been observed only in case
of uncontrolled e-waste recycling (Bi et al., 2007). It clearly indicates
an extensive exposure to PBDEs with different sources from those of
legacy persistent organic pollutants (POPs); nevertheless the highest
PBDE levels in breast milk in this study were still lower than those in
serum of Chinese e-waste dismantling workers from Guiyu (median
600 ng g 1 lipid wt., Bi et al., 2007) by an order of magnitude. This large
difference in lipid weight-normalised concentrations, albeit in two
separate human matrices, again infers that Vietnamese recycling sites
are still less contaminated in terms of PBDEs than their Chinese counterparts, probably on account of a smaller scale of e-waste processing.
Although information on HBCDs in human matrices is still limited,
available data indicate that the accumulation levels of HBCDs in
human breast milk from Asia, USA and several European countries are
very low (<1 ng g 1 lipid wt., Table 4). The HBCD levels in HN, DM
and TM observed in this study also fell within this range, suggesting
that products containing HBCDs may be scarce in Viet Nam and also
uncommon in the e-waste. In contrast, the contamination levels were
reported to be somewhat higher in Japan and very high in Spain
(Table 4), reecting an extensive usage of HBCDs in Japan and some
European countries (Watanabe and Sakai, 2003). In Vietnamese e-waste
recycling sites, exposure to waste materials containing HBCDs appeared
to be limited to recyclers from BD, coincidentally the group most
exposed to PBDEs. The HBCD levels in this group were comparable with
those in Japanese women; nevertheless these exposure levels associated
with e-waste recycling were still much lower than the non-occupational
exposure levels reported in Spain.
4.2. Accumulation patterns
Higher levels of tri- and tetra-CBs in the recycling sites indicate a
specic exposure in e-waste recycling processes. This is further
supported by a signicant positive relationship between LowCB level
and period of involvement time in recycling activities (Table 3). The
source of these congeners may be old electric devices such as
capacitors and small transformers which contain PCBs as heat transfer
and dielectric uids. Several PCB technical mixtures such as Aroclor
1016, 1242 or Kaneclor 300 contain principally congeners with low
degrees of chlorination (Takasuga et al., 2006). Moreover, lowchlorinated biphenyls from e-waste can be more accessible to human
due to their relatively higher volatility (Bamford et al., 2000). This
exposure source may explain the highest levels of tri- and tetra-CBs
found in DM, a site recycling exclusively electrical waste.
The elevated relative concentrations of octa- to deca-BDEs in the
recycling sites were the distinctive feature compared with the PBDE
prole in HN which was dominated by lower-brominated congeners
such as BDE-47 and BDE-153. The latter pattern seems to be common
in human breast milk from many countries in Asia (Inoue et al., 2006;
Sudaryanto et al., 2008a), Europe (Polder et al., 2008a) and North

America (She et al., 2007). There are several plausible explanations

for the preferential accumulation of BDE-47 and BDE-153 in human:
they are major constituents of the PentaBDE technical mixtures (La
Guardia et al., 2006), have relatively good bioavailability (Hakk and
Letcher, 2003) and strong bioaccumulation features (Burreau et al.,
2006) and can be metabolites of higher-brominated congeners
(Stapleton et al., 2004). Therefore secondary exposure via diet may
be the major pathway of BDE-47 and BDE-153. On the other hand,
high-brominated BDEs, notably BDE-209 are poorly biomagnied
through food webs (Burreau et al., 2006). BDE-209 also has a very low
assimilation rate (<1%) and a fast clearance rate in mammals (Hakk
and Letcher, 2003). Thus accumulation of high-brominated BDEs is
often attributed to a sustained exposure to Octa and DecaBDE
technical mixtures at elevated levels, especially in an occupational
context such as the case of rubber and cable manufacturing workers in
Sweden (Thuresson et al., 2005) or e-waste recycling workers in
China (Bi et al., 2007). Therefore the presence of octa- to deca-BDEs in
breast milk of the mothers in Vietnamese e-waste recycling sites
could be an indication of primary exposure to Octa and DecaBDE
technical mixtures from e-waste. The large variation in relative concentrations of these congeners even within the same group suggests
that either human exposure to higher-brominated BDEs may vary
with different microenvironments depending probably on the
composition of the ame retardants contained in waste materials, or
the toxicokinetics of these compounds may be different in individual
donors.
4.3. Exposure pathways
As PBDE levels did not correlate with HighCB levels (Pearson's r =
0.012, p = 0.95), the two groups of compounds may have different
exposure sources/pathways. In case of HighCB, the main pathway is
likely to be dietary intake, evidenced by a positive association with
consumption of food from animal origin (Diet parameter, Table 3). This
is often the case with legacy POPs such as high-chlorinated PCBs that
have been accumulated in biota, especially fatty tissues of animals,
during their extensive release in the past. A dietary exposure also
explains the higher accumulation in the urban population that had
richer diets than the residents of the recycling sites. On the other hand,
exposure to PBDEs and LowCB seems to be mainly non-dietary and
related to the recycling of e-waste, as indicated by a single signicant
positive association with involvement time in recycling activities
(Recycling parameter, Table 3). This occupational exposure may occur
through accidental ingestion/inhalation of particulate matters generated during activities such as dismantling, shredding or thermal treatment of e-waste. In another case of uncontrolled e-waste recycling,
elevated concentrations of air particles and extremely high concentrations of air particle-bound PBDEs have indeed been reported (Wong
et al., 2007). In this study, dietary intake did not appear to be an
important factor contributing to PBDE levels, partly because the main
supplies of food from animal origin were not produced on site and thus
not directly contaminated by the recycling activities.
The exposure to HBCDs may occur in a similar fashion to PBDEs as
their levels correlated with each other (Pearson's r = 0.72, p < 0.0001).
HBCD levels also have a positive association with recycling activities, though not statistically signicant (p = 0.13, Table 3). In case
of PCB congeners in the MediumCB category, the exposure pathways may be both dietary and non-dietary through occupational
contact with e-waste, as suggested by the positive associations
with Diet and Recycling parameters (p = 0.013 and 0.022, respectively, Table 3).
4.4. Depuration by lactation
Another noteworthy detail is the difference in depuration feature
of the target compounds. In the literature, legacy POPs such as PCBs

N.M. Tue et al. / Science of the Total Environment 408 (2010) 21552162

tend to have lower levels in multiparae (mothers having given birth

twice or more) than in primiparae (rst-time mothers) because a
signicant portion of the mother's body burden is transferred to the
child during nursing, as remarked by Tanabe and Kunisue (2007) in a
review on POPs in human milk. However, in the case of emerging POPs
such as BFRs, the decrease in the mother's burden by lactation was
reported to be not appreciable (Hooper et al., 2007; Schecter et al.,
2003; Sudaryanto et al., 2008a) because recent intake may compensate the loss via breastfeeding. In this study, BFR levels also did not
show any negative correlation with nursing time, unlike HighCB,
indicating that human exposure to BFRs is continuous and that the
intake rate may be comparable to the rate of depuration via lactation.
4.5. Infant health risk
As shown in Fig. 3, the health risk for infants exposed to the target
contaminants via breastfeeding in general may not be serious since
the majority of HQ values are below 1, albeit the HQs of PCBs are
relatively high (>0.1) in most cases. Thus PCB accumulation in
Vietnamese human milk, as a consequence of a long usage history
(Minh et al., 2008) rather than e-waste recycling, should still be
considered with respect to safe consumption by infants. HQ values of
BFRs are generally lower than 0.1, with the exception of recyclers in
BD. This group has high HQs related to PBDEs, with several values
close to or exceeding 1, indicating potential health risk for their
children. The health effects for the infant in the event of daily intake
dose of PBDEs exceeding the RfDs, which were derived from studies
on neurobehavioural developmental toxicities (EPA, 2008), may
include altered motor behaviour, decreased habituation capability,
decreased learning/memory ability or more serious effects. More in
depth epidemiological studies are necessary to assess the effects of
PBDE exposure on the development of children in these recycling
sites.
5. Conclusions
The present study found a signicant accumulation of PBDEs in
breast milk of women living in two Vietnamese e-waste dismantling
sites, possibly through non-dietary intake by accidental ingestion/
inhalation of dust. The highest PBDE levels were found in recyclers

Fig. 3. Hazard quotients of total PCBs, BDE-47, BDE-99, BDE-153 and total HBCDs
calculated for breastfeeding infants.

2161

from the village Bui Dau, higher than the reference levels by two
orders of magnitude and comparable to the highest levels reported in
industrialised countries. PBDEs levels in these recyclers also exceeded
those of legacy POPs such as PCBs. These Vietnamese e-waste recycling sites may be less contaminated than their Chinese counterparts in terms of PCBs and PBDEs; nevertheless the levels of BDE-47
and BDE-99 in breast milk of some mothers occupationally involved in
recycling were sufciently high to be considered unsafe for breastfeeding infants. Thus it is clear that the contamination caused by the
recycling of e-waste should be mitigated to reduce human exposure
to PBDEs and also to a multitude of other toxic substances released
during e-waste recycling activities such as heavy metals, dioxin-like
compounds, polyaromatic hydrocarbons, etc. In order to have a more
complete understanding of the impact of e-waste recycling in the
study locations, these contaminants should be considered in future
works and dust may provide a good sample matrix for assessment of
human exposure.
Acknowledgements
The authors thank Mr Bui Hong Nhat for coordinating the sampling
survey. This study was partly supported by the grants-in-aid for
scientic research (S) (no. 20221003) from Japan Society for the
Promotion of Science (JSPS), the global environment research fund
(RF-064) and the waste management research grants (K2062, K2129
and K2121) from the Ministry of the Environment, Japan, and grants
from global COE program from the Japanese Ministry of Education,
Culture, Sports, Science and Technology (MEXT).
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