DSpace at VNU: Methylated and unsubstituted polycyclic aromatic hydrocarbons in street dust from Vietnam and India: Occurrence, distribution and in vitro toxicity evaluation

Environmental Pollution 194 (2014) 272e280

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

Methylated and unsubstituted polycyclic aromatic hydrocarbons in
street dust from Vietnam and India: Occurrence, distribution and
in vitro toxicity evaluation
Le Huu Tuyen a, b, Nguyen Minh Tue a, b, Shin Takahashi d, *, Go Suzuki c, Pham Hung Viet b,
Annamalai Subramanian a, Kesav A. Bulbule e, Peethambaram Parthasarathy f,
Alagappan Ramanathan g, Shinsuke Tanabe a
a

Center for Marine Environmental Studies (CMES), Ehime University, 2-5 Bunkyo-cho, Matsuyama 790-8577, Japan
Research Centre for Environmental Technology and Sustainable Development (CETASD), Hanoi University of Science, 334 Nguyen Trai Street,
Hanoi, Vietnam
c
Center for Material Cycles and Waste Management Research, National Institute for Environmental Studies (NIES), 16-2 Onogawa, Tsukuba, Japan
d
Agricultural Faculty, Ehime University, 3-5-7 Tarumi, Matsuyama, Japan
e
Kle's Nijalingappa College, Bangalore, India
f
E-Parisara Pvt. Ltd., Bangalore, India
g
Jawaharlal Nehru University, New Delhi, India
b

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 29 April 2014
Received in revised form
21 July 2014
Accepted 24 July 2014

Methylated polycyclic aromatic hydrocarbons (MePAHs), unsubstituted PAHs and AhR-mediated activities were determined in street dust collected from Vietnam and India using a combined approach of
chemical analysis and in vitro reporter gene assay. MePAHs and PAHs diagnostic ratios indicated that the
main sources of MePAHs in Vietnam were pyrogenic emissions, whereas in India there were mixed
sources of pyrogenic and petrogenic emissions. AhR-mediated activities determined by using DR-CALUX
assay were observed in urban street dust at mean 40, 29 and 20 ng CALUX-TEQ/g dw for Hanoi, Bangalore
and New Delhi, respectively. MePAHs and PAHs contributed only 5% or less to AhR-mediated activity in
street dust, indicating the occurrence of unknown AhR agonists. The principal contributors to
Theoretical-TEQs among target compounds were methyl benz[a]anthracene, benzo[b]- and benzo[k]
fluoranthene. The present study indicates importance of MePAHs in evaluation of toxic risk related to
AhR-mediated activity in urban polluted areas.
© 2014 Elsevier Ltd. All rights reserved.

Keywords:
MePAHs
AhR
CALUX
Street dust
Vietnam
India

1. Introduction

Methylated polycyclic aromatic hydrocarbons (MePAHs), one of
PAH derivative groups, are widely distributed in the environment
as is the case with like unsubstituted PAHs. MePAHs such as methyl
naphthalene (MeNap), methyl phenanthrene (MePhe), and methyl
chrysen (MeChy) have been identified from industrial, petrogenic
or incomplete combustion sources (Dimitriou-Christidis et al.,
2003; Wang et al., 1999). Vietnam and India are two of the six
countries in Asia reported as having the highest air pollution in the
world (Kim Oanh et al., 2006). Well known as a major contributor of
air pollution and potential source for the emission of PAHs (Tuyen
et al., 2014), the number of motorcycles in Hanoi-Vietnam was

* Corresponding author.
E-mail address: (S. Takahashi).
/>0269-7491/© 2014 Elsevier Ltd. All rights reserved.

reported to be more than 3.9 million in 2011 (Tran et al., 2012), auto
vehicles in New Delhi and Bangalore-India was also shown to be
high in India with an annual growth of the 10% for car and 9.5% for
two-wheelers. The growth rate of the number of motorcycles was
vre,
even higher than the growth rate of population (3.25%) (Lefe
2009). The population of motorcycle was reported at 4.2 million
units in New Delhi in 2004 (Goyal et al., 2010), reached to 6 million
units in 2010 (Goyal et al., 2013) and for Bangalore the numbers are
vre, 2009). Motor vehicles have been
2.2 million in 2005 (Lefe
believed as major contributions of air pollution in urban cities of
Asian developing countries (Agarwal, 2009; Kim Oanh et al., 2012;
Goyal et al., 2013; Hien et al., 2014).

In the urban environment, street dust is known as a sink for
complex mixtures of traffic related pollutants, contains PAHs and it
is also believed to contain PAHs derivatives (Tuyen et al., 2014). We
found significant levels of PAHs (1500 ng/g dry weight) and AhR-


L.H. Tuyen et al. / Environmental Pollution 194 (2014) 272e280

mediated activities (20 ng CALUX-TEQs/g dry weight) in the street
dust with particle-size of less than 500 mm in a previous study. It is
expected that the smaller particles may contain higher levels of
vehicle exhaust contaminants as well have more toxic activity
compared to larger particles. A previously report also showed that
the highest levels of PAHs were in street dust particles less than
63 mm (Zhao et al., 2009). Therefore, the street dust particle-size
less than 63 mm is preferred selection for chemicals' determination as well as toxic risk assessment because of their potential effects on human respiratory system (Saeedi et al., 2012) and
adherence to human skin (Choate et al., 2006).
MePAHs known as generally more persistent and sometimes
more toxic than their unsubstituted analogues (Sauer and P.B.,
1991). The toxicities of MePAHs as well as unsubstituted PAHs are
often involved in binding to the aryl hydrocarbon receptor (AhR),
induction of AhR-related genes and subsequent transformation to
toxic metabolites (Behnisch et al., 2001). Methyl benz[a]anthracene
(MeBaA) has the ability to induce expression of cytochrome P450
1B1 or aldo-keto reductase 1C9 in rat liver epithelial cells similar to
its parent. The AhR has been known to be involved in number of
biological processes, such as development and detoxification of
exogenous compounds (Denison and Whitlock, 1995) (Hahn et al.,
2006). Using an in vitro reporter gene assay, DR-CALUX, aryl hydrocarbon receptor (AhR) mediated activities which had been
known as genotoxic effects produced by many agonist compounds

such as polyhalogenated aromatic hydrocarbons (PHAHs), PAHs or
MePAHs have been determined. Some MePAHs/PAHs have been
reported as potent stimulators of AhR activation (Trilecov
a et al.,
2011). The model rat hepatoma H4IIE cells stably transfected with
luciferase reporter under control of dioxin responsive element
(DRE) have also been used to study the effect of MePAHs on toxic
events associated with tumor promotion (Machala et al., 2008).
Particularly MeBaAs also has ability to induce DNA adduct forma et al., 2008). Methyl anthrancenes (MeAnt) have
tion (Marvanova
been used for study of their inhibition effects on Gap Junctional
Intercellular Communication (GJIC) in rat liver epithelial cells, in
which MeAnt showed a potent role in tumor promotion and their
biological effect on GJIC were depend on the position of methylated
group (Upham et al., 1996). The MePAHs that have structural features with bay-, baylike region could be a potent inhibitor of GJIC
such as MeBaAs (exception of 10-MeBaA), and 1-methyfluorene
(MeFlu), then resulting in disruption of cell proliferation control,
subsequently contributing to tumor promotion (Weis et al., 1998;
Marvanov
a et al., 2008). Dimethylated PAHs were found to be the
inducers of increased blue sac disease in Japanese medaka and also
to affect its embryonic development (Rhodes et al., 2005).
So far, many studies have been carried out on the characterization of MePAHs as well as PAHs in the atmospheric environment
(Fang et al., 2004; Lehndorff and Schwark, 2009; Lee and Dong,
2010; Di Filippo et al., 2010; Lee and Dong, 2011; Ha et al., 2012;
Khairy and Lohmann, 2012, 2013), but there is no study on the
evaluation of AhR-related toxicity for methylated PAHs in street
dust and on identification of toxically relevant compounds. Integrated risk assessment for human health effect due to contaminants exposure in polluted areas requires data on contamination
levels and sources. However, chemical data of specific groups of
contaminants can not provide sufficient information on potential

toxic effects of the complex mixtures of contaminants in the
environment. Therefore, a combination of chemical analysis and
bio assay based on specific mode of action could provide useful
information on distribution and toxicity evaluation of contaminants. The aims of the present study are to determine not only PAHs
but also their methylated analogues in street dust collected from
two Asian developing countries, Vietnam and India and to measure
AhR-mediated activities in street dust by using the dioxin

273

responsive-chemically activated luciferase gene expression (DRCALUX) bioassay, in order to evaluate the contamination status and
to assess the toxic contribution of MePAHs and their parent compounds in overall toxicity.
2. Material and methods
2.1. Sample collection
Street dust samples were collected from the capital cities of Vietnam (Hanoi, n ¼ 16)
and India (New Delhi, n ¼ 7) and a metropolitan city in India (Bangalore, n ¼ 7) during
2012e2013 using straw brooms. The broom was washed with Milli-Q water before
sample collection. A new straw broom was used for each sampling location. Duong
Quang, a rural village in My Hao district, Hung Yen province, Vietnam, was chosen as a
reference site (Fig. S1 and Table S1). Approximately 300 g of street dust was collected
from an area of 50 m in length and 0.5 m in width and kept in an aluminum foil pocket
washed with acetone and hexane and placed inside a zip-locked polyethylene bag. After
collection, the samples were preserved at À25  C until analysis.
2.2. Sample pre-treatment and extraction
Chemicals from one gram of each air-dried and 63 mm sieved street dust samples
were extracted with a mixture of distilled acetone/hexane and then distilled toluene
using a rapid solvent extractor (SE100, Mitsubishi Chemical Analytech) according to
a previously reported method (Tue et al., 2010). A 0.1 g-equivalent portion of the
crude extract was then concentrated, solvent-exchanged into 0.1 ml biochemicalgrade dimethyl sulfoxide and stored at 4  C for in vitro determination of AhRmediated activities using the DR-CALUX assay. The remaining extract was used for
chemical analysis of MePAHs and PAHs. Every set of seven samples was accompanied with a procedural blank.

2.3. Detection of the AhR-mediated activity
The AhR-mediated activities of all crude extract were determined individually
using the DR-CALUX assay (expressed in CALUX-TEQ). This assay utilize the rat
hepatoma cell line H4IIE (BioDetection Systems, The Netherlands) stably transfected
with the firefly luciferase gene containing a multimerized DRE (dioxin response
element) in front of a minimal promoter (Aarts et al., 1995; Garrison et al., 1996). All
assays were performed following BioDetection Systems's protocol described elsewhere (Suzuki et al., 2004, 2006). Briefly, approximately 80,000 cells/well were
seeded on 96-well plates. After 24 h of incubation at 37  C and 5% CO2, the cells were
treated with conditioned medium (0.8% DMSO) containing either the 2,3,7,8tetrachlorobenzo-p-dioxin (TCDD) as a standard reference in a series of concentrations (0e37.5 nM) or the samples (diluted by a factor of 1e1000). Each measurement
was done in triplicates. Plates were incubated for 24 h at 37  C, 5% CO2. After
exposure the cells were subjected to luminescence measurement. The AhR agonist
activities were derived from the diluted samples with similar response to 1e3 pM
TCDD (usually 300 to 1000 time dilution), and expressed in amounts of TCDD
equivalent (CALUX-TEQ) per gram dry weight (dw). The 3-(4,5-dimethylthiazol-2yl)-2,5-diphenyltetrazolium bromide assay was used to evaluate cell viability in
these diluted samples (Suzuki et al., 2013).
2.4. Chemical analysis
Each of the remaining extract was spiked with deuterated PAH surrogate standards and then cleaned-up using 1.2% deactivated alumina chromatography and
activated silica gel chromatography. The target compounds were eluted from
alumina chromatography column with 150 ml acetone/hexane (v/v: 30/70), and
concentrated to 1 ml. After, passing through the activated silica gel chromatography
column the target compounds were eluted with 80 ml of 95:5 hexane:dichloromethane, and then spiked with chrysen-d12 (Chy-d12) as internal standard. Finally,
the extracts were concentrated in 1 ml of iso-octane before being subjected to gas
chromatography-mass spectrometry analyses. All solvents were purchased from
Wako Pure Chemical Ind., Osaka, Japan and distilled before use. Compounds
analyzed in this study were parent PAHs including naphthalene (Nap), acenaphthylene (Acy), acenaphthene (Ace), fluorene (Flu), phenanthrene (Phe), anthracene
(Ant), fluoranthene (Fluh), pyrene (Pyr), benzo[c]phenanthrene (BcPh), cyclopenta
[c,d]pyrene (CPP), benz[a]anthracene (BaA), chrysene (Chy), benzo[b]-, benzo[k]-,
and benzo[j]fluoranthene (BbF, BkF and BjF), benzo[e]- and benzo[a]pyrene (BeP and
BaP), indeno[1,2,3-c,d]pyrene (IDP), dibenz[a,h]anthracene (DBA), benzo[g,h,i]perylene (BgP), dibenzo[a,h]-, dibenzo[a,i]-, dibenzo[a,l]pyrene (DBahP, DBaiP and
DBalP); MePAHs including 1- and 2-MePhe, 2- and 9-MeAnt, 1-, 2-, 3- and 6-MeChy,

1-MePyr, 1-, 2- 3-, 4-, 5-, 6-, 7-, 9- and 10-MeBaA, 10-MeBaP) 3-methylcholanthrene
(MCA), 3,6-Me2Phe, 9,10-Me2Ant, and 7,12-Me2BaA. For surrogate standards, Napd8, Acy-d8, Phe-d10, Ant-d10, Flush-d10, Pyr-d10, BaA-d12, BaP-d12 and BgP-d12 were
used. All surrogate and internal standards were purchased from SigmaeAldrich. The
target compounds were identified and quantified by a gas chromatography mass
spectrometry (GCeMS) following the method described previously (Tuyen et al.,
2014) with slight modification. Briefly, we used Agilent model 7890A coupled
with a mass spectrometer 5975C MSD and equipped a DB1 MS capitally GC column
(30 m  0.25 mm, 0.25 mm), for the determination of MePAHs and PAHs. Average


274

L.H. Tuyen et al. / Environmental Pollution 194 (2014) 272e280

Table 1
Concentrations (ranges and arithmetic means, ng/g dw) of MePAHs and PAHs in street dust.
PAHs

Duong Quang

Hanoi

New Delhi

Bangalore

Nap
Acy
Ace
Flu

Phe
Ant
Fluh
Pyr
BcPh
CPP
BaA
Chy
BbF þ BkF
BjF
BaP
BeP
IDP
DBA
BgP
DBahP
DBaiP
DBalP

2.8 (0.30e8.2)
3.5 (0.80e5.8)
0.60 (Nde1.4)
17 (2.9e28)
140 (43e240)
5.9 (1.8e12)
110 (48e190)
80 (40e140)
Nd
Nd
15 (6.5e31)

58 (25e92)
53 (18e81)
13 (5.7e20)
16 (4.7e30)
34 (12e63)
26 (9.3e39)
Nd
50 (25e78)
Nd
Nd
Nd

8.2 (0.20e32)
5.9 (0.30e19)
1.4 (Nde4.7)
18 (0.4e52)
210 (49e550)
32 (3.2e210)
320 (97e680)
350 (83e820)
Nd
Nd
75 (12e322)
220 (83e650)
180 (69e780)
53 (21e260)
66 (15e250)
100 (34e340)
89 (19e230)
0.60 (Nde9.6)

180 (42e400)
Nd
Nd
Nd

2.1 (0.80e5.1)
1.8 (0.50e3.9)
1.2 (0.40e2.4)
11 (5.5e21)
160 (87e290)
150 (84e280)
170 (120e290)
200 (120e300)
Nd
Nd
11 (Nde22)
73 (40e110)
83 (32e140)
25 (11e40)
62 (36e80)
27 (17e37)
33 (15e48)
Nd
82 (43e110)
Nd
Nd
Nd

13 (7.2e19)
5.6 (3.5e11)

1.2 (0.60e2.1)
14 (4.8e31)
130 (60e260)
150 (4.9e340)
170 (100e300)
260 (160e460)
Nd
Nd
26 (Nde62)
78 (58e98)
67 (48e97)
23 (13e43)
58 (38e77)
21 (13e40)
35 (17e51)
Nd
77 (48e100)
Nd
Nd
Nd

Total PAHs

620 (260e1000)

1900 (530e4700)

1100 (650e1700)

1100 (670e1800)

2-MePhe
1-MePhe
3,6-Me2Phe
2-MeAnt
9-MeAnt
9,10-Me2Ant
1-MePyr
1-MeBaA
2-MeBaA
7/9-MeBaA
4/6-MeBaA/2-MeChy
3/5-MeBaA/6-MeChy
1-MeChy
10-MeBaA
Me2BA
MCA
10-MeBaP

85 (22e150)
47 (15e80)
25 (9e46)
20 (0.80e91)
Nd
0.8 (Nde4.2)
12 (6e21)
Nd
27 (13e51)
2.8 (nde14)
Nd

1.3 (Nde6.3)
15 (Nde36)
Nd
1.5 (Nde7.6)
Nd
7.9 (1.7e22)

160 (30e360)
100 (18e210)
65 (Nde370)
22 (Nde240)
Nd
0.7 (Nde6.6)
47 (11e110)
0.30 (Nde4.2)
32 (Nde180)
210 (Nde480)
21 (Nde89)
12 (Nde30)
72 (23e150)
Nd
Nd
Nd
13 (Nde39)

64 (44e110)
54 (32e87)
15 (Nde24)
59 (36e95)
Nd

Nd
30 (17e55)
Nd
Nd
160 (72e260)
Nd
3.4 (Nde7.5)
3.7 (Nde7.6)
Nd
Nd
Nd
Nd

100 (73e170)
96 (57e220)
42 (Nde67)
160 (93e370)
Nd
Nd
59 (17e110)
Nd
Nd
230 (170e320)
4.8 (Nde34)
8.5 (Nde18)
7.9 (5.1e13)
Nd
Nd
Nd
19 (Nde37)

Total MePAHs

250 (75e460)

750 (170e1500)

390 (230e620)

740 (590e1200)

Theo-TEQ (MePAHs)
Theo-TEQ (PAHs)

0.012 (0.0020e0.045)
0.23 (0.086e0.38)

0.56 (0.0070e1.2)
0.86 (0.29e3.3)

0.41 (0.18e0.64)
0.38 (0.16e0.60)

0.59 (0.42e0.82)
0.34 (0.22e0.49)

Nd: not detected.
recovery rates of surrogate standards of PAHs were from 97% to 116% (Table S2).
Every set of seven samples was accompanied with a procedural blank for checking
interfering compounds in the GCeMS analysis.

2.5. Calculations of Theo-TEQs
The contributions by PAHs and MePAHs to AhR-mediated activities in the street
dust extracts can be evaluated by comparison of CALUX-TEQs measured with DRCALUX and theoretical TEQs (Theo-TEQs) of MePAHs and PAHs. Theo-TEQ of a
compound was calculated as shown in Equation (1). The DR-CALUX relative potency
(REP) of PAHs, MePAHs relative to TCDD is summarized in Table S3.
Theo- TEQs ðng TCDD=gÞ ¼ Concentrationðng=gÞ Â REP

(1)

2.6. Cancer risk assessment
The incremental lifetime cancer risk (ILCR) adopted from (US EPA, 1991) and
described in some publications (Chen and Liao, 2006; Wang et al., 2011; Peng et al.,
2011), was slightly modified by using adaptive parameters and used to quantitatively estimate the exposure risk for street dust PAHs. Eqs. (2)e(4) was applied to
evaluate cancer risk of human exposure to PAHs via ingestion, dermal contact and
inhalation, respectively.

ILCRsIngestion ¼


pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
CS  CSFIngestion  3 BW=70  IRIngestion  EF  ED
BW Â AT Â 106

(2)

ILCRsDermal ¼


pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
CS  CSFDermal  3 BW=70  SA  AF  ABS  EF  ED

ILCRsInhalation ¼

BW Â AT Â 106

pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
CS  CSFInhalation  3 BW=70  IRInhalation  EF  ED
BW Â AT Â PEF

(3)

(4)

where CS is the BaP-equivalent concentration of dust (mg kgÀ1), Carcinogenic potencies relative to BaP (Larsen and Larsen, 1998) was applied to calculate BaPequivalent concentrations (Table S2). CSFs are carcinogenic slope factors based on
the cancer-causing ability of BaP through ingestion (CSFIngestion), dermal contact
(CSFDermal) and inhalation (CSFInhalation), BW is body weight, EF is exposure frequency, ED is exposure duration, IRinhalatin is inhalation rate, IRingestion is dust
ingestion rate, SA is dermal exposure area, AF is dermal adherence factor, ABS is
dermal adsorption fraction, AT is averaging life span, PEF is particle emission factor.
The detail parameters and their values are summarized in Table S4. The risks for
children and adults were calculated separately. The total risks were the sum of risks
associated with each exposure route.
2.7. Statistical analysis
The R software package version 2.15.2 was used to perform statistical analyses.
Pearson's correlation coefficient analysis (log-transformed concentration of target
compounds, at 95 percent confidence interval) was applied to examine the relationship between MePAHs and their corresponding unsubstituted compounds in
street dust samples. In order to examine the significance of the difference in AhRmediated activity and chemical concentration levels between sampling sites we


L.H. Tuyen et al. / Environmental Pollution 194 (2014) 272e280

275

Fig. 1. Plot of IDP/(IDP þ BgP) and BaP/BgP in street dust from different regions.

used the Wilcoxon rank sum test. A p value of <0.05 is considered as indicating
statistically significant.

3. Results and discussion
3.1. AhR-mediated activity
Higher AhR-mediated activities in street dust were found for
metropolitan and urban areas of Hanoi (20e68, mean 40 ng/g dw),
New Delhi (11e29, mean 20 ng/g dw) and Bangalore (19e47, mean
29 ng/g dw) than for the rural site, Duong Quang (8e35, mean
18 ng/g dw) (Fig. S2). The CALUX-TEQs in urban street dust from
Vietnam and India were comparable to those reported for urban
dust from the United States (median: 43 ng CALUX-TEQ/g dw)
(Andrysík et al., 2011), suggesting the presence of large amount AhR
agonists such as PAHs as well as their derivatives in Vietnam and
India's street dust (Fig. S2). The CALUX-TEQs in the 63 mm fraction
of the dust samples from Hanoi and Duong Quang analyzed in this
study were from 2 to 3 times higher than the levels in the coarser
fraction ( 500 mm) reported in our previous study (Fig. S2) (Tuyen
et al., 2014), suggesting that smaller particles contained larger
amount of AhR agonists.
3.2. Concentrations, profiles and potential sources of PAHs
Higher concentrations of S23PAHs were found in street dust
from Hanoi (530e4700, mean 1900 ng/g dw), Bangalore
(670e1800, mean 1100 ng/g dw), and New Delhi (650e1700, mean
1100 ng/g dw) than in street dust from Duong Quang (260e1000,
mean 620 ng/g dw) (Table 1, Fig. S2). BbF, BkF, IDP, Chy, BaA, BjF, the

most potent AhR agonists among PAHs in vitro (Machala et al.,
2001), were found at one to five fold higher concentrations in the
urban sites (Hanoi, Bangalore and New Delhi) than in the rural site
(Duong Quang). Concentrations of PAHs recommended for carcinogenic screening by the European Union and the US Environmental Protection Agency (EU- and EPA-PAHs) in Hanoi street dust
were among the highest levels and were 2 times higher than those
in dust from New Delhi, Bangalore and 3 times higher than Duong
Quang (Table 1), whereas, BaP concentrations in Hanoi street dust

were 4 times higher than those in dust from Duong Quang, and
comparable to New Delhi and slightly higher than the value from
Bangalore only. The compounds having the same molar mass are
assumed to have similar physicochemical properties. PAHs diagnostic ratios are commonly used as tools for identification of
 et al.,
pollution emission sources (Katsoyiannis et al., 2011; Dvorska
2011). The sources were also reported in many previous studies
(Table S5). The results obtained from calculation of the IDP/
(IDP þ BgP) and BaP/BgP ratios were plotted in Fig. 1, indicating that
vehicular traffic was the major contributor of PAHs in all sampling
sites (Yunker et al., 2002; Fang et al., 2004; LI et al., 2006; Kume
et al., 2007; Ravindra et al., 2008; Peng et al., 2011). The diagnostic ratios of Flu/(Flu þ Pyr) > 0.5 indicate that the major source
of PAHs was gasoline and <0.5 indicate a major source from diesel
(Ravindra et al., 2008). We observed this ratio ranged from 0.03 to
0.07 (mean 0.05) for New Delhi and Bangalore, from 0.01 to 0.09
(mean 0.05) for Hanoi and 0.02 to 0.22 (mean 0.13) for Duong
Quang, suggesting that major source was by the combustion of
gasoline rather than diesel. In addition, the ratios of Fluh/
(Fluh þ Pyr) ranged from 0.52 to 0.59 (mean 0.56, Duong Quang),
0.31 to 0.54 (mean 0.46, Hanoi), 0.40 to 0.50 (mean 0.47, New
Delhi), 0.31 to 0.49 (mean 0.39, Bangalore) and the ratios of IDP/
(IDP þ BgP) ranged from 0.27 to 0.42 (mean 0.35, Duong Quang),

0.24 to 0.37 (mean 0.30, Hanoi), 0.25 to 0.36 (mean 0.29, New
Delhi), 0.25 to 0.34 (mean 0.31, Bangalore), which indicated that
pyrogenic pathways was main emission sources in Duong Quang,
Hanoi, and New Delhi whereas emission sources in Bangalore could
be pyrogenic and petrogenic (Katsoyiannis et al., 2011). The strong
positive correlation between the concentrations of BgP and total
PAHs for Hanoi (Pearson's r ¼ 0.96, p < 0.05), Duong Quang
(Pearson's r ¼ 0.91, p < 0.05), New Delhi (Pearson's r ¼ 0.75,
p < 0.05) and Bangalore (Pearson's r ¼ 0.60, p > 0.05) found in street
dust for all study locations also indicated that vehicles emission is
the major source of PAHs in these areas (Fig. S3) (Baek et al., 1991).
However, although diagnostic ratios are useful tools for identification of PAHs emission sources in environment samples including
dust particles or airborne. But still, there are limitations due to PAHs
distribution are depend on the size of particles, organic carbon
contents or transportation and degradation of different particles


276

L.H. Tuyen et al. / Environmental Pollution 194 (2014) 272e280

Fig. 2. Profiles of PAHs in street dust from different regions (The error bars are the variation of chemical proportions in different samples).

Fig. 3. Profiles of MePAHs in street dust from different regions (The error bars represent the ranges).

phase (Tobiszewski and Namiesnik, 2012). PAHs profiles showed
that Pyr, Fluh, Phe, BbF þ BkF, Chy, BgP, BaP, IDP, BeP, BjF and BaA
were predominant in all sampling sites, whereas Ant dominated in
Indian street dust but not in Vietnam street dust (Fig. 2).
3.3. Concentration and profiles of MePAHs

Total and individual MePAH concentrations are shown in
Table 1. Total MePAH concentrations in Hanoi and Bangalore were
similar (mean 750 and 740 ng/g dw, respectively) and 2 and 3 times
fold higher than those in New Delhi and Duong Quang (mean 390
and 250 ng/g dw, respectively). Methyl phenanthrenes, potent AhR
^cek
agonists in reporter gene assay (Barron et al., 2004; Vondra
et al., 2007), were predominant in all sampling sites (Table 1,
Fig. S2). MeBaAs, which had been reported as potent in vitro AhR
 et al., 2008), were found in the urban sites
agonist (Marvanova
(Hanoi, Bangalore, New Delhi) at significantly higher levels than in
the rural site (Table 1). 1-MeChy, a significant contributor which
was found to possess EROD-inducing potency in rainbow trout liver
cell line (RTL-W1) (Brack and Schirmer, 2003), was at significant

level in Hanoi (Table 1). Congener profiles of MePAHs indicated that
MeBaAs were predominant in all urban sites, whereas MePhes
were the most abundant in the rural site (Fig. 3). By examining the
ratios between MePAHs and their corresponding unsubstituted
compounds, we found that MeBaAs were more abundant than BaA
except in Duong Quang (Fig. S4), MePhes more abundant than Phe
in Hanoi and, MeAnts more abundant than Ant in Bangalore only
(Table 1, Fig. S4).
3.4. Correlations between MePAHs and corresponding
unsubstituted PAH (PPAHs) and their potential sources
We found strong correlations between the concentrations of
MePAHs and PPAHs in street dust from all study locations (Pearson's r ¼ 0.86e0.99, p < 0.05), suggesting that MePAHs and their
corresponding unsubstituted PAHs were from the same emission
sources (Fig. S5). Ratios of MePhe and Phe can be used to identify

the emission sources of PAHs: it can be assumed that PAHs could be
released into the environment from fossil fuels combustion if
MePhe/Phe >1 and the source could be petrogenic emission if


L.H. Tuyen et al. / Environmental Pollution 194 (2014) 272e280

277

Fig. 4. Plots of MePAHs/PAHs ratios in street dust.

MePhe/Phe >1.5 (Boonyatumanond et al., 2006). The average of
MePhe/Phe was <1 for New Delhi and Duong Quang, indicating that
MePAHs were from pyrogenic sources in these places. This ratio
was slightly higher than 1 in Hanoi, indicating that the sources of
MePAHs in this site were mostly pyrogenic (Fig. 4A). These results
are consistent with PAH diagnostic ratios of IDP/(IDP þ BgP). But,
the results from Bangalore indicated that the sources of MePAHs
could be mostly petrogenic. Ratio between sums of MeChy/Chy was
also useful for the identification of emission sources, and PAHs
were also identified as pyrogenic if the ratio of MeChy/Chy below 1
(Saha et al., 2009): The values of MeChy/Chy in Fig. 4B indicates that
the emission in Hanoi and Duong Quang could be related to pyrogenic, but in New Delhi and Bangalore this could be related to
petrogenic. On the other hand, MePyr/Pyr (Fig. 4C) values were to
be < 0.5 in all sampling sites, suggesting that pyrogenic activities
were the main emission sources (Saha et al., 2009). Moreover,
MePAHs/PAHs shown in Fig. 4D was at <0.8 in almost all sampling
point of Hanoi, Duong Quang, and New Delhi again confirming that
pyrogenic was mainly emission sources in these site whereas
emission sources in Bangalore could be mostly petrogenic (Saha

et al., 2009).

Hanoi, 3% for Bangalore and 2% for Duong Quang. Besides, much
larger proportions of unexplained activities (95%e98%) than TheoTEQs of total MePAHs/PAHs in the CALUX-TEQs indicate the existence of unknown AhR agonists. Our previous study documented
that contribution of dioxin-related compounds to AhR-mediated
activity in road dust from Hanoi was very small (~0.1%) (Tuyen
et al., 2014). In addition, we found no significant correlations between CALUX-TEQs and total PAHs/MePAHs (p > 0.05). Therefore,
potential compounds contributing as unknown AhR-agonists in the
road dust may be other PAHs-related compounds (e.g., heterocyclic
PAHs, halogenated-, oxygenated-PAHs) (Larsson et al., 2014).
Among MePAHs and PAHs determined in this study, MeBaAs
was the major contributor to Theo-TEQs, which had ranged from 3
to 64%, for all sampling sites, followed by BbF þ BkF (ranged from
21% to 62% in the urban areas) or IDP (ranged from 9 to 25% for all
sampling sites) (Fig. 5). The contribution of MeBaAs to AhRmediated activity was even higher than those of their corresponding unsubstituted compounds (Fig. S6). These results suggest
importance of MeBaAs as well as PPAHs in the evaluation of toxic
risk related to AhR-mediated activity in the Asian metropolitan and
urban areas.

3.5. Contribution by MePAHs and PAHs to the AhR-mediated
toxicity

3.6. Cancer risk assessment

The contributions by PAHs and MePAHs to AhR-mediated activities in the street dust extracts were evaluated by comparison of
CALUX-TEQs measured with DR-CALUX and theoretical TEQs
(Theo-TEQs) of MePAHs and PAHs. Theo-TEQ of a compound was
calculated by multiplying the concentration of the target compound with its TCDD-relative potency in CALUX assays (Table S3).
Higher Theo-TEQs (among PAHs) were observed in Hanoi (mean
0.86 ng/g dw), New Delhi (0.38 ng/g dw), Bangalore (0.34 ng/g dw)

than Duong Quang (mean 0.25 ng/g dw). Significantly higher TheoTEQs of MePAHs were also observed in urban sites (Hanoi: mean
0.56 ng/g dw; New Delhi: mean 0.41 ng/g dw; Bangalore: mean
0.59 ng/g dw) than the rural site (Duong Quang: mean 0.01 ng/g
dw). The contribution of MePAHs and PAHs accounted in average of
5% of AhR-mediated activity in street dust from New Delhi, 4% for

Probabilistic risk assessment for personal exposure to carcinogenic PAHs showed that an ILCR between 10À6 and 10À4 indicates
potential risk, whereas ILCR greater than 10À4 indicates high potential health risk (US EPA, 2005). The acceptable level is equal to or
lower than 10À6 (US EPA, 2005). Our estimated results suggest that
children and adults in both study sites in Vietnam and India are
exposed to high potential carcinogenic risk via both dust ingestion
and dermal contact pathways (detail in Table 2). In which, highest
levels of cancer risk for both children and adults were observed in
Hanoi (Table 2). Particularly, cancer risk levels via ingestion for
children and adults from urban site (Hanoi, New Delhi, and Bangalore) were significantly higher than those in rural site (Duong
Quang). The cancer risk levels via dermal contact for children and
adults from urban site in Vietnam and India were slightly higher
than those of children and adults from rural site. ILCRs of inhalation


278

L.H. Tuyen et al. / Environmental Pollution 194 (2014) 272e280

Fig. 5. Contribution of individual MePAHs and PAHs to total Theo-TEQs (DQ: Duong Quang, HN: Hanoi, ND: New Delhi, BL: Bangalore).

Table 2
Estimated values of incremental life time cancer risk.
Pathways/Sampling sites

Ingestion
Children

Duong Quang

Hanoi

New Delhi

Bangalore

Median
Min
Max
95% Percentile
5% Percentile
Median
Min
Max
95% Percentile
5% Percentile
Median
Min
Max
95% Percentile
5% Percentile
Median
Min
Max
95% Percentile

5% Percentile

3.7
1.4
7.0
6.7
3.7
1.2
4.3
5.3
3.3
1.2
1.1
5.8
1.4
1.4
1.1
8.7
6.8
1.3
1.3
8.7

Â
Â
Â
Â
Â
Â
Â

Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â

À5

10
10À5
10À5
10À5
10À5
10À4
10À5
10À4
10À4
10À4
10À4
10À5
10À4
10À4

10À4
10À5
10À5
10À4
10À4
10À5

Dermal
Adults
4.1
1.5
7.7
7.4
4.1
1.3
4.7
5.8
3.6
1.3
1.2
6.4
1.5
1.5
1.2
9.6
7.5
1.5
1.4
9.5

Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â

Inhalation

Children
À5

10
10À5
10À5
10À5

10À5
10À4
10À5
10À4
10À4
10À4
10À4
10À5
10À4
10À4
10À4
10À5
10À5
10À4
10À4
10À5

pathway were almost negligible when compared to ingestion and
dermal contact pathways (Table 2). The results of cancer risk
assessment found in Hanoi also indicated higher potential cancer
risk due to exposure to smaller dust particles than the lager particles, as reported in our previous study (Tuyen et al., 2014). The
abundance of methylated derivatives of some carcinogenic PAHs,
such as MeBaAs contribute at least with 50% of the total Theo-TEQs,
suggests that carcinogenic potency of MePAHs should also be
considered. But so far, a carcinogenic potency factor of MePAHs has
not been studied. Therefore, the cancer risk model for MePAHs
should be studied and established in future.
4. Conclusions
This is the first report on toxic contribution of MePAHs to AhRmediated activities in street dust from Asian metropolitan and urban areas of developing countries, Vietnam and India. Profiles of
MePAHs/PAHs determined by chemical analysis indicated that pyrogenic combustion is the major sources of MePAHs in Hanoi,

9.3
3.5
1.7
1.7
9.3
3.0
1.1
1.3
8.2
3.0
2.6
1.4
3.4
3.4
2.6
2.4
1.7
3.3
3.2
2.2

Â
Â
Â
Â
Â
Â
Â
Â

Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â

À5

10
10À5
10À4
10À4
10À5
10À4
10À4
10À3
10À4
10À4
10À4
10À4
10À4
10À4
10À4

10À4
10À4
10À4
10À4
10À4

Adults
1.5
5.5
2.7
2.6
1.5
4.7
1.7
2.1
1.3
4.7
4.1
2.3
5.4
5.3
4.1
3.4
2.7
5.2
5.1
3.4

Â
Â

Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â

Children
À4

10
10À5
10À4
10À4
10À4
10À4
10À4
10À3

10À3
10À4
10À4
10À4
10À4
10À4
10À4
10À4
10À4
10À4
10À4
10À4

Adults
À9

1.5 Â 10
5.5 Â 10À10
2.8 Â 10À9
2.6 Â 10À9
1.5 Â 10À9
4.8 Â 10À9
1.7 Â 10À9
2.1 Â 10À8
1.3 Â 10À8
4.8 Â 10À9
4.1 Â 10À9
2.3 Â 10À9
5.4 Â 10À9
5.4 Â 10À9

4.1 Â 10À9
3.4 Â 10À9
2.7 Â 10À9
5.2 Â 10À9
5.1 Â 10À9
3.4 Â 10À9

6.4
2.4
1.2
1.2
6.4
2.1
7.4
9.2
5.7
2.1
1.8
1.0
2.4
2.4
1.8
1.5
1.2
2.3
2.2
1.5

Â
Â

Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â
Â

10À9
10À9
10À8
10À8
10À9
10À8
10À9
10À8
10À8
10À8
10À8

10À8
10À8
10À8
10À8
10À8
10À8
10À8
10À8
10À8

Vietnam, but in Indian urban areas they were mixed of pyrogenic
and petrogenic origin. Total concentrations of MePAHs in Bangalore
were slightly higher than their corresponding unsubstituted compounds. In contrast, PAH concentrations found in Duong Quang,
Hanoi and New Delhi street dust were higher than their methyl
derivatives. The comparison between Theo-TEQs of MePAHs/PAHs
and CALUX-TEQs indicates occurrence of unknown AhR agonists in
the street dust. Further studies are necessary to identify potential
compounds and to evaluate other PAHs-related compounds such as
heterocyclic PAHs, halogenated-, oxygenated-PAHs for understanding their potencies on AhR-mediated activity. The present
study showed that MeBaAs, some of the most abundant methyl
PAHs, has higher contribution to AhR-mediated activities than
corresponding unsubstituted PAHs. The fact that higher concentrations of MePAHs and PAHs are bound to street dust with smaller
diameter size, resulting in the higher AhR-mediated activities was
observed, suggest that contaminant monitoring as well as toxic
effect evaluation of ambient air particles in these areas are need be
done elaborately in the further studies.


L.H. Tuyen et al. / Environmental Pollution 194 (2014) 272e280

Acknowledgments
This study was partly supported by Grants-in-Aid for Scientific
Research (A: 25257403) from Japan Society for the Promotion of
Science (JSPS) and the Environment Research and Technology
Development Fund (K123001 and 3K133010) from the Ministry of
the Environment, Japan. The award of a JSPS postdoctoral fellowship to N. M. Tue (P 13072) is also acknowledged.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.envpol.2014.07.029.
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