Marine Pollution Bulletin 51 (2005) 677–687
www.elsevier.com/locate/marpolbul
Organochlorines and dioxin-like compounds in green-lipped mussels
Perna viridis from Hong Kong mariculture zones
M.K. So a, X. Zhang b, J.P. Giesy a,b, C.N. Fung a, H.W. Fong a, J. Zheng a,
M.J. Kramer b, H. Yoo b, P.K.S. Lam a,*
a
Centre for Coastal Pollution and Conservation, Department of Biology and Chemistry, City University of Hong Kong, 83 Tat Chee Avenue,
Kowloon, Hong Kong SAR, PeopleÕs Republic of China
b
Department of Zoology, National Food Safety and Toxicology Center, Center for Integrative Toxicology, Michigan State University,
East Lansing, MI 48824, USA
Abstract
Concentrations of persistent organic pollutants including polychlorinated biphenyls (PCBs), organochlorine (OC) pesticides and
dioxin-like compounds were measured in green-lipped mussels, Perna viridis, collected from seven mariculture zones in Hong Kong
between September and October in 2002 in order to evaluate the status, spatial distribution and potential sources of pollution in
these areas. Concentrations ranged from 300 to 4400 ng/g lipid weight for total OCs and 170–1000 ng/g lipid weight for total PCBs
(based on 28 congeners). Relatively smaller DDT concentrations in mussels compared with previous studies suggest reduced discharges of DDTs from nearby regions into Hong Kong waters. Detection of a mixture of HCH isomers in the mussels indicated
that Hong Kong waters were predominantly contaminated by technical HCHs rather than lindane. Mussel samples from all sampling locations elicited significant dioxin-like activity in the H4IIE-luc bioassay. The greatest magnitude of dioxin-like response
(39 pg TEQ/g wet wt.) was detected in mussels from Ma Wan in the western waters of Hong Kong, which is strongly influenced
by the Pearl River discharge. Human health risk assessment was undertaken to evaluate potential risks associated with the consumption of the green-lipped mussels. Risk quotient (RQ) for dioxin-like compounds was greater than unity suggesting that adverse
health effects may be associated with high mussel consumption.
Ó 2005 Elsevier Ltd. All rights reserved.
Keywords: Green-lipped mussel; Mariculture zone; Hong Kong; OC pesticides; PCBs; Dioxin-like compounds; H4IIE-luc cell bioassay; Human
health risk assessment
1. Introduction
Persistent organic pollutants (POPs) of particular
concern include organochlorine (OC) pesticides which
had been extensively used in agricultural practices in
the past; polychlorinated biphenyls (PCBs) which were
mainly used for insulation in electrical equipment; polycyclic aromatic hydrocarbons (PAHs) which were emit-
*
Corresponding author. Tel.: +852 2788 7681; fax: +852 2788 7406.
E-mail address: bhpksl@cityu.edu.hk (P.K.S. Lam).
0025-326X/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2005.06.004
ted through processes such as incomplete combustion of
fossil fuel and from petrochemical industrial activities; as
well as dioxin-like compounds (Fu et al., 2003). Dioxinlike compounds, also known as planar halogenated
hydrocarbons (PHHs), include certain co-planar PCBs,
polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and are unintentionally
released through combustion processes, burning of fuel,
production and use of chlorohydrocarbons, and chlorine bleaching in the pulp and paper industry (Fiedler,
1996). Among the POPs, dioxin-like compounds are
considered to be the most toxic man-made chemicals
678
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
(Lai et al., 2004) and the toxic effects arise as a consequence of their abilities to bind to aryl hydrocarbon
receptor (AhR) (Schoeters et al., 2004). Toxicities associated with PHH exposure include hepatoxicity, body
weight loss, thymic atrophy, impairment of immune
responses, dermal lesions and reproductive toxicity
(Giesy et al., 1994; Safe, 1994). While a number of studies in Hong Kong have demonstrated the contamination
with OCs, PCBs, PAHs in bottom sediments (Connell
et al., 1998b; Hong et al., 1995), green-lipped mussels
(Perna viridis) (Phillips, 1985) and fish purchased from
local markets (Chan et al., 1999), information on the
concentrations of dioxin-like compounds in the Hong
Kong coastal environment is limited.
Hong Kong, situated on the southern coast of China,
has experienced severe pollution stress through various
anthropogenic sources. Pearl River discharge is considered to be one of the major pollution sources to the
Hong Kong marine environment, particularly to the
western regions (Broom and Ng, 1995; Wu, 1988). This
influence is relatively greater in the wet summer season
when the Pearl River runoff constitutes about 80% of
the annual total discharge (Xue and Chai, 2001). Other
factors, such as population expansion and rapid urbanization, have resulted in increasing pollution loads being
introduced into Victoria and Tolo Harbours (Blackmore, 1998). Historically, discharges of largely untreated domestic and industrial wastewater and the
disposal of contaminated mud into Hong KongÕs coastal
waters have resulted in high levels of POPs in the water
column, sediment and biota (Connell et al., 1998a,b;
Wu, 1988).
Human breast milk samples from Hong Kong had
been found to contain relatively great concentrations
of DDTs, HCHs (Ip, 1983) and dioxin-like compounds
(Lai et al., 2004). Consumption of contaminated foodstuff, especially marine fish and shellfish, is considered
to be a major pathway for human exposure to POPs
(Lai et al., 2004; Liem et al., 2000). Indeed, over 90%
of human exposure to dioxin-like compounds is thought
to be via ingestion of contaminated food (Winters et al.,
1995). People in Hong Kong are estimated to consume
marine fish or shellfish at least three times a week (Chan
et al., 1999). Therefore, mariculture is an important
industry in Hong Kong, despite the increasing supply
of high quality live fish and shellfish from overseas.
The 28 designated mariculture zones in Hong Kong
are mostly located in the northeast New Territories
(Chan et al., 1999; Lam, 1990). Being located in close
proximity to urban areas, these mariculture zones may
conceivably be impacted by various pollution sources,
and consequently fish or shellfish from these areas could
pose potential public health problems (Chan et al.,
1999).
Green-lipped mussels, P. viridis, are commercially
valuable seafood, and are widely distributed in the
Asian coastal waters. They have been recognized as a
suitable bioindicator for monitoring toxic contaminants
in coastal waters (Monirith et al., 2003). Concentrations
of environmental contaminants in mussels could be used
to assess potential risks to seafood consumers (Fung
et al., 2004).
Most of the previous studies on pollution monitoring
in Hong Kong have been concentrated around Victoria
(Tanner et al., 2000; Yung et al., 1998) and Tolo Harbours (Owen and Sandhu, 1999; Wong et al., 2000),
and relatively limited information is available on the
concentrations of contaminants, particularly POPs, in
mussels from local mariculture farms. In this present
study, green-lipped mussels, P. virids, were collected
from seven mariculture zones in Hong Kong, and analyzed for OC pesticides and PCBs. The concentrations
of dioxin-like compounds were also determined using
H4IIE-luciferiase (H4IIE-luc) bioassay. Human health
risk assessment was also undertaken to evaluate the
risks associated with the consumption of mussels collected from Hong Kong mariculture zones.
2. Materials and methods
2.1. Sampling
Green-lipped mussels, P. virids, were collected from
seven mariculture zones: Kat O (KO), O Pui Tong
(OPT), Tap Mun (TM), Yim Tin Tsai (YTT), Kau Sai
(KS), Lo Tik Wan (LTW) and Ma Wan (MW), during
September and October 2002 in Hong Kong (Fig. 1).
Immediately after collection, samples were stored in
polyethylene bags, kept in ice, and transported to the
laboratory. Upon return to the laboratory, the samples
were stored at 20 °C until analyzed.
2.2. Sample preparation
The procedures for chemical treatment were similar
to those described by Fung et al. (2004), but with some
modifications. The frozen mussel samples were thawed,
and the whole soft tissues of about 30 mussels, sizes
ranging between 80 mm to 120 mm, from each location
were pooled and homogenized in a blender. Approximately 10 g of homogenized tissue was transferred into
a 50 ml centrifuge tube, freeze–dried for 7 d and the
dried tissues were ground into powder. Approximately
1 g of the dried tissue powder was accurately weighed
into a new 50 ml centrifuge tube. Duplicate samples
were prepared for each location. The dried mussel powder was extracted in a 50 ml centrifuge tube, containing
an internal standard [Decachlorobiphenyl (DCB)], 35 ml
methylene chloride, and 1 g of anhydrous sodium sulphate (preheated at 450 °C for 5 h). The combined mixture was then shaken by a horizontal shaker at a rate of
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
679
Fig. 1. Map showing sampling locations of mussels in seven mariculture zones in Hong Kong (KO: Kat O, OPT: O Pui Tong, TM: Tap Mun, YTT:
Yim Tin Tsai, KS: Kau Sai, LTW: Lo Tik Wan, MW: Ma Wan).
20 oscillations per min. The tubes were then centrifuged
at 2000 rpm for 10 min and the supernatant was decanted into a 250 ml round bottom flask. The above
extraction and centrifugation processes were repeated
two more times with all the three supernatants combined
and filtered through a glass fibre filter. The mixture was
then concentrated to approximately 5 ml using a rotary
evaporator under reduced pressure. The solvent was
exchanged by adding 30 ml hexane and the combined
volume was further reduced to about 1 ml. The lipid
content was determined from an aliquot of the extract
by reducing to dryness using nitrogen blowdown (Yu
et al., 2002). The extract was then redissolved in hexane,
and loaded onto a silica gel column for separation.
A fractionation column of internal diameter of 1 cm
was prepared by adding 13 cm in length of activated silica gel with 6 nm average pore size (preheated at 450 °C
for 5 h), followed by 3 cm in length of anhydrous sodium sulphate. The column was then washed sequentially with 15 ml acetone, 15 ml methylene chloride
and 30 ml hexane. The mussel extract was then loaded
onto the silica gel column. The extract was allowed to
pass through into the sodium sulphate. Until the aliquot
reached the surface of sodium sulphate, 15 ml hexane
was added to the column, and the eluate was discarded.
Another 15 ml of 20% methylene chloride in hexane was
loaded onto the column and the eluate was collected for
OC pesticide and PCB determination. The volume of
eluate was reduced to approximately 0.3 ml by rotary
evaporation under reduced pressure. The aliquot extract
was transferred to a 0.3 ml insert in a 1.5 ml vial and
injected into a gas chromatograph for analysis.
2.3. Organochlorine identification and quantification
PCBs, HCHs, HCB, heptachlor, heptachlor epoxide,
aldrin, dieldrin, endrin, kepone, chlordanes, and DDT
and its metabolites were measured. Concentrations of
individual compounds were calculated from the peak
area of the sample to a corresponding external standard.
The PCB standard (SRM 2262) used for quantification
was a mixture with known composition and content,
containing 28 congeners (PCB 1, 8, 18, 28, 29, 44, 50,
52, 66, 77, 87, 101, 104, 105, 118, 126, 128, 138, 153,
154, 170, 180, 187, 188, 194, 195, 200, 206). OCs were
quantified by a Hewlett Packard 6890 series gas chromatograph equipped with a microelectron capture
detector (GC-lECD) employing 30 m HP-5MS capillary column (0.2 mm internal diameter and 0.25 lm
thickness film of 95% dimethyl-5%polysiloxane) and
equipped with an autoinjector (Hewlett Packard 7683
series). The column head pressure was kept at 12 psi.
The oven temperature was programmed from 90 °C at
the beginning, held for 2 min, then increased to 180 °C
at a rate of 20 °C per min, held for 1 min, and finally
raised to 270 °C at a rate of 3 °C per min and held for
20 min. Injector and detector temperatures were set at
230 °C and 300 °C, respectively. Detection limits were
0.05 ng/g dry weight for individual OC pesticide and
0.1 ng/g dry weight for individual PCB. Recoveries of
OC pesticides and PCBs were in the range of 81–108%
and 93–100%, respectively. Concentrations of OC pesticides and PCBs were not corrected for recoveries and
are presented on both ng/g dry weight and lipid weight
basis.
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M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
2.4. H4IIE-luc cell bioassay
The cells employed in the present study were rat hepatoma cells that were stably transfected with a luciferase
reporter gene (Sanderson et al., 1996). The procedures
for the in vitro bioassay were similar to those described
elsewhere (Khim et al., 2000, 2001). In brief, the cells
were trypsinized from culture dishes containing more
than 80% confluent monolayers and were then seeded
into the 96-well culture plates at 250 ll per well. Cells
were incubated overnight before dosing. Test wells were
dosed with 2.5 ll of the mussel extract. The control wells
were dosed with 2.5 ll of solvent, while the blank wells
received no dose. A standard curve was constructed by
adding different concentrations of 2,3,7,8-tetrachlorodibenzo-p-dioxin (2,3,7,8-TCDD) to the standard
wells. Three control wells and blank wells were tested
on each plate. Luciferase assays were conducted after
72 h of exposure. Culture medium was then removed
from the plate. After adding LucLite reagent, the plates
were read with a microplate-scanning Dynatech ML
3000 luminometer (Dynatech Laboratories, Chantilly,
VA, USA). Responses to AhR agonists were quantified
by measuring the relative luminescence units (RLU) and
were converted to percentages of the mean maximum
response observed for the TCDD standard curve
(%-TCDD-max). The dioxin-like potency of each
extract was expressed as relative potency (REP) to
2,3,7,8-TCDD based on EC1 values from the TCDD
standard curve and the sample dose response curve
(Villeneuve et al., 2000).
2.5. Human health risk assessment
The risk of specific contaminants to human health
associated with consumption of mussels is performed
by calculating the risk quotient (RQ), which is a comparison of the exposure concentration to the oral reference dose (RfD). The exposure level for a particular
contaminant is calculated by use of
Average daily exposureðng=kg body weight=dÞ
¼ Consumptionðg=kg body weight=dayÞ
Maximum measured contaminant
concentrationðng=g dry wt:Þ:
ð1Þ
Due to the lack of shellfish consumption data for
Hong Kong people, fish consumption data for high consumption groups in China, 119 g/person/d (Fung et al.,
2004), was adopted. This, together with the maximum
measured contaminant concentration, were used to calculate a ‘‘worst-case’’ RQ. Assuming the average body
weight of an adult is 60 kg, the average consumption
rate becomes 1.98 g/kg bw/d. The RfD values employed
in the present study were the criteria from the US Environmental Protection Agency (USEPA), which is an
estimate of a daily exposure to the human population
that is unlikely to pose significant lifetime health risks.
In this study, risk assessment was only conducted on
PCBs, DDTs, chlordanes, dieldrin and dioxin-like compounds, for which RfDs are available from USEPA.
Using a conservative (worst-case) approach, RQ was
calculated
RQ ¼
Average Daily Exposure
RfD
ð2Þ
RQ less than unity indicates that the chemical involved
is less likely to pose a significant health risk to the consumers. However, RQ greater than unity would indicate
that exposure concentration exceeds RfD and a more refined risk assessment is needed to ascertain whether
appropriate control or management measures are
required.
3. Results and discussion
3.1. Spatial distribution of OC pesticides and PCBs
Concentrations of OC pesticides, on dry and lipid
weight basis, in the mussel samples collected from individual mariculture zones are presented (Table 1). Concentrations of OCs in mussels varied among locations
of mariculture zones. Concentrations of total OCs ranged from 300 to 4400 ng/g lipid wt. Concentrations of
total DDTs, HCHs and chlordanes ranged from 11 to
1400, 18 to 1200 and 59 to 1000 ng/g lipid wt., respectively (Table 1).
Mussels from MW contained the greatest concentrations of total OCs (4100 and 4400 ng/g lipid wt.), followed by YTT (3200 and 4100 ng/g lipid wt.). MW,
with its close proximity to Tsuen Wan and Kwai Chung,
may be subjected to local pollutant discharges from
nearby manufacturing and industrial areas. The degree
of contamination in this area may be further intensified
by the large spate of freshwater discharge from the Pearl
River Estuary, which is known to contain high concentrations of various contaminants. The relatively great
concentrations of contaminants in mussels from YTT
could be attributed to its location within Tolo Harbour.
Tolo Harbour, situated at the northeastern part of Hong
Kong, is a semi-estuarine embayment which is connected to the outer Mirs Bay by a long narrow Tolo
Channel (Wu, 1988). As a consequence of continual
coastal reclamation, tidal flushing within the embayment has been greatly reduced, resulting in long water
residence time and poor oceanic exchange (Blackmore,
1998). The pollution problem in the area is further exacerbated by increased population and industries within
Tolo Harbour (Owen and Sandhu, 1999). The smallest
concentration of total OCs was recorded in mussels
from KO (310 and 460 ng/g lipid wt.). This sampling site
Table 1
Concentrations (ng/g dry wt. and lipid wt.) of organochlorines in mussel samples collected from mariculture zones in Hong Kong
Replicate
Site
KO
1
OPT
2
1
TM
2
1
YTT
2
1
5.5
1.6
1.3
<0.05
<0.05
<0.05
12
<0.05
2.0
1.9
3.9
1.0
<0.05
<0.05
1.1
7.2
3.7
1.5
<0.05
<0.05
<0.05
0.53
<0.05
4.0
2.9
6.9
1.7
<0.05
<0.05
1.7
7.6
4.2
2.5
4.2
<0.05
2.2
3.5
1.9
0.82
6.1
6.9
0.76
<0.05
<0.05
0.81
19
11
1.2
<0.05
<0.05
0.15
<0.05
<0.05
0.91
3.2
4.1
0.72
<0.05
0.52
1.3
19
8.2
4.4
2.2
<0.05
<0.05
12
<0.05
4.1
3.4
7.5
5.0
<0.05
<0.05
5.0
21
12
6.5
<0.05
<0.05
<0.05
20
<0.05
5.4
5.1
10
6.6
<0.05
<0.05
6.6
Total OCsa
26
22
34
36
58
78
Lipid weight basis
HCHs
HCB
Heptachlor
Heptachlor epoxide
Aldrin
Dieldrin
Endrin
Kepone
a-chlordane
c-chlordane
Chlordanes
p,p 0 -DDE
p,p 0 -DDD&o,p 0 -DDT
p,p 0 -DDT
DDTs
97
29
23
<0.90
<0.90
<0.90
220
<0.90
36
33
69
18
<0.90
<0.90
19
100
52
22
<0.70
<0.70
<0.70
7.6
<0.70
57
42
98
24
<0.70
<0.70
24
100
57
34
56
<0.70
29
47
25
11
81
92
10
<0.70
<0.70
11
270
160
17
<0.70
<0.70
2.1
<0.70
<0.70
13
46
59
10
<0.70
7.4
18
Total OCsa
460
310
450
520
a
480
200
110
55
<1.20
<1.20
290
<1.20
100
83
180
120
<1.20
<1.20
120
1400
540
320
170
<1.30
<1.30
<1.30
520
<1.30
140
130
270
170
<1.30
<1.30
170
2000
2
62
35
53
<0.05
<0.05
<0.05
65
<0.05
24
11
35
51
19
17
87
340
750
430
640
<0.60
<0.60
<0.60
790
<0.60
290
140
430
620
230
210
1100
4100
1
49
21
53
<0.05
<0.05
<0.05
44
<0.05
9.9
20
30
56
20
14
89
290
550
240
590
<0.60
<0.60
<0.60
490
<0.60
110
220
330
620
220
150
990
3200
LTW
2
1
MW
2
2.6
4.0
2.3
0.60
3.3
0.53
0.33
<0.05
2.1
5.2
7.3
1.3
1.3
0.53
3.2
1.1
1.6
0.87
0.32
1.5
0.35
0.13
<0.05
9.5
1.2
11
0.35
1.1
0.21
1.6
1.6
2.9
2.9
1.2
3.8
1.1
<0.05
<0.05
16
1.1
17
2.9
0.71
<0.05
3.6
3.8
5.3
5.3
1.0
5.4
0.75
<0.05
<0.05
13
1.6
14
3.1
4.9
<0.05
8.0
24
18
34
44
1
2
38
16
24
<0.05
<0.05
<0.05
32
<0.05
21
18
40
68
<0.05
<0.05
68
220
62
16
31
<0.05
<0.05
<0.05
28
<0.05
32
22
55
23
<0.05
<0.05
23
210
51
79
45
12
66
11
6.6
<1.00
41
100
150
26
26
11
63
18
26
14
5.3
25
5.8
2.1
<0.80
160
20
180
5.8
18
3.5
27
20
36
37
15
48
14
<0.60
<0.60
200
14
220
36
9.0
<0.60
45
46
64
64
12
66
9.1
<0.60
<0.60
150
19
170
37
60
<0.60
98
780
320
480
<1.00
<1.00
<1.00
650
<1.00
440
370
810
1400
<1.00
<1.00
1400
1200
300
590
<1.00
<1.00
<1.00
530
<1.00
610
430
1000
430
<1.00
<1.00
430
480
300
430
530
4400
4100
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
Dry weight basis
HCHs
HCB
Heptachlor
Heptachlor epoxide
Aldrin
Dieldrin
Endrin
Kepone
a-chlordane
c-chlordane
Chlordanes
p,p 0 -DDE
p,p 0 -DDD&o,p 0 -DDT
p,p 0 -DDT
DDTs
KS
Concentration of total OCs is calculated assuming that concentrations of non-detected contaminants are equal to one half of the detection limit.
681
682
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
is located near a remote island with well-circulated oceanic waters. Notwithstanding, this area could still be affected by transboundary transfer of pollutants via
industrial effluents from mainland China where there
are signs of increased industrial activities (Chiu et al.,
2000).
Previous studies reported that DDTs were the most
abundant OC contaminants in sediment (Hong et al.,
1995), mussel (Phillips, 1985; Monirith et al., 2003)
and fish (Chan et al., 1999) samples from Hong Kong
marine waters. However, in the present study, greater
concentrations of PCBs than DDTs were found in mussel samples from most of the mariculture zones. The
greatest residue level of DDTs (1400 ng/g lipid wt.)
was found in MW. DDT concentrations found in the
present study were much smaller than those reported
in previous studies. For example, Monirith et al.
(2003) measured up to 61,000 ng/g lipid wt. of DDTs
in mussels from Cheung Chau. Even greater concentration (130,000 ng/g lipid wt.) was detected in mussels
from Wu Kwai Sha (Phillips, 1985). Greater DDT concentrations were also found in mussels from urbanized
areas in India and Thailand where DDT was still being
used for malaria vector control (Kan-atireklap et al.,
1997; Tanabe et al., 2000). Mussels from YTT, having
a DDE/DDTs ratio of 0.6, had more than 50% of the
DDTs existed in the form DDE. In other locations, such
as KO, TM and MW, the concentrations of p,p 0 -DDT
were below detection. These findings may indicate the
absence of fresh sources of DDTs in Hong Kong waters.
The high level of p,p 0 -DDE in mussels from MW reflects
a history of significant pollution by DDT, probably
attributable to the Pearl River discharge. Indeed, the
use of DDT has continued in China even after the official ban in the production and usage of OC pesticides
in 1983. This is evident from a number of studies
showing high p,p 0 -DDT/total DDTs ratios in sediments from the Zhujiang, Shiziyang, Xijiang Rivers
(Mai et al., 2002) and Daya Bay (Zhou et al., 2001).
Concentrations of DDTs in KO, OPT, TM, KS and
LTW were comparatively low (Table 1), and their occurrence could be attributed to oceanic or atmospheric
inputs from other sources outside Hong Kong (Wong
et al., 2004, 2005).
Concentrations of total HCHs in mussels are shown
in Table 1. Mussels from MW contained the greatest
concentrations (780 and 1200 ng/g lipid wt.), followed
by mussels from YTT (550 and 750 ng/g lipid wt.) and
TM (480 and 540 ng/g lipid wt.). HCHs are known to
be widely used as insecticides against grasshopper and
rice insects, and have also been used for seed protection,
livestock treatment as well as household vector control
in places such as China, India and Japan (Li, 1999).
Information on HCH usage in Hong Kong is limited,
but HCHs have been employed as pesticides and utilized
by some industries in small amounts (Phillips, 1985).
The perceived pollution source of HCHs in MW was
mainly from China. It is noted, however, that discharge
of HCHs has been reduced in China; concentrations of
HCHs in water had decreased from 1700 ng/l in 1979
to 24 ng/l in 1992 (Li, 1999). Again, discharges from
nearby agricultural areas, together with poor oceanic exchange, may account for the relatively great concentrations of HCHs in YTT. Concentrations of total HCHs
measured in the present study were less than those previously reported in mussels from Hong Kong. Mussels
from Reef Island, Mei Foo and Causeway Bay were reported to contain up to 29,000, 7100 and 6800 ng HCH/g
lipid wt., respectively (Phillips, 1985). However, the
present contamination level appears to be significantly
Fig. 2. Profile of HCHs in mussels collected from individual mariculture zones in Hong Kong.
Table 2
Concentrations (ng/g dry wt. and lipid wt.) of 28 PCB congeners in mussel samples collected from mariculture zones in Hong Kong
Replicate
Site
KO
OPT
TM
YTT
1
2
1
2
1
Dry weight basis
PCB1
PCB8
PCB18
PCB28
PCB29
PCB44
PCB50
PCB52
PCB66
PCB77
PCB87
PCB101
PCB104
PCB105
PCB118
PCB126
PCB128
PCB138
PCB153
PCB154
PCB170
PCB180
PCB187
PCB188
PCB194
PCB195
PCB200
PCB206
<0.1
<0.1
0.6
0.4
<0.1
<0.1
<0.1
0.5
<0.1
<0.1
<0.1
1.9
7.6
0.6
1.3
0.7
0.2
<0.1
0.5
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
0.9
4.0
<0.1
<0.1
0.4
0.5
<0.1
<0.1
<0.1
0.7
<0.1
<0.1
<0.1
3.6
7.3
<0.1
1.8
0.7
0.3
<0.1
0.9
<0.1
<0.1
<0.1
0.2
<0.1
<0.1
<0.1
1.6
8.3
<0.1
<0.1
0.8
1.5
<0.1
4.0
<0.1
1.3
<0.1
2.3
0.9
5.9
8.4
<0.1
3.2
7.3
1.7
<0.1
0.7
3.0
<0.1
<0.1
<0.1
3.0
<0.1
<0.1
2.0
4.2
<0.1
<0.1
0.6
0.5
0.7
2.4
0.5
0.2
<0.1
<0.1
0.1
4.6
6.6
<0.1
0.9
4.9
<0.1
<0.1
4.7
2.0
<0.1
<0.1
<0.1
0.2
<0.1
<0.1
1.1
1.1
<0.1
<0.1
1.3
1.0
0.7
<0.1
<0.1
2.1
<0.1
<0.1
<0.1
3.9
5.9
<0.1
1.7
1.4
<0.1
<0.1
1.6
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
4.0
<0.1
<0.1
4.3
1.9
1.5
<0.1
<0.1
3.0
<0.1
<0.1
<0.1
3.5
7.4
<0.1
5.1
2.1
<0.1
<0.1
3.6
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
<0.1
1.1
Total PCBsa
20
27
51
32
25
35
101
Lipid weight basis
PCB1
PCB8
PCB18
PCB28
PCB29
PCB44
PCB50
PCB52
PCB66
PCB77
PCB87
<0.9
<0.9
5
4
<0.9
<0.9
<0.9
5
<0.9
<0.9
<0.9
<0.9
<0.9
3
5
<0.9
<0.9
<0.9
6
<0.9
<0.9
<0.9
<0.9
<0.9
7
13
<0.9
36
<0.9
12
<0.9
21
8
<0.9
<0.9
5
5
7
21
5
2
<0.9
<0.9
1
<0.9
<0.9
12
9
6
<0.9
<0.9
18
<0.9
<0.9
<0.9
<0.9
<0.9
39
17
13
<0.9
<0.9
27
<0.9
<0.9
<0.9
<0.9
<0.9
31
25
<0.9
<0.9
<0.9
141
<0.9
<0.9
<0.9
<0.1
<0.1
3.5
2.8
<0.1
<0.1
<0.1
15.7
<0.1
<0.1
<0.1
7.2
3.6
5.0
8.3
11.0
<0.1
<0.1
6.7
<0.1
<0.1
9.3
8.2
<0.1
9.1
4.5
2.3
3.5
KS
2
4.2
0.1
4.3
6.9
<0.1
<0.1
<0.1
8.3
<0.1
<0.1
<0.1
6.8
5.3
5.6
7.1
9.7
6.9
<0.1
8.5
<0.1
<0.1
8.9
6.8
<0.1
8.7
6.8
5.2
4.3
111
38
0
39
62
<0.9
<0.9
<0.9
74
<0.9
<0.9
<0.9
LTW
MW
1
2
1
2
4.6
<0.1
1.0
<0.1
<0.1
2.0
2.0
0.5
<0.1
<0.1
0.8
5.3
<0.1
1.3
1.7
<0.1
3.8
0.5
<0.1
<0.1
2.7
0.7
<0.1
1.0
1.4
1.5
0.7
55.1
2.4
<0.1
0.4
<0.1
<0.1
0.6
0.9
0.4
0.1
2.0
0.5
1.7
<0.1
0.9
2.3
<0.1
1.9
0.1
<0.1
0.2
2.2
<0.1
<0.1
0.7
1.1
<0.1
0.6
40.1
1.8
<0.1
0.7
0.1
<0.1
3.1
2.4
1.5
0.4
3.9
0.3
3.6
0.2
4.7
7.5
<0.1
0.9
<0.1
9.9
0.2
2.7
<0.1
<0.1
1.3
1.4
<0.1
3.1
7.9
4.0
<0.1
2.8
<0.1
<0.1
2.6
4.3
1.8
4.9
4.3
0.5
6.2
0.2
<0.1
12.9
<0.1
0.9
<0.1
13.1
3.4
3.5
<0.1
<0.1
0.9
1.2
<0.1
2.5
11.0
88
59
57
81
42
<0.9
9
<0.9
<0.9
18
18
5
<0.9
<0.9
7
22
<0.9
4
<0.9
<0.9
5
8
3
1
18
4
16
<0.9
6
1
<0.9
28
21
14
3
35
3
36
<0.9
25
<0.9
<0.9
23
39
16
44
39
4
1
<0.1
<0.1
7.1
11.2
<0.1
<0.1
<0.1
8.2
<0.1
<0.1
<0.1
11.4
9.0
<0.1
9.7
12.0
<0.1
<0.1
6.9
<0.1
<0.1
3.9
2.1
<0.1
1.3
10.1
7.8
6.9
111
<0.9
<0.9
63
101
<0.9
<0.9
<0.9
74
<0.9
<0.9
<0.9
(continued on next
2
<0.1
<0.1
8.6
3.4
<0.1
<0.1
<0.1
7.0
<0.1
<0.1
<0.1
8.2
9.1
9.6
9.3
9.3
<0.1
<0.1
4.8
<0.1
<0.1
5.7
6.3
<0.1
3.0
9.0
9.0
9.8
111
<0.9
<0.9
78
30
<0.9
<0.9
<0.9
63
<0.9
<0.9
<0.9
page)
683
2
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
1
684
Table 2 (continued)
Replicate
Site
1
PCB101
PCB104
PCB105
PCB118
PCB126
PCB128
PCB138
PCB153
PCB154
PCB170
PCB180
PCB187
PCB188
PCB194
PCB195
PCB200
PCB206
Total PCBsa
a
17
68
5
12
6
2
<0.9
5
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
8
36
180
OPT
2
33
65
<0.9
16
6
2
<0.9
8
<0.9
<0.9
<0.9
2
<0.9
<0.9
<0.9
14
74
241
1
53
76
<0.9
28
65
15
<0.9
6
27
<0.9
<0.9
<0.9
27
<0.9
<0.9
18
38
455
TM
2
42
59
<0.9
8
44
<0.9
<0.9
42
18
<0.9
<0.9
<0.9
2
<0.9
<0.9
10
10
286
1
35
53
<0.9
15
13
<0.9
<0.9
14
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
36
218
YTT
2
32
66
<0.9
46
19
<0.9
<0.9
33
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
<0.9
9
308
1
65
32
45
75
99
<0.9
<0.9
61
<0.9
<0.9
84
74
<0.9
82
41
21
31
916
KS
2
61
48
51
64
87
62
<0.9
77
<0.9
<0.9
80
61
<0.9
78
62
47
39
1005
LTW
1
2
48
<0.9
12
15
<0.9
34
5
<0.9
<0.9
24
6
<0.9
9
13
14
6
496
16
<0.9
8
21
<0.9
17
1
<0.9
1
20
<0.9
<0.9
6
10
<0.9
5
361
785
534
1
32
2
42
67
<0.9
8
<0.9
89
2
24
<0.9
<0.9
12
12
<0.9
28
71
523
MW
2
1
55
2
<0.9
116
<0.9
8
<0.9
118
31
32
<0.9
<0.9
<0.9
11
<0.9
22
99
103
81
<0.9
87
108
<0.9
<0.9
62
<0.9
<0.9
35
19
<0.9
12
91
70
62
725
976
Concentration of total 28 PCB congeners is calculated assuming that concentrations of non-detected contaminants are equal to one half of the detection limit.
2
73
81
86
84
84
<0.9
<0.9
43
<0.9
<0.9
51
57
<0.9
27
81
81
88
1006
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
KO
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
greater than those reported in more recent studies in
Hong Kong and China (Hong et al., 1995; Monirith
et al., 2003). The maximum concentration recorded in
the present study was even greater than the greatest concentration, 430 ng/g lipid wt., measured in mussels from
India, one of the largest consumers of HCH in the world
(Monirith et al., 2003). The reason for the temporal variations in HCH concentrations is not known. However,
our results indicate the necessity for continuous monitoring and identifying the relevant sources. The HCH
profiles in Hong Kong mussel samples are shown in
Fig. 2. Compositions of HCH isomers varied among
the seven sampling locations. c-HCH was the dominant
isomer found in mussels from KO, OPT and TM;
whereas b-HCH was predominantly found in mussels
from YTT and MW. Detection of a mixture of HCH
isomers indicated that the mussels were mainly contaminated by technical HCH, rather than lindane which
contained more than 90% of c-HCH (Li, 1999).
Similar to the distribution pattern of HCHs, greatest
concentrations of total PCBs were found in mussels
from MW (980 and 1010 ng/g lipid wt.), followed by
YTT (920 and 1010 ng/g lipid wt.) and KS (530 and
790 ng/g lipid wt.) (Table 2). These contamination levels
were significantly smaller than those reported in 1983
from Causeway Bay (130,000 ng/g lipid wt.) and Rennies Mill (110,000 ng/g lipid wt.) (Phillips, 1985). The
maximum PCB concentration detected in the present
study was also smaller than those found in sites heavily
contaminated by PCBs in Japan and Russia (Monirith
et al., 2003). Concentration of PCBs found in mussels
from Tokyo Bay in Japan and Amursky Bay in Russia
were 5500 and 3700 ng/g lipid wt., respectively.
3.2. Dioxin-like compounds
H4IIE-luc cell bioassay was used to screen for the
presence of dioxin-like activities in the mussel samples
(Giesy and Kannan, 1998). Results of the H4IIE-luc cell
bioassay performed on mussels from different sampling
locations are shown in Table 3. The greatest concentration of dioxin-like compounds (39 pg TEQ/g wet wt.)
was detected in mussels from MW, followed by YTT
(37 pg TEQ/g wet wt.). The lowest concentration was
measured in mussels from KS (8.6 pg TEQ/g wet wt.).
The maximum dioxin-like activity detected in the
present study was less than the maximum activity
(44%-TCDD-max) obtained from blue mussels, Mytilus
edulis, from Korean coastal waters (Khim et al., 2000)
and from the sediment samples from Ulsan Bay, Korea
(Khim et al., 2001). Negative responses that occurred in
other studies (Khim et al., 2001) were not observed in
the present study. There are only a limited number of
studies on dioxin-like compounds in Hong Kong. Significant dioxin-like responses exhibited by mussels indicated the presence of dioxin-like substances, which
685
Table 3
Concentrations of dioxin-like compounds expressed as pg TEQ/g wet
weight (mean ± S.D.) in mussels from individual sampling location
Sampling locations
Concentration (pg TEQ/g wet wt.)
KO
OPT
TM
YTT
KS
LTW
MW
15 ± 5.8
10 ± 0.8
19 ± 10
37 ± 11
8.6 ± 7.2
20 ± 2.2
39 ± 21
may include dioxin-like PCBs, PCDDs, PCDFs, PAHs
and others. Future studies involving instrumental analyses will be required to determine the contaminants
responsible for the dioxin-like activities.
3.3. Human health risk assessment
The maximum measured environmental concentrations of various contaminants, their corresponding
RfDs and estimated RQs are summarized in Table 4.
The risk assessment was only confined to PCBs, DDTs,
chlordane, dieldrin, HCB and dioxin-like compounds
for which RfDs are available from the US EPA. Since
the dioxin-like potency of mussel samples were expressed relative to 2,3,7,8-TCDD, guideline value for
2,3,7,8-TCDD was used for evaluating the risk of dioxin-like compounds to human health. In the present
study, the greatest measured contaminant concentrations present in the mussel samples from all sampling
locations were used for estimating exposure levels. On
this basis, RQ for dioxin-like compounds (20–79) was
greater than unity, suggesting that adverse health effects
may be associated with high shellfish consumption. Possible uncertainties in the present study include: (1) safety
standards employed in the present study were from
USEPA which might not be applicable to the Hong
Kong population; (2) fish, instead of shellfish, consumption rate was used to derive RQ; (3) RQ in the present
Table 4
The RfD and maximum measured environmental concentrations for
individual contaminant
Chemical of concern
RfD from
USEPA
(ng/kg/day)
Maximum
measured
concentration
(ng/g wet wt.)
RQ
Chlordane
HCB
Dieldrin
DDTs
PCBs
Dioxin-like compounds
60
800
50
500
20
0.001–0.004
8.3a
5.3a
0.33a
13a
17a
0.04
0.27
0.01
0.01
0.05
0.85
20–79
a
Concentrations on wet weight basis were converted from the corresponding concentrations expressed on dry weight basis in Tables 1
and 2.
686
M.K. So et al. / Marine Pollution Bulletin 51 (2005) 677–687
study was derived based on consumption rates of heavy
seafood consumers; (4) the highest measured environmental concentration for a particular contaminant was
used to estimate exposure level; (5) different contaminants may interact additively, synergistically or antagonistically to modify effects (Connell et al., 1998a; Fung
et al., 2004); and (6) different age groups will consume
different amounts of food, leading to different exposure
levels (Dougherty et al., 2000). In summary, this preliminary assessment has considered the ‘‘worse-case’’ scenario, and a more refined risk assessment should be
undertaken in subsequent investigations.
Acknowledgement
The work described in this paper was supported by
the Area of Excellence Scheme under the University Grants Committee of the Hong Kong Special
Administration Region, China (Project no. AoE/P-04/
2004).
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