International Biodeterioration & Biodegradation 124 (2017) 314e325

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International Biodeterioration & Biodegradation

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Assessment of heavy metals in aquaculture fishes collected from

southwest coast of Taiwan and human consumption risk
Yun-Ru Ju a, Chiu-Wen Chen a, Chih-Feng Chen a, Xiang-Ying Chuang a,
Cheng-Di Dong a, b, *
a
Department of Marine Environmental Engineering, National Kaohsiung Marine University, Kaohsiung 81157, Taiwan
b
Department of Bioinformatics and Medical Engineering, Asia University, Taichung 41354, Taiwan

a r t i c l e i n f o a b s t r a c t

Article history: The present study determined the metal levels in aquaculture fish of tilapia and water and sediments in
Received 7 February 2017 the southwestern Taiwan and estimated the human health risk assessment for consumption of tilapia.
Received in revised form Bioconcentration factor (BCF) and biota-sediment accumulation factor (BSAF) were used to assess the
5 April 2017
metal accumulation ability of biotas, while metal pollution index (MPI) was assessed to compare the
Accepted 5 April 2017
Available online 8 April 2017
pollution level of total eight metals for the different sampling sites and tissues of tilapia. Metal level in
tissues revealed a tissue-specific bioaccumulation pattern. Except for Cu, the highest metal burden was
found in kidney, showing the significant differences in metal concentration of kidney with the other
Keywords:
Metals
tissues of tilapia. Muscle accumulated the low concentrations of Hg (0.19 ± 0.21 mg g
1 dry wt), Cd
Tilapia (0.05 ± 0.02), As (0.06 ± 0.05), Cu (1.61 ± 1.17), Zn (21.5 ± 10.2), and Ni (1.01 ± 1.03). Results allowed
Bioaccumulation putting the mean MPI of tissues in order from the highest to lowest value, kidney (6.92) > GI tract
Aquaculture (2.06) > liver (1.25) > gill (0.80) > muscle (0.59). In addition to Hg and Cd, the estimate of BCF was greater
Human health risk that of BSAF for other metals, demonstrating that the bioaccumulation of Hg and Cd for tilapia collected
from aquaculture ponds was from the sediments, as well as the bioaccumulation of other metal was from
water. Correlation analysis found that Fulton's condition factor (K) of tilapia had the negative relationship
with MPI for muscle, liver, and kidney, meaning decreasing K of tilapia was with the increasing estimates
of MPI. For the human health risk assessment, tilapia cultured in the southwest coast of Taiwan was
found to be low-risk for consumption and do not surface a potential threat to the health of general
human consumers. Results in this effort can assist the government in determining seafood safety and its
implementation in Taiwan.
© 2017 Elsevier Ltd. All rights reserved.

1. Introduction non-biodegradable and persistent, and that result in bio-

Metals originally present in the natural environments, yet the
anthropogenic sources of metals including mining, industrial,
traffic, domestic sewage, and atmospheric deposition vastly elevate
the metal concentration in the environments, as well as the aquatic
environments (Sapkota et al., 2008; Gu et al., 2015; Saha et al.,
2016). With the sharply rapid population growth and economic
development, the increase in the discharge of wastes into aquatic
environments has led to a significant increase in metal contami-
nation (Dhanakumar et al., 2015). Metals in the environments are
* Corresponding author. Department of Marine Environmental Engineering, Na-
tional Kaohsiung Marine University, Kaohsiung 81157, Taiwan.
E-mail address: cddong@mail.nkmu.edu.tw (C.-D. Dong).
accumulation of metals in organisms (Rajkowska and
Protasowucki, 2013; Zhang et al., 2016). Some essential metals are
required to play the important roles in physiological metabolisms
for organisms, such as Cu, Zn, Ni, and Fe. It also could be toxic for
organisms when the overloading essential metals are accumulated
in body. For the other non-essential metals, including Hg, Pb, and
Cd, those are regarded as uselessness or even hazard for organisms
(Ruelas-Inzunza et al., 2011; Gu et al., 2015).
Measuring the metal bioaccumulation in aquatic organisms
could assess the possible impacts related to metal pollution in the
environments, taking into account bioavailability aspect (Liang
et al., 1999; Abdel-Baki et al., 2011; El-Moselhy et al., 2014; De
Jonge et al., 2015; Dhanakumar et al., 2015; Abdel-Khalek et al.,
2016). For the organisms, the assimilation rate of metals through
the surrounding media greater than the rates of elimination and

http://dx.doi.org/10.1016/j.ibiod.2017.04.003
0964-8305/© 2017 Elsevier Ltd. All rights reserved.
 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325
physiological metabolism derive the metal bioaccumulation (Farkas
et al., 2003). The bioaccumulation pattern of metals in organisms
can be linked to the metal-induced adverse responses to consider
the concept of bioavailability (Bervoets and Blust, 2003; Neff and
Cargnelli, 2004; Couture and Pyle, 2008; Ruelas-Inzunza et al.,
2011; Kasimoglu, 2014). Following the linkage, metal bio-
accumulation in fish tissue can be used to predict the potential
impacts of metal exposure on fish health. In the beginning, no
matter for essential or non-essential metals, the adverse effects are
not appeared immediately when metals penetrated into the or-
ganisms, until the metal burdens accumulated in the organism
exceeded the threshold that organisms can afford (Gu et al., 2015;
Abdel-Khalek et al., 2016). Investigations of metal bio-
accumulation in fish in the aquatic environments have been
executed in food safety fields for years (Liang et al., 1999; Lin et al.,
2005; Ling et al., 2013; Dhanakumar et al., 2015; Hsi et al., 2016).
There are many routes for fish exposure to metals, including direct
uptake through gill and biological membranes (waterborne) and
digestion of food and sediment matters in the digestive tract (di-
etary), and metals end up in the body of fish. Rajkowska and
Protasowucki (2013) indicated that metal distribution among var-
ied tissues is mainly depended on the metal content in water and
food, and therefore it can serve as a pollution indicator of the en-
vironments. Generally, liver and kidney were regarded as the or-
gans having high metal accumulation, while muscle and gill have
relative low metal burden (Rajkowska and Protasowucki, 2013;
Taweel et al., 2013). Farkas et al. (2003) suggested that gill can
directly reflect the metal level in water and the storage mechanism
will be appeared in hepatic metal content. The patterns of uptake
and bioaccumulation depend on metals, species, organs, life stage,
diet type, and environmental factors. Consequently, bio-
accumulation of metals will be a suitable preliminary assessment
for the health of aquaculture fish and human food safety.
In order to provide enough nutrition to rapid growth population
in the 20th century, the demand for seafood products is increasing
(Sapkota et al., 2008). Aquaculture production is also steadily
expanding year by year. Larsen and Roney (2013) analyzed the
global demand for animal protein and found global farmed fish
production exceeded beef production in 2011. Moreover, fish is a
main source of nutrition and is widely consumed in coastal regions
(Saha et al., 2016). As if aquaculture fish farmed in the metal-
contaminated environments, fish could accumulate metals
through water, sediment, and feeds; consequently, human who has
high consumption rate of fish could be exposed to the higher health
risk. For vulnerable population, such as the old, children, and
pregnant woman, the limitation of metal daily uptake for them
should be more stringent than the general population to prevent
them from having the metal-induced adverse effects. (Oken et al.,
2012). As far as we know, the potential non-carcinogenic risks
can be assessed by the hazard quotient (HQ) and total hazard
quotient (THQ) proposed by the US EPA to quantify the health risk
for fish consumption (Cheung et al., 2008; Gu et al., 2015; Abdel-
Khalek et al., 2016; Zhang et al., 2016).
Aquaculture is commonly positioned in the coast area of Taiwan,
ascribing its geographic environment and close to the water source
(Ling et al., 2013). Aquaculture industries play a vital role in the
economy of Taiwan's agriculture. About 0.7% of total global fish
production was from Taiwan recorded by the United Nations Food
and Agriculture Organization (FAO) (Sapkota et al., 2008). However,
coastal areas always have high population density and intense
economic activity (Martínez et al., 2007). For this study area, it is
needed to pay the attention for the metal bioaccumulation of
aquaculture organisms because fish farms are located near the
naphtha cracker plant, which may release metal into air by burning
activity. Moreover, in the aquaculture environments, the Cu-based
315
antifoulants and formulated fish feeds could be also the extra
sources of metals (Sapkota et al., 2008).
Tilapia is a commercially major fish and is stocked traditionally
in Taiwan. Tilapia, an omnivorous filter feeder, was introduced into
Taiwan in 1946. The Fisheries Statistical Yearbook in Taiwan for
2015 reported that the fish production and value of tilapia were
respectively about 70,472 metric tons and NT$ 3.53 billion per year,
with the rank of fourth in the major seafood species in recent years
(Fisheries Agency, 2016). Straus (2003) indicated that tilapia is the
most tolerant fish to exist on the poor water quality than that most
commonly farmed freshwater fish. Tilapia have been reported by
many studies as a suitable vertebral organism for being used
extensively to research in biological, physiological, and toxicolog-
ical (Nussey et al., 1995; Pelgrom et al., 1995; Wong and Wong,
2000).
Under certain conditions, human accumulate metals through
consumption of aquaculture organisms and could have adverse
effects on body (Saha et al., 2016). Previous studies have investi-
gated the metal contents of farmed fish (tilapia and milkfish) in
Taiwan, indicating tilapia might own tendency to accumulate
metals from the aquaculture environments and then pose health
risk to consumers (Ling et al., 2009, 2013; Gu et al., 2015). Therefore,
for clarifying aforementioned doubt, the objectives of the present
study were carried out as following: (i) to discriminate the bio-
accumulation and distribution of metals (Hg, Pb, Cd, Cr, As, Cu, Zn,
and Ni) in the selected tissues (muscle, gill, liver, kidney, and
gastrointestinal tract) of tilapia from aquaculture in the south-
western coast of Taiwan, and (ii) to estimate the daily metal intake
ascribing from the consumption of cultured tilapia and then
conduct a human health risk assessment of metals for Taiwanese.
2. Materials and methods
2.1. Study area and collection
In this study, fish samples (tilapia) were collected from the
aquaculture ponds distribute the area of southwestern Taiwan in
2015 and 2016 (Fig. 1). The locations of sampling site are shown in
Table 1. Sampling sites are close to the naphtha cracker plant, which
is located at the southwestern coast line of Taiwan. The distances
from each sampling site to the naphtha cracker plant are measured
to investigate the effect of them on the metal accumulation in
tilapia (Table 1). Water and sediments samples from each site were
respectively collected in polyethylene bottles of one liter and
polyethylene plastic bags and transported to the laboratory and
preserved in a freezer for further analysis. A total of 26 tilapias were
held in polyethylene bags with ice, labeled and transported to the
laboratory in 24 h. The mean body weight and length of collected
tilapias were measured before they were dissected. Tilapias were
dissected and five tissues of muscle, gill, liver, kidney, and gastro-
intestinal (GI) tract were obtained and ready to freeze-dry.
2.2. Determination of heavy metals
The tissues of fish samples were freeze-dried for 1 day until the
sample was constant weight. Each dried tissue sample was ground
by a set of porcelain mortar and pestle. Tissue sample was weighted
(0.5e1.0 dry weight), and digested with hydrogen peroxide (>35%
H2O2, SHOWA) and nitric acid (67e70% HNO3, Fisher Scientific) in
glass beaker at 95  C until the solution become clear. At the end of
the digestion and after cooling, the samples were diluted to 25 mL
with deionized distilled water and then analyzed for metal content.
The sediment samples were first sieved and particles with
diameter >63 mm were discarded. The sieved sediment samples
were dried naturally at room temperature and gently homogenized
316 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325

Fig. 1. Map of aquaculture ponds locating area and naphtha cracker plant in Yunlin County in Taiwan.

Table 1
The basic information about sample sites and tilapia characteristics.

Site Geographical coordinate Distance to plant (km) Sample size (n) Tilapia characteristics
a
Body weight (g) Body length (cm) K
 0  0 b
1 N23 46.43 , E120 14.00 2.89 3 819 ± 196 33 ± 3.2 2.19 ± 0.12
2 N23 44.430 , E120 16.210 8.33 7 152 ± 44 22 ± 1.6 1.44 ± 0.11
3 N23 47.190 , E120 14.490 2.65 8 165 ± 55 19 ± 2.0 2.26 ± 0.29
4 N23 46.700 , E120 14.090 2.71 2 1201 36 2.63 ± 0.14
5 N23 46.110 , E120 15.320 5.14 3 897 ± 112 32 ± 0.5 2.74 ± 0.34
6 N23 47.610 , E120 14.460 2.12 3 1193 ± 70 35 ± 2.2 2.78 ± 0.41
a
K means Fulton's condition factor.
b
Mean ± SD.

into fine powder with mortar and pestle (Retsch RM 100 Motor
Grinder). The combination of ultra-pure acids (HNO3: HCl ¼ 1:3 by
volume) was added to the sediment sample (1.0 g dry weight) and
then heated at 100  C to digest. Once the digestion process was
completed and after cooling the samples were filtered through
0.45-mm filter paper into a pre-selected final volume.
All samples were analyzed for the following elements: Hg, Pb,
Cd, Cr, As, Cu, Zn, and Ni. The metal content was determined using a
flame atomic absorption spectrophotometry (Hitachi Z-6100). Hy-
dride generator coupled with an atomic absorption spectropho-
tometry was used to analyze total mercury (cold vapor mode).
Blank was carried out for instrument calibration. The quality of the
analytical procedure was verified by analyzing the certified stan-
dard reference material for sediments and benthic invertebrates by
HISS-1 (marine sediments, National Research Council of Canada)
and DORM-2 (dogfish muscle tissue, National Research Council of
Canada), respectively. Replicate analysis of these reference
materials showed good accuracy, with mean recovery rate nearly of
80e120%.
2.3. Data analysis
Based on the collected tilapia measurements, Fulton's condition
factor (K) which is calculated as body weight divided by the cube of
body length was estimated in this study (Froese, 2006).
W
K ¼ 102  ;
L3
where W and L mean the whole body wet weight in gram and body
length in cm of tilapia, a multiplier of 100 is used to bring K close to
unity. It is based on the hypothesis that fish has the higher weight
in a certain body length indicating fish is in a better physiological
condition. Because K is simply to calculate and has its historical
precedence, it is widely applied in conservation and environmental
 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325
biology for fish (Choongo et al., 2005; Stevenson and Woods, 2006;
Yi and Zhang, 2012; Kasimoglu, 2014).
Metal pollution index (MPI) was assessed to compare the total
content of metals for the different tissues of tilapia, the MPI formula
is shown following (Usero et al., 1997),
1
MPI ¼ ðCb1  Cb2  Cb3  …Cbn Þn ;
where Cbn is the concentration of metal n in the analyzed tissue (mg
g
1 dry weight).
Due tilapia has the habit of cleaning the pond bottom of detritus
and decaying algae (Vinyard et al., 1988; Zhou and Wong, 2000),
sediments are a potential media for tilapia exposed to metal in
aquaculture. The ratio of metal in the tissue of tilapia (mg g
1 wet
weight) to the metal concentration in the water (mg L
1) is called
the bioconcentration factor (BCF), whereas the ratio of metal in the
tissue of tilapia (mg g
1 dry weight) to the metal concentration in
the sediments (mg kg
1 dry weight) is called the biota-sediment
accumulation factor (BSAF). The BCF and BSAF were respectively
used to assess the metal accumulation abilities of tilapia for
exposed to water and sediments. They were calculated according to
the following equation,
Cb
BCF ¼ ;
Cw
Cb
BSAF ¼ ;
Cs
where Cb, Cw, and Cs are the mean metal concentration in the biota,
water, and sediments, respectively.
All the results in this study were expressed as mean ± standard
deviation (SD). Duncan's Multiple Range Test was conducted to
determine significant difference in mean metal concentrations
across different tissues and at different sampling sites as indicated
by different case letters as p < 0.05. Spearman's rank correlation
coefficient (r) was utilized to describe the relationships between
determined parameters. Results were considered significant at
p < 0.05. All statistical analyses were carried out with SPSS 12.0
software for Windows.
3. Results and discussion
3.1. Heavy metals in tissues of fish
For the collected tilapia, mean body weight, body length, and
Fulton's condition factor ranged from 152 to 1201 g, 19e36 cm, and
1.44 to 2.78, respectively, are presented in Table 1. Table 2 shows the
mean metal concentrations in five tissues (muscle, gill, liver, kidney,
and GI tract) of tilapia in different sampling sites, expressed on a
dry weight basis. The range of Hg concentration was 0.07 mg g
1 in
gill at Site 3e5.80 mg g
1 in kidney at Site 2. Kidney of tilapia at Site
2 had the highest concentrations of Pb (9.74 mg g
1), Cd
(8.15 mg g
1), and Cr (19.7 mg g
1) compared with tilapia from other
sampling sites. The highest As was detected in kidney at Site 2
(2.87 mg g
1) and the lowest As were measured in muscle at Site 5
and in liver at Site 6 (0.02 mg g
1). Liver of tilapia at Site 1 accu-
mulated the maximum Cu level (288 mg g
1), while muscle accu-
mulated the minimum level (0.93 mg g
1) at Site 6. The
concentration of Zn was the lowest in muscle of tilapia at Site 5,
whereas the highest in liver at Site 2. High Ni concentration was
observed in kidney at Site 3 (21.5 mg g
1). For all tissues of tilapia, Zn
concentrations were the highest among eight metals at all sam-
pling sites except for Cu content in liver. In Site 2, Cd in liver and
kidney, Cr in muscle, As in muscle, Zn in muscle, liver, and kidney,
317
and Ni in muscle were significantly higher than other sampling
sites (p < 0.05). Tilapia acquired in Sites 5 and 6 showed compar-
atively the lower metal concentrations than those from other sites.
Meanwhile, no significant difference of metal accumulation in
different tissues was found among most other sampling sites.
The metal bioaccumulation in different tissues exhibited various
levels of a tissue-specific pattern with raised rate accumulation in
the highly metabolic tissue as kidney (Fig. 2). Except for Cu, the
highest metal burden was found in kidney, showing the significant
differences in metal concentration of kidney with the other tissues
of tilapia. Muscle accumulated the low concentrations of Hg
(0.19 ± 0.21 mg g
1 dry wt), Cd (0.05 ± 0.02), As (0.06 ± 0.05), Cu
(1.61 ± 1.17), Zn (21.5 ± 10.2), and Ni (1.01 ± 1.03), in which was
agreement with the previous studies in the other regions (Gbem
et al., 2001; Allinson et al., 2002; Al-Kahtani, 2009; Taweel et al.,
2013; Dhanakumar et al., 2015). Farkas et al. (2003) and Gbem et al.
(2001) suggested that low concentration of metal in muscle might
be attributed to the growth dilution of fish if growth is faster than
metal accumulation. In addition, it is generally considered that
muscular tissue is not a target ligand for metal biotransformation
and accumulation (El-Moselhy et al., 2014).
Results such as high metal concentration in kidney and low
concentration in muscle were consistent with the report presented
by Abdel-Baki et al. (2011). Moreover, liver contained the maximum
concentration of Cu (153.6 ± 156.9 mg g
1 dry wt), yet exhibited the
lowest concentrations of Pb (0.59 ± 0.86) and Cr (1.00 ± 0.73).
Compared with other metals, liver tends to accumulate the essen-
tial metals of Cu and Zn; this result was consistent with the pre-
vious studies (Rashed, 2001; Nakayama et al., 2010; Abdel-Baki
et al., 2011; Rajkowska and Protasowucki, 2013; El-Moselhy et al.,
2014; Dhanakumar et al., 2015). Dhanakumar et al. (2015) investi-
gated the metal bioaccumulation of commercial fish in the reser-
voir of Cauvery delta region, proposing liver was the target organ to
accumulate a notable level of Cu and Zn in caught fish. High con-
centration of essential metals in hepatic tissue may results from the
essential metals being an indispensable part of the cysteine-rich
proteins, such as metallothionein, which is vast existing in liver
for sequestering and detoxifying metals (Roesijadi, 1996; Gbem
et al., 2001; Wagner and Boman, 2003).
Results expressed that metal bioaccumulation of Hg, Pb, Cr, As,
and Ni had similar pattern in the distribution of varied tissues,
presenting metal prefer to accumulate in kidney and GI tract than
that in muscle, gill, and liver (Fig. 2). Rajkowska and Protasowucki
(2013) observed the higher accumulation of Cu, Zn, and Mn in
kidney and digestive tract of pike and bream. It is suggested that
high concentration of metal in GI tract may be associated with the
dietary exposure being the major source of metals (Rajkowska and
Protasowucki, 2013). Moreover, Vinyard et al. (1988) also indicated
that tilapia has the behavior that pecks the sediments to filter the
organic matter. Hence, metals in the sediments may the important
source for metal bioaccumulation in GI tract of fish (Gbem et al.,
2001).
3.2. Metal pollution index and bioaccumulation
The MPI is used to describe the polluted degree of metals in
tissues of tilapia. It is suggested that the higher the value of esti-
mated MPI, the higher degree of contamination in tissue is
considered (Usero et al., 1997). Results allowed putting the mean
MPI of tissues in order from the highest to lowest value, kidney
(6.92) > GI tract (2.06) > liver (1.25) > gill (0.80) > muscle (0.59)
(Fig. 3). It could be found that MPI ranged from 16.06 in kidney at
Site 2 and 0.30 in muscle at Site 5. Mean estimations of MPI in
tissues indicated that kidney and GI tract had the higher metal
contamination for all metals.
318 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325

Table 2
Mean metal concentrations (±SD, mg g
1 dry wt) in tissues of tilapia sampled from different sites.

Metal Tissue Site 1 Site 2 Site 3 Site 4 Site 5 Site 6

Hg Muscle 0.17 ± 0.12a 0.34 ± 0.35a 0.15 ± 0.09a 0.09a 0.12 ± 0.11a 0.12 ± 0.08a
Gill 0.09 ± 0.05a 0.36 ± 0.56a 0.07 ± 0.05a 0.28a 0.08 ± 0.07a 0.11 ± 0.07a
Liver 0.29 ± 0.07a 0.34 ± 0.25a 0.07 ± 0.05a 0.27a 0.17 ± 0.12a 0.11 ± 0.08a
Kidney 1.71 ± 0.66a 5.80 ± 6.57a 2.10 ± 1.84a 1.02a 0.72 ± 0.26a 0.42 ± 0.19a
GI tract 0.66 ± 0.23a 1.53 ± 1.94a 0.62 ± 0.93a 0.14a 0.16 ± 0.05a 0.23 ± 0.23a
Pb Muscle 0.37 ± 0.15a 0.95 ± 0.67a 0.37 ± 0.23a 0.60 ND 0.41 ± 0.08a
Gill 0.66 ± 0.44a 1.27 ± 0.55a 0.66 ± 0.35a 0.95a 0.49 ± 0.36a 0.66 ± 0.30a
Liver 0.34 ± 0.24a 0.94 ± 1.45a 0.60 ± 0.21a 0.40a 0.32 ± 0.22a 0.21 ± 0.01a
Kidney 6.74 ± 7.63a 9.74 ± 7.09a 2.40 ± 0.48a 3.08a ND 1.59 ± 0.50a
GI tract 1.25 ± 0.34a 0.98 ± 0.61a 3.82 ± 3.53a 0.79a ND 0.67 ± 0.13a
Cd Muscle 0.05 ± 0.01a 0.06 ± 0.02a 0.05 ± 0.02a 0.05 0.03 ± 0.00a 0.03 ± 0.00a
Gill 0.05 ± 0.03a 0.07 ± 0.02a 0.09 ± 0.04a 0.05 ND ND
Liver 0.04 ± 0.02a 1.21 ± 0.93b 0.10 ± 0.06a 0.03a ND ND
Kidney 0.48 ± 0.37a 8.15 ± 2.06b 1.07 ± 0.76a 0.17 0.22 ± 0.13a 0.19 ± 0.11a
GI tract 0.15 ± 0.04a 0.31 ± 0.15a 0.40 ± 0.39a 0.22 0.15 ± 0.16a 0.52 ± 0.65a
Cr Muscle 1.85 ± 0.24ab 2.46 ± 1.29b 1.31 ± 0.96ab 0.79ab 0.54 ± 0.10a 1.23 ± 0.66a
Gill 1.45 ± 1.28a 2.22 ± 1.63a 1.27 ± 1.05a 1.40a 1.32 ± 0.96a 1.10 ± 0.66a
Liver 1.48 ± 1.08a 0.75 ± 0.67a 0.98 ± 0.63a 0.95a 1.13 ± 0.97a 1.03 ± 0.79a
Kidney 12.5 ± 13.2a 19.7 ± 19.2a 17.2 ± 22.0a 18.7a 11.3 ± 8.37a 4.29 ± 2.79a
GI tract 5.15 ± 2.30a 1.76 ± 0.45a 5.84 ± 3.77a 1.95a ND 2.43 ± 1.05a
As Muscle 0.12 ± 0.07b 0.10 ± 0.05ab 0.05 ± 0.02ab 0.02a 0.02 ± 0.01a 0.04 ± 0.03ab
Gill 0.32 ± 0.11b 0.09 ± 0.05a 0.09 ± 0.05a 0.13a 0.08 ± 0.03a 0.09 ± 0.02a
Liver 0.06 ± 0.04a 0.22 ± 0.36a 0.06 ± 0.03a 0.04a 0.03 ± 0.04a 0.02 ± 0.01a
Kidney 2.42 ± 3.66a 2.87 ± 4.09a 0.53 ± 0.98a 0.11a 0.16 ± 0.18a 0.07 ± 0.01a
GI tract 0.64 ± 0.54a 0.26 ± 0.28a 0.67 ± 0.75a 0.23a 0.17 ± 0.11a 0.37 ± 0.25a
Cu Muscle 1.20 ± 0.14a 2.56 ± 1.96a 1.43 ± 0.29a 1.42a 1.08 ± 0.69a 0.93 ± 0.41a
Gill 1.20 ± 0.65a 2.11 ± 1.17a 2.21 ± 0.39a 1.91a 2.44 ± 2.09a 2.47 ± 2.06a
Liver 287.7 ± 221.6a 185.4 ± 208.5a 188.2 ± 108.5a 42.3a 28.3 ± 20.1a 52.4 ± 1.82a
Kidney 12.3 ± 11.9a 81.6 ± 82.4a 14.2 ± 3.1a 6.2a 9.47 ± 1.25a 6.86 ± 3.07a
GI tract 15.0 ± 6.88bc 5.23 ± 3.40a 18.6 ± 6.8c 7.87ab 10.1 ± 4.06ab 7.08 ± 1.61abc
Zn Muscle 20.0 ± 5.8ab 26.2 ± 3.20b 26.0 ± 14.3b 16.2ab 9.06 ± 4.37ab 16.4 ± 6.80a
Gill 52.4 ± 23.9a 63.1 ± 13.6a 61.0 ± 15.1a 56.7a 37.5 ± 9.86a 45.6 ± 18.0a
Liver 45.3 ± 18.5a 162.5 ± 109.4b 50.2 ± 13.1a 44.8a 16.7 ± 9.55a 20.7 ± 4.8a
Kidney 83.5 ± 24.5ab 130.5 ± 45.8b 101.6 ± 9.45ab 95.5ab 59.5 ± 7.59a 73.3 ± 23.3a
GI tract 91.9 ± 44.8a 65.6 ± 15.7a 87.4 ± 29.1a 75.8a 65.6 ± 27.4a 58.6 ± 26.3a
Ni Muscle 2.28 ± 0.56b 1.95 ± 0.97b 0.30 ± 0.24a 0.38a 0.27 ± 0.29a 0.35 ± 0.29a
Gill 1.28 ± 0.87ab 1.78 ± 1.66ab 0.39 ± 0.20a 0.88a 0.36 ± 0.24a 4.23 ± 5.85b
Liver 2.05 ± 1.29b 1.02 ± 1.17ab 0.51 ± 0.42a 0.37a 0.32 ± 0.29a 0.27 ± 0.21a
Kidney 19.5 ± 20.9a 16.0 ± 7.76a 21.5 ± 44.7a 0.88 3.97 ± 2.47a 0.64 ± 0.66a
GI tract 5.90 ± 2.06a 1.87 ± 0.77a 4.22 ± 5.13a 1.09a ND 1.19 ± 0.24a

Values with the same letters in the same row for each metal and tissue are not significantly different (Duncan's test, p < 0.05), whereas values with no letters are not included
in the test. ND means below detectable limits.

Based on the metal concentrations in water (mean concentra-
tion: Hg 0.07, Pb 0.39, Cd 0.20, Cr 0.20, As 0.22, Cu 1.97, Zn 5.39, and
Ni 1.61 in mg L
1), sediments (mean concentration: Hg 0.04, Pb 18.3,
Cd 0.11, Cr 51.4, As 5.20, Cu 39.8, Zn 116.6, and Ni 24.1 in mg kg
1 dry
weight), and tissues of tilapia, the distributions of BCF and BSAF in
different tissues of tilapia were shown in Fig. 4. Results indicated
that the BCF of Cu was highest in liver, whereas that of other metals
were in kidney. The lowest BCF for all accumulate metals was found
in muscle except that for Cd and Ni in liver. For all tissues of tilapia,
the BCF value of Cr and Zn was higher than 1.0, showing the ten-
dency to accumulate Cr and Zn from water. Rajkowska and
Protasowucki (2013) also observed the higher BCF for Cu and Zn
in GI tract. Low bioaccumulation level of Pb, Cd, and Ni in all tissues
excluding in liver (Fig. 4A).
Results showed that the BSAF of Hg in all tissues of tilapia were
greater than 1.0, indicating that tilapia was readily subjected to the
bioaccumulation of Hg from sediments. Moreover, the BSAFs of Cd
in kidney and GI tract and Cu in liver were higher than 1 (Fig. 4B).
Nakayama et al. (2010) studied the metal distribution of tilapia and
sediment in the lakes of Zambia and found BSAF of Cd was greater
than 1, with the range of 13.4e15.1, explaining the high level of Cd
in fish was from the sediments. Apart from above results, the BCFs
of other metals in tissues were lower than 1. In addition to Hg and
Cd, the estimate of BCF was greater that of BSAF for other metals,
demonstrating that the bioaccumulation of Hg and Cd for tilapia
collected from aquaculture ponds was from the sediments, as well
as the bioaccumulation of other metal was from water (Rashed,
2001).
Mercury has been reported that it is easy to accumulate in fish
(Yi and Zhang, 2012). The values of BCF and BSAF for Hg nearly were
higher than the unity, suggesting that Hg was readily accumulated
in tilapia from both water and sediments and was difficultly
excreted from the inside of tilapia. Ruelas-Inzunza et al. (2011)
collected the fish and crustacean in Baluarte River, NW Mexico,
discovering that BSAF greater than 1 was detected only in the case
of Hg in fish. Ruelas-Inzunza et al. (2011) also suggested that the
simultaneous processes of uptake as well as regulation and
detoxification lead the high capacity for the net accumulation of
metals in fish. However, the bioaccumulation level of metal in the
fish may not cause any adverse effect, but may induce the hazard to
their predators, such as piscivorous birds and mammals and human
(Sapkota et al., 2008; Taweel et al., 2013; Kasimoglu, 2014; De Jonge
et al., 2015; Gu et al., 2015).
3.3. Correlation analysis
Correlations among metal concentrations in water, sediments,
and tissues of tilapia were determined by Spearman's rank
 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325 319

Fig. 2. Mean metal concentrations (mg g
1 dry wt) in various tissues of tilapia. Values with the same letter are not significantly different according to Duncan's Multiple Range Test
(p < 0.05).

correlation coefficient (r) (Table 3). Noticeably, negative and no found between Cr in sediments and GI tract, As in sediments and
correlation were observed between all metal in water and the muscle and kidney, Cu in sediments and GI tract, and Zn in sedi-
accumulated metals in almost all tissues except gill content of Ni ments and liver. Nickel level revealed strong positive relationship
(r ¼
0.51, p < 0.01). The significantly positive relationship was with that in tissues of muscle and kidney (Table 3).
320 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325

Fig. 3. Mean metal pollution index (MPI) of tilapia for various tissues in sampling sites.
Table 4 summaries the relationships between metal concen-
trations in varied tissues of tilapia. There were significant positive
correlations between liver and kidney for all accumulated metal
(r ¼ 0.40e0.72, p < 0.01) except for Hg. The strongest positive
relation between liver and kidney was for Cd, for which is in
concordance with the study of De Jonge et al. (2015). Another
positive correlation was discovered between GI tract and liver for
accumulated metals of Hg, Pb, Cr, Cu, and Ni, whereas most accu-
mulated metals in GI tract had no correlation with muscle (except
for Hg), gill (except for Zn), and kidney (except for Hg). Interest-
ingly, for the relationship between the bioaccumulation levels of
muscle and kidney, significantly positive pattern was observed in
the essential metals of Cu, Zn, and Ni. Result was consistent with
the finding of Pyle et al. (2005), indicated that Zn level in muscle
was significantly related to hepatic Zn, which implied that a
transport pathway may exist for passing Zn from liver to muscle.
The estimate of Fulton's condition factor (K) is based on the body
weight and length and could be used to determine the well-being
of fish considering nutritional status, pathogenic effect, and pres-
sured surrounding (De Jonge et al., 2015). Neff and Cargnelli (2004)
demonstrated that K is a good indicator for clarifying the energetic
condition of fish. Results showed that condition factor of tilapia had
the good negative relationship with MPI for muscle (r ¼
0.52,
p < 0.01), liver (r ¼
0.63, p < 0.01), and kidney (r ¼
0.68,
p < 0.01), meaning decreasing K of tilapia was with the increasing
estimates of MPI (Fig. 5). It seems intuitive that fish live in the
higher metal-contained environments are likely to be of lower K
than those living in low-metal environment (Couture and Pyle,
2008). Except the present study, there is less concern was paid on

Fig. 4. Box-and whisker plots of bioaccumulation factors (A) and biota-sediment accumulation factors (B) in tissues of tilapia for different metals. Bold line in the box is the median,
lower and upper limits of box represent 25th and 75th percentiles; whiskers extend to the range between the maximal and minimal values. Open circles represent outliers, dash
line represent the values equal to 1.
 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325 321

Table 3
Spearman's rank correlation coefficient (r) between metal concentrations in water, sediments, and tissues of tilapia collected from the sampling sites.

Water Sediments

Muscle Gill Liver Kidney GI tract Muscle Gill Liver Kidney GI tract
a a
Hg
0.24
0.34
0.69
0.55
0.28
0.28 0.08
0.35
0.38
0.42
Pb 0.13
0.12
0.42 0.00
0.33 0.06
0.05
0.08 0.43 0.16
Cd
0.50 0.00
0.07
0.18
0.27 0.35
0.09
0.22
0.07 0.23
Cr 0.13
0.26
0.37
0.16
0.30
0.26
0.18
0.03
0.15 0.42a
As
0.21 0.22
0.22
0.47a 0.17 0.47a 0.28 0.19 0.45a 0.00
Cu
0.21 0.03
0.48a
0.29
0.38
0.39
0.33
0.09
0.55b 0.40a
Zn
0.32 0.08
0.34
0.25 0.38 0.30 0.09 0.45a 0.31 0.15
Ni 0.28 0.51b
0.02
0.08
0.25 0.63b 0.38 0.33 0.62b 0.29
a
Correlation is significant at the 0.05 level (2-tailed).
b
Correlation is significant at the 0.01 level (2-tailed).

Table 4
Spearman's rank correlation coefficient (r) between metal concentrations in varied tissues of tilapia in different metals.
a
Paired tissues to be compared

M vs G M vs L M vs K M vs T G vs L G vs K G vs T L vs K L vs T K vs T

Hg 0.52c 0.32 0.30 0.71c 0.33 0.42b 0.33 0.32 0.49b 0.55c
Pb 0.54b 0.53b 0.51
0.11 0.46b 0.58b 0.01 0.58b 0.58b
0.07
Cd 0.29 0.33 0.35 0.33 0.32 0.32 0.27 0.72c 0.29 0.34
Cr 0.53c 0.21 0.35 0.00 0.49b 0.57c
0.08 0.40b 0.46b 0.08
As 0.16 0.28 0.44
0.38 0.15
0.07 0.20 0.43b
0.11
0.23
Cu 0.14 0.24 0.52c 0.06 0.13 0.08
0.06 0.40b 0.49b
0.20
Zn 0.32 0.68c 0.59c
0.11 0.46b 0.03 0.51c 0.60c 0.07
0.35
Ni 0.73c 0.66b 0.73c 0.29 0.58c 0.35 0.04 0.52b 0.64c 0.41
a
M: muscle; G: gill; L: liver; K: kidney; T: GI tract; vs: versus.
b
Correlation is significant at the 0.05 level (2-tailed).
c
Correlation is significant at the 0.01 level (2-tailed).

the relationship between K and MPI of tissues in tilapia. Therefore,
result in this study was compared with linear relationships be-
tween K and the mixtures of relative metal load (ML) in the liter-
ature. De Jonge et al. (2015) analyzed the linear relationships
between accumulated metal mixtures in fish and K, showing
strongly negative relations was found for K and ML in gill, liver, and
kidney. However, no significant relation was observed between
individual K and ML in tissues of liver, kidney, and gill in Gobio gobio
collected from Molse Nete-Grote Nete River, yet a conspicuous
threshold in ML was found above which the K was sharply reducing
(Bervoets and Blust, 2003). Additionally, a negative relation be-
tween K and Ni burden in hepatopancreas of crayfish was deter-
mined by Nakayama et al. (2010). Choongo et al. (2005) indicated
the poor value of K in fish was accompanied with the high Cu level
in muscle of fish. Fish of Anguilla Anguilla collected from Tersakan
Stream, Turkey, were found significantly positive relationship
among metals in muscle and fish age, weight, and length, while the
negative correlation between all metals in muscle and K; the
negative relationship between K and metal concentration in muscle
was perhaps resulted from the relative dilution effect of lipid
content of fish tissues (Kasimoglu, 2014). However, fish allocate
more energy to regulate and mitigate the ambient stress (physio-
logical maintenance and detoxification) resulting in the decrease of
energy storage, i.e. lipid formation (Couture and Pyle, 2008; De
Jonge et al., 2015). Hence, the value of K in fish may decrease
with the elevated metal exposure level.
3.4. Discussion
To assess the human health risk of tilapia consumption, this
study compared metal levels in muscle of the present study with
the regular standards established by different organization or
countries (Table 5). The range of metal concentrations in all muscle
of tilapia was below the permissible limits for human consumption
of international guidelines, except for Pb and Cr. In this study, Pb
concentrations of muscle in three tilapias (11.5%) were higher than
the level of guideline proposed by the European Community (2005)
(0.2 mg g
1 wet wt), as well as Cr concentrations in two tilapias
(7.7%) were around or a little bit greater than the level of limits
recommended by the Hong Kong Government (1987) (1 mg g
1 wet
wt). The range of Pb and Cr concentrations in water and sediments
was 0.23e0.75 and 0.10e0.32 mg L
1 and 13.7e23.7 and
34.8e124.0 mg kg
1, respectively, showing there was no high
concentration was observed in the environment of aquaculture. The
slightly higher Pb and Cr levels in muscle may be associated with
the feeding habits of tilapia which except the fish feed also eat the
debris at the bottom of fishpond, including plankton, benthic or-
ganisms, larval fish detritus, decomposing organic matter, as well as
sediment particles, which may contain considerable metal content
(Zhou and Wong, 2000; Nakayama et al., 2010; Leung et al., 2014).
In addition, mean Pb concentration in muscle of tilapia exceeding
the guideline of European Community was also found in the reports
of Zhou et al. (1998), Liang et al. (1999), Al-Kahtani (2009), Ling
et al. (2013), Leung et al. (2014), Abdel-Khalek et al. (2016). How-
ever, the compared results represented that human consuming the
tilapia that cultured in study area and partly accumulated the
higher Pb and Cr burden is possible to result in the human health
risk.
Table 6 summarizes metal concentrations in muscle of similar
tilapia species denoted from the previous studies. The present re-
sults determined in muscle of tilapia was compared with those
found in tilapia species from Hong Kong (Zhou et al., 1998; Liang
et al., 1999; Cheung et al., 2008), China (Leung et al., 2014),
Malaysia (Taweel et al., 2013; Low et al., 2015), India (Dhanakumar
et al., 2015), Sri Lanka (Allinson et al., 2002), Nigeria (Raphael et al.,
2011), Saudi Arabia (Al-Kahtani, 2009; Abdel-Baki et al., 2011),
322 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325

collected tilapia in above two studies (body weight of 62e236 g in

Lin et al. (2005) and body length of 20 ± 2 cm in Ling et al. (2009))
than that in the present study (body weight of 152e1193 g and
body length of 19e36 cm). Canli and Atli (2003) and Ward et al.
(2010) indicated that the increased body sizes should lower metal
concentrations of fish via somatic growth dilution.
Except for Hg, metal concentrations in tilapia observed in pre-
sent study were generally lower or within the ranges of those found
in the tilapia recorded by previous reports (Zhou et al., 1998; Liang
et al., 1999; Allinson et al., 2002; Cheung et al., 2008; Al-Kahtani,
2009; Leung et al., 2014; Taweel et al., 2013; Low et al., 2015;
Abdel-Khalek et al., 2016). Hsi et al. (2016) reported that methyl-
mercury concentration in tilapia collected from markets in north
Taiwan was close 0.05 mg g
1 wet wt, indicating the concentration
of total Hg ought to be higher than that. Although Hg concentration
in muscle of tilapia was higher than other published studies, the
level was still in the reasonable range.
In order to understand the human health risk for long-term
exposure to metals by consuming tilapia that cultivated in this
studied region, the estimated daily intake (EDI) (mg kg
1 d
1) of
Taiwan population was assessed as the following,

Cb;muscle  DCfish
EDI ¼ ;
BW

where Cb,muscle is the mean metal concentration in muscle of tilapia

Fig. 5. Spearman's rank correlations between Fulton's condition factors (K) and metal
pollution index (MPI) of tissues in tilapia.
Palestine (Elnabris et al., 2013), and Egypt (Rashed, 2001; Abdel-
Khalek et al., 2016). Moisture content of the muscle in tilapia was
77.4 ± 2.0% in this study. In order to compare our data to published
values reported on a dry weight basis, we have converted the latter
to wet weight basis using multiplying a dry/wet ratio of 0.23, which
is the mean ratio of freeze-dried and wet muscle tissues of tilapia in
this study. Metal concentrations in the muscle of tilapia in this
study was in good agreement within the metal levels of tilapia
collected in Taiwan from other studies (Lin et al., 2005; Ling et al.,
2009, 2013). The comparing results indicated that the higher
metal contents of tilapia were found in Ling et al. (2013), which
might be caused by the sampling fishpond was located in the vi-
cinity of an industrial complex. The higher concentrations of Cr, As,
and Zn were also observed in Lin et al. (2005) and Ling et al. (2009)
than that in this study, suggesting that the somatic growth dilution
may be the possible reason. It shown that the smaller body size of
(mg g
1 wet weight), DCfish is the daily fish consumption per capita
weight of the target population (g day
1), and BW is the mean body
weight of population (kg). The hazard quotient (HQ) allowing the
assessment of health risk from tilapia consumption, was evaluated
by dividing the EDI by the established reference dose (RfD). No
obvious risk for human consuming fish is pointed out, when the
value of HQ is not over 1. The RfD of Hg, Cd, As, Zn, and Ni
respectively are 0.3, 1, 0.3, 300, and 20 mg kg
1 d
1, those are
adopted from USA risk-based concentration table (USEPA, 2016),
and the doses of Cr and Cu are respectively 5 and 40 mg kg
1 d
1 is
referred from USEPA (2003) and Gu et al. (2015). For Pb, the pro-
visional tolerable weekly intake (PTWI) of 25 mg kg
1 had been
established from WHO in 1999; however, it has been withdraw,
because it has been confirmed the PTWI of Pb could no longer be a
safe dose for human intake (WHO, 2011). Therefore, the hazard
quotient of Pb was not assessed in this study.
Based on the Taiwan National Food Consumption Database, the
mean body weights for adult male and female aged 19e65 years are
69.3 and 57.3 kg, respectively. The estimates for HQ of metals for
adult male and female based on the fish and their products con-
sumption are given in Table 7. None of estimated HQ was greater
than 1, indicating that there was no adverse health effect is likely to
occur for consumption of tilapia whatever for adult male or female.
The highest mean value of HQ was observed for Hg (0.229) while
the lowest was for Cu (0.014). The difference of HQ among male and
female was not significant, but the health risk for female still slight
higher than that for male. Therefore, results of health risk

Table 5
The guidelines of fish in different countries (mg g
1 wet wt).

Organization/country Hg Pb Cd Cr As Cu Zn Reference

Taiwan 0.01e0.26 NDe0.55 NDe0.02 0.11e1.07 NDe0.05 0.16e1.55 1.03e15.3 Present study
Taiwan 0.3 0.3 Ministry of Health and Welfare (2013)
China 0.5 0.1 2.0 0.5 China National Standards Management Department (2001)
Hong Kong 0.5 6 2 1 2.3 Hong Kong Government (1987)
USEPA 0.4 4 1.2 USEPA (2000)
EC 0.5 0.2 0.05 European Community (2005)
ANZFA 1 0.5 2 Australia New Zealand Food Authority (1999)
England 0.3 2.0 20 50 MAFF (2000)
 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325 323

Table 6
Comparison of mean metal concentration (mg g
1 wet wt) in the muscle of tilapia in present study with other studies.

Region Species Hg Pb Cd Cr As Cu Zn Ni Reference

Taiwan Oreochromis spp. 0.05 0.16 0.01 0.39 0.02 0.40 5.38 0.25 Present study
Taiwan Oreochromis niloticusa 0.49 0.01 2.27 1.18 2.37 39.7 2.32 Ling et al. (2013)
Taiwan Oreochromis niloticusa 0.04 0.26 0.08 0.32 11.59 0.86 Ling et al. (2009)
0.51 0.41 0.29 0.92 11.65 0.10
0.08 0.16 0.23 0.35 12.80 0.20
Taiwan Oreochromis mossambicus 0.18 0.01 0.60 0.32 1.34 10.78 0.14 Lin et al. (2005)
Hong Kong Oreochromis mossambicus 0.02 2.15 0.71 0.27 2.24 Cheung et al. (2008)
0.01 2.42 0.25 1.57 0.78
0.03 4.73 1.57 2.63 0.42
0.01 7.74 0.43 0.10 1.29
0.02 0.55 0.08 0.22 1.84
0.07 0.29 0.09 0.15 0.65 0.19 8.61 0.13
Hong Kong Tilapia 1.68 0.15 0.29 6.37 19.3 0.63 Liang et al. (1999)
Hong Kong Tilapia mossambica 0.29 0.10 0.10 0.40 4.26 0.13 Zhou et al. (1998)
0.39 0.10 0.09 0.50 4.68 0.16
0.30 0.08 0.07 0.44 5.87 0.14
China Oreochromis mossambicus 8.62 0.03 0.51 0.03 1.38 29.5 3.50 Leung et al. (2014)
Malaysia Oreochromis spp. 0.0081 0.011 0.05 1.07 0.27 4.0 Low et al. (2015)
0.0067 0.010 0.019 0.91 0.21 3.8
0.0049 0.020 0.020 0.41 0.16 3.5
Malaysia Oreochromis niloticus 0.087 0.009 0.39 5.37 0.81 Taweel et al. (2013)
0.060 0.007 0.34 4.73 0.83
0.227 0.012 0.26 6.01 0.80
0.122 0.009 0.23 5.57 0.89
India Oreochromis mossambicus 0.097 0.28 0.01 2.88 0.06 Dhanakumar et al. (2015)
Sri Lanka Oreochromis mossambicus 0.04 0.03 0.22 0.61 4.09 Allinson et al. (2002)
Nigeria Tilapia nilotica <0.01 0.14 0.01 0.04 Raphael et al. (2011)
Saudi Arabia Tilapia nilotica 0.009 0.002 0.05 0.25 Abdel-Baki et al. (2011)
Saudi Arabia Oreochromis niloticus 0.34 0.064 0.57 4.98 Al-Kahtani (2009)
Palestine Oreochromis niloticus 0.12 0.64 7.52 0.89 Elnabris et al. (2013)
Egypt Oreochromis niloticus 0.05 0.007 0.49 1.26 Abdel-Khalek et al. (2016)
0.22 0.058 1.04 3.19
0.27 0.074 1.74 15.50
0.23 0.081 1.47 3.08
Egypt Tilapia nilotica 0.018 0.06 0.145 0.014 Rashed (2001)
a
Dorsal muscle with skin.

Table 7 values and specific populations, such as recreational and subsis-

Human health risk of tilapia consumption for male and female population in Taiwan. tence fishermen, residents in the vicinity of fishpond, and seafood-
Parametera Male Female loving people (Sapkota et al., 2008). For instance, people who have
a high consumption rate (the maximal values of 896 g d
1 for adult
Age (years) 19e65 19e65
Body weight (kg) 69.3 ± 11.1 57.3 ± 9.8 female, adopted from http://intakes.nhri.org.tw/food-intake-data/)
Fish and their products consumption (g d
1) 96.14 ± 144.92 81.83 ± 121.38 may post a potential health risk (HQ could be exceeded 2.5). In
Hazard quotient (
) addition, metal concentrations of muscle for tilapia depend on
Hg 0.222 0.229
different factors, including the body size, age, and growth rate of
Cd 0.016 0.017
Cr 0.107 0.110
fish, metal levels in its living environment, feed habits, and sam-
As 0.075 0.077 pling season (Allinson et al., 2002; Ling et al., 2013; Saha et al.,
Cu 0.014 0.014 2016). It could not be ignored that the health risk for consump-
Zn 0.025 0.026 tion tilapia under different scenarios.
Ni 0.018 0.018
Furthermore, the sample size of tilapia in the present study
a
Adopted from http://intakes.nhri.org.tw/food-intake-data/. could be a limitation for clearly comprehending the effect of the
distance to naphtha cracker plant on the bioaccumulation and
distribution of metals in tilapia, because only two tilapias were
sampled in Sampling Site 4. However, according to the result of
assessment implied that no deleterious effect on adult population correlation analysis, the bioaccumulation of metals in tilapia was
(19e65 years) consuming tilapia that cultured in the area studied. not associated with the distance to the industrial area, whereas
Furthermore, the cumulative health risk raised by summing the HQ relatively related with the surrounding metal content. For the other
of 7 metals to consider human exposure to mixture metals via main objective in this study, the estimate of human health risk
tilapia consuming. Result showed that the total HQ was also less assessment was based on the mean metal concentration in tilapia
than 1, with 0.477 for male and 0.491 for female, emphasizing the that calculated by total 26 sampled fish. Comparing with other
tilapia might be quite safety seafood for consumption entire life- studies listed in Table 6, the sample size of these studies in the
time. Consequently, tilapia cultured in the southwest coast of range of 9e20 was lower than that of 26 except Lin et al. (2005),
Taiwan was found to be low-risk for consumption and do not sur- Leung et al. (2014), and Rashed (2001). We believe that the sam-
face a potential threat to the health of general human consumers. ple size of tilapia in this study is enough to provide a scientific
However, the health risk assessment in the present study was based based tool for assessing the human health risk.
on the average values of consumption rate and metal concentra-
tions of muscle, yet it was not taken into account the extreme
324 Y.-R. Ju et al. / International Biodeterioration & Biodegradation 124 (2017) 314e325
4. Conclusions
A comprehensive analysis of metals in the water, sediments, and
cultured organisms (tilapia) in the aquaculture pond located along
the area of southwestern Taiwan was carried out to realize the
metal bioaccumulation in important commercial fish and the hu-
man health risk for consumers. However, no significant trend of
accumulated metals with respect to the distance to naphtha cracker
plant could be observed. Metal concentrations in tilapia were most
strongly accumulated in kidney, except for Cu accumulated in liver.
In contrast, the lower metal concentrations were found in muscle of
tilapia. Not surprisingly, the highest estimate of MPI in the present
work was found in kidney. Based on the values of BCF and BSAF, it
may be displayed that the tendency of tilapia to easily accumulate
Cr and Zn from water and Hg and Cd from sediments. Except for Hg,
positive correlations between metal levels in liver and kidney were
confirmed. Fulton's condition factor turned out to be a usable
reference to the adverse effect of accumulated metal-mixtures in
tilapia, and was significantly related to metals levels of kidney, liver,
and muscle. Metal concentrations of Pb and Cr in muscle were
exceeded the limits proposed by the European Community and the
Hong Kong Government, respectively. Results of health risk
assessment implied negligible deleterious effect on adult popula-
tion consuming tilapia cultured in the area studied (total HQ for all
analyzed metals were less than 1). This studied region plays an
important role in aquaculture industry, hence the strict monitoring
must be implemented to control the contents of heavy metal in
fishpond water to decrease the human health risk that caused by
consuming cultured fish.
Conflict of interest
The authors declare that there are no conflicts of interest.
Acknowledgements
The authors wish to express the gratitude to the members of the
Center for the Study of Sediments, National Kaohsiung Marine
University for their assistance.
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