Food Sci. Biotechnol.

24(1): 373-378 (2015)

DOI 10.1007/s10068-015-0049-4

RESEARCH ARTICLE

Determination of Toxic Heavy Metal Levels in Commonly Consumed

Species of Shrimp and Shellfish Using ICP-MS/OES
Girum Habte, Ji Yeon Choi, Eun Yeong Nho, Sang Yeol Oh, Naeem Khan, Hoon Choi, Kyung Su Park, and
Kyong Su Kim

Received May 6, 2014; revised July 25, 2014; accepted July 27, 2014; published online February 28, 2015
KoSFoST and Springer 2015

Abstract Toxic metal concentrations, including lead (Pb),

cadmium (Cd), aluminum (Al), mercury (Hg), and arsenic
(As) in edible tissues of different species of shrimp and
shellfish consumed in South Korea were analyzed. Analysis
was performed using inductively coupled plasma (ICP)MS) for Pb, Cd and As, ICP-optical emission spectrometry
(OES) for Al, and a direct mercury analyzer for Hg.
Methods used were validated. Limited variation in heavy
metal concentrations between shrimp and shellfish were
observed. Al and As concentrations were highest while Hg
was lowest. Heavy metal levels found in edible tissues of
shellfish and shrimp were below international and local
maximum permissible levels for human consumption. The
methods used were accurate and reproducible for use in
determination of toxic heavy metal levels in seafoods.
Keywords: heavy metal, seafood, accumulation, inductively
coupled plasma-MS and inductively coupled plasmaoptical emission spectrometry, South Korea

Introduction
The marine and, more particularly, the aquatic system are
Girum Habte, Ji Yeon Choi, Eun Yeong Nho, Sang Yeol Oh, Naeem Khan,
Kyong Su Kim (
)
Department of Food and Nutrition, Chosun University, Gwangju 501-759,
Korea
Tel: +82-62-230-7724; Fax: +82-62-224-8880
E-mail: kskim@chosun.ac.kr
Hoon Choi
Food Contaminants Division, Food Safety Evaluation, Ministry of Food &
Drug Safety, Cheongwon, Korea
Kyung Su Park
Korea Institute of Science & Technology, Seoul, Korea

the ultimate repository of many types of industrial,

agricultural, municipal, domestic, and nuclear wastes (1).
These pollutants cause undesirable changes in the physicochemical and biological factors of the aquatic ecosystem
(2). Pollution by heavy metals in aquatic environments has
become a concern because of toxicity and persistence in
the environment for decades (3). Many heavy metals
discharged as waste can bioaccumulate in tissues of
resident fish, oysters, crabs, shrimp, seaweed, and shellfish
(4,5). The extent of contamination has increased markedly
in the last 50 years due to technological developments and
increased consumer use of materials containing metals (6).
Aquatic organisms are sensitive to heavy metals in
water, feed, and sediment. This is especially so in the case
of shellfish, crabs, and shrimp because invertebrates tend to
accumulate more heavy metals than fish as a result of
differences in evolutionary phylum specific coping strategies
(7).
Increased levels of arsenic (As), cadmium (Cd), and lead
(Pb) in foods constitute a food safety risk. Ingestion of As
can induce peripheral vascular and skin diseases, such as
hyperkerotosis (8). Intake of Pb can cause damage to the
central and peripheral nervous system and memory
deterioration (9). Both Cd and Pb can cause kidney
damage (10) and long-term exposure to Cd may cause
skeletal damage, which may result in fractures (11).
Aluminum compounds have a potential to affect the
reproductive system (12).
An accurate, precise, and robust analytical method is
required for measurement of heavy metal levels in foodstuffs
to ensure maximum product safety and sustainability. Both
inductively coupled plasma (ICP)-MS and optical emission
spectrometry ICP-OES efficiently address these requirements.
Both methods were used to determine levels of toxic heavy
metals in this study with a high throughput using a plasma-

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Habte et al.

based technique with a single high-energy excitation

source providing precise determination of heavy metal
levels in foods. Trace elements can be identified in a wide
range of matrices from parts per trillion (ppt) to low
percentage levels. A direct mercury analyzer, which was
used to determine mercury levels in this study, is also one
of the best available analytical instruments for mercury
analysis in foods over a number of matrices. Therefore, the
analytical instruments used in this study were up to date
and reliable.
The Korean Peninsula is surrounded by the East, West,
and South Seas, with a coastline that extends for approximately
2,413 km. Endowed with an abundance of marine resources,
Koreans have developed a distinct seafood culture with an
annual per capita seafood consumption of 54.7 kg in 2010
(13). However, considering the growing consumption rate
of seafood, much has yet to be done to make sure that the
safety of seafood is not compromised by heavy metal
pollution in crustaceans and shellfish in coastal regions.
Hence, it is important to investigate the levels of toxic
heavy metals in seafood to assess whether concentrations
are within permissible levels so as not to pose any hazard
to consumers. In this study, concentrations of the toxic
metals (Pb, Cd, Al, Hg, and As) were determined in the
edible tissues of 3 commonly available shrimp species and
3 shellfish species that have great economic and ecological
importance.

Materials and Methods

Collection and sampling procedures A total of 325
samples of 3 shrimp species (Acetes japonicas, Fenneropenaeus chinensis, and Metapenaeus joyneri) and 131
samples of 3 shellfish species (Cipangopaludina japonica,
Corbicula leana, and Anodonta Woodiana) were collected
from supermarkets all over Korea (Table 1) from February
to June, 2012. Samples were placed into sterile bags by
species, kept on ice to maintain a temperature of
approximately 4-5oC, and delivered to the food analysis
laboratory on the same day. Samples were then washed
thoroughly with deionized water, dried on filter paper, and
kept at 20oC in a refrigerator (MICOM CED-0622;

Samsung, Seoul, Korea) until heavy metal analysis.

Preparation of shrimp and shellfish for heavy metal
analysis Frozen shrimp and shellfish samples were thawed
at room temperature and dissected using high-quality
stainless steel scalpels. Edible tissues were collected from
each sample for analysis. All tissue weights, which was
taken by analytical balance (ML204 Analytical Balance;
Mettler-Toledo, Columbus, OH, USA), were expressed as
fresh weights. In all experiments several blanks were included
with reagents, concentrated HNO3 (68%) and H2O2 (32%)
(Dong Woo Fine-Chem Co., Ltd., Iksan, Korea), in order
to check for contamination. All glassware used for heavy
metal analysis was washed with detergent, rinsed in
distilled water, soaked in 5% nitric acid for more than 24 h,
rinsed with deionized water, and allowed to air-dry at room
temperature before use.
Determination of heavy metal levels A slightly modified
version of the method used by Khan et al. (14) was used.
In brief, samples (approximately 1 g of wet tissue) were
placed in 300 mm long Pyrex glass digestion tubes (Foss,
Eden Prairie, MN, USA). Samples were digested using
25 mL of concentrated HNO3 (68%), and 2.0 mL of H2O2
(32%) as a catalyst, and a heating block (Smart Digest 40/
20; Mandel Scientific Company Inc., Ontario, Canada).
The temperature was increased gradually from 50 up to
160oC. Digestion was completed in 12 h, as indicated by
the appearance of approximately 5-7 mL of a colorless
watery solution. After the mixture was left to cool to room
temperature, it was transferred to 50 mL polypropylene
tubes and diluted to 25.0 mL using ultrapure deionized
water. Reagent blanks were processed simultaneously in
triplicate. All digested samples were analyzed in triplicate
to quantify amounts of Pb, Cd, Al, and As. A quadrupole
Elan DRC II (Perkin-Elmer SCIEX, Shelton, CT, USA)
inductively coupled plasma mass spectrometer (ICP-MS)
was used for Pb, Cd, and As analysis. The instrumental
conditions are presented in Table 2. A Model 730-ES
simultaneous CCD ICP-OES (Varian, Wyndmoor, PA,
USA) was used for Al analysis because aluminum is
usually found in higher concentrations than the other
metals under study, which are usually present in trace

Table 1. Information for samples analyzed

Sample

Common name

Scientific name

Sample number

Shrimp

Akiami paste shrimp

Fleshy prawn
Shiba shrimp

Acetes japonicus
Fenneropenaeus chinensis
Metapenaeus joyneri

78
161
86

Shellfish

Japanese mystery snail

Corbicula clam
Chinese pond mussel

Cipangopaludina japonica
Corbicula leana
Anodonta woodiana

71
52
8

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Determination of Toxic Heavy Metals in Commonly

Table 2. ICP-MS operating conditions and measurement
parameters
Spectrometer
Spray chamber
Nebulizer
RF power (kW)
Torch horizontal alignment
(mm)
Torch vertical alignment (mm)
Scanning mode
No. of replicates per sample
Ar gas flow rates (L/min)
Plasma
Auxiliary
Nebulizer
Dwell time (ms)
Sweeps/reading
Lens voltage (V)
Sample uptake rate (mL/min)
Isotopes

Elan 6100 DRC II (SCIEX;

Perkin-Elmer Norwalk, CT, USA)
Cyclonic
Meinhard
1.35
0.5-1.0
0.2-0.5
Peak hopping
3
16
1-1.3
1.0-1.07
50
20
6.25
0.24
208
Pb, 112Cd, 75As

amounts. Hence, Al was more suitable for analysis using

ICP-OES than ICP-MS. The experimental conditions are
listed in Table 3.
To avoid interference from mercury chloride, a Gold
Amalgation-Direct Mercury Analyzer (NIC MA2; Mercury
Instrument, Seattle, WA, USA) was used for Hg analysis.
The method of Chen and Chen (15) was used for this
study. In brief, approximately 50 mg of fresh sample was
placed in a sample boat and heated for 4 min at 350oC. The
sample was heated again for 4 min at 850oC to vaporize
mercury, which was collected in a gold amalgation tube.
The tube was then heated to release mercury to an atomic
absorption spectrophotometer. The experimental conditions
used were a wavelength 253.65 nm, an interface filter of
254 nm, a Silicon UV photodetector, platinum as a catalyst,
purging for 60 s, amalgamation for 12 s, and recording for
30 s. In all cases, each sample was analyzed in triplicate.
All values were expressed as g/g of the wet weight of
tissue. Instruments were calibrated from 10 mg/L multielement standard solution obtained commercially (Merck,
Darmstadt, Germany). The standard addition method of
spiking samples with known amounts of standard solutions
was followed to determine recovery rates (14). Instrumental
detection and quantification limits were also determined.
Analytical blanks were run in the same manner as samples,
and concentrations were determined using standard solutions
prepared with the same reagent (HNO3, 68%) used by the
sample. Analytical quality was checked based on analysis
of a standard reference material [SRM 1566 b-oyster
tissue; National Institute of Standards and Technology
(NIST), Gaithersburg, MD, USA]. The reagents mentioned

Table 3. ICP-OES operating conditions and measurement

parameters
Spectrometer
RF power (kW)
Nebulizer
RF generator
Argon gas flow (L/min)
Plasma
Auxiliary
Nebulizer
Spray chamber
Plasma viewing
Processing mode
Read delay (s)
Rinse (s)
Replicates
Element, wavelengths (nm)

ICP-OES (730-ES simultaneous

CCD;Varian, Paloalto, CA, USA)
1.3
SeaSpray
27.12 MHz
16
1.5
0.94
Cyclonic
Axial
Area
30
30
3
27
Al (308)

above were of analytical grade, and deionized water was

used throughout the study.
Statistical analysis Data were subjected to an analysis of
variance (ANOVA) using Statistical Package for Social
Sciences (SPSS version 9.0, IBM, Armonk, NY, USA)
software to identify significant differences in heavy metal
concentrations between shrimp and shellfish, between
species, and between organs. Statistical significance was
assessed using Duncans multiple range test (DMRT) at
p<0.05. The coefficient of variation (CV) was calculated to
assess dispersion of data. Coefficient of determination (r2)
values was calculated in order to assess correlations
between data.

Results and Discussion

Analytical quality checking showed good results. Instrumental
detection and quantification limits (LOD and LOQ), spiking
recovery values, and r2 values are presented in Table 4.
Mean recovery values were 94.73% and coefficient of
variation values (CV) were <4. Recovery results for the
Oyster Tissue certified reference material (SRM 1566-b;
NIST) indicated good agreement between the certified and
analytical values. Recovery rates were 103.89, 101.21,
94.73, 97.30, and 96.99% for Pb, Cd, Al, Hg, and As,
respectively (Table 5).
Knowledge of heavy metal concentrations in seafood is
important with respect to human health for assessment of
whether heavy metal levels are within maximum permissible
international and local limits. Levels of, Pb, Cd, Al, Hg,
and As in edible tissues of A. japonicas, F. chinensis M.
joyneri, C. japonica, C. leana, and A. woodiana are shown

376

Habte et al.

Table 4. Method validation results obtained using a pure reference standard

ICP-MS

Pb
Cd
As
Al
Hg

ICP-OES
DMA

LOD (g/g)

LOQ (g/g)

0.0024
0.0012
0.0028
0.0040
0.0021

0.0072
0.0037
0.0084
0.0121
0.0063

Shrimp

Shellfish

Recovery (%)

CV

Recovery (%)1)

CV2)

96.86
102.40
97.40
98.40
100.50

3.54
2.77
3.09
3.51
2.44

97.06
98.10
97.20
99.20
101.00

3.26
3.01
3.35
3.38
2.85

r2
0.9994
0.9997
0.9995
0.9995
0.9998

1)

Recovery result for spiking (mean value of 5 determinations)

Coefficient of variation, n=5

2)

Table 5. Concentrations of metals found in Standard Reference Material (SRM 1566 b-oyster tissue) obtained from the National
Institute of Science and Technology in USA
(unit: g/g of dry wt)
Value
Certified
Observed
SD
Recovery (%)

Pb
1)

00.308
0.320
0.010
103.89%

Cd

Al

Hg

As

2.480
2.510
0.059
101.21%

197.2
186.8
2.249
94.73%

0.037
0.036
0.002
97.30%

7.650
7.420
0.119
96.99%

1)

Each value is the mean of 5 determinations.

Table 6. Concentrations of heavy metals found in different species of shrimp and shellfish
Species
Shrimp
Acetes japonicas
Fenneropenaeus chinensis
Metapenaeus joyneri
Shellfish
Cipangopaludina japonica
Corbicula leana
Anodonta woodiana

Pb

(unit: g/g)

Cd

Al

Hg

As

0.0540.093ab1)
0.0390.076a
0.4520.895

0.1560.317a
0.0130.021b
0.0340.088c

15.72220.993a
19.92711.427a
28.84620.635b

0.0100.005
0.0030.003a
0.0070.006b

1.1201.567a
0.9971.076a
3.5592.961 b

0.0610.062b
0.2460.132c
0.1950.100c

0.0100.012b
0.2560.248
0.0240.020c

53.06634.704c
270.106141.025
42.91929.935bc

0.0020.003c
0.0050.007a
0.0520.006e

0.0950.214c
1.6860.345
3.5451.070b

1)

Mean values followed by the same superscript letters within columns are not significantly different (p>0.05).

in Table 6. Mean concentrations of Al (270.106 g/g) in C.

leana and As (3.559, 3.545 g/g) in M. joyneri and A.
woodiana, respectively, were considerably higher, compared
with other metals. Hg exhibited the lowest level of heavy
metal accumulation in edible tissues of both species,
followed by Cd, except for A. japonicas and C. leana,
where Pb exhibited the second lowest mean concentration.
However, a significantly (p<0.05) higher mean concentration
of Al (270.106 g/g) in C. leana, compared with other
species under this study, was a worrying result as frequent
exposure to high concentrations of Al can affect the
reproductive system. However, there are currently no
international or local allowable levels for consumption of
Al.
The mean concentrations of Pb, Cd, Al, Hg, and As in
edible tissues were in the ranges of 0.007-2.969, 0.0010.589, 3.236-77.149, 0.002-0.017, and 0.085-7.458 g/g of
the wet weight of shrimp, and 0.044-0.570, 0.030-0.448,
18.907-290.035, 0.016-0.040, and 1.135-3.061 g/g of the
wet weight of shellfish, respectively. In general, the order

of mean concentrations of metals analyzed in A. japonicus

was Al>As>Cd>Pb>Hg. In F. chinensis, the mean metal
concentration decreased in the order of Al>As>Pb>Cd
>Hg. The mean metal concentration in tissues of M.
joyneri followed the same order as for F. chinensis. The
order of mean concentration of metals in tissues of C.
japonica was also similar to F. chinensis. The amount of
As in tissues of C. japonica was found lower than the As
amounts found in all other shrimp and shellfish species. In
C. leana and A. woodiana, the orders of the mean metal
concentrations were Al>As>Cd>Pb>Hg and Al>As>Pb>
Hg>Cd, respectively. The highest mean concentration of
Hg was observed in A. woodiana. Several possible
explanations can account for variations in metal
accumulations in tissues. Metabolic rates of organisms,
exposure routes, metal mobility values, bioavailability,
chelators present in water, and time spent in contaminated
water are among important contributing factors (16-19). In
addition, the environmental factors of pH, temperature,
salinity, nutrients, organic matter, organic carbon, and

377

Determination of Toxic Heavy Metals in Commonly

conditions of an ecosystem all influence the bioavailability

and bioaccumulation rates of metals (20).
Lower concentrations of metals in muscle tissue are
important because muscle constitutes the greatest mass of
both shrimp and shellfish tissue that is consumed. There
was no significant (p>0.05) difference in tissue metal
accumulation amounts between shrimp and shellfish.
There were also no significant (p>0.05) differences in the
amounts of metal accumulation between shrimp species.
Similarly, no significant (p>0.05) differences were observed
in the amounts of metal accumulation between shellfish
species. Based on mean concentrations of toxic heavy
metals obtained in this study and levels reported by Food
and Agriculture Organization of the United Nations (21),
Commission Regulation (22), and the local Korean Food
and Drug Safety (23) maximum permissible standards,
seafoods tested in this study were safe for consumers.
For an assessment of health risks of subject seefoods in
conjunction with consumer intake levels, the results of this
study were compared with the current provisional tolerable
weekly intakes (PTWI) for As, Cd, Hg, and Pb established
by the Food and Agriculture Organization of the United
Nations/World Health Organization (FAO/WHO) (24). All
analyses were carried out for total arsenic (organic and
inorganic). However, most As found in fish and shellfish is
organic As, which is a less toxic form. The percentage of
inorganic As in fish and shellfish has been reported to be
between 0.02 and 11% (25), whereas the maximum
acceptable daily load for As set by the WHO in 1967 and
revised in 1989 was 3,000 g for a 60 kg person (26). The
intake levels of the general Korean population, according
to a Korean National Health and Nutrition Examination
Survey (27), were 3,200 g/day of shellfish and 1,700 g/
day of crustaceans. Therefore, the mean concentration of
As found in the edible tissue of subject seefoods would not
be of concern for consumers.
Provisional tolerable monthly intake (PTMI) value for
Cd is 25 g/kg of body weight, for Pb previously established
PTWI was 25 g/kg body weight (withdrawn in 2010 and
still new PTWI value is not established), and the previous
PTWI value for total Hg (5 g/kg of body weight) is
currently substituted by inorganic Hg which is 4 g/kg of
body weight (24). Based on daily food intake values for
shellfish and crustaceans in the population of South Korea,
the above provisional tolerable intakes compared with
results for mean concentrations in edible tissues of subject
seafoods under this study, it can be said that there is no risk
for consumers.
Valuable information on the toxic metal concentrations
in shrimp (A. japonicas, F. chinensis, and M. joyneri) and
shellfish (C. japonica, C. leana, and A. woodiana) obtained
from South Korean markets is herein presented. Although
the concentrations of metals in edible tissue of shrimp and

shellfish were below levels of concern published by

international (Food and Agriculture Organization of the
United Nations and Commission Regulation) and local
(Korean Food and Drug Safety) standards, results of this
study demonstrated biomagnification of Al, As, and other
metals in the studied seafoods from coastal areas of South
Korean. Continuous care must be taken to monitor heavy
metal levels in seafood products. The analytical methods
and instruments used in this study were suitable based on
accuracy and reproducibility to determine levels of toxic
heavy metals in seafoods.
Acknowledgments This research was supported by a
grant (12162MFDS014) from the Ministry of Food and
Drug Safety in 2012, Korea.
Disclosure The authors declare no conflict of interest.

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