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Toxic metals in commercial marine fish in

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 Chemosphere 85 (2011) 6773

Contents lists available at ScienceDirect

Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Toxic metals in commercial marine sh in Oman with reference to national

and international standards
M. Al-Busaidi, P. Yesudhason , S. Al-Mughairi, W.A.K. Al-Rahbi, K.S. Al-Harthy, N.A. Al-Mazrooei,
S.H. Al-Habsi
Fishery Quality Control Center, Ministry of Agriculture and Fisheries Wealth, Post Box 427, Postal Code 100, Muscat, Oman

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

Article history: Commercially important fresh (581) and frozen (292) marine sh samples of 10 species were collected
Received 16 February 2011 from seafood factories and evaluated using AAS and ICPOES. Metal levels signicantly (p < 0.05) varied
Received in revised form 5 May 2011 within and between species. However, there were no signicant correlations among metals. There were
Accepted 27 May 2011
signicant interspecic differences for all metals, and yellown tuna had the highest level of cadmium
Available online 22 June 2011
and mercury however, red seabream had maximum numbers above the standards. The metal accumula-
tion signicantly varied between bottom feeders of intermediately size locally caught sh. The mean cad-
Keywords:
mium level ranged from 0.0049 to 0.036 mg kg 1 and 1.37% of the total samples exceeded the EU and FAO
Mercury
Cadmium
standards. Mean lead content varied between 0.029 and 0.196 mg kg 1, few samples crossed the EU
Lead (2.63%) and FAO (1.6%) limits. Mean mercury level ranged from 0.015 to 0.101 mg kg 1 and none of
Seafood the samples exceeded the EU limit. Of the total samples analyzed red seabream (2.06%), yellown tuna
Oman (1.14%), emperor (0.34%), santer bream (0.22%), king sh (0.11%) and skipjack tuna (0.11%) samples
crossed the EU limits. In general, sh from these regions are within the safety levels recommended by
various organizations and do not pose a health risk in terms of human diet.
2011 Elsevier Ltd. All rights reserved.

1. Introduction
Fish consumption is recommended due to all its nutritional and
therapeutic benets. The benets of sh are mainly due to the con-
tent of high quality protein, high content of two kinds of omega 3
poly unsaturated fatty acids: eicosapentaenoic acid (EPA) and
docosahexaenoic acid (DHA) and other nutrients (Castro-Gonzalez,
2002; Clarkson, 2002; Dominogo et al., 2007). Omega 3 fatty acids
(EPA) have protective effects in preventing coronary heart disease,
reducing arrhythmias and thrombosis (Kinsella et al., 1990; Oomen
et al., 2000; Kris-Etherton et al., 2002), lowering plasma triglycer-
ide levels (Harris, 1997; Ismail, 2005) and reducing blood clotting
tendency (Agree et al., 1997; Din et al., 2004; Ismail, 2005). Intake
of sh has shown benets in other diseases such as rheumatoid
arthritis (Cleland et al., 2003; Rahman et al., 2008) and psychiatric
disorders (Cherubini et al., 2007; Song and Zhao, 2007). The Amer-
ican Heart Association suggests, eating sh at least two times per
week in order to reach the daily intake of omega 3 fatty acids rec-
ommended for healthy adults with no history of heart disease
(Kris-Etherton et al., 2002).
Corresponding author. Tel.: +968 24743528; fax: +968 24738222.
E-mail address: yesucift@rediffmail.com (P. Yesudhason).
However, the one potential risk of dietary sh eating is its con-
tent of heavy metals in some sh, which affects the health of peo-
ple consuming large quantities (Stern, 1993; Hites et al., 2004).
Recent evidence suggests that toxic heavy metals, high mercury
content in sh may counteract the cardio protective effect of sh
intake and to damage developing fetuses and young children
(Guallar et al., 2002; Yoshizawa et al., 2002; Chan and Egeland,
2004; NRC, 2000). Mercury poisoning in the adult brain is charac-
terized by damage of discrete visual cortex areas and neuronal loss
in the cerebellum granule layer (Vettori et al., 2003) on the other
hand, mercury poisoning during nervous system development
may cause catastrophic consequences for infants who exhibit wide
spread neural impairment (Harada et al., 1994). In humans, cad-
mium, lead and/or arsenic, have also been associated to serious
health effects on adults and children, and one source of exposition
is the intake of sh with high content of either of these metals. This
has been demonstrated by several authors; Abernathy et al. (2003),
Burger and Gochfeld (2005), Andreji et al. (2006), Falco et al. (2006)
and Has-Schon et al. (2006). Cadmium is known to accumulate in
the human kidney for a relatively long time, from 20 to 30 years,
and at high doses, is also known to produce health effects on the
respiratory system, induce the renal and hepatic toxicity and has
been associated with bone disease (Novelli et al., 1998; Dahiya
et al., 2005), poor reproductive capacity, hyper tensions, tumors
and hepatic disfunction (Waalkes, 2000). In humans, lead has a

0045-6535/$ - see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.chemosphere.2011.05.057
68 M. Al-Busaidi et al. / Chemosphere 85 (2011) 6773

half-life of approximately 20 d in blood and 6003000 d in bone 2. Materials and methods

(Harrison and Laxen, 1981). Lead affects mainly the central
nervous system, kidney and blood. At 40 lg/100 mL of lead in
blood, symptoms of lead poisoning are manifested. For children,
the limit is lower. Prolonged exposure will result in coma, mental
retardation and even death (Ratcliffe, 1981). An important bio-
chemical effect of lead on the hematopoietic system is its inhibi-
tion of the biosynthesis of heme. Lead binds strongly to the
sulfhydryl functional group in d-aminolevulinic acid dehydrase
(ALAD) which is a key enzyme in the formation of heme. ALAD cat-
alyzes the condensation of two molecules of ALA to form a mole-
cule of porphobilinogen (PBG). Inhibition of ALAD occurs at blood
lead concentrations of 1020 lg/100 mL. Lead also inhibits heme
synthetase which is involved in the incorporation of Fe2+ into the
protoporphyrin. This results in elevated metal-free erythrocyte
prophyrin (Harrison and Laxen, 1981).
The lead, cadmium and mercury, have been included in the
regulations of the European Union for hazardous metals (EC,
2001), while the USFDA has included a further three metals chro-
mium, arsenic and nickel in the list (USFDA, 1993). In many coun-
tries, signicant alterations in industrial development lead to an
increased discharge of chemical efuents into the ecosystem,
leading to damage of marine habitats. Heavy metal discharged
into the marine environment can damage both marine species
diversity and ecosystems due to their toxicity and accumulative
behavior (Matta et al., 1999; Gumgum et al., 1994). Sea of Oman,
which is neither deep nor extensively tidal, is being increasingly
surrounded by industrial and urban developments, numerous
ships move from port to port, and such human activities could
easily lead to efuent discharges reaching the sea with unaccept-
able levels of heavy metals. For these reasons, it is important to
determine the concentrations of heavy metals in commercial sh
in order to evaluate the possible risk of sh consumption for hu-
man health, and it often becomes mandatory to check chemical
contaminants in foods from the aquatic environment to under-
stand their hazard levels. In addition, it is very important to have
reliable database on contaminant levels in commonly available
commercial sh for elucidating the present status of heavy metal
contamination.
Therefore, this study aims to take accumulation of selected hea-
vy metals Hg, Cd and Pb concentrations in the edible portion of
fresh and frozen sh collected from different seafood processing
factories in Sultanate of Oman, and imported during 20072009,
in order to evaluate the hazard level in relation to national and
international standards.
2.1. Sample collection
During the period from January 2007 to December 2009, com-
monly available commercial importance fresh and frozen sh sam-
ples (Table 1) were collected from seafood processing units in
Sultanate of Oman and imported from different countries. The
samples were placed in cool box with ice and transported to the
laboratory and then stored at 20 C until further analysis. Pooled
edible portion of the meat was used for extraction of heavy metals.
2.2. Chemicals
High purity, deionized water puried with a MilliQ water puri-
cation system (MilliQ, Millipore, USA) was used for preparation of
reagents and standards. High quality concentrated (65% W/v) nitric
acid (Merck, Darmstadt, Germany) and 35% (W/v) hydrogen perox-
ide (Riedel-de Haen, Seelze, Germany) were used. The standard
solutions for calibration were prepared from a stock solution of
1000 mg L 1 by successive dilutions with 1.5% nitric acid. The stan-
dards were diluted appropriately and used to calibrate the AAS and
ICPOES. Calibration standards of mercury, cadmium and lead
were purchased from Merck, Germany.
2.3. Apparatus
Samples were digested using microwave digestion system
(Milestone ETHOS PLUS, Italy) equipped with TFM closed vessels.
The power system used with the focused microwave apparatus
provides continuous microwave emission at each power level.
The system is a closed vessel microwave apparatus, and equipped
with a fume extraction system.
2.4. Instruments
Determination of cadmium and lead was performed with ICP
OES equipped with ultrasonic nebulizer (Varian, USA). The instru-
ment detection limits on the ICPOES were 0.01 mg kg 1 for cad-
mium and 0.02 mg kg 1 for lead. Determination of total mercury
was performed by the cold vapor hydride generation atomic
absorption spectrometer (AAS 400, FIAS 100, Perkin Elmer), with
an instrument detection level of 0.01 mg kg 1.

Table 1
Characteristics of the sh species collected and analyzed.

Common Scientic name Life style Trophic level

name
Fish species
1 Skipjack tuna Katsuwonus pelamis Epi pelagic, Carnivore (feeds on small pelagic sh, crabs, larvae, anchovies, krill and squids)
oceanic
2 Yellown Thunnus albacares Epi pelagic, Carnivore (feeds on small pelagic organisms including sardines, anchovies, myctophids, squids and
tuna Oceanic crustaceans)
3 Red Pagellus afnis Demersal sh Carnivore (feeds on bivalve mollusks, crustaceans and small sh).
Seabream
4 Santerbream Cheimerius nufar Demersal sh Carnivore (feeds on small sh, squid and crustaceans)
5 Grouper Epinephalus Demersal sh Predatory carnivore (feeds on large variety of crustaceans, mollusks and other shes).
chlorostigma
6 Emperor Lethrinus nebulosus Demersal sh Carnivore (feeds on crabs, mollusk, shrimp, crustaceans and small sh)
7 Amberjack Seriola dumerili Demersal sh Carnivore (feeds on small sh and invertebrates)
8 Catsh Arius bilineatus Demersal sh Carnivore(feeds on crabs, other crustaceans and small sh)
9 Yellowtail Atule mate Pelagic sh Predatory carnivore (feeds on crustacean and cephalopods)
scad
10 Kingsh Scomberomorus Pelagic sh Piscivore (feeds on small sh like sardines, anchovies, lizard sh, lantern sh)
commerson
 M. Al-Busaidi et al. / Chemosphere 85 (2011) 6773 69

2.5. Heavy metals analysis
For each sample, 2.5 g of muscle tissue (wet weight) was
weighed and placed in a Teon digestion vessel and 5 mL of con-
centrated (65%) nitric acid (HNO3) and 1 mL of (30%) hydrogen per-
oxide (H2O2) were added. The sample in the vessel containing
concentrated nitric acid and hydrogen peroxide was then digested
using a microwave programmed as follows: step (1) 25180 C for
30 min at 1000 W; step (2) 180 C for 15 min at 1000 W. Digested
samples were prepared up to 25 mL with milliQ water in pre acid
washed standard asks.
2.6. Quality control
All the samples were taken in triplicates and all measurements
were run in triplicates for standard and samples. Metal concentra-
tions were calculated and expressed in mg kg 1 wet weight. Accu-
racy of analytical method was monitored by analyzing certied
reference materials (Mussel tissue NIST SRM 2976). The standard
reference material was analyzed during each batch and the
measured value (Cd: 0.79 mg kg 1, Hg: 0.057 mg kg 1 and Pb:
1.06 mg kg 1) was well agreed with the certied value (Cd:
0.82 0.16 mg kg 1, Hg: 0.061 0.0036 mg kg 1 and Pb: 1.19
0.18 mg kg 1). A recovery test was carried out by spiking of standard
solutions of heavy metals in homogenized samples. The recovery for
heavy metals during these experiments ranged between 80% and
110%, no batches were outside of these limits.
2.7. Statistical analysis
Results of heavy metal concentrations were analyzed using SPSS
10.0 (SPSS INC., Chicago, IL) software. One-way (KruskalWallis
nonparametric) and two-way ANOVA, Duncan multiple range
and correlation coefcients were used to examine differences
among species and relationship among metals. A signicance level
of 5% was used.
3. Results and discussion
3.1. Cadmium
There were 873 sh samples representing 10 species, where
(581) were in fresh condition and (292) were in frozen condition.
The sh samples were collected from factories, which were in-
tended for international market and imported from various coun-
tries. Table 2 shows the concentrations of cadmium, lead and
mercury detected in the muscle portion of various sh species in
this study. Among 873 samples, cadmium was present above
LOD in 44 samples. The cadmium content for fresh and frozen sh
was in the range of 0.011.0 mg kg 1. For the 10 sh species inves-
tigated, the lowest cadmium concentration was present in skipjack
tuna with mean concentration of 0.0049 mg kg 1 wet weight. Yel-
lown tuna, red seabream and santer bream found to contain the
mean cadmium concentration at a level of >0.009 mg kg 1, while
kingsh with the highest mean concentration at 0.0364 mg kg 1;
followed by yellowtail scad (0.024 mg kg 1). Highest cadmium
concentration was detected in yellown tuna with 1.0 mg kg 1
and it could be due to their feeding habits, as big species feed at
higher tropical levels.
The mean cadmium content (0.00490.0364 mg kg 1) (Table 2)
for seafood in this study is very similar to the mean values reported
by Sivaperumal et al. (2007) and Ysart et al. (2000) for various sh
species. Sankar et al. (2006) detected cadmium content in marine,
brackish water and freshwater sh at a level of 0.1 mg kg 1.
Pimonwan et al. (2009) reported that, concentration of cadmium
in seafood was 0.0090.31 mg kg 1. Mean cadmium content for
most of the sh in this study was lower than that found in study
conducted in other locations; Catalonia, Spain (0.037 mg kg 1)
and Thailand (0.082 mg kg 1) (Llobet et al., 2003; Pimonwan
et al., 2009). However, Vibunpant et al. (2009) found that concen-
tration of cadmium in seafood in the Andaman Sea was lower than
the level obtained in this study. Burger and Gochfeld (2005) re-
ported cadmium ranges from 0.0001 to 0.01 mg kg 1 for various
commercial sh from New Jercy and the FDA results for cadmium
were mainly in the 0.010.21 range. Our results ranged from 0.004
to 0.024 mg kg 1, except kingsh (0.0364 mg kg 1). These values
were found to be lower than the acceptable limit proposed by
the European Union. The mean cadmium concentration in ten
types of commercially important sh species reported in this study
did not exceed the contamination standard limited level of the Na-
tional Health and Medical Council, Australia (2 lg g 1) and maxi-
mum cadmium content set by the European Union (EU in sh
0.050.1 mg kg 1). Humans are exposed to cadmium through food
and the average daily intake for adults has been determined by ex-
pert FAO/WHO as PTWI (Provisional Tolerable Weekly Intake).
PTWI for cadmium is 7 lg per week kg 1 body weight. For person
with body weight 70 kg is 490 lg per week (WHO, 1993).
3.2. Lead
Lead was detected in 279 (31.95%) sh samples and 594
(68.04%) samples were below the LOD value (0.02 mg kg 1). The
details of lead concentration detected for individual sh are given
in Table 2. Among individual species, yellown tuna contained the
lowest lead concentration with mean tissue concentration of
0.0291 mg kg 1; followed by yellowtail scad with 0.0474 mg kg 1
mean value. Santer bream and emperor both contained the highest
mean lead concentration of 0.196 mg kg 1 and 0.180 mg kg 1,
respectively. However, the average values were less than 0.3 mg
kg 1 for all the sh species analyzed. Highest lead concentration

Table 2
Level of cadmium, lead and mercury in sh species studied.
Species name
Fresh/frozen sh
1 Skipjack tuna
2 Yellown tuna
3 Red seabream
4 Grouper
5 Emperor
6 Amberjack
7 Catsh
8 Yellowtail scad
9 Kingsh
10 Santer bream
1 1 1
N Cd (mg kg ) Pb (mg kg ) Hg (mg kg )
102 0.0049 0.010d (0.010.054) 0.0492 0.197b,c (0.021.437) 0.0632 0.104b (0.010.386)
346 0.0099 0.065c,d (0.011.0) 0.0291 0.127c (0.021.08) 0.0326 0.087c (0.010.570)
274 0.0093 0.016c,d (0.010.085) 0.1395 0.224a (0.021.071) 0.0307 0.046c (0.010.282)
82 0.0176 0.007b (0.010.024) 0.0547 0.038b (0.020.134) 0.0156 0.053c (0.010.416)
27 0.0054 0.01d (0.010.060) 0.1803 0.190a (0.0310.567) 0.0176 0.030c (0.010.1005)
10 0.0122 0.020b (0.010.020) 0.068 0.042b (0.020.083) 0.1016 0.167a (0.010.420)
11 0.0068 0.01d (0.010.034) 0.074 0.04b (0.020.154) 0.0473 0.004c (0.010.122)
9 0.024 0.004a,b (0.010.029) 0.0474 0.040b,c (0.020.11) 0.079 0.07b (0.010.163)
4 0.0364 0.001a (0.010.044) 0.1557 0.156a (0.020.381) 0.0677 0.03b (0.010.097)
8 0.0099 0.014c,d (0.010.039) 0.1964 0.310a (0.020.744) 0.0926 0.022a (0.0540.123)

Small letters in superscript are signicantly different among species.

70 M. Al-Busaidi et al. / Chemosphere 85 (2011) 6773
was detected in skipjack tuna at a level of 1.437 mg kg 1, followed
by 1.08 mg kg 1 in yellown tuna. The lowest lead concentration
was found in amberjack with 0.083 mg kg 1.
The lead values are similar to the values of Burger and Gochfeld
(2005) and lower than those reported in literature (Ashraf et al.,
2004; Abou-Arab et al., 1996). Whereas, FDA results range (0.001
0.003 mg kg 1) were lower than our results range (FDA, 2003). San-
kar et al. (2006) reported that lead was not detected in the edible
portion of marine sh analyzed except one sh J. dussumerri with
0.13 mg kg 1. Sivaperumal et al. (2007) reported that lead was pres-
ent in about 25% of the total samples of sh, shellsh and sh prod-
ucts. Al-jedah and Robinson (2001) analyzed various sh samples
caught off the coast of Qatar closer to the study area and found none
of the samples found to contain lead except one sample of
Plectrohynchus pictus with 0.08 mg kg 1. Increased number of lead
detected samples found in this study indicates the need for further
investigation including more variety of species and a larger sample
size. The PTWI for an adult is 25 lg per week kg 1 body weight.
For person with body weight of 70 kg is 1750 lg per week (WHO,
1993). EU acceptable limit for lead is 0.3 mg kg 1 and the range of
international standards for sh is 0.51.0 lg g 1 (EC, 2001).
3.3. Mercury
Mercury was detected in 233 samples (26.68%) and in the rest
of the samples mercury was below the detection level. The concen-
tration of mercury varied from 0.01 to 0.57 mg kg 1. The highest
muscle mercury concentration was detected in amberjack with a
mean value of 0.101 mg kg 1 and the lowest with grouper
(0.015 mg kg 1) followed by emperor (0.017 mg kg 1). The highest
mercury concentration was found in yellown tuna with a value of
0.57 mg kg 1, followed by amberjack with 0.42 mg kg 1.
The levels of mercury in sh sample are not high when com-
pared to some other areas of the world (Burger et al., 2005; Ashraf,
2005; Sivaperumal et al., 2007; Lourenco et al., 2004) and similar
to the range (0.0040.16 mg kg 1) reported by FDA for various sh
species (FDA, 2003). Al-jedah and Robinson (2001) analyzed heavy
metal contents of edible portion of sh popular with consumers
around the Arabian Gulf and found that mercury was present in
all the samples. Sivaperumal et al. (2007) reported that mercury
was not detected in 88% of the total sh samples analyzed and San-
kar et al. (2006) reported trace levels of mercury (0.30.5 mg kg 1)
in 5% of the marine sh. Cirillo et al. (2010) reported mercury at a
level of 0.080.339 mg kg 1 in wild seafood; <0.050.226 mg kg 1
in farmed sh and 0.050.313 mg kg 1 in frozen sh which is in
close agreement with mercury level detected for sh in this study
(0.010.386 mg kg 1) except amberjack (0.010.420 mg kg 1),
grouper (0.010.416 mg kg 1) and yellown tuna (0.01
0.57 mg kg 1). Similarly, Bordajandi et al. (2004) reported mercury
in seash from 0.069 to 0.549 mg kg 1) For humans, the most sig-
nicant source of mercury in the diet is sh. In Minamata Bay, Ja-
pan, an area heavily polluted with mercury, sh found to contain
from 1 to 20 mg kg 1 of the edible esh (NAS-NRC, 1977). The con-
centration of mercury was highest in yellown tuna, however, the
contamination in these sh is still lower than the Omani legisla-
tion, EC and FAO limits. Based on the guideline levels established
by Codex Alimentarius Commission (Joint FAO/WHO food standard
programme) in 1991, the European consumption limits for mer-
cury in sh is 0.5 mg kg 1, except for certain larger predatory spe-
cies having a consumption limit of 1.0 mg kg 1. The variations
observed between mercury concentrations in different species
could be due to their feeding habits or the seasonal variation, but
they also depend on the mercury content in food and on the bio
concentration capacity of each species. In this study, none of the
seafood samples contained mercury content that exceeded the
EU legislation or Omani legislation.
3.4. Changes in species bioaccumulation
A discernible pattern was observed across the sh species with
high number of samples in metal concentration. There were inter-
specic differences in levels of all the three metals. The differences
are due to geography, tropic level, size, foraging method, location
and tendency of metals to undergo biomagnications in the food
chain. That is, the sh that are high on the tropic level might be ex-
pected to accumulate higher levels of bioaccumulative metals such
as mercury (Campbell, 1994; Fairey et al., 1997; Burger et al.,
2001a). Similarly, some metals bioaccumulate with size and age
in sh (Phillips et al., 1980; Braune, 1987; Lange et al., 1994; Lac-
erda et al., 1994; Bidone et al., 1997; Burger et al., 2001b). Yellow-
n tuna that is high on tropic level and larger in size had the
highest level of cadmium and mercury, and red seabream had
the next highest (predators) although, they are not as large as or
long-lived as yellown tuna. However, it is surprising that skipjack
tuna, which are also intermediate sized predators, did not have
higher levels of cadmium and mercury. It was interested to know
that, there was signicant difference in the metal level between
the two tuna species. Yellown tuna contained highest concentra-
tion for cadmium and mercury; however, skipjack tuna had the
highest concentration for lead. Yellown tuna is normally larger
in size and skipjack tuna is lower in size compared to yellown
tuna and its feed on high tropic level. It is surprising that grouper,
which are also predator, did not have higher level of all the three
metals. However, the same sh species had higher mean concen-
tration for cadmium. The variation observed could be due to size,
metal content in food and bio concentration capacity of each spe-
cies. Yellown tuna and skipjack tuna are migratory, oceanic, epi
pelagic species and while others are bottom living predators (Siva-
subramaniam, 1985; Al-Abdessalaam, 1995). Other than yellown
tuna, all the other three sh are locally caught and the high con-
centration in yellown tuna could not be predictable as the sh
is migratory, oceanic and moves for long distances (Burger and
Gochfeld, 2005). Other sh species are mid water to bottom level
predators on small to intermediate sized sh (Al-Abdessalaam,
1995). Bottom feeders are expected to have more metals than sur-
face feeders and the same was found in this study for skipjack tuna
(surface feeder). However, signicant difference (p < 0.05) was
found in metal level between locally caught bottom feeders of
intermediate size, indicate the species-specic metal accumulation
capacity.
Highest concentrations of most of the metals were observed in
yellown tuna and red seabream. Several factors may be responsi-
ble for this variation in metal uptake within the same locality (Phil-
lips, 1990; Karadede et al., 2004). The variation is also indicative of
the degree to which particular species pick up particulate matter
from the surrounding water and in particular, sediment while
feeding. Both yellown tuna and red seabream are carnivores sh
and are generally expected to concentrate more than herbivores
sh (Phillips, 1990; Allen-Gil and Martynov, 1995). No signicant
differences (p > 0.05) were observed between metal levels for all
the four species with highest sample size. Out of 44 samples de-
tected for cadmium, majority (65%) of the samples were red sea-
bream. High number of detection level in red seabream may be
due to its feeding habit and metal accumulation capacity. Lead
was detected in 279 samples and maximum number of samples
was of red seabream (72.2%) as like cadmium, and then followed
by yellown tuna (12.5%). Out of 233 samples detected for mer-
cury, as like cadmium and lead, red seabream samples exhibited
the highest percentage (54.8%); followed by yellown tuna
(23.7%). Out of 35 samples (12 Cd, 23 Pb) exceeded the standard
limit, 18 samples were of red seabream, followed by yellown tuna
(10), emperor (3), santer bream (2), king sh (1) and skipjack tuna
(1). Red seabream are bottom feeding sh and the maximum
 M. Al-Busaidi et al. / Chemosphere 85 (2011) 6773 71

numbers above MRL for cadmium and lead could also be based on
a good sample size (274).

3.5. Relationship between metals

No signicant difference was observed between metal levels for

all the four species with highest sample size. Out of the 12 samples
detected with cadmium >0.05 mg kg 1, only two samples showed
higher lead content, likewise, out of 23 samples detected for lead
at higher concentration >0.3 mg kg 1, two samples showed cad-
mium at higher levels. This indicates that there was no signicant
correlation between metals for all the sh species in this study, and
the concentrations of cadmium or lead did not indicate of what
would be the other metal. Burger and Gochfeld (2005) reported Fig. 1. Distribution of cadmium (relative frequency, %) in fresh/frozen sh (A: 0.01
that no signicant correlation was found for metals for commercial 0.03), (B: 0.030.04), (C: 0.040.05), (D: 0.050.06), (E: 0.060.07), (F: 0.070.08),
sh from New Jersy. (G: 0.080.09), (H: 0.090.1).

3.6. Distribution of heavy metals content and their relative frequency

percentage

In order to express the distribution of cadmium in the high

number of samples, namely yellown tuna, skipjack tuna, red sea-
bream and grouper, all values are presented in the histogram (rel-
ative frequency of cadmium, lead and mercury in percentage)
shown in Figs. 13. The levels expressed in mg kg 1 wet weight,
were clustered in several classes, indicating a range of concentra-
tions higher, equal to MRL, or lower than). For cadmium, majority
of the samples (28.1%) showed the level between 0.04 and
0.05 mg kg 1. Red seabream samples exhibited higher frequency
level at 0.040.05 mg kg 1 (38%) and six samples (28%) reached
the EU limit of 0.05 mg kg 1. In yellown tuna, ve samples
(71%) showed the frequency level at 0.050.1 mg kg 1. Of the Fig. 2. Distribution of lead (relative frequency, %) in fresh/frozen sh (A: 0.020.05),
102 skipjack tuna analyzed, only one sample showed class level be- (B: 0.050.1), (C: 0.10.2), (D: 0.20.3), (E: 0.30.4), (F: 0.40.5), (G: >0.5 mg/kg).
tween 0.05 and above. In grouper, all the samples exhibited the
class level between 0.02 and 0.03 mg kg 1. About 1.37% of the total
samples crossed the EU recommended limit of 0.05 mg kg 1. Six of
12 crossed the EU limit were red seabream and others were one
emperor sh and ve yellown tuna. Cirillo et al. (2010) reported
on cadmium below EU limits for fresh, farmed and frozen sh
and shellsh samples collected from Italy and Pimonwan et al.
(2009) found all samples were lower than the standard limit level
issued by EC. Sivaperumal et al. (2007) reported that 53% of the
samples contained cadmium at a level of 0.021.32 mg kg 1 and
cadmium was above the limit in one of the six samples of E. surat-
ensis. In this study, ve of 12 samples exceeded the EU limit were
yellown tuna which is closer to those found by Burger and Goch-
feld (2005) in commercial sh from New Jersey where 11 samples
exceeded 0.05 mg kg 1 and seven of 11 samples exceeded 0.5
mg kg 1 were yellown tuna. Fig. 3. Distribution of mercury (relative frequency, %) in fresh/frozen sh (A: 0.01
The majority of the samples (38.8%) showed lead level between 0.05), (B: 0.050.1), (C:0.10.2), (D: 0.20.3), (E: 0.30.4), (F: 0.40.5), (G: >0.5).
0.05 and 0.1 mg kg 1 relative frequency levels. Red seabream sam-
ples exhibited higher frequency level at 0.050.1 mg kg 1 (42.3%) ported to Egypt. Sankar et al. (2006) reported that about 67% of
and yellown tuna samples exhibited at higher frequency level the samples contained lead in their edible portion (0.040.38
0.30.4 mg kg 1 (33.3%). About 2.63% of the total samples crossed lg g 1) and 22% of the samples contained marginally higher lead
the EU limit of 0.3 mg kg 1 and 1.6% of the total samples exceeded content above the legal limit of EC. Burger and Gochfeld (2005) re-
the FAO limit of 0.5 mg kg 1. The samples exceeded were red sea- ported that none of the sh samples exceeded the average lead
bream (12), yellown tuna (5), santer bream (2), emperor (2), skip- content above 0.2 mg kg 1 however, 12 sh samples exceeded
jack tuna (1) and king sh (1). Cirillo et al. (2010) reported that 0.2 mg kg 1. Sivaperumal et al. (2007) reported that lead was pres-
lead level in fresh and frozen sh species ranged between 0.02 ent at a level of 0.011.32 mg kg 1 in the edible portion of sh and
and 0.689 and 0.02 to 0.541 mg kg 1, respectively and four samples about 70% of the samples contained lead below 0.4 mg kg 1 and
exceeded EU limits for lead. Yilmaz (2005) reported that lead levels 82% below 0.5 mg kg 1; however, about 22% of the fresh water sh
in muscle of seabream and mullet samples were higher than the contained marginally higher lead content above the legal limit of
acceptable values for human consumption. Lowe et al. (1985) in EC. In this study, a total of 23 sh samples exceeded the EU limit
their study found on lead below legal levels in the fresh water sh and it indicates that lead levels bear further study in sh.
collected from rivers of USA over years and Abou-Arab et al. (1996) Fish samples showed mercury in the range of 0.010.05 mg
reported on the higher mean level of lead in the sh samples im- kg 1 (34.01%), followed by 0.050.1 mg kg 1 (29.8%) and 0.1
72 M. Al-Busaidi et al. / Chemosphere 85 (2011) 6773
0.2 mg kg 1 (20.1%). For red seabream the major relative frequency
exhibited by class 0.050.1 mg kg 1 (47.7%); for yellown tuna at
0.010.05 mg kg 1 with 46%; for skipjack tuna major relative fre-
quency presented by class 0.10.2 mg kg 1 (37.5%) and for grouper
between 0.01 and 0.1 mg kg 1 (72%). The majority (93.1%) of the
samples showed mercury levels between 0.01 and 0.3 mg kg 1,
being the higher relative frequency presented by class 0.01
0.05 mg kg 1. Such distribution was similar to that found by sev-
eral authors for sh and shellsh (Duve, 1981; Schindler, 1985; Ga-
jewska et al., 1995; Voegborlo et al., 1999; Lourenco et al., 2004)
Sivaperumal et al. (2007) reported that mercury was not detected
in 88% of the total samples and only 3% of the total samples con-
tained mercury above the permitted limit. Burger et al. (2005) re-
ported that 42% of the tuna llets and 2% of the blue sh llets had
mercury levels above 0.5 mg kg 1. Burger and Gochfeld (2005) re-
ported that 22% of the yellown tuna samples exceeded the
1.0 mg kg 1. However, in this study, no yellown tuna samples ex-
ceeded the EU limit. In this study, mercury was detected at trace
levels in majority of the samples and were lower than the EU limit
in all samples studied, which is in agreement with values reported
by Sankar et al. (2006) for marine sh, Cirillo et al. (2010) for fresh,
farmed and frozen marine sh and Al-jedah and Robinson (2001)
for commercial marine sh.
3.7. Above Maximum Residual Limit
EC (2001), FAO (1983) and FDA (2003) have recommended MRL
for heavy metal residues in sh and shellsh meant for human
consumption. For cadmium, the mean of studied sh was far below
the median international standard of 0.3 mg kg 1 and were even
below the lowest standard of 0.05 mg kg 1 for most species. About
1.37% of the total samples had marginally higher cadmium content
above the EC limit. Only one sample was found to contain cad-
mium above the EC as well as FAO limits. 11 out of 12 samples
exceeding cadmium at 0.05 mg kg 1 were red seabream (6) and
yellown tuna (5). Mean lead level did not reach or came closer
to MRL for any of the sh in this study. The lead content in samples
was much less than the permitted level of 0.3 mg kg 1 (EC, 2001)
and 2.63% of the samples had above the EC limit. 23 sh samples
(yellown tuna 5, red seabream 12, santer bream 2, emperor 2,
skipjack tuna 1 and king sh 1) exceeded the maximum residual
level of 0.3 mg kg 1. Mercury concentrations in most of the sh
were below the EC limit. None of the species in this study had aver-
age mercury level 0.5 mg kg 1. Most nations used a standard of
0.5 mg kg 1, which exceeded by one yellown tuna in this study
however; EU and some nations allow an exemption for predatory
sh like tuna (1.0 mg kg 1). None of the samples crossed the EU
standard limit.
4. Conclusions
The levels of toxic metals in sh samples are not high when
compared to some other areas of the world and a range of interna-
tional standards. Our results showed that the values are lower than
these guidelines. Therefore, we can conclude that these metals
have pose no threat for consumption of these sh. This study indi-
cates that fresh and frozen sh follows a pattern of Pb > Cd > Hg
and species wise red seabream > yellown tuna. Majority (84%)
of the mercury detected samples showed the prevalence between
0.01 and 0.2 mg kg 1 and 1.37% of the total samples exceeded
the limit for cadmium, and maximum (62.5%) of the lead detected
samples exhibited in the range of 0.020.2 mg kg 1. However,
2.63% of the samples exceeded the limit indicates that this metal
to be studied more. The data in this paper suggests that most of
the species have relatively low levels of contaminants of concern,
such as cadmium, lead and mercury except, few yellown tuna
and red seabream. Also, the mean concentrations for all the sh
species were lower than the standard limits proposed by the EU
and FAO.
Acknowledgement
We would like to thank Nada Al-Abri, Analyst specialist of Fish-
ery Quality Control Centre, Oman, for her constant assistance and
contribution in sample preparation and analysis during this
project.
References
Abernathy, O.C.H., Thomas, D.J., Calderon, L.R., 2003. Health effects and risk
assessment of arsenic. J. Nutr. 133, 53655385.
Abou-Arab, A.K., Ayesh, A.M., Amra, H.A., Naguib, K., 1996. Characteristic levels of
some pesticides and heavy metals in imported sh. Food Chem. 57, 478492.
Agree, J.J., Vaisanen, S., Hanneien, O., Muller, A.D., Hornstra, G., 1997. Hemostatic
factors and platelet aggregation after sh-enriched diet or sh oil or
docosahexaenoic acid supplementation. Prostag. Leukot. Essent. Fatty Acids
57, 419421.
Al-Abdessalaam, T.Z.S., 1995. Marine Species of the Sultanate of Oman. Marine
Science and Fisheries Centre, Ministry of Agriculture and Fisheries. p. 412.
Al-Jedah, J.H., Robinson, R.K., 2001. Aspects of the safety of the sh caught off the
Coast of Qatar. Food Cont. 12, 549552.
Allen-Gil, S.M., Martynov, V.G., 1995. Heavy metals burdens in nine species of
freshwater and anadromous sh from the Pechora River, Northern Russia. Sci.
Tot. Environ. 160, 653659.
Andreji, J., Stranai, I., Massayi, P., Valent, M., 2006. Accumulation of some metals in
muscles of ve sh species from lower Nitra River. J. Environ. Sci. Health 41,
26072622.
Ashraf, W., 2005. Accumulation of heavy metals in kidney and heart tissues of
Epinephelus microdon sh from the Arabian Gulf. Environ. Monit. Assess. 101,
311316.
Ashraf, W., Seddigi, Z., Abulkibash, A., Khalid, M., 2004. Levels of selected metals in
canned sh consumed in Kingdom of Saudi Arabia. Environ. Monit. Assess. 117,
271279.
Bidone, E.D., Castilhos, Z.C., Santos, T.J.S., Souza, T.M.C., Lacerda, L.D., 1997. Fish
contamination and human exposure to mercury in Tartarugalzinho River,
Northern Amazon, Brazil. A screening approach. Water Air Soil Pollut. 97, 915.
Bordajandi, R.L., Gmez, G., Abad, E., Rivera, J., Fernndez, M.M., Blasco, J., Gonzlez,
M.J., 2004. Survey of persistent organochlorine contaminants (PCBS, PCDD/Fs,
and PAH), heavy metals (Cu, Cd, Zn, Pb, and Hg), and arsenic in food samples
from Huelva (Spain): levels and health implications. J. Agric. Food Chem. 52,
9921001.
Braune, B.M., 1987. Mercury accumulation in relation to size and age of Atlantic
herring (Clupea harengus harengus) from the southwestern Bay of Fundy.
Canada. Arch. Environ. Contamin. Toxicol. 16, 311320.
Burger, J., Gochfeld, M., 2005. Heavy metals in commercial sh in New Jersey.
Environ. Res. 99, 403413.
Burger, J., Gaines, K.F., Boring, C.S., Stephens Jr., W.L., Snodgrass, J., Gochfeld, M.,
2001a. Mercury and selenium in sh from the Savannah River: species, trophic
level, and locational differences. Environ. Res. 87, 108118.
Burger, J., Gaines, K.F., Gochfeld, M., 2001b. Ethnic differences in risk from mercury
among Savannah River shermen. Risk Anal. 21, 533544.
Burger, J., Stern, A.H., Gochfeld, M., 2005. Mercury in commercial sh: optimizing
individual choices to reduce risk. Environ. Health Pers. 113, 16.
Campbell, K.R., 1994. Concentrations of heavy metals associated with urban runoff
in sh living in storm water treatment ponds. Arch. Environ. Contamin. Toxicol.
27, 352356.
Castro-Gonzalez, I.M., 2002. Acidos grasos omega-3: beneciosy Fuentes.
Interciencia 27, 128136.
Chan, M.H., Egeland, M.G., 2004. Fish consumption, mercury exposure, and heart
disease. Nitr. Rev. 62, 6872.
Cherubini, A., Andres-Lacueva, C., Martin, A., Lauretani, F., Lorio, A.D., Bartali, B.,
Corsi, A., Bandinelli, S., Mattson, M.P., Ferrucci, L., 2007. Low plasma N-3 fatty
acids and dementia in older persons: the In CHIANTI study. J. Gerontol. Biol. Sci.
Med. Sci. 62, 11201126.
Cirillo, T., Fasano, E., Viscardi, V., Arnese, A., Cocchieri, R.A., 2010. Survey of lead,
cadmium, mercury and arsenic in seafood purchased in Campania, Italy. Food
Add. Cont. 3, 3038.
Clarkson, W.T., 2002. The three modern faces of mercury. Environ. Health Perspect.
110, 1123.
Cleland, L.G., Proudman, S.M., Hall, C., Stamp, L.K., McWlliams, L., Wylie, N.,
Neumann, M., Gibson, R.A., James, M.J., 2003. A biomarker of n-3 compliance in
patients taking sh oil for rheumatoid arthritis. Lipids 38, 419424.
Sudhir, Dahiya, Rupali, Karpe, Hegde, A.G., Sharma, R.M., 2005. Lead, cadmium and
nickel in chocolates and candies from suburban areas of Mumbai, India. J. Food
Comp. Anal. 18, 517522.
Din, J.N., Newby, D.E., Flapan, A.D., 2004. Omega 3 fatty acids in cardiovascular
disease-shing for natural treatment. BMJ 328, 3035.
 M. Al-Busaidi et al. / Chemosphere 85 (2011) 6773
Dominogo, J.L., Bocio, A., Flaco, G., Llobet, J.M., 2007. Benets and risk of sh
consumption. Part I. A quantitative analysis of the intake of omega-3fatty acids
and chemical contaminants. Toxicol 230, 219226.
Duve, R.N., 1981. Mercury content of canned tuna exported from Fiji. Fiji Agri. J.
43, 4748.
EC, 2001. Commission regulation (EC) No. 466/2001 of 8 March 2001. Ofcial J. Eur.
Commun. 1. 77/1.
Fairey, R., Taberski, K., Lamerdin, S., Johnson, E., Clark, R.P., Downing, J.W., Newman,
J., Petreas, M., 1997. Organochlorines and other environmental contaminants in
muscle tissue of sport sh collected from San Francisco Bay. Mar. Pollut. Bull.
34, 10581071.
Falco, G., Llobet, J.M., Bocio, A., Domingo, J.L., 2006. Daily intake of arsenic,
cadmium, mercury, and lead consumption of edible marine species. J. Agric.
Food Chem. 54, 61066112.
FAO, 1983. Compilation of legal limits for hazardous substance in sh and shery
products (Food and Agricultural Organization). FAO shery circular, No. 464, pp.
5100.
FDA, 2003. FDA Consumer Advisory. Food and Drug Administration, Washington,
DC. Available from: <http://www.fda.gov/bbs/topics/ANSWERS/2000/advisory.
html>.
Gajewska, R., Ganowiak, R., Nabrzyski, M., Kozarzewska, E., 1995. Determination of
mercury in canned and some unstable sh products. Bromat I Chem. Toksyk 28,
249252.
Guallar, E., Sanz-Gallardo, M.I., Vant Veer, P., Bode, P., Aro, A., Gomez-Aracena, J.,
Kark, J.D., Riemersma, A.R., Martin-Moreno, J.M., Frans, J.K., 2002. Mercury, sh
oil, and the risk of myocardial infarction. N. Engl. J. Med. 437, 1747
1754.
Gumgum, B., Unlu, E., Tez, Z., Gulsun, Z., 1994. Heavy metal pollution in water,
sediment and sh from the Tigris River in Turkey. Chemosphere 290, 111
116.
Harada, M., Nakachi, S., Chen, T., Hamada, H., Ono, Y., Tsuda, T., Yanagida, K., Kizaki,
T., Ohno, H., 1994. Monitoring of mercury pollution in Tanzinaia: relation
between head hair mercury and health. Sci. Total Environ. 156, 269277.
Harris, W.S., 1997. N-3 fatty acids and serum lipoproteins: human studies. Am. J.
Clin. Nutr. 65, 1645S1654S.
Harrison, R.M., Laxen, D.P.H., 1981. Lead Pollution: Causes and Control. Chapman
Hall, London.
Has-Schon, E., Bogut, I., Strelec, I., 2006. Heavy metal prole in ve sh species
included in human diet. Domiciled in the end ow of River Neretva (Croatia).
Arch. Environ. Contamin. Toxicol. 50, 545551.
Hites, R.A., Foran, J.A., Carpenter, D.O., Hamilton, M.C., Knuth, B.A., Schwager, S.J.,
2004. Global assessment of organic contaminants in farmed salmon. Science
303, 226229.
Ismail, H.M., 2005. The role of omega-3 fatty acids in cardiac protection: on
overview front. Bioscience 10, 10791088.
Karadede, H., Oymak, S.A., Unlu, E., 2004. Heavy metals in mullet, Liza abu, and
catsh, Silurus triostegus, from the Atalurk Dam Lake (Euphrates). Turkety
Environ. Int. 30, 183188.
Kinsella, J.E., Lokesh, B., Stone, R.A., 1990. Dietary n-3 poly unsaturated fatty acids in
amelioration of cardiovascular disease: possible mechanisms. Am. J. Clin. Nutr.
52, 128.
Kris-Etherton, P.M., Harris, W.S., Appel, L.J., 2002. Fish consumption, sh oil. Omega-
3 fatty acids, and cardiovascular disease. Circulation 106, 27472757.
Lacerda, L.D., Bidone, E.D., Giumaraes, A.F., Pfeiffer, W.C., 1994. Mercury
concentrations in sh from the Itacaiunas-Parauapebas River system, Carajas
region. Amazon Ann. Acad. Bras. Sci. 66, 373379.
Lange, T.R., Royals, H.E., Connor, L.L., 1994. Mercury accumulation in largemouth
bass (Micropterus salmoides) in a Florida lake. Arch. Environ. Contamin. Toxicol.
27, 466471.
Llobet, J.M., Falco, G., Casas, C., Teixido, A., Domingo, J.L., 2003. Concentrations of
arsenic, cadmium, mercury and lead in common foods and estimated daily
intake by children, adolescents, adults and seniors of Catalonia, Spain. J. Agric.
Food Chem. 51, 838842.
Lourenco, H.M., Afonso, C., Martins, M.F., Rosa, A., 2004. Levels of toxic metals in
canned seafood. J. Aqua. Food Prod. Tech. 13, 117125.
Lowe, T.P., May, T.W., Brubangh, W.G., 1985. National contaminant monitoring
program, concentrations of seven elements in fresh water sh, 19791981.
Arch. Environ. Contamin. Toxicol. 14, 363383.
Matta, J., Milad, M., Manger, R., Tosteson, T., 1999. Heavy metals, lipid peroxidation,
and cigaterotoxicity in the liver of the Caribben barracuda (Sphyraena
barracuda). Biol. Trace Element Res. 70, 6979.
View publication stats
73
NAS-NRC, 1977. National Academy of Sciences National Research Council.
Drinking Water and health, vol. 1. National Academic Press, Washington, DC.
pp. 1939.
Novelli, E.L., Vieira, E.P., Rodrigues, N.L., Ribas, B.O., 1998. Risk assessment of
cadmium toxicity on hepatic and renal tissues of rats. Environ. Res. 79, 102
105.
NRC (National Research Council), 2000. Toxicological Effects of Methylmercury.
National Academy Press, Washington, DC.
Oomen, C.M., Feskens, E.J., Rasanem, L., Fidanza, F., Nissinem, A.M., Menotti, A., Kok,
F.J., Kromhout, D., 2000. Fish consumption of coronary heart disease mortality
in Finland, Italy and The Netherlands. Am. J. Epidemiol. 151, 9991006.
Phillips, D.J.H., 1990. Heavy metals in marine environment. In: Rainbow, P.S. (Ed.),
Furness RW. CRC Press, Boca Raton.
Phillips, G.R., Lenhart, T.E., Gregory, R.W., 1980. Relations between trophic position
and mercury accumulation among shes from the Tongue River Reservoir,
Montana. Environ. Res. 22, 7380.
Pimonwan, K., Linna, T., Laddawan, R., 2009. Concentrations of cadmium and
arsenic in seafood from Muang District, Rayong province. J. Health Res. 4, 179
184.
Rahman, M.M., Bhattacharya, A., Fernandes, G., 2008. Docosahexaenoic acid is more
potent inhibitor of osteoclast differentiation in RAW 264.7 cells than
eicosapentaenoic acid. J. Cell Physiol. 214, 201209.
Ratcliffe, J.M., 1981. Lead in Man and the Environment. Ellis Horwood, Chichester,
England. pp. 3447.
Sankar, T.V., Zynudheen, A.A., Anandan, R., Viswanathan Nair, P.G., 2006.
Distribution of organochlorine pesticides and heavy metal residues in sh
and shellsh from Calicut region, Kerala, India. Chemosphere 65, 583590.
Schindler, E., 1985. Lead, cadmium, copper and mercury in canned tuna and
mussels. Deutsche-Lensmittel_Rundschau 81, 218220.
Sivaperumal, P., Sankar, T.V., Viswanathan Nair, P.G., 2007. Heavy metal
concentrations in sh, shellsh and sh products from internal markets of
India vis--vis international standards. Food Chem. 102, 612620.
Sivasubramaniam, K., 1985. The tuna shery in the EEZ of India, Maldives and
Srilanka. BOBP Working Paper 31: pp. 1942, FAO, Rome.
Song, C., Zhao, S., 2007. Omega-3 fatty acids eicosapentaenoic acid. A new treatment
for psychiatric and neurodegenerative diseases: a review of clinical
investigations. Expert Opin. Invest. Drugs 16, 16271638.
Stern, A.H., 1993. Re-evaluation of the reference dose for methylmercury and
assessment of current exposure levels. Risk Anal. 13, 355364.
USFDA, 1993a. Food and drug administration. Guidance document for chromium in
shellsh. DHHA/PHS/FDA/CFSAN/Ofce of Seafood, Washington, DC.
USFDA, 1993b. Food and drug administration. Guidance document for arsenic in
shellsh. DHHA/PHS/FDA/CFSAN/Ofce of Seafood, Washington, DC.
USFDA, 1993c. Food and drug administration. Guidance document for nickel in
shellsh. DHHA/PHS/FDA/CFSAN/Ofce of Seafood, Washington, DC.
Vettori, M.V., Alinovi, R., Belletti, S., Goldoni, M., Franchini, I., Mutti, A., 2003. In vitro
models for the evaluation of the neurotoxicity of methylmercury. Current state
of knowledge. Med. Lav. 94 (2), 183191.
Vibunpant, S., Thaochalee, P., Singharachai, C., Munprasit, R., Krajandgdara, T., 2009.
Heavy metals in marine animals from trawlers and purse seiners in Thai waters.
Technical paper of marine sheries Research and Development Bureau,
Department of Fisheries, Ministry of Agriculture and Cooperatives 1, 161.
Voegborlo, R.B., El-Methnani, A.M., Abedin, M.Z., 1999. Mercury, cadmium and lead
content of canned tuna sh. Food Chem. 67, 341345.
Waalkes, M.P., 2000. Cadmium carcinogenesis in review. J. Inorg. Biochem. 79, 241
244.
WHO, 1993. Evaluation of certain food additives and contaminants. Technical
Report No. 837. Genewa: World Health Organization.
Yilmaz, A.B., 2005. Comparison of heavy metal levels of grey mullet (Mugil cephalus)
and seabream (Sparus aurata) caught in Iskenderun Bay (Turkey). Turk. J. Vet.
Ani. Sci. 29, 257262.
Yoshizawa, K., Rimm, E.B., Morris, J.S., Spate, V.L., Hsieh, C.C., Spiegelman, D.,
Stamfer, M.J., Willet, W.C., 2002. Mercury and the risk of coronary heart disease
in men. N. Engl. J. Med. 347, 17551760.
Ysart, G., Miller, P., Croasdale, M., Crews, H., Robb, P., Baxter, M., 2000. 1997 UK
Total Diet Study dietary exposures to aluminum, arsenic, cadmium, chromium,
copper, lead, mercury, nickel, selenium, tin and zinc. Food Addit. Cont. 17, 775
786.