Brazil: new citation of the research at Moscow University.
http://5bio5.blogspot.com/2012/09/brazil-new-citation-of-research-at.html**
Brazil. Faculty at: Universidade de São Paulo. Journal: Food and Nutrition Sciences. Cited Moscow University research on marine ecology, ecotoxicology.
Brazilian paper:
D Grotto, BL Batista, MFH Carneiro, F Barbosa Jr
Denise Grotto*, Bruno Lemos Batista, Maria Fernanda Hornos Carneiro, Fernando Barbosa Jr.
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples. - Food and Nutrition Sciences, 2012, 3, ***-***.
**
Affiliation of the authors:
Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade
de São Paulo, Ribeirão Preto, Brazil.
**
The Moscow University paper that was cited:
S. A. Ostroumov, “Some aspects of water filtering activity of filter-feeders,” Hydrobiologia, Vol, 542, No. 1, 2005, pp. 275–286.
The publication that was cited in this Brazilian paper:
About this paper:
New terminology was introduced in the paper: ecological tax; ecological repair of water quality;
Ostroumov S.A. Some aspects of water filtering activity of filter-feeders. - Hydrobiologia. 2005. Vol. 542, No. 1. P. 275 – 286. www.scribd.com/doc/44105992
DOI: 10.1007/s10750-004-1875-1
**
is an openly accessible and peer-reviewed journal.
**
JWebsite: http://www.scirp.org/journal/fns
ISSN Print:
ISSN Online:
**
More info and the text of the Brazilian paper:
Food and Nutrition Sciences, 2012, 3, ***-***
Published Online September 2012 (http://www.SciRP.org/journal/fns)
Copyright © 2012 SciRes. FNS
1
Evaluation by ICP-MS of Essential, Nonessential and Toxic
Elements in Brazilian Fish and Seafood Samples
Denise Grotto*, Bruno Lemos Batista, Maria Fernanda Hornos Carneiro, Fernando Barbosa Jr
Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil.
Email: *denisegrotto@yahoo.com.br
Received *************** 2012
ABSTRACT
Fish is considered one of the healthiest foods due to the high levels of several important cardioprotective compounds such as long chain omega-3 polyunsaturated fatty acids and vitamin E. However, due to widespread environmental pollution, high levels of contaminants may also be present in fish and seafood samples, which may counteract the beneficial effects of consumption of this food. With this in mind, the aims of this study were: 1) to examine both toxic and essential chemical elements in seafood and river and sea fish samples sold in different Brazilian regions by inductively
coupled plasma mass spectrometer (ICP-MS); 2) to estimate the daily intake of these chemical elements by Brazilians.
The toxic elements Ba, Cd, Pb, Sr, V and Sb were found in higher concentrations in seafood than in either sea or river fish, while As concentrations were higher in both seafood and sea fish than in river fish. On the other hand, Hg levels were higher in river and sea fish. Concentrations of the essential chemical elements Co, Mn, Cu, Fe, Mg, Zn and Mo were significantly higher in seafood compared with both sorts of fish except for Se, whose levels were similar in seafood and sea fish. Daily intake of all chemical elements was estimated on the basis of a calculation of the amount of fish
consumed by Brazilian households (mean fish and seafood consumption of 11.0 g/person/day). The amount of toxic element in fish and seafood did not represent a risk for the Brazilian people. Moreover, fish and seafood seem to be a good source of selenium.
Keywords: River Fish; Sea Fish; Seafood; Toxic Elements; Essential Elements; Estimated Daily Intake; ICP-MS
1. Introduction
Diet quality is very important for promoting health and
lowering risk of nutritional-related chronic diseases such
as osteoporosis, diabetes and cardiovascular disease [1].
Fish is considered one of the healthiest foods, due to its
mainly cardioprotective effects [2]. Most of the benefit is
probably related to high levels of long-chain omega-3
polyunsaturated fatty acids (PUFAs), especially eicosapentaenoic
acid (EPA) and docosahexaenoic acid (DHA),
known for promoting anti-inflammatory effects [3,4]. Fish
is also a source of important nutrients besides PUFAs such
as vitamin E and essential chemical elements [5,6].
However, due to widespread environmental contamination
with possible accumulation of toxic elements in fish
samples [7,8] it is also of great importance to consider
the risks of fish consumption.
Of the many pollutants found in fish samples, mercury
(Hg) is one of the most widely recognized, especially
since the 1960’s, when methylmercury was discharged
from an industrial plant into Minamata Bay, Japan. Marine
life in the surrounding area was contaminated as was
the local population, for who fish and seafood are the main
source of proteins [7]. Fish contaminated with Hg as a
result of gold mining [9] or leaching from naturally contaminated
soils in this region [10] are also of great concern
in Amazonian rivers. This contamination increases
the risks of adverse toxic effects on riparian and indigenous
communities who rely on fish as a daily dietary
mainstay [11].
Other toxic chemical elements, such as arsenic (As),
cadmium (Cd) and lead (Pb), have also been measured in
fish and seafood samples in several regions of the world
[12-14]. The U.S. Food and Drug Administration [15]
has shown that fish and seafood are responsible for 90%
of Americans’ total As exposure. Moreover, Tressou et
al., 2004 [16] demonstrated in a probabilistic exposure
assessment that seafood may represent from 8 to 25% of
the total human dietary intake of Cd.
Despite the conflict between “fish as a source of essential
nutrients” and “risk of ingestion of contaminated
*Corresponding author. fish or seafood”, there is a paucity of studies examining
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
2
toxic and essential chemical elements in samples of seafood
and fish sold in Brazil. Therefore, this study aims to
evaluate essential, nonessential, and toxic elements in river
fish, sea fish and seafood from different Brazilian regions
by inductively coupled plasma mass spectrometry (ICPMS).
Furthermore, the daily intake of these chemical elements
by Brazilians was estimated.
2. Material and Methods
2.1. Chemicals and Instruments
High purity water (Milli-Q system, resistivity 18.2
MΩ·cm−1) was used in all experiments (Millipore RiOs-
DITM, Bedford, MA, USA). HNO3 was distilled in subboiling
stills (Kürner Analysentechnik) before use. Triton®
X-100 and tetramethyl ammonium hydroxide (TMAH)
25% (w/v) in water were purchased from Sigma–Aldrich
(St. Louis, USA). Before use, all materials used to prepare
and store the solution and samples (bottles and Falcon
® tubes) were cleaned in an acid bath (10% v/v)
HNO3 for 24 h. After this procedure, they were rinsed six
times with Milli-Q water and dried in the laminar flow
hood. All experiments were carried out in a clean room
(class 1000). All the standard solutions for calibration
were purchased from PerkinElmer (Shelton, CT, USA).
Essential, nonessential and toxic elements were all determined
with an inductively coupled plasma mass spectrometer
equipped with a reaction cell (DRC-ICP-MS
ELAN DRCII, PerkinElmer, SCIEX, Norwalk, CT, USA)
operating with high-purity argon (99.999%, Praxaair, Brazil).
The sample introduction system was composed of a
quartz cyclonic spray chamber and a Meinhard® nebulizer
connected by Tygon® tubes to the peristaltic pump
of the ICP-MS. The instrument settings and other operating
conditions for analysis were according to Batista
and colleagues [17].
2.2. Sample Selection and Chemical Assessment
Samples were collected between 2009-2011 in different
regions of Brazil (South, Southeast and Northeast). We
selected the fish and seafood most commonly consumed
by the Brazilian people. The samples were categorized as
1) river fish (n = 19); 2) sea fish (n = 18); and 3) seafood
(n = 14).
River fish samples included eyetail cichlids (Cichla spp),
pacu (Piaractus mesopotamicus), barred sorubim (Pseudoplatystoma
fasciatum), tilapia (Oreochromis niloticus),
piratinga (Piaractus brachypomus), threespot leporinus
(Leporinus friderici), spotted sorubim (Pseudoplatystoma
corruscans), gilded catfish (Brachplathystoma flavicans),
prochilods nei (Prochilodus spp), and piraiba (Brachyplathystoma
filamentosum). Sea fish samples included tuna
(Tunnus spp – Scombridae), Caribbean red snapper (Lutjanus
purpureus), blacktip shark (Carcharrhinus spp), sardine
(Sardinella spp), angel shark (Squatina squatina), hake
(Merluccius spp), weakfish (Cynoscion spp) and caitipa
mojarra (Diapterus rhombeus). From the seafood group,
we selected octopus (Octopus vulgaris), clam (Mytilus
galloprovincialis), shrimp (Caridina sp), squid (Loligo farbesi),
and mussel (Mytella guianensis).
For all groups, only the edible parts (muscle) of the
samples were used for the analysis. First, about 15 g of
each sample was weighed, frozen to –80°C and freezedried
(Liobrás L101, Brazil). Subsequently the samples
were weighed again and the percentage of water was
calculated. Then, the samples were milled and sieved (406
μm pore size) and then stored in Falcon® tubes in a dry
location until analysis.
Chemical elements were determined as follows: samples
(75 - 100 mg) were accurately weighed in triplicate
and 1 mL of TMAH 50% v/v was added. Samples were
homogenized rotationally (Tecnal TE 165, Brazil) for 24
hours. After that the volume was made up to 10 mL with
a diluent containing 0.5% v/v HNO3 and 0.01% p/v Triton
X-100 [17]. Analytical calibration standards were
prepared daily over the range of 0 - 20 ng·g−1 for the
trace elements (As, barium (Ba), Cd, Pb, Hg, antimony
(Sb), cobalt (Co), manganese (Mn), Se, molybdenum
(Mo), strontium (Sr) and vanadium (V) and from 0 -
5,000 ng·g−1 for the other elements, Cu, Fe, Mg) and Zn,
in the same diluent (0.5% v/v HNO3 and 0.01% p/v Triton
X-100). The correlation coefficient for calibration
curves was better than 0.9999. In all experiments 10 μg
L-1 of the internal standard Rh was used. As, Ba, Cd, Pb,
Hg, Sb, Co, Mn, Se, Fe, Mg, Zn, Cu, Mo, Sr and V detection
limits were 0.0023, 0.0060, 0.0021, 0.0076, 0.103,
0.0013, 0.0026, 0.0039, 0.024, 0.571, 0.147, 0.092, 0.019,
0.0051, 0.0042 and 0.181 ng·g−1, respectively.
In order to verify the accuracy of the data, the following
reference materials (RMs) were analyzed: 1) Fish
Protein DORM-3 from the NRC Institute for National
Measurement Standards, Canada; 2) Bovine liver SRM
1577; 3) Bovine muscle SRM 8414 and 4) Whole egg
powder SRM 8415, all from the National Institute of Standards
and Technology, USA.
2.3. Estimation of Daily Intake
Daily intake (EDI) of chemical elements was estimated
on the basis of a survey of the amount of fish consumed
by Brazilian households [18] and on the concentration of
elements in raw fish. T The average percentage of water
in the fish and seafood was 74%. Therefore, the EDI was
calculated using the formula:
EDI = Ec × M
in which EDI means the estimated daily intake of an element
(mg/day/person or μg/day/person); Ec is the element
concentration in raw fish and/or seafood; and M is
the mass of raw fish and/or seafood consumed daily in
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
3
Brazil. Risk characterization for toxic elements intake was
performed based on toxicological reference values provided
by the Joint Expert Committee on Food Additives
(JECFA) or European Food Safety Authority (EFSA)
(detailed in Table 4).
For essential elements the results were compared to the
dietary reference intakes (DRIs) from the Food and Nutrition
Board of the Institute of Medicine, 1997-2001 [19].
2.4. Statistical Analysis
Data for essential, nonessential and toxic elements were
reported as mean dry weight ± standard deviation (SD).
Levels of chemical elements in the river fish, sea fish and
seafood groups were compared using the Kruskal-Wallis
test, followed by Duncan’s post hoc. P values < 0.05 were
considered significant. Statistica® 8.0 (Statsoft Software
–USA) was used to analyze data.
3. Results and Discussion
Prior to analysis, quality controls were (reference materials)
were analyzed and the chemical element levels
obtained were very close to the certified reference values
(Table 1), ensuring the accuracy of the method used for
ordinary sample analysis.
Levels of chemical elements in the samples analyzed
in the present study are shown in Tables 2 and 3. The
concentrations of the toxic elements Ba, Cd, Pb, Sr, V and
Sb were statistically higher in seafood than in either river
or sea fish (Table 2). Arsenic levels were higher in seafood
and sea fish than in river fish. On the other hand,
Hg levels were higher in fish (river and sea) than in marine
invertebrates, suggesting that this element bioaccumulates
in the food web.
Similarly, the concentrations of essential chemical elements
except Se were significantly higher in seafood than
in either kind of fish. Se levels in sea fish and sea food
were comparable (Table 3).
Furthermore, As is the toxic element with the highest
magnitude of concentration in fish, with the other toxic
elements listed in descending order: As > Sr > Hg >
Ba-V > Pb-Cd > Sb. In seafood, however, this order was
different: Sr > As > Ba > Cd > V > Pb > Hg > Sb (Table
2). The same pattern held true for essential elements. In
thetissues of both types of fish, the magnitude order of
the essential elements was similar (Mg > Zn > Fe > Se >
Cu > Mn > Mo > Co) but in seafood it differed somewhat
(Mg > Fe > Zn > Cu > Se > Mn > Mo > Co) (Table 3).
Anthropogenic activities have resulted in massive environmental
pollution, making both aquatic and terrestrial
environments vulnerable to a range of contaminants [20,21].
Several studies have been carried out to determine the
distribution of chemical elements in aquatic ecosystems
[20-22]. However, there is no consensus among the available
studies. This may be due to different habitats, species,
growth rates or metal accumulation and detoxification
mechanisms [23-24]. Most of the chemical elements evaluated
in the present study accumulated more intensely in
Table 1. Analytical performance for the determination of essential and non-essential elements in certified reference materials
DORM-3 (fish protein), SRM 1577 (bovine liver), SRM 8414 (bovine muscle), and SRM 8415 (whole egg powder) (values are
denoted as mean ± SD).
DORM-3
Fish protein
SRM 1577
Bovine Liver
SRM 8414)
Bovine Muscle
(SRM 8415)
Whole egg
Chemical
elements Target Found Target Found Target Found Target Found
Co (ng/g) - - 250 225±27 7±3 8±3 12±5 15±2
Mn (μg/g) 4.6* 4.4 ± 0.4 10.5 ± 1.7 9.2 ± 0.9 0.37 ± 0.09 0.39 ± 0.1 1.78 ± 0.38 1.71 ± 0.64
Se (μg/g) 3.3* 3.6 ± 0.3 0.73 ± 0.06 0.75 ± 0.14 0.076 ± 0.010 0.083 ± 0.011 1.39 ± 0.17 1.49 ± 0.12
Fe (μg/g) 347 ± 20 359 ± 18 184 ± 15 163 ± 14 71.2 ± 9.2 65 ± 11 112 ± 16 117 ± 10
Mg (μg/g) - - 601 ± 28 615 ± 24 960 ± 95 982 ± 56 305 ± 27 308 ± 21
Zn (μg/g) 51.3 ± 3.1 53.6 ± 2.4 127 ± 16 138 ± 11 142 ± 14 149 ± 10 67.5 ± 7.6 68.6 ± 3.9
Cu (μg/g) 15.5 ± 0.63 15.1 ± 0.84 160 ± 8 150 ± 9 2.84 ± 0.45 2.48 ± 0.38 2.7 ± 0.35 3.0 ± 0.28
Mo (μg/g) - - 3.5 ± 0.3 3.2 ± 0.3 0.08 ± 0.06 0.07 ± 0.04 0.247 ± 0.023 0.246 ± 0.09
As (ng/g) 6,880 ± 300 6,570 ± 237 50 53 ± 2 9 ± 3 8 ± 3 10 14 ± 3
Ba (μg/g) - - - - 0.05 0.04 ± 0.01 3 3.3 ± 0.4
Cd (ng/g) 2 90 ± 20 276 ± 21 500 ± 30 471 ± 34 13 ± 11 12 ± 4 5 6 ± 2
Pb (ng/g) 395 ± 50 377 ± 18 129 ± 4 119 ± 7 380 ± 240 371 ± 35 61 ± 12 54 ± 13
Sr (ng/g) - - 136 ± 1 129 ± 7 52 ± 15 62 ± 9 5630 ± 430 5617 ± 387
V (ng/g-) - - - - - - 459 ± 81 456 ± 12
Hg (ng/g) 382 ± 60 350 ± 34 4 ± 2 5 ± 2 5 ± 3 4 ± 2 4 ± 3 3 ± 1
Sb (ng/g) - - - - 10 12 ± 3 - -
*Informative values.
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
4
Table 2. Concentrations of nonessential and toxic elements in river fish, sea fish, and seafood from different regions of Brazil,
represented by mean ± standard deviation (SD) and range.
Toxic/non essential elements River fish
(n = 19)
Sea fish
(n = 18)
Seafood
(n = 14)
As (ng/g) 240 ± 369 (3 - 1,571)* 18,785 ± 20,835 (3,029 - 61,522) 22,726 ± 19,998 (1,043 - 61,439)
Ba (ng/g) 92 ± 106 (5 - 409) 117 ± 113 (3 - 522) 1,617 ± 1,085 (118 - 4,482)*
Cd (ng/g) 4 ± 4 (1 - 25) 72 ± 127 (3 - 605) 680 ± 1,059 (9 - 3,473) *
Pb (ng/g) 8 ± 7 (1 - 55) 13 ± 17 (2 - 89) 130 ± 202 (9 - 754)*
Sr (ng/g) 276 ± 186 (74 - 828) 1,479 ± 1,223 (248 - 4,995) 53,144 ± 34,546 (3,176 - 107,741)*
V (ng/g) 19 ± 22 (1 - 86)# 129 ± 118 (20 - 452) 414 ± 386 (39 - 1,568)*
Hg (ng/g) 152 ± 261 (2 - 1,613) 181 ± 237 (6 - 894) 38 ± 35 (5 - 137)*
Sb (ng/g) 3 ± 5 (1 - 22) 3 ± 2 (1 - 8) 8 ± 7 (1 - 32)*
*Statistically different from the others (p < 0.01). #Statistically different from sea fish (P < 0.01).
Table 3. Concentrations of essential elements in river fish, sea fish, and seafood from different regions of Brazil, represented
by mean ± standard deviation (SD) and range.
Essential elements River fish
(n = 19)
Sea fish
(n = 18)
Seafood
(n = 14)
Co (ng/g) 22 ± 25 (3 - 102) 18 ± 11 (5 - 55) 91 ± 111 (11 – 402)*
Mn (ng/g) 161 ± 115 (30 - 376) 328 ± 252 (37 - 1,064) 1,394 ± 988 (417 - 3,855)*
Se (ng/g) 1,013 ± 703 (200 - 2,840)* 2,998 ± 1,235 (320 - 5.514) 2,446 ± 1,071 (917 - 6,028)
Cu (ng/g) 719 ± 377 (214 - 1,969) 2,202 ± 1,284 (549 - 5,359) 17,390 ± 11,730 (5,788- 4,364)*
Mo (ng/g) 77 ± 69 (2 - 302) 94 ± 98 (14 - 403) 193 ± 204 (35 - 690)*
Fe (μg/g) 3 ± 1 (1 - 7) 14 ± 19 (2 - 87) 58 ± 85 (2 - 286)*
Mg (μg/g) 265 ± 171 (23 - 622) 198 ± 146 (12 - 471) 555 ± 416 (36 - 1,497)*
Zn (μg/g) 11 ± 6 (3 - 33)# 20 ± 15 (3 - 67) 46 ± 21 (11 - 119)*
*Statistically different from the others (p < 0.01). #Statistically different from sea fish (P < 0.01).
seafood invertebrates than in fish. The species classified
as seafood in this study are in general shrimps and mollusks,
known to be the scavengers of the sea [25]. Therefore,
the higher content of most chemical elements found
in seafood may be attributed to the high filtering activity
of these animals.
Hg levels in fish (both river and sea) were similar to
those presented by Cui and colleagues [22]. The authors
showed higher Hg levels moving up the food chain.
Hence, the higher Hg levels observed in fish compared to
seafood imply that feeding habits may affect Hg accumulation
at higher trophic levels [26]. In addition, it is
worth pointing out that our study also evaluated fish from
the Brazilian Amazon, a region known to be contaminated
with Hg [27]. Despite the wide range of Hg levels,
our results showed mean levels of 152 ng/g in river fish
and 181 ng/g in saltwater fish. The Hg levels found by
Burger et al. [28] sea fish from New Jersey were similar
to our outcomes (around 170 ng/g Hg) while Tuzen [29]
reported values from 25 to 84 ng/g Hg in sea fish from
Turkey. On the other hand, the Hg values (mean of 309
ng/g Hg) in fish from the Savannah River in the southeastern
United States were considerably higher than
those in our river fish group [30].
Levels of As were significantly higher in sea fish (mean
of 18.7 μg/g) and seafood (mean of 22.7 μg/g) than in
river fish (mean of 0.24 μg/g) (Table 2). However these
concentrations are considerable lower than those recently
reported in edible freshwater fish species (41 - 61.5 μg/g)
collected from the Ravi River, Pakistan [31]. It must be
pointed out that the toxic properties of As are directly
related to its chemical form [32]. Although the As levels
found in our samples were high, unfortunately they are
only total As amounts. Most of this As is in organic form,
mainly arsenobetaine or arsenocholine, which are nontoxic
forms of this metalloid. The widespread occurrences of
Pb and Cd in the environment pose a threat to human
health and nowadays there is debate about whether a
there is any safe exposure threshold for lead. Storelli et al.
[14] determined Cd and Pb levels in salted anchovies in
Italy. They found Cd levels around 225 ng/g while we
found sea fish with mean Cd levels of 72 ng/g. They found
a mean of 80 ng/g for Pb compared to 13 ng/g in our
samples. Storelli showed higher Cd than Pb levels while
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
5
our data show similar levels in sea fish [14].
In order to determine the concentrations of elements
including Ba in the 2006 UK Total Diet Study, a several
kinds of food were examined [33]. Their fish samples had
a mean Ba level of 140 ng/g, which is very similar to the
mean found in the present study for Brazilian river fish
samples (mean 92 ng/g Ba) and sea fish samples (mean
117 ng/g Ba). On the other hand, Ba levels in seafood
samples in our study were much higher (mean of 1.61
μg/g Ba) which indicates that seafood is an important Ba
source for Brazilians.
Levels of strontium (Sr), antimony (Sb) and vanadium
(V) in edible fish and seafood have been poorly investigated.
The Sb levels we found are in close agreement with
those of Rose and colleagues [33], who found a mean of
2.6 ng/g compared to the 3 ng/g observed here (for both
river and sea fish). In UK fish, Sr mean levels were 2.5
μg/g [33]. This value was higher than those found in our
Brazilian samples: 276 ng/g for river fish and 1.5 μg/g
for sea fish. Fish samples from the Adriatic Sea had V
levels of around 70 ng/g [34] while the V level in our sea
fish sample was 129 ng/g. Antimony, Sr and V were also
determined in fish and seafood from the marketplace in
France [35]. In fresh fish samples, means were 1.5 ± 2.9
ng/g for Sr, 32 ± 49 ng/g for V, and 1 ng/g for Sb. The
same authors found means of 12.6 ± 14.5; 200 ± 252 and
3 ± 2 ng/g for Sr, V and Sb, respectively. In contrast to
fish, French seafood Sr and Sb levels were similar to
those of the Brazilian samples. However, V levels were
lower for French seafood.
The mean levels of the important antioxidant Se in the
present study were approximately 1 μg/g and 3 μg/g for
river fish and sea fish, respectively (Table 3). These levels
may be considered high when compared with those
reported in previous studies in other geographic regions.
For instance, the mean Se concentration for 19 fish species
in New Jersey was 300 ng/g [28]. A Turkish report
found a mean Se level of 440ng/g for ten different Black
Sea fish species [29]. Few studies provide Se levels in
river fish samples and the values are in general lower than
those found in the present study. This variability may be
due to different species, ages and also different study
locations. Cobalt (Co) is an essential trace element whose
main source for humans is beef [36]. Co levels ranged
from 3 to 402 ng/g (dry weight) in the three groups of
food samples analyzed in this study. Other studies have
also shown low Co levels in fish. Mean Co levels of 10 ±
20 ng/g (dry weight) for edible marine fishes, and 10 ±
20 ng/g (dry weight) for mollusks were reported in marine
fish and mollusks from the Lakshadweep Archipelago
in the Arabian Sea [37]. Both values were lower
than those found in this study with Brazilian samples: 18
± 11 ng/g for sea fish and 91 ± 111 for seafood. The
mean levels of Co in French fish and seafood samples,
however, were 5 ± 7 ng/g (fresh mass) and 67 ± 104 ng/g
(fresh mass), respectively [35]. These values are in close
agreement with our findings. Conversely, the Co levels of
three commercial sea fish from Turkey northeast Mediterranean
Sea) were much higher than our results: around
1,500 ng/g (ranging from 30 to 5,610 ng/g (dry weight)
[38].
Copper levels in Brazilian fish samples varied from
214 to 5,359 ng/g (for both river and sea fish) (Table 3).
Our findings are in close agreement with Storelli [39]
and Ersoy and Çelik [40]. These authors found mean
levels of 1.35 ± 0.57 μg/g in fish samples from the Mediterranean
Sea [41], and from 1.06 to 2.09 mg/kg in fish
from the eastern Mediterranean in Turkey [39]. The
mean values for sea fish samples were 2,202 ± 1,284
ng/g. The copper level in Brazilian seafood samples were
17,390 ± 11,730 ng/g. These values are in agreement
with those reported for the same samples in Poland (Cu
range: 0.1 - 18.4 mg/kg) [41].
Our values for the essential element Mn are in close
agreement with those found in other geographic regions
[40]. For fish samples from the eastern Mediterranean
Sea, Mn values ranged from 0.11 to 0.64 μg/g [40], while
our mean sea fish Mn levels were 328 ± 252 ng/g. On the
other hand, Mn levels are considerably lower in Brazilian
than in Polish seafood (417 - 3,855 ng/g against 0.1 - 40
μg/g in Poland [41]).
The Mg levels of both sorts of Brazilian fish in our study
were very comparable while seafood presented somewhat
higher Mg concentrations (Table 3). In agreement with
our findings, Mg levels varied from 94.1 to 210 mg/kg
(wet weight) in Turkish fish [40], and from 52.6 - 532
mg/kg (wet weight) in Polish seafood [41].
It is interesting that of the chemical elements evaluated
here, Mg, Fe and Zn were found most abundantly in both
Brazilian fish and seafood samples. Moreover, Fe and Zn
levels were higher in seafood than in fish (Table 3). Fe
levels varied from 0.4 to 26.1 μg/g (wet weight) and Zn
levels varied from 0.06 to 39.3 μg/g (wet weight) in marine
fish samples from Rio de Janeiro State, Brazil [42].
Likewise, in French fish samples, mean Fe and Zn concentrations
were, respectively, 4.42 ± 4.51 and 5.43 ± 4.85
μg/g (fresh weight) [35]. Finally, seafood from France had
about twice the levels found in this study for Fe and Zn.
Furthermore, the Zn concentrations found in the
present study are comparable to those found in a previous
study of samples collected in Italian markets. Although
these researchers measured Zn levels in fresh samples,
mean Zn levels in fish (8.43 mg/kg) and in seafood, or
more specifically, mollusks (33 mg/kg) [39], were very
similar to our values (Table 2).
Little is known about the levels of molybdenum (Mo),
another essential element, in edible fish and seafood. We
found higher levels of Mo in seafood (mean of 193 ± 204
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
6
ng/g) than in river or sea fish samples (mean of 77 ± 69
and 94 ± 98 ng/g). In comparison, fish and seafood from
French markets had Mo means of 13 ± 14 ng/g and 123 ±
106 ng/g, respectively [35].
The mean consumption of fish and seafood in Brazil is
11.0 g/person/day. However, consumption varies considerably
from region to region. For instance, people in the
North and Northeast consume 48 and 14 g/person/day,
respectively, while in the South the consumption is only
4 g/person/day [18]. Seafood and fish are important sources
of proteins for many people. Therefore estimating the daily
intake (EDI) of essential and toxic elements from the
ingestion of this food is fundamental to evaluate risk.
Table 4 shows Brazilian EDI for toxic, essential and
nonessential elements based on the mean 11 g/person/day.
EDI for Cd and Pb in both types of fish and seafood
were 0.91 and 0.18 μg·day–1, respectively. These values
are relatively low. For example, based on a consumption
of 20 g/person/day, Turkish EDI levels for Cd and Pb
were 1.7 and 4.4 μg·day–1, respectively [40] and for Spanish
men and women As, Cd, Hg and Pb EDIs were 195,
1.1, 9.4 and 2.1μg·day–1, respectively [48]. From this it is
clear that the Spanish fish- and seafood- based EDI for
As and Hg are around 4 and 20 times higher than the
estimated values for Brazilians. Nevertheless, despite none
of them exceeded the limits established by JECFA/FAO
to methylmercury [46], or to arsenic [43], it is important
to keep in mind the power of bioaccumulation of some
elements, such Hg, whose chronic exposure could
represent a risk for Brazilians [27]. And although the
considerable As daily intake for Brazilians, it must be
considered that commonly the least toxic As form – arsenobetaine
– is present in fish and seafood [49].
Regarding essential elements fish and seafood contributed
moderately to the dietary reference intake (DRI)
for Se (>14%) and Cu (3.5%). For the other elements
(Mn, Fe, Mg, Zn and Mo) the contribution to the DRI is
lower than 1.2% (Table 4). However, considering the
highest Brazilian fish/seafood consumption (48
g/person/day), these sorts of food represent a source of
Se and Cu (61 and 15%, respectively). On the other hand,
Northern people also intake more levels of toxic elements,
although none of them, except As, exceeded the
toxicological reference values.
Thus, considering Brazilians’ moderate fish and seafood
consumption, the present study sheds new light on the
occurrence of essential, nonessential and toxic elements in
river and sea fish and seafood from different Brazilian
regions. There was a significant difference between chemical
element concentrations in fish and in seafood samples,
with a predominance and higher accumulation in seafood
Table 4. Estimated daily intake of toxic, essential and nonessential and considerations regarding the potential health risk
through consumption of in nature fishes (sea and river) and seafood by Brazilians.
Estimated Daily Intake
Analytes River fish Sea fish Seafood Sum of intake Toxicological reference valuesa
Toxic elementsa
As (μg·day–1) 0.290 22.7 27.5 50.4 21 - 560b
Ba (μg·day–1) 0.111 0.141 1.954 2.2 -
Cd (μg·day–1) 0.005 0.087 0.822 0.91 58.3c
Pb (μg·day–1) 0.010 0.016 0.157 0.18 105d
Hg (μg·day–1) 0.184 0.219 0.046 0.45 16e
Sb (μg·day–1) 0.004 0.004 0.010 0.02 60f
Essential elementsa Sum of intake (% DRI) DRIg
Co (μg·day–1) 0.027 0.022 0.110 0.16 -
Mn (μg·day–1) 0.195 0.396 1.684 2.28(0.13 W/0.10 M) 1800W/2300M
Se (μg·day–1) 1.224 3.622 2.955 7.80(14.2) 55
Fe (mg·day–1) 0.004 0.017 0.070 0.09(0.5 W/1.1 M) 8 W/18 M
Mg (mg·day–1) 0.320 0.239 0.671 1.23(0.38 W/0.29 M) 320 W/420 M
Zn (mg·day–1) 0.013 0.024 0.056 0.09(1.18 W/0.85 M) 8 W/11 M
Cu (μg·day–1) 0.869 2.661 21.011 24.5(3.5) 700
Mo (μg·day–1) 0.093 0.114 0.233 0.44(0.98) 45
Nonessentiala
Sr (μg·day–1) 0.334 1.787 64.211 66.332 -
V (μg·day–1) 0.023 0.156 0.500 0.679 -
Notes: a Considering a person weighing 70 kg. W: women; and M: men. b Range of values for the 95% lower confidence limit of the benchmark dose of 1%
extra risk (BMDL01) [43]. c Provisional Tolerable Monthly Intake/30 [44]; d BMDL: benchmark dose lower confidence limit, based on cardiovascular effects
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
7
[45]; eProvisional tolerable daily intake for methylmercury PTWI/7 [46];.f Tolerable dose Intake (TDI) [47]; gDietary reference intakes (DRI) for essential
elements are the most recent set of dietary recommendations established by the Food and Nutrition Board of the Institute of Medicine [19].
samples.
Finally, the estimated daily intake for toxic elements
shows that fish and seafood consumption apparently do
not represent a risk for Brazilians. Nonetheless since there
are evidences for bioaccumulation for some toxic chemical
elements such as Hg and As, data have to be interpreted
cautiously, even with low intake of these elements.
Moreover, fishes and seafood are an interesting source of
the essential element Se for Brazilians. However, due to
different dietary habits, Brazilian regions differ considerably
regarding fish and seafood consumption, especially
North and South. Thus, specific analysis of population
sub-groups is essential to acquire more precise
toxicological risk data.
4. Acknowledgements
The authors would like to acknowledge the financial support
of the São Paulo State Foundation for Scientific Research
(FAPESP, Brazil) and thank the Brazilian National
Council for Scientific and Technological Development
(CNPq) and the Foundation for the Coordination of Improvement
of Higher Education Personnel (CAPES) for
fellowships.
REFERENCES
[1] “Dietary Guidelines for Americans.” U. S. Department of
Agriculture, U. S. Department of Health and Human Services,
2010.
[2] H. O. Bang, J. Dyerberg, H. M. Sinclair, “The composition
of the Eskimo food in northwestern Greenland,” The
American Journal of Clinical Nutrition, Vol. 33, 1980, pp.
2657-2661.
[3] D. N. Carroll, M. T. Roth, “Evidence for the Cardioprotective
Effects of Omega-3 Fatty Acids,” The Annals of
pharmacotherapy, Vol. 36, 2002, pp. 1950-1956.
[4] A. P. Simopoulos, “Omega-3 fatty acids in inflammation
and autoimmune diseases,” Journal of the American College
of Nutrition, Vol. 21, No. 6, 2002, pp. 495–505.
[5] C. Afonso, H. M. Lourenço, C. Pereira, M. F. Martins, M.
L. Carvalho, M. Castro, M. L. Nunes, “Total and organic
mercury, selenium and a-tocopherol in some deep-water
fish species,” Journal of the science of food and agriculture,
Vol. 88, 2008, pp. 2543–2550.
[6] S. Serini, E. Piccioni, C. Rinaldi, D. Mostra, G. Damiani,
G. Calviello, “Fish from an artificial lake: n-3 PUFA
content and chemical–physical and ecological features of
the lake,” Journal of Food Composition and Analyses,
Vol. 23, 2010, pp. 133–141.
[7] M. Harada, “Minamata Disease: Methylmercury Poisoning
in Japan Caused by Environmental Pollution” Critical
Reviews in Toxicology, Vol. 25, No 1, 1995, pp. 1-24.
[8] C. R. Estrellan, F. Iino, “Toxic emissions from open
burning”, Chemosphere, Vol. 80, 2010, pp. 193–207.
[9] O. Malm, W. C. Pfeiffer, C. M. M. Souza, R. Reuther,
“Mercury pollution due to gold mining in the Madeira
river basin, Brazil,” Ambio, Vol. 19, 1990, pp. 11-15.
[10] M. Roulet, M. Lucotte, "Geochemistry of mercury in
pristine and flooded ferralitic soils of a tropical rain forest
in French Guiana, South America,” Water, Air and Soil
Pollution, Vol. 80, 1995, pp. 1079-1088.
[11] C. J. S. Passos, D. Mergler, M. Lemire, M. Fillion, J. R.
D. Guimarães, “Fish consumption and bioindicators of
inorganic mercury exposure,” The Science of the total
Environmental, Vol. 373, 2007, pp. 68–76.
[12] X. Liao, T. B. Chen, H. Xie, Y. R. Liu, “Soil As contamination
and its risk assessment in areas near the industrial
districts of Chenzhou city, Southern China,” Environment
International, Vol. 31, 2005, pp. 791–798.
[13] A. Gupta, D. K. Rai, R. S. Pandey, B. Sharma, “Analysis
of some heavy metals in the riverine water, sediments and
fish from river Ganges at Allahabad,” Environmental
Monitoring and Assessment, Vol. 157, 2009, pp. 449-458.
[14] M. M. Storelli, L. Giachi, D. Giungato, A. Storelli, “Occurrence
of heavy metals (Hg, Cd, and Pb) and polychlorinated
biphenyls in salted anchovies,” Journal of Food
Protection, Vol. 74, No. 5, 2011, pp. 796-800.
[15] United States Food and Drug Administration, “Guidance
document for arsenic in shellfish,” Washington, DC: U.S.
Food and Drug Administration, 1993, pp 25–27.
[16] J. Tressou, A. Crépet, P. Bertail, M. H. Feinberg, J. Ch.
Leblanc, “Probabilistic exposure assessment to food
chemicals based on extreme value theory. Application to
heavy metals from fish and sea products”, Food and
Chemical Toxicology, Vol. 42, No. 8, 2004, pp.
1349-1358.
[17] B. L. Batista, D. Grotto, J. L. Rodrigues, V. C. O. Souza,
F. Barbosa, “Determination of trace elements in biological
samples by inductively coupled plasma mass spectrometry
with tetramethylammonium hydroxide solubilization
at room temperature,” Analytical Chimica Acta,
Vol. 646, No. 1-2, 2009, pp. 23–29.
[18] Instituto Brasileiro de Geografia e Estatística – IBGE,
“Aquisição alimentar domiciliar per capita anual, por
Grandes Regiões, segundo os produtos, período
2008–2009,” Brasilia, Brazil, 2010.
[19] Institute of Medicine – IOM, “Dietary reference intakes
for vitamin A, vitamin K, arsenic, boron, chromium,
copper, iodine, manganese, molybdenum, nickel, silicon,
vanadium and zinc,” Washington (DC, USA): National
Academy Press, 2002.
[20] P. B. P. Kfouri, R. C. L. Figueira, A. M. G. Figueiredo, S.
H. M. Souza, B. B. Eichler, “Metal levels and foraminifera
occurrence in sediment cores from Guanabara Bay,
Rio de Janeiro, Brazil”, Journal of Radioanalytical and
Nucelar Chemistry, Vol. 265, N. 3, 2005, pp. 459-466.
[21] M. Longjiang, F. Qiang, M. Duowen, H. Ke, Y. Jinghong,
“Contamination assessment of heavy metal in surface seEvaluation
by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
8
diments of the Wuding River, northern China” Journal of
Radioanalytical and Nucelar Chemistry, Vol. 290, No. 2,
2001, pp. 409-414.
[22] B. Cui, Q. Zhang, K. Zhang, X. Liu, H. Zhang, “Analyzing
trophic transfer of heavy metals for food webs in the
newly-formed wetlands of the Yellow River Delta, China,”
Environmental Pollution, Vol. 159, No. 5, 2011, pp.
1297-306.
[23] L. Marin-Guirao, J. Llotet, A. Marin, “Carbon and nitrogen
stable isotopes and metal concentration in food webs
from a mining-impacted coastal lagoon” The Science of
the Total Environmental, Vol. 393, 2008, pp. 118-130.
[24] V. Laura, “Metallothioneins in aquatic organisms: fish,
Crustaceans, Molluscs, and Echinoderms”, Metal Ions in
Life Sciences, Vol, 5, 2009, pp. 99-237.
[25] S. A. Oustromov, “Some aspects of water filtering activity
of filter-feeders,” Hydrobiologia, Vol, 542, No. 1,
2005, pp. 275–286.
[26] Z. S. Zhang, X. G. Lu, Q. C. Wang, D. M. Zheng, “Mercury,
cadmium and lead biogeochemistry in the
soil-plant-insect system in Huludao city,” Bulletin of Environmental
Contamination and Toxicology, Vol. 83,
2009, pp. 255-259.
[27] D. Grotto, J. Valentini, M. Fillion, C. J. S. Passos, S. C.
Garcia, D. Mergler, F. Jr. Barbosa, “Mercury exposure
and oxidative stress in communities of the Brazilian
Amazon,” The Science of the Total Environmental, Vol.
408, 2010, pp. 806–811.
[28] J. Burger, C. Jeitner, M. Gochfeld , “Locational differences
in mercury and selenium levels in 19 species of
saltwater fish from New Jersey,” Journal of toxicology
and environmental health A, Vol, 74, No. 13, 2011, pp.
863-874.
[29] M. Tuzen, “Toxic and essential trace elemental contents
in fish species from the Black Sea, Turkey,” Food and
Chemical Toxicology, Vol. 47, 2009, pp. 1785–1790.
[30] J. Burger, K. F. Gaines, C. S. Boring, W. L. Jr. Stephens,
J. Snodgrass, M. Gochfeld, “Mercury and selenium in
fish from the Savannah river: species, trophic level, and
locational differences,” Environmental Research, Vol. 87,
No. 2, 2001, pp. 108-118.
[31] S. Nawaz, S. A. Nagra, Y. Saleem, A. Priydarshi, “Determination
of heavy metals in fresh water fish species of
the River Ravi, Pakistan compared to farmed fish varieties”
Environment Monitoring and Assessment, Vol. 167,
2010, pp. 461–471.
[32] National Research Council, US – NRC, “Arsenic in
drinking water: 2001 update. Subcommittee on Arsenic in
Drinking Water,” National Academies Press, 2001, 225
pages.
[33] M. Rose, M. Baxter, N. Brereton, C. Baskaran, “Dietary
exposure to metals and other elements in the 2006 UK
Total Diet Study and some trends over the last 30 years,”
Food Additives and Contaminants Part A, Vol. 27, No.10,
2010, pp. 1380-1404.
[34] A. Sepe, L. Ciaralli, M. Ciprotti, R. Giordano, E. Funari,
S. Costantini, “Determination of cadmium, chromium,
lead and vanadium in six fish species from the Adriatic
Sea,” Food Additives and Contaminants Part A, Vol. 20,
No. 6, 2003, pp. 543-552.
[35] T. Guérin, R. Chekri, C. Vastel, V. Sirot, J. C. Volatier, J.
C. Leblanc, L. Noël, Determination of 20 trace elements
in fish and other seafood from the French market. Food
Chemistry, Vol. 127, 2011, pp. 934–942.
[36] United States Department of Agriculture – USDA - Nutrient
Data Laboratory. Available at
http://www.ars.usda.gov/services/docs.htm?docid=9673.
Accessed on 25 October 2011.
[37] K. V. Dhaneesh, M. Gopi, R. Ganeshamurthy, T. T. A.
Kumar, T. Balasubramanian, “Bio-accumulation of metals
on reef associated organisms of Lakshadweep Archipelago,”
Food Chemistry, Vol. 131, No. 3, 2011, pp.
985-991.
[38] A. Türkmen, M. Türkmen, Y. Tepe, I. Akyurt, “Heavy
metals in three commercially valuable fish species from
Iskenderun Bay, Northern East Mediterranean Sea, Turkey,”
Food Chemistry, Vol. 91, 2005, pp. 167–172.
[39] M. M. Storelli, “Intake of essential minerals and metals
via consumption of seafood from the Mediterranean Sea,”
Journal of Food Protection, Vol. 72, No. 5, 2009, pp.
1116-1120.
[40] B. Ersoy, M. Celik, “The essential and toxic elements in
tissues of six commercial demersal fish from Eastern Mediterranean
Sea,” Food and Chemical Toxicology, Vol. 48,
No. 5, 2010, pp. 1377-1382.
[41] M. Kwoczek, P. Szefer, E. Hać, M. Grembecka, “Essential
and toxic elements in seafood available in poland
from different geographical regions,” Journal of Agricultural
and Food Chemistry, Vol. 54, No. 8, 2006, pp.
3015-3024.
[42] R. J. Medeiros, L. M. dos Santos, A. S. Freire, R. E. Santelli,
A. M. C. B. Braga, T. M. Krauss, S. C. Jacob, “Determination
of inorganic trace elements in edible marine
fish from Rio de Janeiro State, Brazil,” Food Control,
Vol. 23, 2012, pp. 535-541.
[43] EFSA - European Food Safety Authority Panel on Contaminants
in the Food Chain (CONTAM) “Scientific
Opinion on Arsenic in Food”, EFSA Journal Vol. 7, No.
10, 2009, 1351.
[44] JECFA - Joint FAO/WHO Expert Committee on Food
Additives, Seventy-third meeting, Geneva, 2010.
[45] EFSA - European Food Safety Authority Panel on Contaminants
in the Food Chain (CONTAM) (2010) Scientific
Opinion on Lead in Food. EFSA Journal, 8(4):1570.
[46] JECFA - Joint FAO/WHO Expert Committee on Food
Additives, Sixty-first meeting, Rome, 2003.
[47] World Health Organization – WHO, “Antimony in
drinking water”, Background document for preparation of
WHO guidelines for drinking water quality
(WHO/SDEWSH/03.04/74). Geneva. Switzerland, 2003.
[48] G. Falcó, J. M. Llobet, A. Bocio, J. L. Domingo, “Daily
Intake of Arsenic, Cadmium, Mercury, and Lead by
Consumption of Edible Marine Species”, Journal of
Agricultural and Food Chemistry, Vol. 54, 2006, pp.
6106-6112.
Evaluation by ICP-MS of Essential, Nonessential and Toxic Elements in Brazilian Fish and Seafood Samples
Copyright © 2012 SciRes. FNS
9
[49] Y. Shibata, M. Morita, K. Fuwa, “Selenium and arsenic in
biology: their chemical forms and biological functions”,
Advances in Biophysics, Vol. 28, 1992, pp. 31-80.