Heavy metals: Implications associated to fish consumption

Heavy metals: Implications associated to fish consumption

Environmental Toxicology and Pharmacology 26 (2008) 263–271 Contents lists available at ScienceDirect Environmental Toxicology and Pharmacology jour...

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Environmental Toxicology and Pharmacology 26 (2008) 263–271

Contents lists available at ScienceDirect

Environmental Toxicology and Pharmacology journal homepage: www.elsevier.com/locate/etap

Mini-review

Heavy metals: Implications associated to fish consumption M.I. Castro-González a , M. Méndez-Armenta b,∗ a b

Depto. Nutrición Animal, Instituto Nacional de Ciencias Médicas y Nutrición SZ, Mexico Lab. Neuropatología Experimental, Instituto Nacional de Neurología y Neurocirugía MVS, Insurgentes Sur 3877, La Fama, Tlalpan, C.P. 14269, Mexico

a r t i c l e

i n f o

Article history: Received 15 February 2008 Received in revised form 30 May 2008 Accepted 10 June 2008 Available online 18 June 2008 Keywords: Fish consumption Mercury Cadmium Lead Arsenic Heavy metals

a b s t r a c t Metals are being utilized of ways in industries and agriculture; particularly heavy metals such as mercury, cadmium, lead and arsenic constitute a significant potential threat to human health because they are associated to many adverse effects on health. The consumption of fish is recommended because it is a good source of omega-3 fatty acids, which have been associated with health benefits due to its cardio-protective effects. However, the content of heavy metals discovered in some fish makes it difficult to establish clearly the role of fish consumption on a healthy diet. Therefore the present mini-review accounts for the recent evidence of the effect of these toxic metals on the human health and their possible implications in fish consumption. © 2008 Elsevier B.V. All rights reserved.

Contents 1. 2.

3. 4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Heavy metals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Mercury . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Cadmium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Lead . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Arsenic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Health effects of fish consumption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Final commentary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Metals differ from other toxic substances in that they are neither created nor destroyed by humans. Humans have used heavy metals in many different areas for thousands of years; this use influences their potential for health effects in at least two major ways: first, by environmental transport, that is, by human or anthropogenic contributions to air, water, soil, and food, and second by altering the speciation or biochemical form of the element (Beijer and Jernelov, 1986). Although several adverse health effects of heavy metals have

∗ Corresponding author. E-mail address: [email protected] (M. Méndez-Armenta). 1382-6689/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.etap.2008.06.001

263 264 264 266 266 267 268 269 269 269

been known for a long time, the exposure to these elements continues; moreover, it is even increasing in some parts of world, in particular in the less developed countries, though emissions have declined in most developed countries over the last 100 years (Jarup, 2003). Owing to their toxicity persistence and tendency to accumulate in water and sediment, heavy metals and metalloids, when occurring in higher concentrations, become severe poisons for all living organisms (Has-Schön et al., 2006). Diet is the main route of exposure to heavy metals in the case of population no-exposed to them. Although the basic role of nutritionally essential metals is to provide some components of a vital biochemical or enzymatic reaction, a number of metabolic interactions between nutritionally essential and nonessential toxic metals may reduce the health hazard of the toxic metal (Goyer, 1997).

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Increased concentrations of metals; mainly mercury, cadmium and lead; have been observed in freshwater fish in open waters. This is important because the water metal concentration correlates positively with concentrations in fish tissue (Svobodova et al., 1996). The level of heavy metal bioaccumulation in fish tissues is influenced by biotic and abiotic factors, such as fish biological habitat, chemical form of metal in the water, water temperature and pH value, dissolved oxygen concentration, water transparency, as well as by fish age, gender, body mass, and physiologic conditions (Has-Schön et al., 2006). After the catastrophe in Minamata, Japan, caused by fish consumption containing methyl mercury, the study of the effects of heavy metals present in fresh fish heavy metals in fresh fish as part of human diet is of particular interest. On the other hand, the nutritional benefits of fish are mainly due to the content of high-quality protein and high content of the two kinds of omega-3 polyunsaturated fatty acids: eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) in different comestible species (Castro-González, 2002; Clarkson, 2002; Domingo et al., 2007). Omega-3 fatty acids (EPA) have probed to have protective effects in preventing coronary heart disease, reducing arrhythmias and thrombosis (Kinsella et al., 1990; Oomen et al., 2000; KrisEtherton et al., 2002) lowering plasma triglyceride levels (Harris, 1997; Ismail, 2005) and reducing blood clotting tendency (Agree et al., 1997; Din et al., 2004; Ismail, 2005). However, the content of toxic heavy metals in fish can counteract the positive effects of the omega-3 fatty acids present in fish and their beneficial effects on heart disease risk (Chan and Egeland, 2004). The present minireview highlights some aspects of how mercury, cadmium, lead and arsenic are implicated in fish consumption.

2. Heavy metals 2.1. Mercury Mercury (Hg) is one of the most toxic heavy metals in our environment including the lithosphere, hydrosphere, atmosphere and biosphere. A series of complex chemical transformations allows the three-oxidation states of Hg cycle in the environment (Barbosa et al., 2001). In the zero oxidation state (Hg0 ), mercury exists in its metallic form, vapor is the most abundant form (98%). The mercurous and mercuric states are the two higher oxidation states where the mercury atom has lost one (Hg+ ) or two electrons (Hg2+ ), respectively; methyl mercury is the most important form of mercury in terms of toxicity and health effects from environmental exposures (Jackson, 1997; Goyer and Clarsksom, 2001; ATSDR, 2003c). Natural and anthropogenic and re-emitted sources are the three major sources of Hg emissions, whereas the most important anthropogenic sources of Hg pollution in the environment are urban discharges, agricultural materials, mining and combustion and industrial discharges (Jackson, 1997; Zhang and Wong, 2007). The contamination chain of Hg follows, closely, the cyclic order: industry, atmosphere, soil, water, phytoplankton, zooplankton, fish and human (Kadar et al., 2000). The general population is most commonly exposed to mercury primarily from two sources: (1) eating fish and marine mammals (e.g., whales, seals) that may contain some methyl mercury in their tissues or (2) from the release of elemental mercury from the dental amalgam because it may dissolve in saliva and be ingested (Sallsten et al., 1996; ATSDR, 2003c); relative contribution of mercury from these two main sources will vary considerably for different individuals (ATSDR, 2003c). The main molecular mechanisms involved in methyl mercury toxicity are inhibition of protein synthesis, microtubule disruption, increase of intracellular Ca2+ with disturbance of neurotransmitter function due to mainly binding of methyl mercury to thiol or

sulfhydryl groups (CTE, 2000; Sanfeliu et al., 2003; Bridges and Zalups, 2005). Intracellular mercury therefore attaches itself to thiol residues of proteins resulting in activation of sulfur and blocks related enzymes, cofactors and hormones (Mathieson, 1995) Also, free radical’s overproduction may result from indirect interactions of methyl mercury at critical cellular sites or as a consequence of protective mechanisms inhibition, the formation of reactive oxygen species in, kidney, liver and brain have been observed following administration of methylmercuric chloride to rodents, fish and in vitro cells (Ali et al., 1992; Berntssen et al., 2003; Mori et al., 2007; Costa et al., 2007). The gastrointestinal absorption of methyl mercury is on the order of 90–95%. Absorbed methyl mercury is transported bound to red blood cells and it is widely distributed throughout the body; then methyl mercury is excreted from the body in urine and feces. All forms of mercury go through the blood–brain barrier and placenta to the fetus. The biological half-life of methyl mercury in humans is approximately 65 days (Clarkson, 2002; GwalteneyBrant, 2002). Methyl mercury poisoning mostly affects the nervous system and it is especially harmful to infant’s developing nervous system. Maternal exposure can threaten the fetus because chemicals can be transferred to the developing fetus through the placenta (Slikker, 1994; Gochfeld, 2003); in fact, fetal brain is more susceptible than adult brain to mercury-induced damage (Clarkson et al., 2003). In adults, methyl mercury has a latency of 1 month or longer after acute exposure and the main symptoms of methyl mercury exposition related with intoxication to nervous system are parestesias and numbness in the hands and feet, coordination difficulties and concentric constriction of the visual field, auditory symptoms, ischemic stroke, dementia and depression (Jarup, 2003; He et al., 2004; Morris et al., 2005); moreover the methyl mercury can cause, nephrotoxicity and gastrointestinal toxicity with ulcerations and hemorrhage (Stohs and Bagghi, 1995; Gwalteney-Brant, 2002). Mercury is present in some fish and is of considerable interest because of its potential hazard to the health of people who consume them and its toxicity increases as consequence of metals accumulated in aquatic organisms. Bioaccumulation of methyl mercury in fish depends on the trophic level, age or length of fish (Zhang and Wong, 2007) as walleye, pike swordfish, tuna and shark can have high levels of methyl mercury due to bioaccumulation and biomagnification (ATSDR, 2003c). Rivers, lakes and sea have abundance of fish diversity; an important number of authors have reported concentrations of mercury in some species such as tuna, carp, tench, gray mullet, ell, sual, bagrus, snakehead, and bighead, grass and common carp. Mercury levels in rivers Neretva, Croatia (Has-Schön et al., 2006), Catalonia, Spain (Falcó et al., 2006), Kahanawake, Canada (Chan et al., 1999), and Nile, Egypt (Sallam et al., 1999), have been reported to be below permissible limits according to the international standard concentrations and therefore it has been advised that the consumption of the species coming from these places is safe for human health (Table 1). However, fish coming from Lower Nitra River, Slovakia have showed methyl mercury concentrations between 0.08 and 1.20 mg/kg wet weight (Andreji et al., 2005, 2006), those coming from New Jersey, USA had 0.65 ± 0.1–0.05 ± 0.001 ppm, wet weight (Burger and Gochfeld, 2005), the ones from Mojana, Colombia had 0.346 ± 0.171 in carnivorous fish—0.146 ± 0.102 mg/g fresh wt (fw) in non-fish carnivorous (Marrugo-Negrete et al., 2008) has been reported. Usero et al. (2003) found that concentrations of mercury in three species (eel, common sole and gray mullet) of fish muscle were considerably lower than the maximum levels for human consumption in southern Atlantic coast of Spain (Table 1). Due to the health hazards consequence of excess of mercury exposure, ATSDR (2003c) 2003c estimated mean dietary exposure

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Table 1 Comparison of some heavy metals present average values in fish Country/region

Fish species

Range mg/kg wet weight (mg/kg or ␮g/g) ppm Hg

Cd

Pb

Nitra River Slovakia

Chub Barbel Roach Perch

1.35–3.88 1.93–4.57 1.52–2.18 2.73–6.52

0.06–0.34 0.06–0.32 0.19–0.58 0.09–0.031

0.26–2.48 0.24–0.89 0.20–0.38 0.40–5.81

Andreji et al. (2005)

Lower Nitra River, Slovak Republic.

Chub Common carp Prussian carp Roach Wels catfish

0.35–1.41 0.46–0.95 0.34–1.10 0.15–1.02 0.44–3.64

0.24–2.37 0.23–1.81 0.06–2.55 0.18–0.92 0.39–2.76

0.32–24.3 0.30–0.49 0.36–10.98 0.33–34.59 0.08–1.11

Andreji et al. (2006)

River Neretva, Croatia

Carp Tench Sval Grey mullet Eel

0.11–0.287 0.094–0.167 0.03–0.109 0.115–0.248 0.095–0.124

0.016–0.155 0.01–0.105 0.01–0.048 0.014–0.1 0.016–0.041

0.211–0.432 0.085–0.174 0.1–0.146 0.1–0.115 0.031–0.142

Catalonia, Spain

Sardine Tuna Anchovy Mackerel Sworffish Salmon Hake Red mullet Sole Cuttle fish

0.07–0.09 0.38–0.58 0.08–0.09 0.06–0.15 1.59–2.22 0.04–0.05 0.12–0.29 0.14–0.36 0.04–0.13 0.04–0.08

0.002–0.01 0.01–0.02 0.001–0.02 0.003–0.01 0.02–0.10 0.01–0.01 0.005–0.01 0.001–0.01 0.0004–0.01 0.01–0.09

0.01–0.08 0.01–0.02 0.01–0.02 0.01–0.02 0.01–0.02 0.01–0.25 0.01–0.13 0.002–0.07 0.01–0.08 0.01–0.10

River Nile, Egypt

Bagrus

0.026–0.391

0.28–0.053

0.022–0.654

New Jersey, USA

Blue fish Chilean sea bass Cod Croaker Flounder Porgie Red snapper Whiting Yellow fin tuna

0.26 ± 0.02 0.38 ± 0.06 0.11 ± 0.01 0.14 ± 0.02 0.05 ± 0.001 0.10 ± 0.01 0.24 ± 0.01 0.04 ± 0.004 0.65 ± 0.1

0.006 ± 0.002 0.004 ± 0.001 0.0005 ± 0.0003 0.001 ± 0.0004 0.01 ± 0.002 0.004 ± 0.001 0.002 ± 0.001 0.009 ± 0.005 0.03 ± 0.005

0.06 ± 0.01 0.11 ± 0.01 0.12 ± 0.01 0.09 ± 0.01 0.06 ± 0.01 0.14 ± 0.017 0.12 ± 0.01 0.09 ± 0.011 0.04 ± 0.01

0.26 ± 0.04 1.17 ± 0.3 2.2 ± 0.5 1.9 ± 0.2 3.3 ± 0.4 1.8 ± 0.17 0.23 ± 0.04 1.9 ± 0.4 1.0 ± 0.1

Grey mullet Eel Common sole

0.013 0.011 0.014

0.030 0.032 0.028

0.03 0.09 0.05

1.98 2.91 3.96

Liebre

Grey mullet Eel Common sole

0.013 0.023 0.012

0.021 0.050 0.028

0.03 0.05 0.05

2.00 2.37 3.56

San Carlos

Grey mullet Eel Common sole

0.010 0.018 0.017

0.013 0.015 0.010

0.04 0.05 0.04

1.36 0.52 2.62

San Juan

Grey mullet Eel Common sole

0.010 0.010 0.013

0.018 0.020 0.025

0.05 0.03 0.03

1.38 0.63 3.16

Spain regions Bacuta

Reference As

0.016–0.07 0.028–0.101 0.034–0.121 0.255–0.42 0.084–0.124 3.53–3.94 0.99–1.25 3.93–5.42 1.73–7.47 1.78–2.44 1.60–2.37 3.22–4.55 15.39–17.77 4.55–8.40 2.45–5.33

Has-Schön et al. (2006)

Falcó et al. (2006)

Sallam et al. (1999) Burger and Gochfeld (2005)

Usero et al. (2003)

of 8.2 ␮g/d (range, 0.37–203.5 ␮g/day) for females and 8.6 ␮g/day (range, 0.22–165.7 ␮g/day) for males. For an average body weight (bw) of 65 kg for women and 70 kg for men, the daily intakes of mercury would be 0.126 ␮g/(kg day) (range, 5.7–3.131 ng/(kg day)) for women and 0.123 ␮g/(kg day) (range, 3.1–2.367 ng/(kg day)) for men, respectively. Recently the Environmental Protection Agency (EPA, 1999) created a reference dose (RfD) for mercury of 0.1 ␮g/(kg bw d), the RfD is a numerical estimate of the daily oral exposure oh the human population, which includes sensitive subgroups such as children. In the year 2003, the Joint FAO/WHO Expert Committee on Food Additives (JECFA) revised its risk assessment on methylmercury in fish and adopted a lower Provisional

Weekly Intake (PTWI) of 1.6 ␮g/(kg bw week) to replace the previous PTWI of 3.3 ␮g/(kg bw week) of total mercury for the general population. This risk assessment is based on two major epidemiology studies which researched about the relationship between maternal exposure to mercury and impaired neurodevelopment in their children from two regions where consumption of fish and seafood is high and adverse effects on child neurodevelopment have been reported (Grandjean et al., 1997; Murata et al., 2007). Actually, in contrast to the EPA, the Joint FAO/WHO Expert Committee on Food Additives calculated the called “provisional tolerable weekly intake” (PTWI) of 1.6 ␮g/(kg weight week) (Smith and Sahyoun, 2005).

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2.2. Cadmium Cadmium is an industrial and environmental pollutant that affects adversely a number of organs in humans. Cadmium is a metal from group II B that has an atomic weight of 112.41; the ionic form of cadmium (Cd2+ ) is usually combined with ionic forms of oxygen (cadmium oxide, CdO2 ), chlorine (cadmium chloride, CdCl2 ), or sulfur (cadmium sulfate, CdSO4 ). There are estimates that 30,000 tons of cadmium are released into the environment each year, with an estimated 4000–13,000 tons coming from human activities (ATSDR, 2003b). Natural as well as anthropogenic sources of cadmium, which include industrial emissions and the application of fertilizer and sewage sludge to farm land, increased cadmium environmental levels (ATSDR, 2003b). It has been established that, although cadmium occurs in the aquatic organism and marine environment only in trace concentrations, the salinity can affect the speciation of this metal, and bioaccumulation is affected both by temperature and salinity (Ray, 1986). In the general human population, cadmium exposure occurs mainly through two sources. The first is the oral route through water and food contaminated with cadmium, particularly leafy vegetables, grains, cereals, fruits, organ meat, and fish. The second source is through inhalation of cadmium particles during industrial or everyday activities, among which the inhaled Cd2+ from cigarette smoke should be considered as highly hazardous because cadmium is easily absorbed by the lungs (Goyer, 1997; Saldivar et al., 1991; Stohs et al., 1997). In humans and other mammals, the absorption of cadmium occurs through a process similar to that of the absorption of essential metals such as iron. This absorption is enhanced by dietary deficiencies of calcium and iron and by low protein diets; the cadmium is transported by the blood and distributed primarily to liver and kidney (Goyer and Clarsksom, 2001). The liver and kidney are its principal sites of long-term storage in the body; cadmium has a long biological half-life, from 17 to 30 years in humans. Cadmium affects adversely a number of organs and tissues such as: kidney (induces renal tubular dysfunction, proteinuria and chronic renal insufficiency), heart (aortic and coronary artherosclerosis, increases cholesterol and free fatty acids) (Houston, 2007), lung (fibrosis), skeletal system, testes, placenta, brain and the central nervous system (CNS) (ATSDR, 2003b). Cadmium affects the CNS of children; thus neurological disorders, such as learning disabilities and hyperactivity may occur (Thatcher et al., 1982) however, Wong and Klaassen (1982) reported that cadmium is more toxic to newborn and young rats that adult rat and this age difference in susceptibility might be due to differences in the blood–brain barrier integrity and immaturity. The molecular mechanisms of cadmium toxicity are no well understood yet. Cadmium is known to enhance lipid peroxidation by increasing the production of free radicals in several organs, mainly lung and brain; likewise to interfere with the cellular mechanisms against oxidation (glutathione peroxidase and catalase) and this should be considered as a potential significant event in the generation of free radicals which lead to tissue damage and cellular death (Manca et al., 1991; Shukla et al., 1987, 1996; Kumar et al., 1996; Méndez-Armenta et al., 2003; Méndez-Armenta and Ríos, 2007; Casalino et al., 2002). Cadmium’s ability to generate free radicals also leads to the oxidation of nuclei acids and alteration of DNA repair mechanisms (Hartwig et al., 2002), alterations of membrane structure/function (Kumar et al., 1996) and inhibition of energy metabolism (Muller, 1986). The levels of contamination by cadmium in fish are of considerable interest because fish consumption is an important source of intake cadmium for the general population. Most of the cadmium content in fish or other seafood is highly absorbable in CdCl2 form;

in humans, the efficiency of gastrointestinal absorption of cadmium has been reported to be approximately 3–8% of the ingested load. Cadmium is particularly accumulated in kidney; in muscles the concentrations are low (ATSDR, 2003b). Several studies have demonstrated the variability in concentrations of cadmium in fish. In the Lower Niitra River in the Slovak Republic elevated concentration of cadmium was found in muscle of five fish species; which suggests that consumption of fish from this river its not recommended (Andreji et al., 2005, 2006). Concentrations of cadmium were determined in five species of fish from River Neretva, Croatia; the results showed that concentrations of cadmium are very high in carp, sval and mullet kidney, which indicate the kidney tendency to accumulate cadmium, whereas the concentrations of cadmium in muscle were lower (Has-Schön et al., 2006). In Egypt, 50 samples of Bagrus collected from various localities of River Nile were analyzed and the results reveled that the concentrations of Cd in fish muscles were elevated in 24% and 6% of the examined fish samples (Cd concentration ranged from 0.028 to 0.053) (Sallam et al., 1999). However, high metal concentrations in samples of fish (Mugil cephalus and Mallus barbatus) from the Mediterranean Sea showed that the highest levels of cadmium were found in liver, gill and muscle of both species; moreover, seasonal changes in metal concentration were also observed (Cogun et al., 2006). On the other hand, in four seawater reservoirs coast of Spain the cadmium concentrations in fish muscle of eel, common sole and gray mullet were reported below the maximum levels permitted for human consumption (Usero et al., 2003). Falcó et al. (2006) and Burger and Gochfeld (2005) reported different levels of heavy metals such as cadmium, arsenic, lead, mercury, selenium and manganese, in species of fish obtained from local markets and supermarkets in Catalonia, Spain and New Jersey USA. The results showed that there are significant interspecific differences for all metals and no fish type had the highest levels of more than two metals, which suggests that the differences are due to geography, throphic levels, size foraging method/localization and propensity of metals to undergo biomagnification in the food chain (Burger and Gochfeld, 2005). According to the report from Catalonia, the highest mean metal concentrations found were the following: arsenic, in red muller; cadmium, in clam and mussel; mercury, in swordfish; and finally, the highest lead concentrations were found in mussel and salmon. These results indicate a remarkable contribution of these species to the intake of these metals (Falcó et al., 2006). The European Community (EEC, 2001) established the maximum levels permitted of cadmium in seafood as follows 0.05 mg/kg fw in fish, 0.5 mg/kg fw in crustaceans (crab excluded), 1.0 mg/kg fw in molluscs and crab. Moreover, the Joint FAO/World Health Organization has recommended the provisional tolerable weekly intake (PTWI) as 0.007 mg/kg bw for cadmium (420 ␮g/week for a 60-kg person); the committee evaluated the impact of different maximum levels of cadmium on the overall intake (FAO/WHO, 2005). 2.3. Lead Lead (Pb) is one of the most ubiquitous and useful metals known to humans and it is detectable in practically all phases of the inert environment and in all biological systems. Environmental levels of lead have increased more than 1000-fold over the past three centuries as a result of human activity; the greatest increase occurred between the years 1950 and 2000 (ATSDR, 2005). Lead is a naturally occurring element; it is a member of Group 14 (IVA) of the periodic table, has an atomic weight of 207.2 and exists in three states: Pb (0), the metal; Pb (II); and Pb (IV). Lead is a blush-gray heavy metal and it is usually found combined with two or more other

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elements to form lead compounds (ATSDR, 2005). Lead reaches the aquatic system because of superficial soil erosion and atmospheric deposition. The concentration of lead in deep ocean waters is about 0.01–0.02 ␮g/l, but in surface ocean waters is about 0.3 ␮g/l (Sepe et al., 2003). The main route of exposure for general population is food and air. Occupational exposure to lead occurs for workers in the lead smelting and refining industries, battery, manufacturing plants, plastics and printing industries. Children are particularly sensitive to the effects of lead, which is considered a primary environmental hazard. Metal intoxication in young children produces a critical effect in the developing nervous system due to its susceptibility to lead toxicity (Goyer, 1993; Goyer and Clarsksom, 2001; Jarup, 2003). Lead may enter the body through intestines, ingestion; through the lungs, inhalation; through the skin, adsorption; or by direct swallowing and ingestion. The metal is absorbed into and transported by the bloodstream to other tissues. Once absorbed, lead accumulates in high concentrations in bone, teeth, liver, lung, kidney, brain, and spleen, and it goes through the blood–brain barrier and the placenta (Goyer and Clarsksom, 2001; Gwalteney-Brant, 2002). The biological half-life of lead may be considerably longer in children than in adults; lead in blood has an estimate half-life of 35 days, in soft tissue 40 days and in bones 20–30 years (Papanikolaou et al., 2005). The major route of excretion of absorbed lead is the urinary tract, usually with glomerular filtrate in the kidney; it can also be excreted with bile through the gastrointestinal tract (Goyer and Clarsksom, 2001). The most sensitive targets for lead toxicity are the developing nervous system, the haematological and cardiovascular systems, and the kidney. The symptoms of lead poisoning are headache, irritability, abdominal pain and various symptoms related to the nervous system (Jarup, 2003). Chronic lead toxicity in humans often develop dullness, irritability, poor attention span, epigastric, constipation, vomiting, convulsions, coma and death. Children may be affected by encephalopathy with lethargy, mental dullness, vomiting, irritability, and anorexia; in severe cases, the prolonged exposition of lead can decrease the cognitive function and increase behavior disorders, specially aggression, psychosis, confusion and mental deficit (Bellinger et al., 1992; Gwalteney-Brant, 2002; Jarup, 2003; ATSDR, 2005). The relationship between lead exposure and cognitive dysfunctions is similar cross-species, which indicates that exposure to lead results in similar manifestations (Costa et al., 2004). Chronic lead toxicity affects gastrointestinal, neuromuscular, renal and haematological systems (ATSDR, 2005). Blood lead level indicates a recent exposure, whereas bone lead level, which forms 90–95% of lead burden in adults and 80–95% of total lead in children indicates a chronic exposure (Kakkar and Jaffery, 2005). However, blood lead levels in children below 10 ␮g/dl have so far been considered acceptable. The main mechanisms of lead toxicity are the activation of cellular functions due to this metal’s calcium mimicking effect, and the inhibition of the activity of different proteins through its binding to sulfhydryl groups. Lead has high affinity for sulfhydryl groups and can inactivate enzymes, especially those involved in heme synthesis, such as ␦-aminolevulinic acid dehydratsase and ferrochelatase (Gwalteney-Brant, 2002.) On the other hand, lead has a higher affinity than calcium for calmodulin and can activate some calmodulin-dependent processes, inhibit the calcium bombs (calcium–ATPase, sodium–potassium) and channels and replace calcium in several of its receptors (Simons, 1986; Goyer, 1997; Bridges and Zalups, 2005). This interaction between lead and calcium has been identified in numerous papers, which show that lead absorption is inversely related to dietary calcium; thus it seems that a low dietary intake of calcium can lead to higher levels of lead in blood (Bogden et al., 1992).

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Accumulation of lead in different fish species has been determined in several works, Table 1 resume results where the concentrations of lead in fish varied until exceeded the permissible limit for consumption of humans. Has-Schön et al. (2006) showed that lead concentration is similar in all fish species except carp which evidently tends to accumulate this heavy metal in all tissue apart from gonads; the muscle values are shown in Table 1. Falcó et al. (2006), reported lead concentrations in various edible marine species which varied from 0.002 to 0.21 ␮g/g fw; whereas that from a study in commercial fish obtained from supermarkets and specialty fish markets in New Jersey reported that average lead concentrations in none fish exceeded the maximum recommended levels of lead in seafood (Burger and Gochfeld, 2005). Andreji et al. (2006) determined lead concentrations which exceeded the limit for lead content in fish muscle, 0.2 mg/kg wet weight; otherwise a determination of lead in six fish species from the Adriatic Sea showed that concentrations of lead in all species examined were below the maximum levels recommended by the European Community for this element in seafood, which would lead to exposure levels lower than the provisional tolerable daily intakes (Sepe et al., 2003). Ashraf et al. (2006) found levels of lead in canned fish (salmon, sardines and tuna) at range of 0.23–0.84 ␮g/g, which indicates that canned fish have concentrations within WHO/FAO permissible limits. Likewise, the concentrations of lead in muscle of tree species (grey mullet, eel and common sole) were considerably lower that the permissible limits (Table 1). The ingestion of fish is an obvious means of exposure to metals because they accumulate substantial amounts of metals in their tissues, especially in the muscles, and thus they represent a major dietary source of lead for general population. The Joint FAO/WHO Expert Committee on Food Additives established a provisional tolerable weekly intake (PTWI) for lead as 0.025 mg/kg bw. Whereas the European Community (EEC, 2001) established the maximum levels of lead in seafood as 0.2 mg/kg fw in fish, 0.5 mg/kg fw in crustaceans (crab excluded), and 1.0 mg/kg fw in bivalves molluscs and crab (Sepe et al., 2003). 2.4. Arsenic Arsenic, a naturally occurring element, is a worldwide contaminant that is found in rock, soil, water, air and food. Arsenic has a complex chemical structure and can be found in elemental, trivalent (+3 arsenite), and pentavalent (+5 arsenate) inorganic forms and trivalent and pentavalent organic forms. Organic arsenic is formed when arsenic ions are combined with carbon and hydrogen. Inorganic arsenic is present in groundwater, which is used for drinking in several countries all over the world; whereas organic arsenic compounds are primarily found in fish and shellfish (ATSDR, 2003a). Inorganic arsenic, the form found in soil and water, is classified by the Environmental Protection Agency (EPA) as a Group A human carcinogen (EPA, 1999; ATSDR, 2003a). High doses of organic arsenic can produce the same toxicological effects as a lower dose of inorganic arsenic (ATSDR, 2003a). Inorganic arsenic is released into the environment from a number of anthropogenic sources, which include geothermal discharges, industrial products and wastes, copper and lead smelters, and glass manufactures that add arsenic to raw materials (Goyer and Clarsksom, 2001). The use of arsenic compounds as herbicides, pesticides, and fungicides are other sources of environmental arsenic contamination. Occupational exposures have also been reported in several industries such as electronics, non-ferrous metal smelting, glass manufacturing, manufacture and use of arsenical pesticides and wood preservatives. The major sources of exposition for general population are from food and water; food contains both organic and inorganic arsenic, whereas drinking water contains primarily

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inorganic forms of arsenic (ATSDR, 2003a; Jarup, 2003). Exposure of millions to arsenic contaminated waters coming from hand tube wells is a major concern in many Asiatic countries such as Taiwan, Inner Mongolia and China (Chatterjee et al., 1995; Abernathy et al., 1999). In Bangladesh, where the population is exposed to arsenic through drinking water, the arsenic contamination of groundwater is considered a severe public health. The general population has had long-term exposure to arsenic from groundwater; studies indicate that one out of ten people who drink water containing 500 ␮g of arsenic per liter may ultimately die from cancer caused by arsenic (Smith et al., 2000). The World Health Organization established the guideline level of arsenic in drinking water as 0.01 mg/l, calculated as total arsenic (WHO, 2004). Absorption of arsenic in inhaled particles is highly dependent on the solubility and the size of particles, which are deposited in the respiratory tract, and the oral arsenic is well absorbed from the gastrointestinal tract (soluble arsenic compounds are easily absorbed from the gastrointestinal tract). The biological half-life of ingested inorganic arsenic is about 10 h, and 50–80% is excreted in about 3 days whereas the methylated arsenic has a half-life of 30 h (Goyer and Clarsksom, 2001; Gwalteney-Brant, 2002). Ingested arsenic can go through the placenta and result in cord blood concentrations that resemble maternal blood concentrations (Patrick, 2003). Arsenic is transported in blood by binding to red blood cells and it is distributed throughout the body; once absorbed, arsenites are oxidized to arsenates and methylated. The As(+3) form undergoes enzymic methylation primarily in the liver to form monomethylarsinic acid (MMA) and dimethylarsinic acid (DMA); this process may then be repeated to result in dimethylated arsenic metabolites. Most arsenic is promptly excreted in the urine as a mixture of As(+3), As(+5), MMA, and DMA; DMA is usually the primary form in the urine (Goyer and Clarsksom, 2001; ATSDR, 2003a; Abernathy et al., 2003). Arsenic has a predilection for sulfhydryl-rich keratin (skin) and tends to concentrate in the skin, but it can also be deposited in bones, teeth, hair and nails, mainly when exposure is chronic (Goyer and Clarsksom, 2001; Gwalteney-Brant, 2002). The most commonly used biomarkers for identification and quantification of arsenic exposure are urine, blood, hair and nails (Kakkar and Jaffery, 2005). Apparent signs of chronic arsenic toxicity are skin changes that include generalized hyperkeratosis and formation of hyperkeratotic warts or corns on the palms and soles, along with areas of hyperpigmentation interspersed with small areas of hypopigmentation on the face, neck, and back (Kakkar and Jaffery, 2005). Chronic exposure to inorganic arsenic compounds may lead to neurotoxicity of both the peripheral and central nervous system (Goyer and Clarsksom, 2001); whereas the mainly signs of acute toxicity of arsenic are an acute onset of profused vomiting, diarrhea, colic, salivation, fever, disturbances of the cardiovascular and central nervous system which may lead to death (Gwalteney-Brant, 2002; Jarup, 2003). Arsenic is considered to be carcinogenic and is related mainly to cancer in the lung, kidney, bladder, and skin (ATSDR, 2003a). The mechanisms of arsenic toxicity involve a number of sulfhydryl-containing proteins and enzyme systems which are altered by exposure to arsenic (Thomas et al., 2001). The mitochondria accumulates arsenic mediated by inhibition of pyruvate oxidases and phosphatases; arsenic also inhibits succinic dehydrogenase activity and uncocoupling of oxidative phosphorilation. The resulting fall in ATP levels affects, virtually, all cellular functions (Na+ /K+ balance, protein synthesis, etc.) that induce generation of reactive oxygen species and impair tissue respiration (Goyer and Clarsksom, 2001; Thomas et al., 2001; Gwalteney-Brant, 2002; ATSDR, 2003a). Moreover, arsenic interferes with DNA repair processes (nucleotide excision repair) (Hartwig et al., 2002) and

products changes in DNA methylation patterns that could affect gene expression (Abernathy et al., 2003). Humans can be exposed to arsenic through the intake of food and drinking water, but for most people, the major exposure source is the diet, mainly fish and sea food. It is well known that sea food contains larger amounts of arsenic than other foods (Uneyama et al., 2007). However, the organic arsenic in food and seafood appears to be much less toxic than the inorganic forms (Abernathy et al., 2003). The presence of arsenic in fish has been determinated in several species such as; blue fish, porgie, red sapper, carp, mullet tuna, and salmon. Concentrations of arsenic were determined in five fish species of the river Neretva, Croatia. The results show that arsenic concentration is low in most fish, being always its highest concentration in muscle (Has-Schön et al., 2006). Falcó et al. (2006), Burger and Gochfeld (2005), reported high levels of arsenic in some species of fish (Table 1). On the other hand, Usero et al. (2003) found high concentrations of arsenic in muscle of grey mullet, eel and common sole on tree regions of coast Spain (Table 1). The joint FAO/WHO Expert committee on Food Additives (JECFA) established a provisional tolerable weekly intake (PTWI) for inorganic arsenic as 0.015 mg/kg bw (FAO/WHO, 2005); organo-arsenic intakes of about 0.05 mg/(kg bw day) seemed not to be associated to hazardous effects (Uneyama et al., 2007).

3. Health effects of fish consumption The beneficial health effects of fish are based on several studies from the last 25 years, most of which have linked fish consumption to several health benefits (Kinsella et al., 1990; Oomen et al., 2000; Kris-Etherton et al., 2002). Nevertheless, several areas of uncertainty remain as the optimal intake of n − 3 fatty acids (EPA and DHA) is not clearly established. Some studies have reported contradictory results, since exist an increases levels of heavy metals that can affected the health of consumers however, fish consumption is recommend due to all its nutritional benefits not only by n − 3 fatty acids (Foran et al., 2006; Domingo et al., 2007). The beneficial effects of fish oil are attributed to their eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) which are polyunsaturated omega-3 fatty acids (omega-3 PUFAs) formed from alpha-linolenic acid. These fatty acids are produced by monocellular algae or phytoplankton, which represent the beginning of food chain, and accumulate in the fresh of marine fish (Judé et al., 2006). The omega-3 PUFAS can act at very different levels of the cellular physiology, and the mainly mechanisms of actions proposed include effect on sensitivity of some ionic channels and/or modify intracellular calcium homeostasis (Judé et al., 2006). Other pathways involved in cellular signaling mechanisms are activation of phospholipases, synthesis of eicosanoids, regulation of receptorassociated enzymes and protein kinases (Siddiqui et al., 2008). Some studies support the idea that the intake of DHA and EPA reduce high blood pressure, and significantly reduce blood triglyceride levels (Harris, 1997); well-conducted randomized controlled trials report that for people with a history of heart attack, the regular consumption of (oily fish or fish oil/omega-3 supplements reduces the risk of non-fatal heart attack, fatal heart attack and sudden death (Oomen et al., 2000; Kris-Etherton et al., 2002; Din et al., 2004; Harris, 2004; Mozaffarian et al., 2005; Jarvinen et al., 2006). The action mechanisms for these effects still are not fully defined; but involve changes in membrane fluidity, receptor response and binding to intracellular receptors regulating gene transcription (Torrejon et al., 2007); Das (2000) suggested an explain of the cardio-protective effects of n − 3 fatty acids, showed that the mainly mechanisms can be due to the suppressions of the tumor necrosis factor (TNF␣) and interleukinin-1

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(IL-1) and the release and modulation of hypothalamic-piyuitaryadrenal anti-inflammatory responses. On the other hand, Din et al. (2008) suggested that reduced platelet monocyte aggregation can be provides probably mechanism through which fish oils exert the cardio-protective effects. Moreover, the intake of fish has shown benefits in other diseases such as rheumatoid arthritis (Cleland et al., 2003; Goldberg and Katz, 2007; Rahman et al., 2008); psychiatric disorders (Cherubini et al., 2007; Song and Zhao, 2007; Peet and Strokes, 2005) and lung disease (Cerchietti et al., 2007; Romieu and Trenga, 2001). Recently, preliminary evidence regarding the role of dietary omega-3 polyunsaturated fatty acids in modulating each of the components of the triad of adiposity, inflammation, and fatty acid metabolism in the metabolic syndrome has been studied (Robinson et al., 2007; Douglas, 2007; Lombardo et al., 2007). However, one potential risk of dietary fish intake is its content of heavy metals, methylmercury mainly, recent evidence suggests that high mercury content in fish may diminish the cardioprotective effect of fish intake (Salonen et al., 2000; Guallar et al., 2002; Yoshizawa et al., 2002). In humans, cadmium, 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 fish 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); Falcó et al. (2006); Has-Schön et al. (2006) have determined the levels of these metals in different fish species which may be out of permissible limits. PTWI for adults or children increased due to fish accumulation of substantial amounts of metals in the fish tissue and thus, risk is also dependent on the different metals residing in different fish. The American Heart Association suggests eating fish at least two times per week in order to reach the daily intake of omega-3 fatty acids recommended for healthy adults with no history of heart disease (Kris-Etherton et al., 2002). In particular fatty fish such as anchovies, bluefish, carp, catfish, halibut, herring, lake trout, mackerel, pompano, salmon, striped sea bass, tuna (albacore), and whitefish, or an equivalent of 0.3–0.5 g/d e PUFAs are also recommended. Therefore the intake of fish should be regulated; information regarding the specie of fish consumed and its possible levels of content of heavy metals can be of benefit to diminish the hazard to public health (Domingo et al., 2007). The potential harm from other metals suggests that not only should people eat smaller quantities of fish known to accumulate mercury but they also should eat a diversity of fish in order to avoid consuming unhealthy quantities of heavy metals; however, public should bear in mind that standards have a margin of safety (Burger and Gochfeld, 2005). 4. Final commentary In summary, we consume a large number of sea food mainly fish that can be detectable amounts of heavy metals, however the potential benefit of fish consumption is very important and your consumption is suggested by the rich nutrimental value but is necessary that the levels of heavy metal do not exceed the permissible limits for intake of fish. Health institutions, public and private organizations must have a continuous communication about riskbenefit of fish consumption, this confirms the interest to analyze of bases on which a public policy is elaborated, as well as, the responsibility for regulating the quality and improve the balance between benefit and risk of the fish human consumption. Acknowledgment This work was supported by Consejo Nacional de Ciencia y Tecnología (CONACyT), México grant 52811-Q.

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References Abernathy, O.Ch., Liu, Y.P., Longfellow, D., Aposhian, V.H., Beck, B., Fowler, B., Goyer, R., Menzer, R., Rossman, T., Thompson, C., Waalkes, M., 1999. Arsenic: health effects mechanisms of actions and research issue. Environ. Health Perspect. 107, 593–597. Abernathy, O.Ch., Thomas, D.J., Calderon, L.R., 2003. Health effects and risk assessment of arsenic. J. Nutr. 133, 536S–1538S. Agency for Toxic Substance and Disease Registry, 2003a. Toxicological Profile for Arsenic U.S. Department of Health and Humans Services, Public Health Service, Centres for Diseases Control, Atlanta, GA. Agency for Toxic Substance and Disease Registry, 2003b. Toxicological Profile for Cadmium, U.S. Department of Health and Humans Services, Public Health Service, Centres for Diseases Control, Atlanta, GA. Agency for Toxic Substance and Disease Registry, 2005. Toxicological Profile for Lead, U.S. Department of Health and Humans Services, Public Health Service, Centres for Diseases Control, Atlanta, GA. Agency for Toxic Substance and Disease Registry, 2003c. Toxicological Profile for Mercury U.S. Department of Health and Humans Services, Public Health Service, Centres for Diseases Control, Atlanta, GA. Agree, J.J., Vaisanen, S., Hannien, O., Muller, A.D., Hornstra, G., 1997. Hemostatic factors and platelet aggregation after fish-enriched diet or fish oil or docosahexaenoic acid supplementation. Prostag. Leukot. Essent. Fatty Acids 57, 419–421. Ali, S.F., LeBel, C.P., Bondy, S.C., 1992. Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity. Neurotoxicology 13, 637–648. Andreji, J., Stránai, I., Massàyi, P., Valent, M., 2005. Concentration of selected metal in muscle of various fish species. J. Environ. Sci. Health 40, 899–912. Andreji, J., Stránai, I., Massàyi, P., Valent, M., 2006. Accumulation of some metals in muscles of five fish species from Lower Nitra River. J. Environ. Sci. Health Part A 41, 2607–2622. Ashraf, W., Seddigi, Z., Abulkibash, A., Khalid, M., 2006. Levels of selected metals in canned fish consumed in Kingdom of Saudi Arabia. Environ. Monit. Assess. 117, 271–279. Barbosa, A.C., Jardim, W., Dòrea, J.G., Fosberg, B., Souza, J., 2001. Air mercury speciation as a functioning of gender, age, and body mass index in habitants of the Negro River Basin, Amazon. Brazil. Arch. Environ. Contamin. Toxicol. 40, 439–444. Beijer, K., Jernelov, A., 1986. Sources, transport and transformation of metals in the environment. In: Friberg, L., Nordberg, G.F., Vouk, V.B. (Eds.). Handbook on the Toxicology of Metals. General Aspects, 2a Ed., Amsterdam, pp. 68–74. Bellinger, D.C., Stiles, K.M., Needelman, H.L., 1992. Low-level lead exposure, intelligence and cademic achievement: a long-term follow-up study. Pediatrics 90, 855–861. Berntssen, M.H., Aatland, A., Handy, R.D., 2003. Chronic dietary mercury exposure causes oxidative stress, brain lesions, and altered behaviour in Atlantic salmon (Salmo salar) parr. Aquat. Toxicol. 65, 55–72. Bridges, C.C., Zalups, R.K., 2005. Molecular and ionic mimicry and the transport to toxic metals. Toxicol. Appl. Pharmacol. 204, 274–308. Bogden, J.D., Gertner, S.B., Christakos, S., Kemp, F.W., Yang, Z., Katz, S.R., Chu, C., 1992. Dietary calcium modified concentrations of lead and other metals and renal calbindinn in rats. J. Nutr. 122, 1351–1360. Burger, J., Gochfeld, M., 2005. Heavy metals in commercial fish in New Jersey. Environ. Res. 99, 403–413. Casalino, E., Calzaretti, G., Sblano, C., Landriscin, C., 2002. Molecular inhibitory mechanism of antioxidant enzymes in rat liver and kidney by cadmium. Toxicology 179, 37–50. Castro-González, I.M., 2002. Ácidos grasos omega-3: beneficios y fuentes. Interciencia 27, 128–136. Cerchietti, L.C., Navigante, A.H., Castro, M.A., 2007. Effects of eicosapentaenoic and docosahexaenoic n − 3 fatty acids from fish oil and preferential Cox-2 inhibition on systemic syndromes in patients with advanced lung cancer. Nutr. Cancer 59, 14–20. Chan, M.H., Egeland, M.G., 2004. Fish consumption, mercury exposure, and heart disease. Nutr. Rev. 62, 68–72. Chan, H.M., Trifonopoulos, M., Ing, A., Receveur, O., Johnson, E., 1999. Consumption of freshwater fish in Kahnawake: risk and benefits. Environ. Res. 80, S213–S222. Chatterjee, A., Das, D., Mandal, B.K., Chowdhury, T.R., Samanta, G., Chakraborti, D., 1995. Arsenic in ground water in six districts of West Bengal, India—the biggest arsenic calamity in the world. Part 1. Arsenic species in drinking water and urine of the people. Analyst 70, 643–650. Cherubini, A., Andres-Lacueva, C., Martin, A., Lauretani, F., Iorio, 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, 1120–1126. Clarkson, T.W., Magos, L., Meyers, G., 2003. The toxicology of mercury: current exposures and clinical manifestations. N. Engl. J. Med. 18, 1337–1731. Clarkson, W.T., 2002. The three modern faces of mercury. Environ. Health Perspect. 110 (Suppl. 1), 11–23. 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 fish oil for rheumatoid arthritis. Lipids 38, 419–424.

270

M.I. Castro-González, M. Méndez-Armenta / Environmental Toxicology and Pharmacology 26 (2008) 263–271

Cogun, H.Y., Yuzereroglu, T., Firat, O., Gok, G., Kargin, F., 2006. Metal concentrations in fish species from the northeast Mediterranean Sea. Environ. Monit. Assess. 121, 431–438. Committee on Toxicological Effects (CTE), 2000. Methylmercury, Board on Environmental Studies and Toxicology; Commission on Life Sciences, National Research Council. Toxicological Effects of Methylmercury. National Academies Press, Washington, DC. Costa, L.G., Aschner, M., Vitalone, A., Syversen, T., Soldin, P.O., 2004. Developmental neuropathology of environmental agents. Annu. Rev. Pharmacol. Toxicol. 44, 87–110. Costa, L.G., Fattori, V., Giordano, G., Vitalone, A., 2007. An in vitro approach to assess the toxicity of certain food contaminants methylmercury and polychlorinated biphenyls. Toxciology 237, 65–76. Das, U.N., 2000. Beneficial effect(s) of n − 3 fatty acids in cardiovascular diseases: but, why and how? Prostaglandins. Leukot. Essent. Fatty Acids 63, 351–362. Din, J.N., Newby, D.E., Flapan, A.D., 2004. Omega 3 fatty acids and cardiovascular disease-fishing for natural treatment. BMJ 328, 30–35. Din, J.N., Harding, S.A., Valerio, C.J., Sarma, J., Lyall, K., Riemersma, R.A., Newby, D.E., Flapan, A.D., 2008. Dietary intervention with oil rich fish reduces plateletmonocyte aggregation in man. Atherosclerosis 197, 290–296. Domingo, J.L., Bocio, A., Flaco, G., Llobet, J.M., 2007. Benefits and risks of fish consumption. Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology 230, 219–226. Douglas, E.B., 2007. The role of consumption of Alpha-Linolenic, Eicosapentaenoic and Docosahexaenoic Acids in human metabolic syndrome and type 2 diabetes. J. Oleo Sci. 56, 319–325. Environmental Protection Agency (EPA), 1999. Integrated Risk Information Systems (IRIS) on Arsenic. National Center for Environmental Assessment, Office of Research and Development, Washington, DC. EEC, 2001. Regolamento no. 466/2001 della Commissione dell’ 8 marzo 2001 che definisce I tenori massimi di taluni contaminanti presenti nelle derrate alimentary. Gazzetta Ufficiale delle Comunita Europee, L77. Falcó, G., Llobet, J.M., Bocio, A., Domingo, J.L., 2006. Daily intake of arsenic, camdium, mercury, and lead by consumption of edible marine species. J. Agric. Food Chem. 54, 6106–6112. FAO/WHO Expert Committee on Food Additives, Arsenic 2005. http://www.inchem. org/documents/jecfa/jeceval/jec 159.htm. FAO/WHO Expert Committee on Food Additives, Cadmium 2005. http://www. inchem.org/documents/jecfa/jeceval/jec 297.htm. Foran, J.A., Carpenter, D.O., Good, D.H., Hamilton, M.C., Hites, R.A., Knuth, B.A., Schwager, S.J., 2006. Risk and benefits of seafood consumption. Am. J. Prev. Med. 30, 438–439. Gochfeld, M., 2003. Cases of mercury exposure bioavailability and absorption. Ecotoxicol. Environ. Saf. 56, 174–179. Goldberg, R.J., Katz, J., 2007. A meta-analysis of the analgesic effects of omega-3 polyunsaturated fatty acid supplementation for inflammatory joint pain. Pain 129, 210–223. Goyer, R.A., 1993. Lead toxicity: current concerns. Environ. Health Perspect. 100, 177–187. Goyer, A.R., 1997. Toxic metals and essential metal interactions. Annu. Rev. Nutr. 17, 37–50. Goyer, R.A., Clarsksom, W.T., 2001. Toxic effects of metals. In: Klaassen, C.D. (Ed.), Casarett and Doull’s Toxicology. The basic Science of Poisons. McGraw-Hill, New York, pp. 811–867. Grandjean, P., Weihe, P., White, R.F., Debes, F., Araki, S., Yokoyama, K., Murata, K., Sorensen, N., Dohl, R., Jorgensen, P.J., 1997. Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicol. Teratol. 19, 417–428. Guallar, E., Sanz-Gallardo, M.I., Van’t Veer, P., Bode, P., Aro, A., Gomez-Aracena, J., Kark, J.D., Riemersma, A.R., Martín-Moreno, J.M., Frans, J.K., 2002. Mercury, fish oil, and the risk of myocardial infarction. N. Engl. J. Med. 347, 1747–1754. Gwalteney-Brant, S.M., 2002. Heavy metals. In: Haschek, W.M., Rosseaux, C.G., Wallig, A.M. (Eds.), Handbook of Toxicologic Pathology. Academic Press, New York, pp. 701–732. Harris, W.S., 1997. N − 3 fatty acids and serum lipoproteins: human studies. Am. J. Clin. Nutr. 65, 1645S–1654S. Harris, W.S., 2004. Are omega-3 fatty acids the most important nutritional modulators of coronary heart disease risk? Curr. Atheroscler. Rep. 6, 447–452. Hartwig, A., Asmuss, M., Eleven, I., Herzer, U., Kostelac, D., Pelzer, A., Scwerdtle, T., Bürkle, A., 2002. Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Environ. Health Perspect. 110 (Suppl. 5), 797–799. Has-Schön, E., Bogut, I., Strelec, I., 2006. Heavy metal profile in five fish species included in human diet, domiciled in the end flow of River Neretva (Croatia). Arch. Environ. Contam. Toxicol. 50, 545–551. He, K., Song, Y., Daviglus, M.L., Liu, K., Van Horn, L., Dyer, A., Goldbourt, U., Greenland, P., 2004. Fish consumption and incidence of stroke: a meta-analysis of cohort studies. Stroke 35, 1538–1542. Houston, M.C., 2007. The role of mercury and cadmium heavy metals in vascular disease, hypertension, coronary heart disease, and myocardial infraction. Altern. Ther. Health Med. 13, S128–S133. Ismail, H.M., 2005. The role of omega-3 fatty acids in cardiac protection: on overview. Front. Biosci. 10, 1079–1088. Jackson, T.A., 1997. Long-range atmospheric transport of mercury to ecosystems, and the importance of anthropogenic emissions—a critical review and evaluation of the published evidence. Environ. Rev. 5, 99–120.

Jarup, L., 2003. Hazards of heavy metal contamination. Brit. Med. Bull. 68, 167–182. Jarvinen, R., Knekt, P., Rissanen, H., Reunanen, A., 2006. Intake of fish and long-chain n − 3 fatty cids and the risk of cornary Herat mortality in men and women. Br. J. Nutr. 95, 229–824. Judé, S., Roger, S., Martel, E., Besson, P., Richard, S., Bougnoux, P., Champeroux, P., LeGuennec, J.Y., 2006. Dietary long-chain omega-3 fatty acids of marine origin: a comparison of their protective effects on coronary heart disease and breast cancers. Prog. Biophys. Mol. Biol. 90, 299–325. Kadar, I., Koncz, J., Fekete, S., 2000. Experimental study of Cd, Hg, Mo, Pb and Se movement in soil-plant-animal systems. In: Kniva, International Conference Proceedings, Patija, Croatia, pp. 72–76. Kakkar, P., Jaffery, N.F., 2005. Biological markers for metal toxicity. ETAP 19, 335–349. Kinsella, J.E., Lokesh, B., Stone, R.A., 1990. Dietary n − 3 polyunsaturated fatty acids in amelioration of cardiovascular disease: possible mechanisms. Am. J. Clin. Nutr. 52, 1–28. Kris-Etherton, P.M., Harris, W.S., Appel, L.J., 2002. Fish consumption, fish oil. Omega3 fatty acids, and cardiovascular disease. Circulation 106, 2747–2757. Kumar, R., Agarwal, A.K., Seth, P.K., 1996. Oxidative stress-mediated neurotoxicity of cadmium. Toxicol. Lett. 89, 65–69. Lombardo, Y.B., Hein, G., Chicco, A., 2007. Metabolic syndrome: effects of n − 3 PUFAs on a model of dyslipidemia, insulin resistance and adiposity. Lipids 42, 427–437. Manca, D., Ricard, A.C., Trotter, B., Chevalier, G., 1991. Studies for lipid peroxidation in rat tissues following administration of low and moderate doses of cadmium chloride. Toxicology 67, 303–323. Marrugo-Negrete, J., Verbel, J.O., Cevallos, E.L., Benitez, L.N., 2008. Total mercury and methylmercury concentrations in fish from the Mojana regions of Colombia. Environ. Geochem. Health 30, 21–30. Mathieson, P.W., 1995. Mercury: god of TH2 cells. Clin. Exp. Immunol. 102, 229–230. Méndez-Armenta, M., Villeda-Hernández, J., Barroso-Moguel, R., Nava-Ruíz, C., Jiménez-Capdeville, M.E., Ríos, C., 2003. Brain regional lipid peroxidation and metallothionein levels of developing rats exponed to cadmium and dexamethasone. Toxicol. Lett. 144, 151–157. Méndez-Armenta, M., Ríos, C., 2007. Cadmium neurotoxicity. ETAP 23, 350–358. Mori, N., Yasutake, A., Hirayama, K., 2007. Comparative study of activities in reactive oxygen species production/defense system in mitochondria of rat brain and liver, and their susceptibility to methylmercury toxicity. Arch. Toxicol. 81, 769–776. Morris, M.C., Evans, D.A., Tangney, C.C., Bienias, J.L., Wilson, R.S., 2005. Fish consumption and cognitive decline with age in a large community study. Arch. Neurol. 62, 1849–1853. Mozaffarian, D., Ascherio, A., Hu, F.B., Stampfer, M.J., Willett, C.W., Siscovick, S.D., Rimm, E.B., 2005. Interplay between different polyunsaturated fatty acids and risk of coronary heart disease in men. Circulation 111, 157–164. Muller, L., 1986. Consequences of cadmium toxicity in rat hepatocytes: mitochondrial dysfunction and lipid peroxidation. Toxicology 40, 285–295. Murata, K., Grandjean, P., Dakeishi, M., 2007. Neurophysiological evidence of methylmercury neurotoxicity. Am. J. Int. Med. 50, 765–771. Oomen, C.M., Feskens, E.J., Räsänen, L., Fidanza, F., Nissinem, A.M., Menotti, A., Kok, F.J., Kromhout, D., 2000. Fish consumption and coronary heart disease mortality in Finland, Italy and The Netherlands. Am. J. Epidemiol. 151, 999–1006. Papanikolaou, C.N., Hatzidaki, G.E., Belivanis, S., Tzanakakis, G.N., Tsatsakis, M.A., 2005. Lead toxicity update. A brief review. Med. Sci. Monit. 11, RA329–336. Patrick, L., 2003. Toxic metals and antioxidants. Part II. The role of antioxidants in arsenic and cadmium toxicity. Altern. Med. Rev. 8, 106128. Peet, M., Strokes, C., 2005. Omega-3 fatty acids in the treatment of psychiatric disorders. Drugs 65, 1051–1059. 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, 201–209. Ray, S., 1986. Bioaccumulation of cadmium in marine organisms. Experientia 50 (Suppl.), 65–75. Robinson, L.E., Buchholz, A.C., Mazurak, V.C., 2007. Inflammation, obesity, and fatty acid metabolism: influence of n − 3 polyunsaturated fatty acids on factors contributing to metabolic syndrome. Appl. Physiol. Nutr. Metab. 32, 1008–1024. Romieu, I., Trenga, C., 2001. Diet and obstructive lung disease. Epidemiol. Rev. 23, 268–287. Saldivar, R.L., Luna, M., Reyes, E., Soto, R., Fortul, T., 1991. Cadmium determination in Mexican-produced tobacco. Environ. Res. 55, 91–96. Salonen, J.T., Seppänen, K., Lakka, T.A., Salonen, R., Kaplan, G.A., 2000. Mercury accumulation and acceleration progresión of carotid artherosclerosis: a population based prospective 4-year follow-up study in mean in eastern Finland. Atherosclerosis 148, 265–273. Sallsten, G., Thoren, J., Barregard, L., Schutz, A., Skarping, G., 1996. Long-term use nicotine chewing gum and mercury exposure from dental amalgam fillings. J. Dent. Res. 75, 594–598. Sallam, K.H., El-Sebaey, E.S., Morshdy, A.M., 1999. Mercury, cadmiunm and lead levels in Bagrus bayad fish from the river Nile, Delta region, Egypt. J. Egypt. Public Health Assoc. 74, 17–26. Sanfeliu, C., Sebastià, J., Cristòfol, R., Rodríguez-Farré, E., 2003. Neurotoxicity of organomercurial compounds. Neurotox. Res. 5, 283–305. Sepe, A., Ciaralli, L., Ciprotti, M., Giordano, R., Fumari, E., Costantini, S., 2003. Determination of cadmium, chromium, lead and vanadium in six fish species from the Adriatic Sea. Food Addit. Contam. 20, 543–552. Shukla, G.S., Hussain, T., Chandra, S.V., 1987. Possible role of regional, superoxide dismutase activity and lipid peroxide levels in cadmium neurotoxicity: in vivo and in vitro studies in growing rats. Life Sci. 41, 2215–2221.

M.I. Castro-González, M. Méndez-Armenta / Environmental Toxicology and Pharmacology 26 (2008) 263–271 Shukla, A., Shukla, G.S., Srimal, R.C., 1996. Cadmium-induced alterations in blood-brain barrier permeability and its possible correlation with decreased microvessel antioxidant potential in rat. Hum. Exp. Toxicol. 15, 400–405. Siddiqui, R.A., Harvey, K.A., Zaloga, G.P., 2008. Modulation of enzymatic activities by n − 3 polyunsaturated fatty acids to sˇıpport cardiovascular health. J. Nutr. Biochem. 19, 417–437. Simons, T.J., 1986. Cellular interactions between lead and calcium. Br. Med. Bull. 42, 431–434. Slikker Jr., W., 1994. Placental transfer and pharmacokinetics of developmental neurotoxicants. In: Chang, L.W. (Ed.), Principles of Neurotoxicology. Marcel Dekker Inc., New York, pp. 659–680. Smith, A.H., Lingas, E.O., Rahman, M., 2000. Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bull. World Health Organ. 78, 1093–1103. Smith, M.K., Sahyoun, N.R., 2005. Fish consumption: recommendations versus advisories, can they be reconciled? Nutr. Rev. 63, 39–46. Song, C., Zhao, S., 2007. Omega-3 fatty acid eicosapentaenoic acid. A new treatment for psychiatric and neurodegenerative diseases: a review of clinical investigations. Expert Opin. Invest. Drugs 16, 1627–1638. Stohs, S.J., Bagghi, D., 1995. Oxidative mechanisms in the toxicity of metal ions. Free Radical Biol. Med. 18, 321–336. Stohs, S.J., Bagchi, D., Bagchi, M., 1997. Toxicity of trace elements in tobacco smoke. Inhal. Toxicol. 9, 867–890. Svobodova, Z., Beklova, M., Machala, M., Drabeck, P., Dvorakova, D., Kolarova, J., Marˇsalek, B., Modra, H., 1996. Evaluation of the effect of chemical substances,

271

preparation, wastes and waste waters to organisms in the aquatic environment. Bull. VURH Vodnany 32, 76–96. Thatcher, R.W., Lester, M.L., McAlester, R., Horts, R., 1982. Effects of low levels of cadmium and lead on cognitive functions in children. Arch. Environ. Health 37, 159–166. Thomas, J.D., Styblo, M., Lin, S., 2001. The cellular metabolism and systemic toxicity of arsenic. Toxicol. Appl. Pharmacol. 176, 127–144. Torrejon, C., Jung, U.J., Deckelbaum, R.J., 2007. n − 3 fatty acids and cardiovascular disease: actions and molecular mechanisms. Prostaglandins Leukot. Essent. Fatty Acids 77, 319–326. Uneyama, C., Toda, M., Yamamoto, M., Morikawa, K., 2007. Arsenic in various foods: cumulative data. Food Addit. Contam. 24, 447–534. Usero, J., Izquierdo, C., Morillo, J., Gracia, I., 2003. Heavy metals in fish (Solea vulgaris, Anguilla anguilla and Liza aurata) from SALT marshes on the southern Atlantic coast of Spain. Environ. Int. 29, 949–956. World Health Organization WHO.2004 Guidelines or drinking-water qualiti. Joint FAO/WHO Expert Committee on Food Additives. Sixty-first meeting, Rome, 10–19 June 2003. Available at: ftp://ftp.fao.org/es/esn/jecfa/jecfa61sc.pdf. Accessed January 27, 2004. Wong, K.L., Klaassen, D.C., 1982. Neurotoxic effects of cadmium in Young rats. Toxicol. Appl. Pharmacol. 63, 330–337. Yoshizawa, K., Rimm, E.B., Morris, J.S., Spate, V.L., Hsieh, C.C., Spiegelman, D., Stampfer, M.J., Willet, W.C., 2002. Mercury and the risk of coronary heart disease in men. N. Engl. J. Med. 347, 1755–1760. Zhang, I., Wong, M.H., 2007. Environmental mercury contamination in China: sources and impacts. Environ. Int. 33, 108–121.