Persistent, bioaccumulative and toxic substances in fish: Human health considerations

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Abstract

Fish are important dietary items that provide essential nutrients. Fish however, bioaccumulate monomethyl mercury (MMHg) and organo-halogenated pollutants (OHP) that are persistent bioaccumulative and toxic substances (PBTS). Unlike man-made OHP, MMHg is mainly of natural origin but background concentrations of aquatic systems are determined by the environmental Hg-methylating potential. Industrial activities can modulate environmental discharges and fish bioaccumulation of PBTS. Fish and seafood consumption are associated with human body load of PBTS, but farming practices that utilize fishmeal increase the terrestrial food chain resulting in farm-animal accumulation of PBTS. These substances are neurotoxic and endocrine active that can impact humans and wild life, but chemical characteristics of MMHg and OHP modulate interactions with animal tissues. MMHg is protein reactive with a faster metabolism (months) than OHP that are stored and slowly (years) metabolized in fat tissues. Except for brain-Hg, neither Hg nor OHP in tissues are markers of toxic effects; however, deficits in neurobehavioral test-scores of children have been shown in some fish-eating populations. These deficits are transient and within normal range, and are not prodromes of neurological diseases. Although population studies show that consumption of fish at current levels of contamination do not explain neurological disorders, endocrine activity remains controversial. Understanding risk of hazard caused by fish-PBTS consumption requires a wide range of expertise. We discuss chemical, toxic, metabolic, and ecological characteristics associated with PBTS in fish. There are proven health outcome derived from fish consumption, while risk of exposure to avoidable PBTS is a chance that can be minimized by societal actions.

Introduction

Industrial activities have produced substances that persist in the environment. Some of them are harmful to ecosystems and human health. Because they bioaccumulate in animal tissues, they bioconcentrate at the top of the food chain. Fish and seafood are dietary items with such characteristics, i.e., they are bioaccumulators with the highest potential to transfer residues from water to humans (Dórea, 2006a, Dórea, 2006b). They are also special carriers of much-needed nutrients and functional substances that are crucial to human health. Thus, in order to fairly and accurately assess toxic risks (of fish xenobiotics) and health benefits derived from fish consumption, it is of fundamental importance to understand the chemistry and eco-toxicology of these substances.

Chemical pollutants are produced by industrial societies, are released by complex human activities, and eventually end up in aquatic environments. There, they remain as the ultimate sink. Because they are persistent in the environment, they are widely distributed and bioaccumulated in the human food chain. The best examples of these chemicals are organic substances, such as monomethyl mercury (MMHg), and various halogenated pollutants: pp'-DDT (1,1,1-tichloro-2,2,bis (4-chlorophenyl)ethane), 1,1-dichloro-2,2-bis(p-chlorophenyl) ethylene (DDE), pp'-dichlorophenyldichlorodiene (DDD), hexachlorobenzene (HCB), hexachlorohexana (HCH), polychlorinated biphenyls (PCB), organochlorine pesticides (OCP), polycyclic aromatic hydrocarbons (PAH), polychlorinated dibenzofurans (PCDF) and dibenzo-p-dioxins (PCDD), polybrominated diphenyl ethers (PBDE), and other halogenated hydrocarbons; these substances are here designated as organo-halogenated pollutants (OHP). Environmental disasters in the latter half of the last century dramatically illustrated the potential long-term adverse effects of these chemicals on ecosystems and, in particular, on human health (Clarkson, 1998). Thus, while health experts recommend fish consumption to fight degenerative diseases in industrial societies and to improve children nutritional-status and chances of survival in impoverished countries (Dórea, 2003) toxicologists (rightfully concerned with toxicity of PBTS) have issued advisories on fish consumption.

Persistent substances such as MMHg and OHP are neurotoxic (Newland, 2002). Others such as PCB (Abdelouahab et al., 2008) and phthalate esters-PEs (Schoeters et al., 2008) cause thyroid and gonad hormone imbalance;). These substances accumulate in fish as a function of age (size), fat composition and length of food chain. Therefore, human exposure to pollutants, when consuming fish or seafood, is rarely limited to a single chemical (Muckle et al., 2001a, Muckle et al., 2001b), especially when consuming large predatory species coming from a marine environment (Grandjean et al., 1995a). The propagation of PBTS depends on the chemical characteristics of each compound and its metabolism in the food chain. While environmental Hg-methylating potential determines MMHg bioaccumulation in aquatic-food chains, the degree of chlorination of OHP modulates its metabolism along food chain structures.

Neither environmental issues concerning pollution and PBTS toxicity per se, nor occupational issues are the focus of this paper. The objective is to center our attention on chemical, ecological and metabolic features of these substances in fish in order to develop a framework that allows a consistent and harmonized approach to safety assessment of fish consumption.

Section snippets

Inorganic and organic mercury

Mercury occurs naturally in the environment in three oxidation states (Hg0, Hg+1, Hg+2). Its widespread distribution is due to a series of complex chemical transformations. Anthropogenic sources of Hg include industrial products, but coal combustors remain the major atmospheric source. Schofield (2004) proposes that converting atomic mercury to water-soluble dichloride could control emission chemistry. However, the natural occurrence and release of Hg from soil, its atmospheric transport and

Conventional exposure

Fish-MMHg is the most important route of organic-Hg acquisition while dental filling (metallic Hg) is the most important route of inorganic-Hg (iHg) exposure (Clarkson, 2002). The human organism metabolizes these chemical forms of Hg differently. The biological half-life of serum iHg is 23.5d (Suzuki et al., 1992) while MMHg in the human body has a half-life of 45 to 70d (Clarkson, 2002, Cernichiari et al., 2007). Attempts to remove MMHg from fish proved ineffective by industrial (Aizpurua et

Monomethyl mercury

It is recognized that reproduction accelerates protein turnover which in turn affects maternal-Hg metabolism. The effect of pregnancy and lactation on lowering hair-Hg (HHg) has been shown in fish-eating Amazonian mothers; issues related to Hg metabolism during human reproduction has been discussed elsewhere (Dórea, 2004b, Dórea, 2007a). The estimated half-life of MMHg in muscle is 72d but the blood-clearance half-time of Hg is faster (42d) in lactating than in non-lactating women. However,

Biomarkers of exposure to fish PBTS

The presence of a substance or its metabolite in human fluids and tissues is largely utilized in nutrition and toxicology to characterize consumption of a food or nutrient, exposure to a toxic agent, biological effect and susceptibility to health conditions (Kosatsky and Weber, 2002). Sakamoto et al. (2004) observed significant correlations between maternal and fetal DHA concentrations and also between red-blood-cell Hg and plasma DHA in fetus of fish-eating mothers. Actually, fish consumption

Fish PBTS and health impacts: balanced considerations

Fish and seafood are important bioaccumulators of PBTS and the main source of human exposure. Faroese mothers who had routinely consumed pilot-whale meat had relatively high blood concentrations of Hg and OHP (Grandjean et al., 1995a). Environmental substances with estrogenic-like activity (PCBs and PEs) were found in human seminal plasma in the following order: urban fish eaters > rural fish eaters > urban vegetarians > rural vegetarians (Rozati et al., 2002). Because fish PBTS occur at low

Conclusions

The health hazard of single substances is characterized by toxicological and pharmacological studies based on specific effects. So far, it is not clear how a mixture of fish PBTS (sometimes with antagonic effects) might harm humans. It is clear, however, that the risk of reducing fish consumption and thereby health benefits of fish nutritional and functional properties can compromise health status of vulnerable populations. Thus, a comprehensible conclusion of hazard risk caused by fish-PBTS

Acknowledgements

This work was partially supported by grants 193.000.121/2004 (DCT/FAPDF/MCT/CNPq) and 555516/2006-7 (Edital 45/2006-CTHidro-MCT/CNPq).

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